Analysis of activity and motor coordination in rats undergoing stereotactic surgery and implantation of a cannula into the dorsal hippocampus

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Hernández-López, J.F. Rodríguez-Landa, A. Puga-Olguín, L.J. Germán-Ponciano, E. Rivadeneyra-Domínguez, B. Bernal-Morales" "autores" => array:6 [ 0 => array:3 [ "nombre" => "F." "apellidos" => "Hernández-López" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 1 => array:4 [ "nombre" => "J.F." "apellidos" => "Rodríguez-Landa" "email" => array:1 [ 0 => "juarodriguez@uv.mx" ] "referencia" => array:3 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] 1 => array:2 [ "etiqueta" => "c" "identificador" => "aff0015" ] 2 => array:2 [ "etiqueta" => "*" "identificador" => "cor0005" ] ] ] 2 => array:3 [ "nombre" => "A." "apellidos" => "Puga-Olguín" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 3 => array:3 [ "nombre" => "L.J." "apellidos" => "Germán-Ponciano" "referencia" => array:1 [ 0 => array:2 [ "etiqueta" => "a" "identificador" => "aff0005" ] ] ] 4 => array:3 [ "nombre" => "E." 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"apellidos" => "Bernal-Morales" "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "b" "identificador" => "aff0010" ] 1 => array:2 [ "etiqueta" => "c" "identificador" => "aff0015" ] ] ] ] "afiliaciones" => array:3 [ 0 => array:3 [ "entidad" => "Posgrado en Neuroetología, Universidad Veracruzana, Xalapa, Veracruz, Mexico" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Laboratorio de Neurofarmacología, Instituto de Neuroetología, Universidad Veracruzana, Xalapa, Veracruz, Mexico" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Facultad de Química Farmacéutica Biológica, Universidad Veracruzana, Xalapa, Veracruz, Mexico" "etiqueta" => "c" "identificador" => "aff0015" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Análisis de la actividad y coordinación motora en ratas con cirugía estereotáxica e implante de cánula en el hipocampo dorsal" ] ] "resumenGrafico" => array:2 [ "original" => 0 "multimedia" => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1925 "Ancho" => 1719 "Tamanyo" => 231979 ] ] "descripcion" => array:1 [ "en" => "(a) Image of the rat brain showing the site of cannula implantation at the anteroposterior level (dashed line) and a coronal section of the brain showing the site of cannula injection (white arrow). (b) Diagram of brain coronal sections, displaying the site of cannula implantation into hippocampal CA1 (black circles). Based on Paxinos and Watson's rat brain atlas (1998 edition)." ] ] ] "textoCompleto" => "IntroductionStereotactic surgery is a technique enabling brain structures to be located for electrode or cannula implantation, with the ultimate aim of exploring brain function.<a class="elsevierStyleCrossRef" href="#bib0235">1</a> These procedures have enabled the identification of neuroanatomical and neurochemical circuits involved in brain function and certain neurological disorders (epilepsy, movement disorders, and neurodegenerative diseases),<a class="elsevierStyleCrossRefs" href="#bib0240">2–5</a> learning and memory impairment,<a class="elsevierStyleCrossRefs" href="#bib0260">6,7</a> and emotional<a class="elsevierStyleCrossRefs" href="#bib0270">8,9</a> and affective disorders.<a class="elsevierStyleCrossRef" href="#bib0280">10</a> Furthermore, stereotactic surgery is used to explore the therapeutic potential and action mechanisms of potentially effective substances for the treatment of the previously mentioned disorders in humans.<a class="elsevierStyleCrossRefs" href="#bib0275">9,11–14</a>The hippocampus is one of the most frequently studied brain structures due to its involvement in the neurobiology of multiple neurological, cognitive, emotional, and affective disorders. Intrahippocampal microinjection of such substances as kainic acid or pilocarpine<a class="elsevierStyleCrossRefs" href="#bib0245">3,4</a> has been used to experimentally reproduce temporal lobe epilepsy, which is associated with a reduction in the number of neurons in the hippocampal CA1 region.<a class="elsevierStyleCrossRef" href="#bib0305">15</a> Under these experimental conditions, status epilepticus leads to memory and learning impairment,<a class="elsevierStyleCrossRefs" href="#bib0310">16,17</a> which may be minimised by administering anticonvulsants.<a class="elsevierStyleCrossRef" href="#bib0300">14</a>Other studies have explored the role of the hippocampus in neurological disorders associated with consumption of certain foods. Intrahippocampal microinjection of such neurotoxins as methylazoxymethanol, present in cycad seeds (Dioon spinulosum),<a class="elsevierStyleCrossRef" href="#bib0240">2</a> or linamarin, found in cassava root (Manihot esculenta Crantz),<a class="elsevierStyleCrossRef" href="#bib0320">18</a> promotes the loss of motor coordination and reduces the number of neurons in the hippocampal CA1 in rats.<a class="elsevierStyleCrossRef" href="#bib0320">18</a> These experimentally-induced alterations seem to be analogous to some of the neurological symptoms associated with consumption of cycad seeds or cassava root in humans (amyotrophic lateral sclerosis-parkinsonian dementia, tropical ataxic neuropathy, and konzo).<a class="elsevierStyleCrossRefs" href="#bib0325">19–21</a>Experimental models of locomotor impairment are used to evaluate the effects of intrahippocampal microinjection of neurotoxic compounds and substances that are potentially beneficial in humans (for example, as treatments for some neurological or psychiatric disorders).<a class="elsevierStyleCrossRefs" href="#bib0240">2,11,14,15</a> However, very few studies have used specific tests to evaluate the intrinsic locomotory impact of stereotactic surgery. This study aimed to evaluate the effects of stereotactic surgery on locomotor activity and coordination in female rats in order to confirm or rule out any associated neurological alterations that may interfere with the interpretation of results in studies employing this type of experimental manipulation.MethodsSubjectsWe used 56 3-month-old female Wistar rats weighing between 250 and 300g at the beginning of the study. Rats were housed in acrylic cages (4-5 rats per cage) in a vivarium. They were kept at room temperature (25±1°C) with a 12:12 light–dark cycle (lights on at 7:00am) and had ad libitum access to food and water. Rats were managed following the international ethical standards established in the Guide for care and use of laboratory animals,<a class="elsevierStyleCrossRef" href="#bib0340">22</a> and the Mexican official guidelines for the care and use of laboratory animals.<a class="elsevierStyleCrossRef" href="#bib0345">23</a>Vaginal smearsPrior to behavioural tests, vaginal smears were obtained once daily from each rat. Only the rats with 3 consecutive regular cycles (4-5 days) were included in our study. After behavioural tests, we obtained vaginal smears with cotton buds dampened in saline solution to determine the phase of the oestrus cycle. Vaginal discharge was examined under a light microscope (40×). Rats were divided into 2 groups based on vaginal smear results<a class="elsevierStyleCrossRef" href="#bib0350">24</a>: pro-oestrus/oestrus phase, characterised by high levels of ovarian hormones, and metoestrus/dioestrus phase, with low levels of these hormones.<a class="elsevierStyleCrossRef" href="#bib0355">25</a>Experimental groupsTwo experiments were conducted. In the first, rats were randomly allocated to 2 groups: 1) an intact group (n=14), where rats did not undergo stereotactic surgery, and 2) a surgery group (n=14), with rats undergoing stereotactic surgery plus dorsal hippocampal microinjection of a vehicle used in various experimental protocols (0.3μL of cyclodextrin solution 35%). Rats in both groups were evaluated using the forced swim and locomotor activity tests. The second experiment included 2 groups: 1) an intact group (n=14) and 2) a surgery group (n=14), with rats undergoing surgery and vehicle microinjection. Both groups were assessed using the rotarod test.After all behavioural tests were completed, vaginal smears were obtained to identify the phase of the oestrus cycle. Rats were then classified in 2 groups according to the level of ovarian hormones (high in pro-oestrus and oestrus phases and low in metoestrus and dioestrus phases) to minimise the influence of hormonal differences on the analysis of the results.Stereotactic surgeryRats were administered 0.05mg/kg atropine sulfate i.p. (Sigma–Aldrich Co.; St. Louis, MO, USA) and subsequently anaesthetised<a class="elsevierStyleCrossRef" href="#bib0360">26</a> with pentobarbital sodium (50mg/kgi.p.; Anestesal®, Pfizer; Mexico City, Mexico). During deep anaesthesia, the rats’ heads were placed in a stereotactic apparatus (Stoelting; Wood Dale, IL, USA). The cranium was exposed and a dental lab drill (35000rpm; Saeshin Dental Lab, South Korea) was used to drill a hole to implant a cannula into the dorsal hippocampus (AP=−3.8mm; ML=−2mm; DV=−2mm) according to the stereotactic coordinates of Paxinos and Watson's<a class="elsevierStyleCrossRef" href="#bib0235">1</a> rat brain atlas (1998 edition). A stainless steel guide cannula (8mm long, 0.7mm in diameter) was subsequently implanted and secured to the skull with dental acrylic (Arias Distribuidora Dental; Tlalnepantla, Mexico). After surgery, lidocaine (Laboratorios PISA; Mexico City, Mexico) was applied topically to the area surrounding the cannula implant. For the first 3 days after surgery, an analgesic agent (dipyrone 50, Virbac; Guadalajara, Mexico) was administered intraperitoneally to reduce pain. Rats were allowed to recover from surgery for 4 days before behavioural tests were conducted.MicroinjectionA vehicle was injected through the stainless steel cannula, which was connected to a 10μL Hamilton syringe by means of a polyethylene tube. An automatic infusion pump (KD Scientific; Holliston, MA, USA) was used to microinject 0.3μL of vehicle over 5 minutes (speed: 0.06μL/min). Rats were able to move freely during this procedure. Rats were left to rest for 5 minutes after microinjection to prevent the vehicle from returning by capillarity. The rats were then evaluated with a series of behavioural tests.Locomotor activity testEach rat was placed for 5 minutes inside an acrylic cage (44×33×20cm) whose base was divided into squares measuring 11×11cm. We assessed the following: 1) number of squares crossed (the rat was considered to have crossed a square when at least three-fourths of its body passed from one square to another); 2) vertical time in seconds (total time spent in a rearing position), and 3) grooming time in seconds (total time spent grooming, including elliptical movements of both front legs over the nose, ears, body, and genital area following a cephalocaudal direction).<a class="elsevierStyleCrossRef" href="#bib0365">27</a>Forced swim testEach rat was placed for 5 minutes inside a glass tank (26×29×50cm) filled with water at a temperature of 25±1°C (water level: 30cm). This test evaluated the following variables: 1) latency to first episode of immobility, in seconds (time elapsed from the moment when the rat was placed inside the container to the first episode of immobility); 2) total immobility time (sum of all immobility episodes; rats were considered to be immobile when they made only the necessary movements to keep the head above water); 3) total lateral swimming time, in seconds (sum of all episodes of uncoordinated swimming on one side); and 4) total number of spins (total number of episodes of rats turning on their own axes while swimming).<a class="elsevierStyleCrossRefs" href="#bib0240">2,28</a>We recorded video footage of all sessions. Variables were quantified by 2 independent observers using software specifically designed for recording rat behaviour.Rotarod testRats completed 4 training sessions (one session daily) on an accelerating rotarod (speed 4 to 20rpm; LE 8300, LSI Letica, Panlab Scientific Instruments; Barcelona, Spain); each session lasted 5 minutes. Stereotactic surgery was performed after training was complete. Four days later, rats were placed on an accelerating rotarod (speed 4 to 20rpm), completing 5 sessions with 3-minute resting periods between sessions. We evaluated latency to fall, that is, the time it took for the rat to fall from the rod. This variable is used to identify any alterations in motor coordination and balance.<a class="elsevierStyleCrossRef" href="#bib0375">29</a>Verification of the site of cannula implantation and microinjectionAfter the completion of behavioural tests, vaginal smears were obtained and animals euthanised with pentobarbital overdose (PISA-Agropecuaria; Guadalajara, Mexico). The cannula was used to mark the injection site with Evans blue (Sigma–Aldrich Co.; St. Louis, MO, USA). Rats’ brains were perfusion fixed, extracted, and sliced. The site of cannula implantation was checked with a light microscope; Paxinos and Watson's<a class="elsevierStyleCrossRef" href="#bib0235">1</a> rat brain atlas was used for reference. The statistical analysis included only data from those rats in which cannulas were found to have been implanted correctly in the hippocampal CA1 region.Statistical analysisData were analysed using 2-way ANOVA for independent samples; factors were surgical condition (intact or subjected to stereotactic surgery) and phase of oestrus cycle (pro-oestrus/oestrus and metoestrus/dioestrus). Given P-values ≤.05, we applied the post hoc Student–Newman–Keuls test. Results were expressed as means±SD.ResultsPhase of the oestrus cycleAccording to the analysis of vaginal smears, 7 rats were in the pro-oestrus/oestrus phase and 7 in the metoestrus/dioestrus phase in each of the experimental groups.Site of cannula implantationOf all rats included in the study, 2 were excluded from statistical analysis (one rat in the pro-oestrus/oestrus phase in experiment 1 and another one in the metoestrus/dioestrus phase in experiment 2), due to the presence of oedema in the area surrounding the implantation site and extending from the dorsal hippocampus to the cerebral cortex. In the remaining rats, the histological study confirmed correct cannula implantation into the dorsal hippocampus (CA1) between coordinates AP=−3.3 and AP=−4.6mm from bregma (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>).<elsevierMultimedia ident="fig0005"></elsevierMultimedia>Open-field testCrossed squaresNo significant difference in the number of crossed squares was observed between the intact and surgery groups (F[1, 23]=1.38; P=.25) (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>a). We did, however, find statistically significant differences between rats in the pro-oestrus/oestrus and in the metoestrus/dioestrus phases (F[1, 23]=6.58; P<.02). According to the post hoc test, rats in the metoestrus/dioestrus phase crossed a higher number of squares than those in the pro-oestrus/oestrus phase (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>b). Factor interaction revealed no significant differences (F[1, 23]=1.42; P=.25) (intact rats in pro-oestrus/oestrus phase [n=7]: 33.28±2.19; sham-operated rats in pro-oestrus/oestrus phase [n=6]: 33.34±3.07; intact rats in metoestrus/dioestrus phase [n=7]: 43.71±2.23; sham-operated rats in metoestrus/dioestrus phase [n=7]: 37.14±3.62).<elsevierMultimedia ident="fig0010"></elsevierMultimedia>GroomingNo significant differences in grooming time were observed between intact and sham-operated rats (F[1,23]=0.63; P=.43; intact: 40.06±1.47s vs surgery: 41.51±1.23s) or related to phase of the oestrus cycle (F[1, 23]=2.89; P=.10; pro-oestrus/oestrus: 39.23±1.37s vs metoestrus/dioestrus: 42.34±1.24s). Likewise, interaction between factors revealed no significant differences (F[1, 23]=1.42; P=.25) (intact rats in pro-oestrus/oestrus phase [n=7]: 37.17±2.09s; sham-operated rats in pro-oestrus/oestrus phase [n=6]: 41.29±1.35s; intact rats in metoestrus/dioestrus phase [n=7]: 42.94±1.51s; sham-operated rats in metoestrus/dioestrus phase [n=7]: 42.74±2.06s).Vertical behaviourNo significant differences in vertical time were observed between intact and sham-operated rats (F[1, 23]=1.43; P=.24; intact: 65.66±1.79s vs surgery: 68.47±1.49s) or in terms of phase of the oestrus cycle (F[1, 23]=2.18; P=.15; pro-oestrus/oestrus: 65.33±2.07s vs metoestrus/dioestrus: 68.79±1.14s). Factor interaction revealed no significant differences (F[1, 23]=0.14; P=.70) (intact rats in pro-oestrus/oestrus phase [n=7]: 63.47±3.03s; sham-operated rats in pro-oestrus/oestrus phase [n=6]: 67.17±2.83s; intact rats in metoestrus/dioestrus phase [n=7]: 67.84±1.79s; sham-operated rats in metoestrus/dioestrus phase [n=7]: 69.75±1.43s).Forced swim testLateral swimming time and number of spinsAll animals, whether intact or sham-operated, showed a normal swimming pattern in the forced swim test; none displayed lateral swimming or spinning behaviour.Latency to first immobility episodeWe observed no significant differences in latency to the first episode of immobility between intact and sham-operated rats (F[1, 23]=0.04; P=.83; intact: 26.84±2.25s vs surgery: 27.53±2.42s) or in terms of phase of the oestrus cycle (F[1, 23]=2.07; P=.16; pro-oestrus/oestrus: 29.54±1.84s vs metoestrus/dioestrus: 24.84±2.52s). Factor interaction revealed no significant differences (F[1, 23]=0.39; P=.53) (intact rats in pro-oestrus/oestrus phase [n=7]: 30.22±2.68s; sham-operated rats in pro-oestrus/oestrus phase [n=6]: 28.86±2.73s; intact rats in metoestrus/dioestrus phase [n=7]: 23.47±3.32s; sham-operated rats in metoestrus/dioestrus phase [n=7]: 26.21±3.96s).Total immobility timeNo significant difference in total immobility time was observed between the intact and sham-operated groups (F[1, 23]=21.06; P=.62) (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>a). However, there were statistically significant differences between rats in the pro-oestrus/oestrus phase and the metoestrus/dioestrus phase (F[1, 23]=90.95; P<.001). According to the post hoc test, rats in the pro-oestrus/oestrus phase were immobile for less time than those in the metoestrus/dioestrus phase (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>b). Nevertheless, factor interaction revealed no significant differences (F[1, 23]=77.21; P=.35) (intact rats in pro-oestrus/oestrus phase [n=7]: 44.00±6.61s; sham-operated rats in pro-oestrus/oestrus phase [n=6]: 42.38±7.75s; intact rats in metoestrus/dioestrus phase [n=7]: 74.91±9.07s; sham-operated rats in metoestrus/dioestrus phase [n=7]: 80.07±10.68s).<elsevierMultimedia ident="fig0015"></elsevierMultimedia>Rotarod testLatency to fallWe observed no significant difference in latency to fall between the intact and sham-operated groups (F[1, 23]=0.03; P=.85; intact: 151.47±5.36s vs surgery: 149.92±6.64s) or in terms of the phase of the oestrus cycle (F[1, 23]=3.40; P=.07; pro-oestrus/oestrus: 142.10±2.94s vs metoestrus/dioestrus: 158.29±7.11s). Factor interaction revealed no significant differences (F[1, 23]=0.14; P=.70) (intact rats in pro-oestrus/oestrus phase [n=7]: 142.32±3.78s; sham-operated rats in pro-oestrus/oestrus phase [n=7]: 143.10±4.96s; intact rats in metoestrus/dioestrus phase [n=7]: 160.62±9.08s; sham-operated rats in metoestrus/dioestrus phase [n=6]: 155.29±11.61s).DiscussionIn our study, stereotactic surgery for cannula implantation plus vehicle microinjection into the hippocampal CA1 region had no negative impact on activity and motor coordination. All Wistar rats displayed the behavioural patterns typical of their oestrus cycle phase regardless of whether they had undergone stereotactic surgery.The locomotor activity test is frequently used to quantify variables of displacement, exploration, and emotional status under experimental circumstances.<a class="elsevierStyleCrossRefs" href="#bib0380">30,31</a> In our study, the locomotor activity test was used to confirm that the experimental manipulation (stereotactic surgery for cannula implantation through the motor cortex plus vehicle microinjection into the dorsal hippocampus) caused no motor hyper- or hypoactivity (larger or smaller numbers of crossed squares), changes in exploration behaviour (vertical time), or changes in motivation (grooming time). Our results support the hypothesis that surgical manipulation and microinjection do not cause neurological damage. In line with this idea, neurotoxic lesions to the dorsal hippocampus have been reported to cause motor hyperactivity.<a class="elsevierStyleCrossRefs" href="#bib0285">11,18</a> Similarly, large quantities of cassava or cycad seeds have been observed to cause neurological alterations in humans.<a class="elsevierStyleCrossRefs" href="#bib0255">5,20,21,32</a> Our findings suggest that stereotactic surgery, cannula implantation, and microinjection in rats do not cause brain damage with potential to impair locomotor activity. Changes in motor activity were found to be associated with the phase of the oestrus cycle, but not with surgical manipulation. Rats in the metoestrus/dioestrus phase crossed a higher number of squares than rats in the pro-oestrus/oestrus phase. This increase in motor activity may be associated with higher levels of anxiety during the metoestrus/dioestrus phase, which is characterised by low concentrations of ovarian hormones.<a class="elsevierStyleCrossRefs" href="#bib0355">25,33</a>Grooming is regarded as a marker of emotional and motivational status in rats. Grooming time increases in rats experiencing mild stress<a class="elsevierStyleCrossRefs" href="#bib0400">34,35</a> and decreases under severe stress<a class="elsevierStyleCrossRefs" href="#bib0410">36,37</a> compared to intact rats. Our study found no significant differences in grooming time between intact and sham-operated rats, which suggests that stereotactic surgery and cannula implantation into the dorsal hippocampus have no impact on emotionality and motivation in rats. Likewise, our study revealed no association between vertical time and surgery or the phase of the oestrus cycle. Vertical behaviour is considered to be an indicator of exploration,<a class="elsevierStyleCrossRefs" href="#bib0420">38,39</a> which requires a high level of motor coordination. Vertical behaviour increases in rats with neuronal damage to the dorsal hippocampus, which is probably associated with hyperactivity and poor motor coordination.<a class="elsevierStyleCrossRef" href="#bib0320">18</a> Rats that underwent surgery displayed no behavioural changes, suggesting that the surgical procedures described in this study cause no brain damage.Rats with vestibular lesions<a class="elsevierStyleCrossRef" href="#bib0430">40</a> or neurological impairment associated with the consumption of foods containing neurotoxic compounds<a class="elsevierStyleCrossRefs" href="#bib0320">18,19</a> display lateral swimming and spinning behaviour due to poor motor coordination. In our study, however, none of the rats (whether intact or sham-operated) displayed an abnormal swimming pattern, which rules out the possibility of surgery-related neurological damage. Latency to first immobility period and total immobility time in the forced swim test were similar in both groups (intact and sham-operated). Differences in total immobility time were linked only to the phase of the oestrus cycle. Rats in the metoestrus/dioestrus phase were immobile for a longer total time than rats in the pro-oestrus/oestrus phase. Our findings are consistent with results reported in the literature: rats in the metoestrus/dioestrus phase are more vulnerable to stress and are immobile for a longer time during the forced swim test, whereas rats in the pro-oestrus/oestrus phase, with high concentrations of ovarian hormones, are immobile for a shorter time, as occurs after administration of such hormones as progesterone and allopregnanolone.<a class="elsevierStyleCrossRefs" href="#bib0435">41,42</a>The rotarod test assesses motor coordination and balance.<a class="elsevierStyleCrossRef" href="#bib0445">43</a> Intact (healthy) animals will be able to remain on the rotating rod for longer periods due to preserved limb coordination and balance.<a class="elsevierStyleCrossRef" href="#bib0450">44</a> In contrast, animals with neurological alterations or receiving neurotoxic compounds or sedatives usually display shorter latencies to fall.<a class="elsevierStyleCrossRefs" href="#bib0455">45,46</a> In our study, rats that underwent stereotactic surgery for cannula implantation into the dorsal hippocampus displayed no significant difference in latency to fall compared to intact rats. Likewise, no differences were found between rats in the pro-oestrus/oestrus phase and those in the metoestrus/dioestrus phase. This suggests that experimental manipulations caused no neurological alterations potentially affecting motor coordination and activity.Our results show that stereotactic surgery and cannula implantation into the dorsal hippocampus cause no alterations in locomotor activity and coordination in rats, ruling out the possibility that this type of manipulation may cause neurological impairment interfering with the interpretation of results from experimental studies.FundingThis study was funded by grants I010/458/2013, C-703/2013 and I010/152/2014, C-133/2014.Conflicts of interestThe authors have no conflicts of interest to declare." "textoCompletoSecciones" => array:1 [ "secciones" => array:12 [ 0 => array:3 [ "identificador" => "xres937609" "titulo" => "Abstract" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Introduction" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Methods" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Conclusion" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec911448" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres937610" "titulo" => "Resumen" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0025" "titulo" => "Introducción" ] 1 => array:2 [ "identificador" => "abst0030" "titulo" => "Métodos" ] 2 => array:2 [ "identificador" => "abst0035" "titulo" => "Resultados" ] 3 => array:2 [ "identificador" => "abst0040" "titulo" => "Conclusión" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec911449" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:3 [ "identificador" => "sec0010" "titulo" => "Methods" "secciones" => array:10 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Subjects" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Vaginal smears" ] 2 => array:2 [ "identificador" => "sec0025" "titulo" => "Experimental groups" ] 3 => array:2 [ "identificador" => "sec0030" "titulo" => "Stereotactic surgery" ] 4 => array:2 [ "identificador" => "sec0035" "titulo" => "Microinjection" ] 5 => array:2 [ "identificador" => "sec0040" "titulo" => "Locomotor activity test" ] 6 => array:2 [ "identificador" => "sec0045" "titulo" => "Forced swim test" ] 7 => array:2 [ "identificador" => "sec0050" "titulo" => "Rotarod test" ] 8 => array:2 [ "identificador" => "sec0055" "titulo" => "Verification of the site of cannula implantation and microinjection" ] 9 => array:2 [ "identificador" => "sec0060" "titulo" => "Statistical analysis" ] ] ] 6 => array:3 [ "identificador" => "sec0065" "titulo" => "Results" "secciones" => array:5 [ 0 => array:2 [ "identificador" => "sec0070" "titulo" => "Phase of the oestrus cycle" ] 1 => array:2 [ "identificador" => "sec0075" "titulo" => "Site of cannula implantation" ] 2 => array:3 [ "identificador" => "sec0080" "titulo" => "Open-field test" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0085" "titulo" => "Crossed squares" ] 1 => array:2 [ "identificador" => "sec0090" "titulo" => "Grooming" ] 2 => array:2 [ "identificador" => "sec0095" "titulo" => "Vertical behaviour" ] ] ] 3 => array:3 [ "identificador" => "sec0100" "titulo" => "Forced swim test" "secciones" => array:3 [ 0 => array:2 [ "identificador" => "sec0105" "titulo" => "Lateral swimming time and number of spins" ] 1 => array:2 [ "identificador" => "sec0110" "titulo" => "Latency to first immobility episode" ] 2 => array:2 [ "identificador" => "sec0115" "titulo" => "Total immobility time" ] ] ] 4 => array:3 [ "identificador" => "sec0120" "titulo" => "Rotarod test" "secciones" => array:1 [ 0 => array:2 [ "identificador" => "sec0125" "titulo" => "Latency to fall" ] ] ] ] ] 7 => array:2 [ "identificador" => "sec0130" "titulo" => "Discussion" ] 8 => array:2 [ "identificador" => "sec0135" "titulo" => "Funding" ] 9 => array:2 [ "identificador" => "sec0140" "titulo" => "Conflicts of interest" ] 10 => array:2 [ "identificador" => "xack316724" "titulo" => "Acknowledgements" ] 11 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2015-02-07" "fechaAceptado" => "2016-03-08" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec911448" "palabras" => array:6 [ 0 => "Stereotactic surgery" 1 => "Cannula placement" 2 => "Hippocampus" 3 => "Motor coordination" 4 => "Locomotor activity" 5 => "Microinjection" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec911449" "palabras" => array:6 [ 0 => "Cirugía estereotáxica" 1 => "Implante de cánula" 2 => "Hipocampo" 3 => "Coordinación motriz" 4 => "Actividad locomotora" 5 => "Microinyección" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:3 [ "titulo" => "Abstract" "resumen" => "IntroductionStereotactic surgery is used to place electrodes or cannulas in the brain in order to study the function of several brain structures in preclinical research. The hippocampus has been extensively studied with this methodology due to its involvement in a wide range of neurological, cognitive, emotional, and affective disorders. However, the effects of stereotactic surgery on coordination and motor activity should be evaluated in order to determine whether this surgical procedure causes any neurological alterations that may bias the results of studies incorporating this technique. MethodsWe evaluated the effects of stereotactic surgery and implantation of a cannula into the hippocampus of female Wistar rats on the motor activity, forced swim, and rotarod tests. The stage of the oestrous cycle was included in the statistical analysis. ResultsStereotactic surgery had no impact on any of the motor activity variables assessed in the open field (squares crossed, time spent in grooming, and rearing), forced swim (turning behaviour, lateral swimming, latency to first immobility, and time spent immobile), and rotarod (latency to fall) tests, compared with intact rats. Regardless of surgical manipulation, rats in the metestrus and diestrus stages crossed a greater number of squares and displayed longer immobility times than those in the proestrus and estrus stages. ConclusionStereotactic surgery for cannula placement in the dorsal hippocampus does not affect coordination and motor activity in rats. We can therefore conclude that this procedure has no neurological complications that may interfere in the interpretation of results of studies applying this technique." "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0005" "titulo" => "Introduction" ] 1 => array:2 [ "identificador" => "abst0010" "titulo" => "Methods" ] 2 => array:2 [ "identificador" => "abst0015" "titulo" => "Results" ] 3 => array:2 [ "identificador" => "abst0020" "titulo" => "Conclusion" ] ] ] "es" => array:3 [ "titulo" => "Resumen" "resumen" => "IntroducciónLa cirugía estereotáxica permite el implante de electrodos o cánulas para estudiar el funcionamiento de diversas estructuras cerebrales a nivel preclínico. El hipocampo ha sido ampliamente estudiado con esta metodología, debido a su participación en desórdenes neurológicos, cognitivos, emocionales y afectivos. Sin embargo, el efecto per se de esta metodología sobre la coordinación y la actividad motora, para identificar o descartar alteraciones neurológicas que pudieran influir en los resultados de protocolos que la utilizan, requiere ser explorado. MétodosSe evaluó el efecto de la cirugía estereotáxica y el implante de cánula en el hipocampo de ratas hembra Wistar en las pruebas de actividad locomotora, nado y Rota-rod. El análisis estadístico consideró la fase del ciclo estral de las ratas. ResultadosNinguna de las variables evaluadas en las pruebas de actividad locomotora (cuadros cruzados, tiempo de acicalamiento y conducta vertical), nado (giros, nado lateral, latencia a la primera inmovilidad y tiempo de inmovilidad) o Rota-rod (latencia a la caída), fueron modificadas por la manipulación quirúrgica, en relación con ratas intactas. Independientemente de la manipulación quirúrgica, las ratas en metaestro-diestro cruzaron más cuadros y tuvieron mayor tiempo de inmovilidad, que las ratas en proestro-estro. ConclusiónLa cirugía estereotáxica y el implante de cánula en el hipocampo dorsal carecen de efectos sobre la coordinación y la actividad locomotora de la rata, por lo que se descarta algún daño neurológico que pudiera interferir en la interpretación de resultados en protocolos que incluyen esta manipulación experimental." "secciones" => array:4 [ 0 => array:2 [ "identificador" => "abst0025" "titulo" => "Introducción" ] 1 => array:2 [ "identificador" => "abst0030" "titulo" => "Métodos" ] 2 => array:2 [ "identificador" => "abst0035" "titulo" => "Resultados" ] 3 => array:2 [ "identificador" => "abst0040" "titulo" => "Conclusión" ] ] ] ] "NotaPie" => array:1 [ 0 => array:2 [ "etiqueta" => "☆" "nota" => "Please cite this article as: Hernández-López F, Rodríguez-Landa JF, Puga-Olguín A, Germán-Ponciano LJ, Rivadeneyra-Domínguez E, Bernal-Morales B. Análisis de la actividad y coordinación motora en ratas con cirugía estereotáxica e implante de cánula en el hipocampo dorsal. Neurología. 2017;32:579–586." ] ] "multimedia" => array:3 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1925 "Ancho" => 1719 "Tamanyo" => 231979 ] ] "descripcion" => array:1 [ "en" => "(a) Image of the rat brain showing the site of cannula implantation at the anteroposterior level (dashed line) and a coronal section of the brain showing the site of cannula injection (white arrow). (b) Diagram of brain coronal sections, displaying the site of cannula implantation into hippocampal CA1 (black circles). Based on Paxinos and Watson's rat brain atlas (1998 edition)." ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 2102 "Ancho" => 1295 "Tamanyo" => 79117 ] ] "descripcion" => array:1 [ "en" => "Number of crossed squares in the locomotor activity test. (a) Surgery caused no significant changes in the number of crossed squares compared to intact rats. (b) Rats in the metoestrus/dioestrus (M/D) phase crossed a significantly higher number of squares than rats in the pro-oestrus/oestrus phase (P/O). *P<.05 vs P/O." ] ] 2 => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 2112 "Ancho" => 1277 "Tamanyo" => 73000 ] ] "descripcion" => array:1 [ "en" => "Total immobility time in the forced swim test. (a) Surgery caused no significant changes in this variable compared to intact rats. (b) Rats in the metoestrus/dioestrus (M/D) phase remained immobile for a longer time than rats in the pro-oestrus/oestrus phase (P/O). *P<.05 vs P/O." ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:46 [ 0 => array:3 [ "identificador" => "bib0235" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "The rat brain in stereotaxic coordinates" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "G. Paxinos" 1 => "C. 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Análisis de la actividad y coordinación motora en ratas con cirugía estereotáxica e implante de cánula en el hipocampo dorsal

F. Hernández-Lópeza, J.F. Rodríguez-Landab,c,

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juarodriguez@uv.mx

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, A. Puga-Olguína, L.J. Germán-Poncianoa, E. Rivadeneyra-Domínguezc, B. Bernal-Moralesb,c

a Posgrado en Neuroetología, Universidad Veracruzana, Xalapa, Veracruz, Mexico

b Laboratorio de Neurofarmacología, Instituto de Neuroetología, Universidad Veracruzana, Xalapa, Veracruz, Mexico

c Facultad de Química Farmacéutica Biológica, Universidad Veracruzana, Xalapa, Veracruz, Mexico

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tropical ataxic neuropathy&#44; and konzo&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib0325"><span class="elsevierStyleSup">19&#8211;21</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">Experimental models of locomotor impairment are used to evaluate the effects of intrahippocampal microinjection of neurotoxic compounds and substances that are potentially beneficial in humans &#40;for example&#44; as treatments for some neurological or psychiatric disorders&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib0240"><span class="elsevierStyleSup">2&#44;11&#44;14&#44;15</span></a> However&#44; very few studies have used specific tests to evaluate the intrinsic locomotory impact of stereotactic surgery&#46; This study aimed to evaluate the effects of stereotactic surgery on locomotor activity and coordination in female rats in order to confirm or rule out any associated neurological alterations that may interfere with the interpretation of results in studies employing this type of experimental manipulation&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Subjects</span><p id="par0025" class="elsevierStylePara elsevierViewall">We used 56 3-month-old female Wistar rats weighing between 250 and 300<span class="elsevierStyleHsp" style=""></span>g at the beginning of the study&#46; Rats were housed in acrylic cages &#40;4-5 rats per cage&#41; in a vivarium&#46; They were kept at room temperature &#40;25<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1<span class="elsevierStyleHsp" style=""></span>&#176;C&#41; with a 12&#58;12 light&#8211;dark cycle &#40;lights on at 7&#58;00<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleSmallCaps">am</span>&#41; and had ad libitum access to food and water&#46; Rats were managed following the international ethical standards established in the <span class="elsevierStyleItalic">Guide for care and use of laboratory animals</span>&#44;<a class="elsevierStyleCrossRef" href="#bib0340"><span class="elsevierStyleSup">22</span></a> and the Mexican official guidelines for the care and use of laboratory animals&#46;<a class="elsevierStyleCrossRef" href="#bib0345"><span class="elsevierStyleSup">23</span></a></p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Vaginal smears</span><p id="par0030" class="elsevierStylePara elsevierViewall">Prior to behavioural tests&#44; vaginal smears were obtained once daily from each rat&#46; Only the rats with 3 consecutive regular cycles &#40;4-5 days&#41; were included in our study&#46; After behavioural tests&#44; we obtained vaginal smears with cotton buds dampened in saline solution to determine the phase of the oestrus cycle&#46; Vaginal discharge was examined under a light microscope &#40;40&#215;&#41;&#46; Rats were divided into 2 groups based on vaginal smear results<a class="elsevierStyleCrossRef" href="#bib0350"><span class="elsevierStyleSup">24</span></a>&#58; pro-oestrus&#47;oestrus phase&#44; characterised by high levels of ovarian hormones&#44; and metoestrus&#47;dioestrus phase&#44; with low levels of these hormones&#46;<a class="elsevierStyleCrossRef" href="#bib0355"><span class="elsevierStyleSup">25</span></a></p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Experimental groups</span><p id="par0035" class="elsevierStylePara elsevierViewall">Two experiments were conducted&#46; In the first&#44; rats were randomly allocated to 2 groups&#58; 1&#41; an intact group &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>14&#41;&#44; where rats did not undergo stereotactic surgery&#44; and 2&#41; a surgery group &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>14&#41;&#44; with rats undergoing stereotactic surgery plus dorsal hippocampal microinjection of a vehicle used in various experimental protocols &#40;0&#46;3<span class="elsevierStyleHsp" style=""></span>&#956;L of cyclodextrin solution 35&#37;&#41;&#46; Rats in both groups were evaluated using the forced swim and locomotor activity tests&#46; The second experiment included 2 groups&#58; 1&#41; an intact group &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>14&#41; and 2&#41; a surgery group &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>14&#41;&#44; with rats undergoing surgery and vehicle microinjection&#46; Both groups were assessed using the rotarod test&#46;</p><p id="par0040" class="elsevierStylePara elsevierViewall">After all behavioural tests were completed&#44; vaginal smears were obtained to identify the phase of the oestrus cycle&#46; Rats were then classified in 2 groups according to the level of ovarian hormones &#40;high in pro-oestrus and oestrus phases and low in metoestrus and dioestrus phases&#41; to minimise the influence of hormonal differences on the analysis of the results&#46;</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Stereotactic surgery</span><p id="par0045" class="elsevierStylePara elsevierViewall">Rats were administered 0&#46;05<span class="elsevierStyleHsp" style=""></span>mg&#47;kg atropine sulfate i&#46;p&#46; &#40;Sigma&#8211;Aldrich Co&#46;&#59; St&#46; Louis&#44; MO&#44; USA&#41; and subsequently anaesthetised<a class="elsevierStyleCrossRef" href="#bib0360"><span class="elsevierStyleSup">26</span></a> with pentobarbital sodium &#40;50<span class="elsevierStyleHsp" style=""></span>mg&#47;kg<span class="elsevierStyleHsp" style=""></span>i&#46;p&#46;&#59; Anestesal<span class="elsevierStyleSup">&#174;</span>&#44; Pfizer&#59; Mexico City&#44; Mexico&#41;&#46; During deep anaesthesia&#44; the rats&#8217; heads were placed in a stereotactic apparatus &#40;Stoelting&#59; Wood Dale&#44; IL&#44; USA&#41;&#46; The cranium was exposed and a dental lab drill &#40;35<span class="elsevierStyleHsp" style=""></span>000<span class="elsevierStyleHsp" style=""></span>rpm&#59; Saeshin Dental Lab&#44; South Korea&#41; was used to drill a hole to implant a cannula into the dorsal hippocampus &#40;AP<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;3&#46;8<span class="elsevierStyleHsp" style=""></span>mm&#59; ML<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;2<span class="elsevierStyleHsp" style=""></span>mm&#59; DV<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;2<span class="elsevierStyleHsp" style=""></span>mm&#41; according to the stereotactic coordinates of Paxinos and Watson&#39;s<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">1</span></a> rat brain atlas &#40;1998 edition&#41;&#46; A stainless steel guide cannula &#40;8<span class="elsevierStyleHsp" style=""></span>mm long&#44; 0&#46;7<span class="elsevierStyleHsp" style=""></span>mm in diameter&#41; was subsequently implanted and secured to the skull with dental acrylic &#40;Arias Distribuidora Dental&#59; Tlalnepantla&#44; Mexico&#41;&#46; After surgery&#44; lidocaine &#40;Laboratorios PISA&#59; Mexico City&#44; Mexico&#41; was applied topically to the area surrounding the cannula implant&#46; For the first 3 days after surgery&#44; an analgesic agent &#40;dipyrone 50&#44; Virbac&#59; Guadalajara&#44; Mexico&#41; was administered intraperitoneally to reduce pain&#46; Rats were allowed to recover from surgery for 4 days before behavioural tests were conducted&#46;</p></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Microinjection</span><p id="par0050" class="elsevierStylePara elsevierViewall">A vehicle was injected through the stainless steel cannula&#44; which was connected to a 10<span class="elsevierStyleHsp" style=""></span>&#956;L Hamilton syringe by means of a polyethylene tube&#46; An automatic infusion pump &#40;KD Scientific&#59; Holliston&#44; MA&#44; USA&#41; was used to microinject 0&#46;3<span class="elsevierStyleHsp" style=""></span>&#956;L of vehicle over 5 minutes &#40;speed&#58; 0&#46;06<span class="elsevierStyleHsp" style=""></span>&#956;L&#47;min&#41;&#46; Rats were able to move freely during this procedure&#46; Rats were left to rest for 5 minutes after microinjection to prevent the vehicle from returning by capillarity&#46; The rats were then evaluated with a series of behavioural tests&#46;</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Locomotor activity test</span><p id="par0055" class="elsevierStylePara elsevierViewall">Each rat was placed for 5 minutes inside an acrylic cage &#40;44<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>33<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>20<span class="elsevierStyleHsp" style=""></span>cm&#41; whose base was divided into squares measuring 11<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>11<span class="elsevierStyleHsp" style=""></span>cm&#46; We assessed the following&#58; 1&#41; number of squares crossed &#40;the rat was considered to have crossed a square when at least three-fourths of its body passed from one square to another&#41;&#59; 2&#41; vertical time in seconds &#40;total time spent in a rearing position&#41;&#44; and 3&#41; grooming time in seconds &#40;total time spent grooming&#44; including elliptical movements of both front legs over the nose&#44; ears&#44; body&#44; and genital area following a cephalocaudal direction&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0365"><span class="elsevierStyleSup">27</span></a></p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Forced swim test</span><p id="par0060" class="elsevierStylePara elsevierViewall">Each rat was placed for 5 minutes inside a glass tank &#40;26<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>29<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>50<span class="elsevierStyleHsp" style=""></span>cm&#41; filled with water at a temperature of 25<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1<span class="elsevierStyleHsp" style=""></span>&#176;C &#40;water level&#58; 30<span class="elsevierStyleHsp" style=""></span>cm&#41;&#46; This test evaluated the following variables&#58; 1&#41; latency to first episode of immobility&#44; in seconds &#40;time elapsed from the moment when the rat was placed inside the container to the first episode of immobility&#41;&#59; 2&#41; total immobility time &#40;sum of all immobility episodes&#59; rats were considered to be immobile when they made only the necessary movements to keep the head above water&#41;&#59; 3&#41; total lateral swimming time&#44; in seconds &#40;sum of all episodes of uncoordinated swimming on one side&#41;&#59; and 4&#41; total number of spins &#40;total number of episodes of rats turning on their own axes while swimming&#41;&#46;<a class="elsevierStyleCrossRefs" href="#bib0240"><span class="elsevierStyleSup">2&#44;28</span></a></p><p id="par0065" class="elsevierStylePara elsevierViewall">We recorded video footage of all sessions&#46; Variables were quantified by 2 independent observers using software specifically designed for recording rat behaviour&#46;</p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Rotarod test</span><p id="par0070" class="elsevierStylePara elsevierViewall">Rats completed 4 training sessions &#40;one session daily&#41; on an accelerating rotarod &#40;speed 4 to 20<span class="elsevierStyleHsp" style=""></span>rpm&#59; LE 8300&#44; LSI Letica&#44; Panlab Scientific Instruments&#59; Barcelona&#44; Spain&#41;&#59; each session lasted 5 minutes&#46; Stereotactic surgery was performed after training was complete&#46; Four days later&#44; rats were placed on an accelerating rotarod &#40;speed 4 to 20<span class="elsevierStyleHsp" style=""></span>rpm&#41;&#44; completing 5 sessions with 3-minute resting periods between sessions&#46; We evaluated latency to fall&#44; that is&#44; the time it took for the rat to fall from the rod&#46; This variable is used to identify any alterations in motor coordination and balance&#46;<a class="elsevierStyleCrossRef" href="#bib0375"><span class="elsevierStyleSup">29</span></a></p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0115">Verification of the site of cannula implantation and microinjection</span><p id="par0075" class="elsevierStylePara elsevierViewall">After the completion of behavioural tests&#44; vaginal smears were obtained and animals euthanised with pentobarbital overdose &#40;PISA-Agropecuaria&#59; Guadalajara&#44; Mexico&#41;&#46; The cannula was used to mark the injection site with Evans blue &#40;Sigma&#8211;Aldrich Co&#46;&#59; St&#46; Louis&#44; MO&#44; USA&#41;&#46; Rats&#8217; brains were perfusion fixed&#44; extracted&#44; and sliced&#46; The site of cannula implantation was checked with a light microscope&#59; Paxinos and Watson&#39;s<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">1</span></a> rat brain atlas was used for reference&#46; The statistical analysis included only data from those rats in which cannulas were found to have been implanted correctly in the hippocampal CA1 region&#46;</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0120">Statistical analysis</span><p id="par0080" class="elsevierStylePara elsevierViewall">Data were analysed using 2-way ANOVA for independent samples&#59; factors were surgical condition &#40;intact or subjected to stereotactic surgery&#41; and phase of oestrus cycle &#40;pro-oestrus&#47;oestrus and metoestrus&#47;dioestrus&#41;&#46; Given <span class="elsevierStyleItalic">P</span>-values &#8804;&#46;05&#44; we applied the post hoc Student&#8211;Newman&#8211;Keuls test&#46; Results were expressed as means<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>SD&#46;</p></span></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0125">Results</span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0130">Phase of the oestrus cycle</span><p id="par0085" class="elsevierStylePara elsevierViewall">According to the analysis of vaginal smears&#44; 7 rats were in the pro-oestrus&#47;oestrus phase and 7 in the metoestrus&#47;dioestrus phase in each of the experimental groups&#46;</p></span><span id="sec0075" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0135">Site of cannula implantation</span><p id="par0090" class="elsevierStylePara elsevierViewall">Of all rats included in the study&#44; 2 were excluded from statistical analysis &#40;one rat in the pro-oestrus&#47;oestrus phase in experiment 1 and another one in the metoestrus&#47;dioestrus phase in experiment 2&#41;&#44; due to the presence of oedema in the area surrounding the implantation site and extending from the dorsal hippocampus to the cerebral cortex&#46; In the remaining rats&#44; the histological study confirmed correct cannula implantation into the dorsal hippocampus &#40;CA1&#41; between coordinates AP<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;3&#46;3 and AP<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;4&#46;6<span class="elsevierStyleHsp" style=""></span>mm from bregma &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46;</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span><span id="sec0080" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0140">Open-field test</span><span id="sec0085" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0145">Crossed squares</span><p id="par0095" class="elsevierStylePara elsevierViewall">No significant difference in the number of crossed squares was observed between the intact and surgery groups &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1&#44; 23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#46;38&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#46;25&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>a&#41;&#46; We did&#44; however&#44; find statistically significant differences between rats in the pro-oestrus&#47;oestrus and in the metoestrus&#47;dioestrus phases &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1&#44; 23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>6&#46;58&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;02&#41;&#46; According to the post hoc test&#44; rats in the metoestrus&#47;dioestrus phase crossed a higher number of squares than those in the pro-oestrus&#47;oestrus phase &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>b&#41;&#46; Factor interaction revealed no significant differences &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1&#44; 23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#46;42&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#46;25&#41; &#40;intact rats in pro-oestrus&#47;oestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 33&#46;28<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;19&#59; sham-operated rats in pro-oestrus&#47;oestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>6&#93;&#58; 33&#46;34<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>3&#46;07&#59; intact rats in metoestrus&#47;dioestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 43&#46;71<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;23&#59; sham-operated rats in metoestrus&#47;dioestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 37&#46;14<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>3&#46;62&#41;&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia></span><span id="sec0090" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0150">Grooming</span><p id="par0100" class="elsevierStylePara elsevierViewall">No significant differences in grooming time were observed between intact and sham-operated rats &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1</span>&#44;<span class="elsevierStyleHsp" style=""></span><span class="elsevierStyleInf">23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;63&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#46;43&#59; intact&#58; 40&#46;06<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;47<span class="elsevierStyleHsp" style=""></span>s vs surgery&#58; 41&#46;51<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;23<span class="elsevierStyleHsp" style=""></span>s&#41; or related to phase of the oestrus cycle &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1&#44; 23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>2&#46;89&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#46;10&#59; pro-oestrus&#47;oestrus&#58; 39&#46;23<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;37<span class="elsevierStyleHsp" style=""></span>s vs metoestrus&#47;dioestrus&#58; 42&#46;34<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;24<span class="elsevierStyleHsp" style=""></span>s&#41;&#46; Likewise&#44; interaction between factors revealed no significant differences &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1&#44; 23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#46;42&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#46;25&#41; &#40;intact rats in pro-oestrus&#47;oestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 37&#46;17<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;09<span class="elsevierStyleHsp" style=""></span>s&#59; sham-operated rats in pro-oestrus&#47;oestrus phase &#91;n<span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>6&#93;&#58; 41&#46;29<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;35<span class="elsevierStyleHsp" style=""></span>s&#59; intact rats in metoestrus&#47;dioestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 42&#46;94<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;51<span class="elsevierStyleHsp" style=""></span>s&#59; sham-operated rats in metoestrus&#47;dioestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 42&#46;74<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;06<span class="elsevierStyleHsp" style=""></span>s&#41;&#46;</p></span><span id="sec0095" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0155">Vertical behaviour</span><p id="par0105" class="elsevierStylePara elsevierViewall">No significant differences in vertical time were observed between intact and sham-operated rats &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1&#44; 23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>1&#46;43&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#46;24&#59; intact&#58; 65&#46;66<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;79<span class="elsevierStyleHsp" style=""></span>s vs surgery&#58; 68&#46;47<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;49<span class="elsevierStyleHsp" style=""></span>s&#41; or in terms of phase of the oestrus cycle &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1&#44; 23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>2&#46;18&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#46;15&#59; pro-oestrus&#47;oestrus&#58; 65&#46;33<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;07<span class="elsevierStyleHsp" style=""></span>s vs metoestrus&#47;dioestrus&#58; 68&#46;79<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;14<span class="elsevierStyleHsp" style=""></span>s&#41;&#46; Factor interaction revealed no significant differences &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1&#44; 23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;14&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#46;70&#41; &#40;intact rats in pro-oestrus&#47;oestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 63&#46;47<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>3&#46;03<span class="elsevierStyleHsp" style=""></span>s&#59; sham-operated rats in pro-oestrus&#47;oestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>6&#93;&#58; 67&#46;17<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;83<span class="elsevierStyleHsp" style=""></span>s&#59; intact rats in metoestrus&#47;dioestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 67&#46;84<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;79<span class="elsevierStyleHsp" style=""></span>s&#59; sham-operated rats in metoestrus&#47;dioestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 69&#46;75<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;43<span class="elsevierStyleHsp" style=""></span>s&#41;&#46;</p></span></span><span id="sec0100" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0160">Forced swim test</span><span id="sec0105" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0165">Lateral swimming time and number of spins</span><p id="par0110" class="elsevierStylePara elsevierViewall">All animals&#44; whether intact or sham-operated&#44; showed a normal swimming pattern in the forced swim test&#59; none displayed lateral swimming or spinning behaviour&#46;</p></span><span id="sec0110" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0170">Latency to first immobility episode</span><p id="par0115" class="elsevierStylePara elsevierViewall">We observed no significant differences in latency to the first episode of immobility between intact and sham-operated rats &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1&#44; 23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;04&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#46;83&#59; intact&#58; 26&#46;84<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;25<span class="elsevierStyleHsp" style=""></span>s vs surgery&#58; 27&#46;53<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;42<span class="elsevierStyleHsp" style=""></span>s&#41; or in terms of phase of the oestrus cycle &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1&#44; 23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>2&#46;07&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#46;16&#59; pro-oestrus&#47;oestrus&#58; 29&#46;54<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>1&#46;84<span class="elsevierStyleHsp" style=""></span>s vs metoestrus&#47;dioestrus&#58; 24&#46;84<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;52<span class="elsevierStyleHsp" style=""></span>s&#41;&#46; Factor interaction revealed no significant differences &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1&#44; 23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;39&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#46;53&#41; &#40;intact rats in pro-oestrus&#47;oestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 30&#46;22<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;68<span class="elsevierStyleHsp" style=""></span>s&#59; sham-operated rats in pro-oestrus&#47;oestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>6&#93;&#58; 28&#46;86<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;73<span class="elsevierStyleHsp" style=""></span>s&#59; intact rats in metoestrus&#47;dioestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 23&#46;47<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>3&#46;32<span class="elsevierStyleHsp" style=""></span>s&#59; sham-operated rats in metoestrus&#47;dioestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 26&#46;21<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>3&#46;96<span class="elsevierStyleHsp" style=""></span>s&#41;&#46;</p></span><span id="sec0115" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0175">Total immobility time</span><p id="par0120" class="elsevierStylePara elsevierViewall">No significant difference in total immobility time was observed between the intact and sham-operated groups &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1&#44; 23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>21&#46;06&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#46;62&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>a&#41;&#46; However&#44; there were statistically significant differences between rats in the pro-oestrus&#47;oestrus phase and the metoestrus&#47;dioestrus phase &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1&#44; 23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>90&#46;95&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;001&#41;&#46; According to the post hoc test&#44; rats in the pro-oestrus&#47;oestrus phase were immobile for less time than those in the metoestrus&#47;dioestrus phase &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>b&#41;&#46; Nevertheless&#44; factor interaction revealed no significant differences &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1&#44; 23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>77&#46;21&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#46;35&#41; &#40;intact rats in pro-oestrus&#47;oestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 44&#46;00<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>6&#46;61<span class="elsevierStyleHsp" style=""></span>s&#59; sham-operated rats in pro-oestrus&#47;oestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>6&#93;&#58; 42&#46;38<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>7&#46;75<span class="elsevierStyleHsp" style=""></span>s&#59; intact rats in metoestrus&#47;dioestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 74&#46;91<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>9&#46;07<span class="elsevierStyleHsp" style=""></span>s&#59; sham-operated rats in metoestrus&#47;dioestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 80&#46;07<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>10&#46;68<span class="elsevierStyleHsp" style=""></span>s&#41;&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia></span></span><span id="sec0120" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0180">Rotarod test</span><span id="sec0125" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0185">Latency to fall</span><p id="par0125" class="elsevierStylePara elsevierViewall">We observed no significant difference in latency to fall between the intact and sham-operated groups &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1&#44; 23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;03&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#46;85&#59; intact&#58; 151&#46;47<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>5&#46;36<span class="elsevierStyleHsp" style=""></span>s vs surgery&#58; 149&#46;92<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>6&#46;64<span class="elsevierStyleHsp" style=""></span>s&#41; or in terms of the phase of the oestrus cycle &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1&#44; 23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>3&#46;40&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#46;07&#59; pro-oestrus&#47;oestrus&#58; 142&#46;10<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2&#46;94<span class="elsevierStyleHsp" style=""></span>s vs metoestrus&#47;dioestrus&#58; 158&#46;29<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>7&#46;11<span class="elsevierStyleHsp" style=""></span>s&#41;&#46; Factor interaction revealed no significant differences &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleInf">&#91;1&#44; 23&#93;</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>0&#46;14&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#46;70&#41; &#40;intact rats in pro-oestrus&#47;oestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 142&#46;32<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>3&#46;78<span class="elsevierStyleHsp" style=""></span>s&#59; sham-operated rats in pro-oestrus&#47;oestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 143&#46;10<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>4&#46;96<span class="elsevierStyleHsp" style=""></span>s&#59; intact rats in metoestrus&#47;dioestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>7&#93;&#58; 160&#46;62<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>9&#46;08<span class="elsevierStyleHsp" style=""></span>s&#59; sham-operated rats in metoestrus&#47;dioestrus phase &#91;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>6&#93;&#58; 155&#46;29<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>11&#46;61<span class="elsevierStyleHsp" style=""></span>s&#41;&#46;</p></span></span></span><span id="sec0130" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0190">Discussion</span><p id="par0130" class="elsevierStylePara elsevierViewall">In our study&#44; stereotactic surgery for cannula implantation plus vehicle microinjection into the hippocampal CA1 region had no negative impact on activity and motor coordination&#46; All Wistar rats displayed the behavioural patterns typical of their oestrus cycle phase regardless of whether they had undergone stereotactic surgery&#46;</p><p id="par0135" class="elsevierStylePara elsevierViewall">The locomotor activity test is frequently used to quantify variables of displacement&#44; exploration&#44; and emotional status under experimental circumstances&#46;<a class="elsevierStyleCrossRefs" href="#bib0380"><span class="elsevierStyleSup">30&#44;31</span></a> In our study&#44; the locomotor activity test was used to confirm that the experimental manipulation &#40;stereotactic surgery for cannula implantation through the motor cortex plus vehicle microinjection into the dorsal hippocampus&#41; caused no motor hyper- or hypoactivity &#40;larger or smaller numbers of crossed squares&#41;&#44; changes in exploration behaviour &#40;vertical time&#41;&#44; or changes in motivation &#40;grooming time&#41;&#46; Our results support the hypothesis that surgical manipulation and microinjection do not cause neurological damage&#46; In line with this idea&#44; neurotoxic lesions to the dorsal hippocampus have been reported to cause motor hyperactivity&#46;<a class="elsevierStyleCrossRefs" href="#bib0285"><span class="elsevierStyleSup">11&#44;18</span></a> Similarly&#44; large quantities of cassava or cycad seeds have been observed to cause neurological alterations in humans&#46;<a class="elsevierStyleCrossRefs" href="#bib0255"><span class="elsevierStyleSup">5&#44;20&#44;21&#44;32</span></a> Our findings suggest that stereotactic surgery&#44; cannula implantation&#44; and microinjection in rats do not cause brain damage with potential to impair locomotor activity&#46; Changes in motor activity were found to be associated with the phase of the oestrus cycle&#44; but not with surgical manipulation&#46; Rats in the metoestrus&#47;dioestrus phase crossed a higher number of squares than rats in the pro-oestrus&#47;oestrus phase&#46; This increase in motor activity may be associated with higher levels of anxiety during the metoestrus&#47;dioestrus phase&#44; which is characterised by low concentrations of ovarian hormones&#46;<a class="elsevierStyleCrossRefs" href="#bib0355"><span class="elsevierStyleSup">25&#44;33</span></a></p><p id="par0140" class="elsevierStylePara elsevierViewall">Grooming is regarded as a marker of emotional and motivational status in rats&#46; Grooming time increases in rats experiencing mild stress<a class="elsevierStyleCrossRefs" href="#bib0400"><span class="elsevierStyleSup">34&#44;35</span></a> and decreases under severe stress<a class="elsevierStyleCrossRefs" href="#bib0410"><span class="elsevierStyleSup">36&#44;37</span></a> compared to intact rats&#46; Our study found no significant differences in grooming time between intact and sham-operated rats&#44; which suggests that stereotactic surgery and cannula implantation into the dorsal hippocampus have no impact on emotionality and motivation in rats&#46; Likewise&#44; our study revealed no association between vertical time and surgery or the phase of the oestrus cycle&#46; Vertical behaviour is considered to be an indicator of exploration&#44;<a class="elsevierStyleCrossRefs" href="#bib0420"><span class="elsevierStyleSup">38&#44;39</span></a> which requires a high level of motor coordination&#46; Vertical behaviour increases in rats with neuronal damage to the dorsal hippocampus&#44; which is probably associated with hyperactivity and poor motor coordination&#46;<a class="elsevierStyleCrossRef" href="#bib0320"><span class="elsevierStyleSup">18</span></a> Rats that underwent surgery displayed no behavioural changes&#44; suggesting that the surgical procedures described in this study cause no brain damage&#46;</p><p id="par0145" class="elsevierStylePara elsevierViewall">Rats with vestibular lesions<a class="elsevierStyleCrossRef" href="#bib0430"><span class="elsevierStyleSup">40</span></a> or neurological impairment associated with the consumption of foods containing neurotoxic compounds<a class="elsevierStyleCrossRefs" href="#bib0320"><span class="elsevierStyleSup">18&#44;19</span></a> display lateral swimming and spinning behaviour due to poor motor coordination&#46; In our study&#44; however&#44; none of the rats &#40;whether intact or sham-operated&#41; displayed an abnormal swimming pattern&#44; which rules out the possibility of surgery-related neurological damage&#46; Latency to first immobility period and total immobility time in the forced swim test were similar in both groups &#40;intact and sham-operated&#41;&#46; Differences in total immobility time were linked only to the phase of the oestrus cycle&#46; Rats in the metoestrus&#47;dioestrus phase were immobile for a longer total time than rats in the pro-oestrus&#47;oestrus phase&#46; Our findings are consistent with results reported in the literature&#58; rats in the metoestrus&#47;dioestrus phase are more vulnerable to stress and are immobile for a longer time during the forced swim test&#44; whereas rats in the pro-oestrus&#47;oestrus phase&#44; with high concentrations of ovarian hormones&#44; are immobile for a shorter time&#44; as occurs after administration of such hormones as progesterone and allopregnanolone&#46;<a class="elsevierStyleCrossRefs" href="#bib0435"><span class="elsevierStyleSup">41&#44;42</span></a></p><p id="par0150" class="elsevierStylePara elsevierViewall">The rotarod test assesses motor coordination and balance&#46;<a class="elsevierStyleCrossRef" href="#bib0445"><span class="elsevierStyleSup">43</span></a> Intact &#40;healthy&#41; animals will be able to remain on the rotating rod for longer periods due to preserved limb coordination and balance&#46;<a class="elsevierStyleCrossRef" href="#bib0450"><span class="elsevierStyleSup">44</span></a> In contrast&#44; animals with neurological alterations or receiving neurotoxic compounds or sedatives usually display shorter latencies to fall&#46;<a class="elsevierStyleCrossRefs" href="#bib0455"><span class="elsevierStyleSup">45&#44;46</span></a> In our study&#44; rats that underwent stereotactic surgery for cannula implantation into the dorsal hippocampus displayed no significant difference in latency to fall compared to intact rats&#46; Likewise&#44; no differences were found between rats in the pro-oestrus&#47;oestrus phase and those in the metoestrus&#47;dioestrus phase&#46; This suggests that experimental manipulations caused no neurological alterations potentially affecting motor coordination and activity&#46;</p><p id="par0155" class="elsevierStylePara elsevierViewall">Our results show that stereotactic surgery and cannula implantation into the dorsal hippocampus cause no alterations in locomotor activity and coordination in rats&#44; ruling out the possibility that this type of manipulation may cause neurological impairment interfering with the interpretation of results from experimental studies&#46;</p></span><span id="sec0135" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0195">Funding</span><p id="par0160" class="elsevierStylePara elsevierViewall">This study was funded by grants I010&#47;458&#47;2013&#44; C-703&#47;2013 and I010&#47;152&#47;2014&#44; C-133&#47;2014&#46;</p></span><span id="sec0140" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0200">Conflicts of interest</span><p id="par0165" class="elsevierStylePara elsevierViewall">The authors have no conflicts of interest to declare&#46;</p></span></span>"
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              "titulo" => "Introducci&#243;n"
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            1 => array:2 [
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              "titulo" => "Vaginal smears"
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              "identificador" => "sec0025"
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          "titulo" => "Results"
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            0 => array:2 [
              "identificador" => "sec0070"
              "titulo" => "Phase of the oestrus cycle"
            ]
            1 => array:2 [
              "identificador" => "sec0075"
              "titulo" => "Site of cannula implantation"
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            2 => array:3 [
              "identificador" => "sec0080"
              "titulo" => "Open-field test"
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                0 => array:2 [
                  "identificador" => "sec0085"
                  "titulo" => "Crossed squares"
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                1 => array:2 [
                  "identificador" => "sec0090"
                  "titulo" => "Grooming"
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                2 => array:2 [
                  "identificador" => "sec0095"
                  "titulo" => "Vertical behaviour"
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              "titulo" => "Forced swim test"
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                0 => array:2 [
                  "identificador" => "sec0105"
                  "titulo" => "Lateral swimming time and number of spins"
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                1 => array:2 [
                  "identificador" => "sec0110"
                  "titulo" => "Latency to first immobility episode"
                ]
                2 => array:2 [
                  "identificador" => "sec0115"
                  "titulo" => "Total immobility time"
                ]
              ]
            ]
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              "identificador" => "sec0120"
              "titulo" => "Rotarod test"
              "secciones" => array:1 [
                0 => array:2 [
                  "identificador" => "sec0125"
                  "titulo" => "Latency to fall"
                ]
              ]
            ]
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          "identificador" => "sec0130"
          "titulo" => "Discussion"
        ]
        8 => array:2 [
          "identificador" => "sec0135"
          "titulo" => "Funding"
        ]
        9 => array:2 [
          "identificador" => "sec0140"
          "titulo" => "Conflicts of interest"
        ]
        10 => array:2 [
          "identificador" => "xack316724"
          "titulo" => "Acknowledgements"
        ]
        11 => array:1 [
          "titulo" => "References"
        ]
      ]
    ]
    "pdfFichero" => "main.pdf"
    "tienePdf" => true
    "fechaRecibido" => "2015-02-07"
    "fechaAceptado" => "2016-03-08"
    "PalabrasClave" => array:2 [
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        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Keywords"
          "identificador" => "xpalclavsec911448"
          "palabras" => array:6 [
            0 => "Stereotactic surgery"
            1 => "Cannula placement"
            2 => "Hippocampus"
            3 => "Motor coordination"
            4 => "Locomotor activity"
            5 => "Microinjection"
          ]
        ]
      ]
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        0 => array:4 [
          "clase" => "keyword"
          "titulo" => "Palabras clave"
          "identificador" => "xpalclavsec911449"
          "palabras" => array:6 [
            0 => "Cirug&#237;a estereot&#225;xica"
            1 => "Implante de c&#225;nula"
            2 => "Hipocampo"
            3 => "Coordinaci&#243;n motriz"
            4 => "Actividad locomotora"
            5 => "Microinyecci&#243;n"
          ]
        ]
      ]
    ]
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      "en" => array:3 [
        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Introduction</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Stereotactic surgery is used to place electrodes or cannulas in the brain in order to study the function of several brain structures in preclinical research&#46; The hippocampus has been extensively studied with this methodology due to its involvement in a wide range of neurological&#44; cognitive&#44; emotional&#44; and affective disorders&#46; However&#44; the effects of stereotactic surgery on coordination and motor activity should be evaluated in order to determine whether this surgical procedure causes any neurological alterations that may bias the results of studies incorporating this technique&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Methods</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">We evaluated the effects of stereotactic surgery and implantation of a cannula into the hippocampus of female Wistar rats on the motor activity&#44; forced swim&#44; and rotarod tests&#46; The stage of the oestrous cycle was included in the statistical analysis&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Stereotactic surgery had no impact on any of the motor activity variables assessed in the open field &#40;squares crossed&#44; time spent in grooming&#44; and rearing&#41;&#44; forced swim &#40;turning behaviour&#44; lateral swimming&#44; latency to first immobility&#44; and time spent immobile&#41;&#44; and rotarod &#40;latency to fall&#41; tests&#44; compared with intact rats&#46; Regardless of surgical manipulation&#44; rats in the metestrus and diestrus stages crossed a greater number of squares and displayed longer immobility times than those in the proestrus and estrus stages&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusion</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">Stereotactic surgery for cannula placement in the dorsal hippocampus does not affect coordination and motor activity in rats&#46; We can therefore conclude that this procedure has no neurological complications that may interfere in the interpretation of results of studies applying this technique&#46;</p></span>"
        "secciones" => array:4 [
          0 => array:2 [
            "identificador" => "abst0005"
            "titulo" => "Introduction"
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          1 => array:2 [
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            "titulo" => "Results"
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      "es" => array:3 [
        "titulo" => "Resumen"
        "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Introducci&#243;n</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">La cirug&#237;a estereot&#225;xica permite el implante de electrodos o c&#225;nulas para estudiar el funcionamiento de diversas estructuras cerebrales a nivel precl&#237;nico&#46; El hipocampo ha sido ampliamente estudiado con esta metodolog&#237;a&#44; debido a su participaci&#243;n en des&#243;rdenes neurol&#243;gicos&#44; cognitivos&#44; emocionales y afectivos&#46; Sin embargo&#44; el efecto <span class="elsevierStyleItalic">per se</span> de esta metodolog&#237;a sobre la coordinaci&#243;n y la actividad motora&#44; para identificar o descartar alteraciones neurol&#243;gicas que pudieran influir en los resultados de protocolos que la utilizan&#44; requiere ser explorado&#46;</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">M&#233;todos</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Se evalu&#243; el efecto de la cirug&#237;a estereot&#225;xica y el implante de c&#225;nula en el hipocampo de ratas hembra Wistar en las pruebas de actividad locomotora&#44; nado y Rota-rod&#46; El an&#225;lisis estad&#237;stico consider&#243; la fase del ciclo estral de las ratas&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Ninguna de las variables evaluadas en las pruebas de actividad locomotora &#40;cuadros cruzados&#44; tiempo de acicalamiento y conducta vertical&#41;&#44; nado &#40;giros&#44; nado lateral&#44; latencia a la primera inmovilidad y tiempo de inmovilidad&#41; o Rota-rod &#40;latencia a la ca&#237;da&#41;&#44; fueron modificadas por la manipulaci&#243;n quir&#250;rgica&#44; en relaci&#243;n con ratas intactas&#46; Independientemente de la manipulaci&#243;n quir&#250;rgica&#44; las ratas en metaestro-diestro cruzaron m&#225;s cuadros y tuvieron mayor tiempo de inmovilidad&#44; que las ratas en proestro-estro&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusi&#243;n</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">La cirug&#237;a estereot&#225;xica y el implante de c&#225;nula en el hipocampo dorsal carecen de efectos sobre la coordinaci&#243;n y la actividad locomotora de la rata&#44; por lo que se descarta alg&#250;n da&#241;o neurol&#243;gico que pudiera interferir en la interpretaci&#243;n de resultados en protocolos que incluyen esta manipulaci&#243;n experimental&#46;</p></span>"
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      0 => array:2 [
        "etiqueta" => "&#9734;"
        "nota" => "<p class="elsevierStyleNotepara" id="npar0005">Please cite this article as&#58; Hern&#225;ndez-L&#243;pez F&#44; Rodr&#237;guez-Landa JF&#44; Puga-Olgu&#237;n A&#44; Germ&#225;n-Ponciano LJ&#44; Rivadeneyra-Dom&#237;nguez E&#44; Bernal-Morales B&#46; An&#225;lisis de la actividad y coordinaci&#243;n motora en ratas con cirug&#237;a estereot&#225;xica e implante de c&#225;nula en el hipocampo dorsal&#46; Neurolog&#237;a&#46; 2017&#59;32&#58;579&#8211;586&#46;</p>"
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          "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">&#40;a&#41; Image of the rat brain showing the site of cannula implantation at the anteroposterior level &#40;dashed line&#41; and a coronal section of the brain showing the site of cannula injection &#40;white arrow&#41;&#46; &#40;b&#41; Diagram of brain coronal sections&#44; displaying the site of cannula implantation into hippocampal CA1 &#40;black circles&#41;&#46; Based on Paxinos and Watson&#39;s rat brain atlas &#40;1998 edition&#41;&#46;</p>"
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          "en" => "<p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">Number of crossed squares in the locomotor activity test&#46; &#40;a&#41; Surgery caused no significant changes in the number of crossed squares compared to intact rats&#46; &#40;b&#41; Rats in the metoestrus&#47;dioestrus &#40;M&#47;D&#41; phase crossed a significantly higher number of squares than rats in the pro-oestrus&#47;oestrus phase &#40;P&#47;O&#41;&#46;</p> <p id="spar0055" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleSup">&#42;</span><span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;05 vs P&#47;O&#46;</p>"
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          "en" => "<p id="spar0060" class="elsevierStyleSimplePara elsevierViewall">Total immobility time in the forced swim test&#46; &#40;a&#41; Surgery caused no significant changes in this variable compared to intact rats&#46; &#40;b&#41; Rats in the metoestrus&#47;dioestrus &#40;M&#47;D&#41; phase remained immobile for a longer time than rats in the pro-oestrus&#47;oestrus phase &#40;P&#47;O&#41;&#46;</p> <p id="spar0065" class="elsevierStyleSimplePara elsevierViewall"><span class="elsevierStyleSup">&#42;</span><span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;05 vs P&#47;O&#46;</p>"
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Article information

ISSN: 21735808
Original language: English

DOI:10.1016/j.nrleng.2016.03.002

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Year/Month	Html	Pdf	Total

2024 November	8	3	11
2024 October	29	3	32
2024 September	42	9	51
2024 August	46	4	50
2024 July	55	6	61
2024 June	66	10	76
2024 May	75	1	76
2024 April	93	11	104
2024 March	64	12	76
2024 February	87	16	103
2024 January	97	10	107
2023 December	99	11	110
2023 November	93	12	105
2023 October	100	13	113
2023 September	50	3	53
2023 August	56	8	64
2023 July	72	5	77
2023 June	69	11	80
2023 May	137	12	149
2023 April	61	6	67
2023 March	98	7	105
2023 February	89	12	101
2023 January	80	11	91
2022 December	45	7	52
2022 November	64	14	78
2022 October	64	17	81
2022 September	55	11	66
2022 August	67	17	84
2022 July	45	8	53
2022 June	35	17	52
2022 May	53	12	65
2022 April	61	12	73
2022 March	57	7	64
2022 February	66	7	73
2022 January	118	13	131
2021 December	62	14	76
2021 November	66	14	80
2021 October	57	15	72
2021 September	58	9	67
2021 August	55	4	59
2021 July	48	9	57
2021 June	43	10	53
2021 May	76	6	82
2021 April	97	10	107
2021 March	39	6	45
2021 February	30	6	36
2021 January	44	13	57
2020 December	47	9	56
2020 November	51	7	58
2020 October	33	3	36
2020 September	40	11	51
2020 August	47	11	58
2020 July	35	10	45
2020 June	43	12	55
2020 May	51	15	66
2020 April	46	3	49
2020 March	45	7	52
2020 February	39	8	47
2020 January	58	5	63
2019 December	62	12	74
2019 November	40	7	47
2019 October	40	8	48
2019 September	44	14	58
2019 August	36	3	39
2019 July	52	11	63
2019 June	55	23	78
2019 May	93	31	124
2019 April	83	8	91
2019 March	27	18	45
2019 February	32	5	37
2019 January	30	4	34
2018 December	16	4	20
2018 November	26	3	29
2018 October	51	5	56
2018 September	62	6	68
2018 August	48	7	55
2018 July	29	3	32
2018 June	33	6	39
2018 May	39	14	53
2018 April	32	10	42
2018 March	22	5	27
2018 February	33	4	37
2018 January	33	0	33
2017 December	24	2	26
2017 November	21	5	26
2017 October	0	1	1

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