Original article
Spinogenesis in spinal cord motor neurons following pharmacological lesions to the rat motor cortex
Espinogénesis en motoneuronas de la médula espinal tras la lesión farmacológica de la corteza motora de ratas
N.I. Martínez-Torresa,b, D. González-Tapiaa,c,d, M. Flores-Sotoa, N. Vázquez-Hernándeza, H. Salgado-Ceballose,f, I. González-Burgosa,
Corresponding author
a División de Neurociencias, Centro de Investigación Biomédica de Occidente, IMSS, Guadalajara, Jalisco, Mexico
b Centro Universitario del Norte, Universidad de Guadalajara, Colotlán, Jalisco, Mexico
c Instituto de Ciencias de la Rehabilitación Integral, Guadalajara, Jalisco, Mexico
d Universidad Politécnica de la Zona Metropolitana de Guadalajara, Tlajomulco de Zúñiga, Jalisco, Mexico
e Unidad de Investigación Médica en Enfermedades Neurológicas, Hospital de Especialidades, Centro Médico Nacional S-XXI, IMSS, Ciudad de México, Mexico
f Proyecto Camina, A.C., Ciudad de México, Mexico
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"apellidos" => "González-Burgos" "email" => array:1 [ 0 => "igonbur@hotmail.com" ] "referencia" => array:2 [ 0 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">a</span>" "identificador" => "aff0005" ] 1 => array:2 [ "etiqueta" => "<span class="elsevierStyleSup">*</span>" "identificador" => "cor0005" ] ] ] ] "afiliaciones" => array:6 [ 0 => array:3 [ "entidad" => "División de Neurociencias, Centro de Investigación Biomédica de Occidente, IMSS, Guadalajara, Jalisco, Mexico" "etiqueta" => "a" "identificador" => "aff0005" ] 1 => array:3 [ "entidad" => "Centro Universitario del Norte, Universidad de Guadalajara, Colotlán, Jalisco, Mexico" "etiqueta" => "b" "identificador" => "aff0010" ] 2 => array:3 [ "entidad" => "Instituto de Ciencias de la Rehabilitación Integral, Guadalajara, Jalisco, Mexico" "etiqueta" => "c" "identificador" => "aff0015" ] 3 => array:3 [ "entidad" => "Universidad Politécnica de la Zona Metropolitana de Guadalajara, Tlajomulco de Zúñiga, Jalisco, Mexico" "etiqueta" => "d" "identificador" => "aff0020" ] 4 => array:3 [ "entidad" => "Unidad de Investigación Médica en Enfermedades Neurológicas, Hospital de Especialidades, Centro Médico Nacional S-XXI, IMSS, Ciudad de México, Mexico" "etiqueta" => "e" "identificador" => "aff0025" ] 5 => array:3 [ "entidad" => "Proyecto Camina, A.C., Ciudad de México, Mexico" "etiqueta" => "f" "identificador" => "aff0030" ] ] "correspondencia" => array:1 [ 0 => array:3 [ "identificador" => "cor0005" "etiqueta" => "⁎" "correspondencia" => "Corresponding author." ] ] ] ] "titulosAlternativos" => array:1 [ "es" => array:1 [ "titulo" => "Espinogénesis en motoneuronas de la médula espinal tras la lesión farmacológica de la corteza motora de ratas" ] ] "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" => 2559 "Ancho" => 2333 "Tamanyo" => 1217384 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Above: panoramic microphotograph of the dorsal and ventral horns in a thoracic section from a rat spinal cord; the tissue was stained using a modified Golgi method. Arrows indicate motor neurons in the ventral horn containing the primary dendrites where dendritic spines were counted. Scale bar: 100<span class="elsevierStyleHsp" style=""></span>μm. Below: representative photomicrographs showing a typical thin spine (t), mushroom spine (m), and stubby spine (s) (arrows), which were counted in our study. Scale bar: 2<span class="elsevierStyleHsp" style=""></span>μm.</p>" ] ] ] "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">The organisation of voluntary movement depends on the coordinated function of different brain areas.<a class="elsevierStyleCrossRefs" href="#bib0210"><span class="elsevierStyleSup">1,2</span></a> Pyramidal cells in the 5th layer of the primary motor cortex (M1) integrate information related to voluntary movement,<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">3</span></a> whose execution is associated with the direct connections between these cortical neurons and the spinal cord through the corticospinal pyramidal tract.<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">1</span></a></p><p id="par0010" class="elsevierStylePara elsevierViewall">Several movement alterations are associated with M1 lesions, including paralysis, paraesthesias,<a class="elsevierStyleCrossRefs" href="#bib0225"><span class="elsevierStyleSup">4,5</span></a> and hyperreflexia.<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">6</span></a> The neuropathologies underlying these alterations are the main cause of disability, and clinical evidence reveals that recovery is usually limited to partial functional recovery, both sensory and motor.<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">7</span></a></p><p id="par0015" class="elsevierStylePara elsevierViewall">The main histopathological damage associated with paralysis or paraesthesia is wallerian degeneration, which occurs after a cortical lesion. Wallerian degeneration is characterised by axonal degeneration after a lesion distal to the neuronal soma. In cortical lesions, this type of degeneration causes loss of communication between cortical neurons and spinal cord motor neurons.<a class="elsevierStyleCrossRefs" href="#bib0245"><span class="elsevierStyleSup">8,9</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">There is clinical<a class="elsevierStyleCrossRefs" href="#bib0255"><span class="elsevierStyleSup">10,11</span></a> and experimental<a class="elsevierStyleCrossRefs" href="#bib0240"><span class="elsevierStyleSup">7,12</span></a> evidence of partial functional recovery after lesions to the motor cortex. The eventual incipient recovery is reported to be partially responsible for such plastic processes as cortical reorganisation, axonal regrowth of viable afferent pathways to spinal cord motor neurons, and dendritic elongation or generation in spinal cord motor neurons.<a class="elsevierStyleCrossRefs" href="#bib0270"><span class="elsevierStyleSup">13–15</span></a></p><p id="par0025" class="elsevierStylePara elsevierViewall">Recent studies show epileptogenesis in spinal cord motor neurons, caused by an experimental spinal cord injury. However, there is no experimental evidence on plastic changes associated with synaptic activity mediated by dendritic spines in spinal cord motor neurons resulting from a degenerative lesion to the corticospinal pyramidal tract.</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Material and methods</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Animals</span><p id="par0030" class="elsevierStylePara elsevierViewall">We used 26 female Sprague-Dawley rats (200–250<span class="elsevierStyleHsp" style=""></span>g) kept under standard vivarium conditions (25<span class="elsevierStyleHsp" style=""></span>°C, 12-hour light/dark cycles) with ad libitum access to water and small rodent chow.</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Surgery</span><p id="par0035" class="elsevierStylePara elsevierViewall">Animals were assigned to one of 2 study groups. In a stereotactic procedure, the experimental group (<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>13) was administered a single dose of 5<span class="elsevierStyleHsp" style=""></span>nM of kainic acid diluted in 0.3<span class="elsevierStyleHsp" style=""></span>μL of physiological saline solution at 2 different points of the M1 bilaterally to induce a lesion. The coordinates used were: (1) anterior-posterior to Bregma<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>2.7; dorso-ventral<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>2.4, lateral<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>±3.0; and (2) antero-posterior to Bregma<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>−1.8, dorso-ventral<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>1.6, lateral<span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>±1.4.<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">17</span></a> A second group of rats were used as controls (<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>13). Using the same stereotactic coordinates as in the experimental group, we administered 0.3<span class="elsevierStyleHsp" style=""></span>μL of physiological saline solution. Prior to stereotactic surgery, animals were anaesthetised with intramuscular injections of 13<span class="elsevierStyleHsp" style=""></span>mg/kg of xylazine followed by 80<span class="elsevierStyleHsp" style=""></span>mg/kg of ketamine.</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Behavioural study</span><p id="par0040" class="elsevierStylePara elsevierViewall">All the animals underwent a behavioural assessment 15 days after lesion induction. For the assessment of changes in motor performance caused by the injury, we used the BBB<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">18</span></a> functional scale for assessing locomotor performance and a balance and motor coordination test on a rotarod.</p><p id="par0045" class="elsevierStylePara elsevierViewall">The BBB scale is scored from 0 to 21, where 0 represents complete absence of spontaneous movement and 21 indicates normal gait. The test was performed in a delimited circular area; movements of the hip, knee, and ankle were recorded, as well as the capacity to stand on the hind legs, plantar position, steps, tail position, and coordination. Rats were assessed during a single session for 4<span class="elsevierStyleHsp" style=""></span>minutes. Thirty minutes after finishing assessment with the BBB functional scale, animals were assessed on the rotarod. We used 2 habituation procedures: first, for 15<span class="elsevierStyleHsp" style=""></span>minutes prior to the experiment, they were kept in their cages in the space where the tests were to be conducted; secondly, each rat was placed on the stationary rotarod for 2 to 3<span class="elsevierStyleHsp" style=""></span>minutes. The assessment was conducted in a single session of 3 trials with 15-minute intervals between trials. At the beginning of the first trial, rats were placed in an individual lane of the rotarod; the rotarod was started at a constant speed of 4<span class="elsevierStyleHsp" style=""></span>rpm and we checked that rats were able to walk on the rotarod for approximately 5<span class="elsevierStyleHsp" style=""></span>seconds. In the test, the rotarod was started at a constant acceleration, increasing from 4 to 40<span class="elsevierStyleHsp" style=""></span>rpm over 5<span class="elsevierStyleHsp" style=""></span>minutes. We recorded both latency to fall and the rotation speed (rpm) at which the animal fell from the rotarod. After each trial, we cleaned the rotarod surfaces with 70% ethyl alcohol.</p></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Neuronal cytoarchitecture</span><p id="par0050" class="elsevierStylePara elsevierViewall">We randomly selected 6 animals from each group for the study of the neuronal cytoarchitecture. Animals were anaesthetised with intramuscular injection of 13<span class="elsevierStyleHsp" style=""></span>mg/kg of xylazine followed by 80<span class="elsevierStyleHsp" style=""></span>mg/kg of ketamine. They were immediately administered a transcardial perfusion of 200<span class="elsevierStyleHsp" style=""></span>mL of phosphate buffer solution (pH 7.4; 0.1<span class="elsevierStyleHsp" style=""></span>M), to which we added sodium heparin (1000<span class="elsevierStyleHsp" style=""></span>IU/L) for anticoagulation and procaine hydrochloride (1<span class="elsevierStyleHsp" style=""></span>g/L) for vasodilation.<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">19</span></a> Immediately thereafter, we administered transcardial perfusion of 200<span class="elsevierStyleHsp" style=""></span>mL of 4% formaldehyde in phosphate buffer solution (pH 7.4, 0.1<span class="elsevierStyleHsp" style=""></span>M). We obtained 3-cm sections from between the thoracic and the lumbar regions of the spinal cord and preserved these in fresh 4% formaldehyde in phosphate buffer solution for at least 24<span class="elsevierStyleHsp" style=""></span>hours. We dissected 4<span class="elsevierStyleHsp" style=""></span>mm-thick tissue blocks, which were processed using the fast Golgi method<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">20</span></a> for the neuronal cytoarchitecture study. Using 100<span class="elsevierStyleHsp" style=""></span>μm thick horizontal slices, we selected 6 neurons per animal and recorded the number of dendritic spines, their density, and the proportional density of thin, mushroom, and stubby spines<a class="elsevierStyleCrossRef" href="#bib0310"><span class="elsevierStyleSup">21</span></a> (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>).</p><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Western blot</span><p id="par0055" class="elsevierStylePara elsevierViewall">Six animals per group were euthanised by decapitation for protein quantification. We obtained 3-cm sections of thoracic and lumbar spinal cord to be processed for quantification of the proteins β III tubulin (56<span class="elsevierStyleHsp" style=""></span>kD), synaptophysin (47<span class="elsevierStyleHsp" style=""></span>kD), and spinophilin (117<span class="elsevierStyleHsp" style=""></span>kD), using the Western blot technique. For the analysis, we used digital images of the resulting membrane from a photo documentation system; the data obtained are reported in arbitrary units of intensity.</p></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Statistical analysis</span><p id="par0060" class="elsevierStylePara elsevierViewall">The <span class="elsevierStyleItalic">t</span> test for independent samples was used to analyse the results of behavioural, morphological, and molecular studies.</p></span></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Results</span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Basso, Beattie, Bresnahan functional scale</span><p id="par0065" class="elsevierStylePara elsevierViewall">We observed significant differences between the 2 groups analysed, with the experimental group scoring lower than the control group (<span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>4.924, <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>.0001) (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>).</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0115">Rotarod</span><p id="par0070" class="elsevierStylePara elsevierViewall">Latency to fall in the experimental group was lower than in the control group (<span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>4.883, <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>.0001) (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>). Experimental animals fell from the rotarod at a lower rotation speed than did control animals (<span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>4.747, <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>.0001) (<a class="elsevierStyleCrossRef" href="#fig0020">Fig. 4</a>).</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia><elsevierMultimedia ident="fig0020"></elsevierMultimedia></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0120">Dendritic spines</span><p id="par0075" class="elsevierStylePara elsevierViewall">The density of dendritic spines was higher in the experimental group than in the control group (<span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>−3.508, <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>.006) (<a class="elsevierStyleCrossRef" href="#fig0025">Fig. 5</a>). Specifically, we observed more thin (<span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>−2.624, <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>.02) and stubby spines (<span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>−4.447, <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>.001) in the experimental group than in the control group. We observed no significant differences between groups in the proportion of mushroom spines (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>).</p><elsevierMultimedia ident="fig0025"></elsevierMultimedia><elsevierMultimedia ident="tbl0005"></elsevierMultimedia></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0125">Western blot</span><p id="par0080" class="elsevierStylePara elsevierViewall">The experimental group showed higher levels of β III tubulin (<span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>−11.9, <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>.0001) (<a class="elsevierStyleCrossRef" href="#fig0030">Fig. 6</a>), synaptophysin (<span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>−3.451, <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>.006) (<a class="elsevierStyleCrossRef" href="#fig0035">Fig. 7</a>), and spinophilin (<span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>−8.370, <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>.0001) (<a class="elsevierStyleCrossRef" href="#fig0040">Fig. 8</a>).</p><elsevierMultimedia ident="fig0030"></elsevierMultimedia><elsevierMultimedia ident="fig0035"></elsevierMultimedia><elsevierMultimedia ident="fig0040"></elsevierMultimedia></span></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0130">Discussion</span><p id="par0085" class="elsevierStylePara elsevierViewall">Several demyelinating diseases of the corticospinal tract progress with neurological damage and motor impairment.<a class="elsevierStyleCrossRefs" href="#bib0225"><span class="elsevierStyleSup">4,5</span></a> Our study assessed motor function and the underlying plasticity of thoracic/lumbar spinal cord motor neurons after experimental M1 injury.</p><p id="par0090" class="elsevierStylePara elsevierViewall">The functional neurological assessment using the BBB scale and the rotarod revealed impaired motor performance. This was observed concomitantly with an increased numerical density of dendritic spines, specifically thin and stubby spines.</p><p id="par0095" class="elsevierStylePara elsevierViewall">The increased number of dendritic spines observed in the spinal cord motor neurons following M1 injury may be interpreted as a compensatory plastic response that, in the case of functional spines,<a class="elsevierStyleCrossRefs" href="#bib0315"><span class="elsevierStyleSup">22–24</span></a> would represent an increase in the associative capacity of afferent synaptic inputs<a class="elsevierStyleCrossRef" href="#bib0330"><span class="elsevierStyleSup">25</span></a> and eventually promote functional recovery.<a class="elsevierStyleCrossRef" href="#bib0335"><span class="elsevierStyleSup">26</span></a></p><p id="par0100" class="elsevierStylePara elsevierViewall">Various studies using different experimental models of motor injury,<a class="elsevierStyleCrossRefs" href="#bib0340"><span class="elsevierStyleSup">27–30</span></a> including spinal cord lesions,<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">16</span></a> have shown that not only is the numerical density of dendritic spines important as a plastic response to an altered synaptic microenvironment, but also that variations in the proportional density of the different types of spines also represent critical plastic events.</p><p id="par0105" class="elsevierStylePara elsevierViewall">Thin spines have classically been associated with the acquisition of new information<a class="elsevierStyleCrossRefs" href="#bib0360"><span class="elsevierStyleSup">31,32</span></a> due to their characteristic fast processing of afferent synaptic inputs.<a class="elsevierStyleCrossRefs" href="#bib0370"><span class="elsevierStyleSup">33,34</span></a> Although the synaptic information processed in the spinal cord is not related to learning, the underlying electrophysiological phenomena share common mechanisms.<a class="elsevierStyleCrossRef" href="#bib0345"><span class="elsevierStyleSup">28</span></a> In this study, such bioelectrical phenomena constitute a spontaneous plastic response to help acquire the decreased chemical information from those nervous fibres that: (a) remain viable after the lesion; (b) result from subsequent axonal sprouting; or (c) are the result of both events. In fact, previous studies report an increase in β III tubulin levels, as observed in our study, after an injury; this would reflect the sprouting of new axon terminals.<a class="elsevierStyleCrossRef" href="#bib0380"><span class="elsevierStyleSup">35</span></a> In any case, the increased density of thin spines may be interpreted as a spontaneous plastic response to experimentally induced Wallerian degeneration, tending to compensate for the reduced transmission of afferent inputs to the spinal cord motor neurons.</p><p id="par0110" class="elsevierStylePara elsevierViewall">As with thin spines, the number of stubby spines also increased after the experimental lesion. Stubby spines lack a neck, which confers them the functional characteristic of providing little resistance to calcium-mediated current<a class="elsevierStyleCrossRef" href="#bib0385"><span class="elsevierStyleSup">36</span></a>; according to circumstantial evidence,<a class="elsevierStyleCrossRefs" href="#bib0310"><span class="elsevierStyleSup">21,32,37,38</span></a> the functional activity of this type of spines would consist in regulating postsynaptic neuronal excitability. Thus, the proportional increase in stubby spines suggests, on the one hand, that the afferent excitatory activity to spinal motor neurons may have increased after the lesion to the corticospinal tract, and on the other hand, that there is a plastic response that tends to regulate the bioelectrical homeostasis of motor neurons. This proposal is supported by the greater expression of synaptophysin, a marker of the release of the neurotransmitter into the intersynaptic space,<a class="elsevierStyleCrossRef" href="#bib0400"><span class="elsevierStyleSup">39</span></a> in tissues from animals in the experimental group. Furthermore, increased synaptophysin levels would correlate with an increase in spinophilin expression, which would indicate the presence of a greater number of dendritic spines,<a class="elsevierStyleCrossRef" href="#bib0405"><span class="elsevierStyleSup">40</span></a> as we observed in our study.</p><p id="par0115" class="elsevierStylePara elsevierViewall">The study did not find changes in the proportional density of mushroom spines. Synaptic transmission mediated by this type of spines is slower than in any other type of spines,<a class="elsevierStyleCrossRef" href="#bib0360"><span class="elsevierStyleSup">31</span></a> since they are potentiated by afferent stimulation.<a class="elsevierStyleCrossRef" href="#bib0410"><span class="elsevierStyleSup">41</span></a> Based on the above, functional activity of this type of spines has been linked to long-term information storage.<a class="elsevierStyleCrossRef" href="#bib0360"><span class="elsevierStyleSup">31</span></a></p><p id="par0120" class="elsevierStylePara elsevierViewall">The fact that mushroom spines did not undergo any changes suggests that plastic processes in the dendritic spines of spinal motor neurons do not tend to consolidate the afferent synaptic inputs, which would maintain the latent capacity to make dynamic adjustments to synaptic information, represented by the predominance of thin spines. In that case, in a bioelectrical microenvironment regulated by the high density of stubby spines, this could enable more effective patterns of motor activity to be established in early rehabilitation treatment of patients with this type of motor neuron alterations.</p></span><span id="sec0075" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0135">Funding</span><p id="par0125" class="elsevierStylePara elsevierViewall">This study was financed by the Health Research Fund of the <span class="elsevierStyleGrantSponsor" id="gs1">Mexican Institute of Health</span>, with registry number <span class="elsevierStyleGrantNumber" refid="gs1">FIS/IMSS/PROT/G11-2/1028</span>.</p></span><span id="sec0080" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0140">Conflicts of interest</span><p id="par0130" class="elsevierStylePara elsevierViewall">The authors have no conflicts of interest to declare.</p></span></span>" "textoCompletoSecciones" => array:1 [ "secciones" => array:11 [ 0 => array:3 [ "identificador" => "xres1469038" "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" => "xpalclavsec1338100" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres1469039" "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" => "xpalclavsec1338099" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:3 [ "identificador" => "sec0010" "titulo" => "Material and methods" "secciones" => array:6 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Animals" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Surgery" ] 2 => array:2 [ "identificador" => "sec0025" "titulo" => "Behavioural study" ] 3 => array:2 [ "identificador" => "sec0030" "titulo" => "Neuronal cytoarchitecture" ] 4 => array:2 [ "identificador" => "sec0035" "titulo" => "Western blot" ] 5 => array:2 [ "identificador" => "sec0040" "titulo" => "Statistical analysis" ] ] ] 6 => array:3 [ "identificador" => "sec0045" "titulo" => "Results" "secciones" => array:4 [ 0 => array:2 [ "identificador" => "sec0050" "titulo" => "Basso, Beattie, Bresnahan functional scale" ] 1 => array:2 [ "identificador" => "sec0055" "titulo" => "Rotarod" ] 2 => array:2 [ "identificador" => "sec0060" "titulo" => "Dendritic spines" ] 3 => array:2 [ "identificador" => "sec0065" "titulo" => "Western blot" ] ] ] 7 => array:2 [ "identificador" => "sec0070" "titulo" => "Discussion" ] 8 => array:2 [ "identificador" => "sec0075" "titulo" => "Funding" ] 9 => array:2 [ "identificador" => "sec0080" "titulo" => "Conflicts of interest" ] 10 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2017-10-26" "fechaAceptado" => "2017-12-01" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1338100" "palabras" => array:6 [ 0 => "Demyelinating diseases" 1 => "Motor cortex" 2 => "Pyramidal tract" 3 => "Spinal cord" 4 => "Motor neurons" 5 => "Dendritic spines" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1338099" "palabras" => array:6 [ 0 => "Enfermedades desmielinizantes" 1 => "Corteza motora" 2 => "Vía piramidal" 3 => "Médula espinal" 4 => "Motoneuronas" 5 => "Espinas dendríticas" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "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">Motor function is impaired in multiple neurological diseases associated with corticospinal tract degeneration. Motor impairment has been linked to plastic changes at both the presynaptic and postsynaptic levels. However, there is no evidence of changes in information transmission from the cortex to spinal motor neurons.</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Methods</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">We used kainic acid to induce stereotactic lesions to the primary motor cortex of female adult rats. Fifteen days later, we evaluated motor function with the Basso, Beattie, Bresnahan (BBB) scale and the rotarod and determined the density of thin, stubby, and mushroom spines of motor neurons from a thoracolumbar segment of the spinal cord. Spinophilin, synaptophysin, and β III tubulin expression was also measured.</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">Pharmacological lesions resulted in poor motor performance. Spine density and the proportion of thin and stubby spines were greater. We also observed increased expression of the 3 proteins analysed.</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusion</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">The clinical symptoms of neurological damage secondary to Wallerian degeneration of the corticospinal tract are associated with spontaneous, compensatory plastic changes at the synaptic level. Based on these findings, spontaneous plasticity is a factor to consider when designing more efficient strategies in the early phase of rehabilitation.</p></span>" "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" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Introducción</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">Diversas enfermedades neuropatologías asociadas a la degeneración del tracto corticoespinal muestran deterioro de las funciones motoras. Tales alteraciones neurológicas se asocian a diversos fenómenos plásticos subsecuentes, a nivel tanto presináptico como postsináptico. Sin embargo, no existe evidencia que indique la existencia de modificaciones en la transmisión de información del tracto corticoespinal a las motoneuronas espinales.</p></span> <span id="abst0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Métodos</span><p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">Se indujo una lesión por vía estereotáxica en la corteza motora primaria de ratas hembra adultas con ácido kaínico y, 15 días después, se evaluó el desempeño motor mediante la escala BBB y en un dispositivo Rota-Rod. Paralelamente, se cuantificó la densidad numérica y proporcional de las espinas delgadas, en hongo y gordas, en motoneuronas de un segmento torácico-lumbar de la médula espinal. Así mismo, se registró la expresión de las proteínas espinofilina, sinaptofisina β III-tubulina.</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">La lesión farmacológica provocó un desempeño motor deficiente. Así mismo, tanto la densidad de espinas como la proporción de espinas delgadas y gordas fue mayor, al igual que la expresión de las 3 proteínas estudiadas.</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusión</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">La aparición de los síntomas clínicos de daño neurológico provocado por la degeneración walleriana del tracto corticoespinal se acompaña de respuestas plásticas espontáneas de tipo compensador, a nivel sináptico. Lo anterior indica que durante la rehabilitación temprana de este tipo de pacientes, la plasticidad espontánea constituye un factor que se debe considerar para el diseño de estrategias de intervención más eficientes.</p></span>" "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" => "<p class="elsevierStyleNotepara" id="npar0010">Please cite this article as: Martínez-Torres NI, González-Tapia D, Flores-Soto M, Vázquez-Hernández N, Salgado-Ceballos H, González-Burgos I. Espinogénesis en motoneuronas de la médula espinal tras la lesión farmacológica de la corteza motora de ratas. Neurología. 2021;36:119–126.</p>" ] ] "multimedia" => array:9 [ 0 => array:7 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 2559 "Ancho" => 2333 "Tamanyo" => 1217384 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0045" class="elsevierStyleSimplePara elsevierViewall">Above: panoramic microphotograph of the dorsal and ventral horns in a thoracic section from a rat spinal cord; the tissue was stained using a modified Golgi method. Arrows indicate motor neurons in the ventral horn containing the primary dendrites where dendritic spines were counted. Scale bar: 100<span class="elsevierStyleHsp" style=""></span>μm. Below: representative photomicrographs showing a typical thin spine (t), mushroom spine (m), and stubby spine (s) (arrows), which were counted in our study. Scale bar: 2<span class="elsevierStyleHsp" style=""></span>μm.</p>" ] ] 1 => array:7 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 1008 "Ancho" => 1582 "Tamanyo" => 47709 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0050" class="elsevierStyleSimplePara elsevierViewall">Graph showing the BBB motor activity scores in both animal study groups.</p> <p id="spar0055" class="elsevierStyleSimplePara elsevierViewall">Data are expressed as means (SEM). Statistical significance was set at <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>.05 (*).</p>" ] ] 2 => array:7 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 986 "Ancho" => 1582 "Tamanyo" => 39756 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0060" class="elsevierStyleSimplePara elsevierViewall">Comparison of latencies to fall from the rota-rod in both groups of animals.</p> <p id="spar0065" class="elsevierStyleSimplePara elsevierViewall">Data are expressed as means (SEM). Statistical significance was set at <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>.05 (*).</p>" ] ] 3 => array:7 [ "identificador" => "fig0020" "etiqueta" => "Figure 4" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr4.jpeg" "Alto" => 1017 "Ancho" => 1582 "Tamanyo" => 41210 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0070" class="elsevierStyleSimplePara elsevierViewall">Comparison of the rotation speed at which animals from each study group fell from the rota-rod.</p> <p id="spar0075" class="elsevierStyleSimplePara elsevierViewall">Data are expressed as means (SEM). Statistical significance was set at <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>.05 (*).</p>" ] ] 4 => array:7 [ "identificador" => "fig0025" "etiqueta" => "Figure 5" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr5.jpeg" "Alto" => 1002 "Ancho" => 1574 "Tamanyo" => 39550 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0080" class="elsevierStyleSimplePara elsevierViewall">Density of primary dendritic spines of spinal motor neurons in each animal group.</p> <p id="spar0085" class="elsevierStyleSimplePara elsevierViewall">Data are expressed as means (SEM). Statistical significance was set at <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>.05 (*).</p>" ] ] 5 => array:7 [ "identificador" => "fig0030" "etiqueta" => "Figure 6" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr6.jpeg" "Alto" => 1382 "Ancho" => 1582 "Tamanyo" => 92700 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0090" class="elsevierStyleSimplePara elsevierViewall">Expression of β III tubulin in spinal tissue from control and experimental animals. Statistical significance was set at <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>.05 (*).</p>" ] ] 6 => array:7 [ "identificador" => "fig0035" "etiqueta" => "Figure 7" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr7.jpeg" "Alto" => 1415 "Ancho" => 1581 "Tamanyo" => 80664 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0095" class="elsevierStyleSimplePara elsevierViewall">Expression of synaptophysin in spinal tissue from control and experimental animals. Statistical significance was set at <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>.05 (*).</p>" ] ] 7 => array:7 [ "identificador" => "fig0040" "etiqueta" => "Figure 8" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr8.jpeg" "Alto" => 1399 "Ancho" => 1579 "Tamanyo" => 84130 ] ] "descripcion" => array:1 [ "en" => "<p id="spar0100" class="elsevierStyleSimplePara elsevierViewall">Expression of spinophilin in spinal tissue from control and experimental animals.</p> <p id="spar0105" class="elsevierStyleSimplePara elsevierViewall">Statistical significance was set at <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>=<span class="elsevierStyleHsp" style=""></span>.05 (*).</p>" ] ] 8 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at1" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:3 [ "leyenda" => "<p id="spar0115" class="elsevierStyleSimplePara elsevierViewall">Data are expressed as means (SEM).</p>" "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Type of spineGroup \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Thin \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Mushroom \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Stubby \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Control \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1.56 (0.2) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1.25 (0.3) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">0.66 (0.1) \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Experimental \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">2.57 (0.2)<a class="elsevierStyleCrossRef" href="#tblfn0005">*</a> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1.38 (0.2) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="char" valign="\n \t\t\t\t\ttop\n \t\t\t\t">1.63 (0.1)<a class="elsevierStyleCrossRef" href="#tblfn0005">*</a> \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab2527917.png" ] ] ] "notaPie" => array:1 [ 0 => array:3 [ "identificador" => "tblfn0005" "etiqueta" => "*" "nota" => "<p class="elsevierStyleNotepara" id="npar0005"><span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span><<span class="elsevierStyleHsp" style=""></span>.05.</p>" ] ] ] "descripcion" => array:1 [ "en" => "<p id="spar0110" class="elsevierStyleSimplePara elsevierViewall">Proportional density of the different types of dendritic spines studied in the spinal motor neurons.</p>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0015" "bibliografiaReferencia" => array:41 [ 0 => array:3 [ "identificador" => "bib0210" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "Corticospinal function and voluntary movement" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:2 [ 0 => "R. 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| Year/Month | Html | Total | |
|---|---|---|---|
| 2024 November | 9 | 0 | 9 |
| 2024 October | 119 | 4 | 123 |
| 2024 September | 112 | 6 | 118 |
| 2024 August | 31 | 5 | 36 |
| 2024 July | 42 | 7 | 49 |
| 2024 June | 49 | 13 | 62 |
| 2024 May | 46 | 6 | 52 |
| 2024 April | 37 | 12 | 49 |
| 2024 March | 29 | 8 | 37 |
| 2024 February | 32 | 5 | 37 |
| 2024 January | 23 | 6 | 29 |
| 2023 December | 32 | 15 | 47 |
| 2023 November | 35 | 16 | 51 |
| 2023 October | 21 | 14 | 35 |
| 2023 September | 13 | 4 | 17 |
| 2023 August | 20 | 5 | 25 |
| 2023 July | 20 | 14 | 34 |
| 2023 June | 44 | 4 | 48 |
| 2023 May | 56 | 7 | 63 |
| 2023 April | 98 | 4 | 102 |
| 2023 March | 22 | 4 | 26 |
| 2023 February | 10 | 1 | 11 |
| 2023 January | 28 | 5 | 33 |
| 2022 December | 27 | 8 | 35 |
| 2022 November | 34 | 13 | 47 |
| 2022 October | 33 | 7 | 40 |
| 2022 September | 18 | 16 | 34 |
| 2022 August | 26 | 10 | 36 |
| 2022 July | 19 | 6 | 25 |
| 2022 June | 16 | 11 | 27 |
| 2022 May | 34 | 9 | 43 |
| 2022 April | 46 | 11 | 57 |
| 2022 March | 61 | 12 | 73 |
| 2022 February | 30 | 14 | 44 |
| 2022 January | 46 | 12 | 58 |
| 2021 December | 62 | 13 | 75 |
| 2021 November | 56 | 11 | 67 |
| 2021 October | 45 | 9 | 54 |
| 2021 September | 25 | 9 | 34 |
| 2021 August | 28 | 8 | 36 |
| 2021 July | 25 | 11 | 36 |
| 2021 June | 24 | 9 | 33 |
| 2021 May | 28 | 8 | 36 |
| 2021 April | 91 | 7 | 98 |
| 2021 March | 33 | 8 | 41 |
| 2021 February | 16 | 12 | 28 |
| 2021 January | 15 | 5 | 20 |
| 2020 December | 18 | 8 | 26 |
| 2020 November | 15 | 6 | 21 |
| 2020 October | 8 | 3 | 11 |
| 2020 September | 19 | 9 | 28 |
| 2020 August | 22 | 4 | 26 |
| 2020 July | 20 | 6 | 26 |
| 2020 June | 18 | 10 | 28 |
| 2020 May | 12 | 12 | 24 |
| 2020 April | 15 | 9 | 24 |
| 2020 March | 15 | 5 | 20 |
| 2020 February | 16 | 6 | 22 |
| 2020 January | 11 | 2 | 13 |
| 2019 December | 18 | 14 | 32 |
| 2019 November | 4 | 6 | 10 |
| 2019 October | 8 | 9 | 17 |
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