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Original article
Motor learning induces plastic changes in Purkinje cell dendritic spines in the rat cerebellum
El aprendizaje motor induce cambios plásticos en las espinas dendríticas de las células de Purkinje del cerebelo de ratas
D. González-Tapiaa,b,c, M.M. González-Ramíreza, N. Vázquez-Hernándeza, I. González-Burgosa,
Corresponding author
igonbur@hotmail.com

Corresponding author.
a División de Neurociencias, Centro de Investigación Biomédica de Occidente, IMSS, Guadalajara, Jalisco, Mexico
b Universidad Politécnica de la Zona Metropolitana de Guadalajara, Tlajomulco de Zúñiga, Jalisco, Mexico
c Instituto de Ciencias de la Rehabilitación Integral, Guadalajara, Jalisco, Mexico
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Neuroplasticity underlies brain repair in response to environmental factors that alter neurobiological processes&#46; The neuropathological damage that causes motor dysfunction is commonly followed by plasticity responses that act to restore normal activity at different levels&#44; including at the level of synaptic contacts&#46; However&#44; spontaneous recovery of the lost motor function is infrequent&#44; which suggests that some of the neuroplastic events taking place during the recovery period are not effective&#46; In fact&#44; these events are largely unknown&#46;</p><p id="par0010" class="elsevierStylePara elsevierViewall">The recovery of certain skills requires them to be relearned&#44; a process in which cerebellar activity plays a significant role&#46;<a class="elsevierStyleCrossRefs" href="#bib0215"><span class="elsevierStyleSup">1&#8211;3</span></a> The paramedian lobule of the cerebellar cortex is closely related to motor learning&#46; Purkinje cells &#40;PC&#41; in this region integrate afferent information from both extrinsic and intrinsic neural systems&#44; which is necessary for encoding the patterns underlying motor learning&#46; Plastic changes have been reported in the distal synapses between PCs and granule cell parallel fibres &#40;PF&#41;&#44; which underlie motor learning in rats trained to learn new motor skills&#46;<a class="elsevierStyleCrossRefs" href="#bib0230"><span class="elsevierStyleSup">4&#8211;6</span></a> Similarly&#44; increased numbers of dendritic spines have been reported in the distal dendrites of PCs after 26 days of acrobatic motor learning&#44; in which the number of foot faults observed decreased during the first 6 days&#44; then asymptotically stabilised&#46;<a class="elsevierStyleCrossRefs" href="#bib0230"><span class="elsevierStyleSup">4&#44;7&#44;8</span></a> These findings point to the occurrence of neuroplastic events at the level of distal synapses between PFs and PCs mediated by dendritic spines in the cerebellar paramedian lobule during the critical period of motor learning&#46; According to studies by Doyon and Benali<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">2</span></a> and Dayan and Cohen&#44;<a class="elsevierStyleCrossRef" href="#bib0255"><span class="elsevierStyleSup">9</span></a> motor skills are learnt after several different stages&#44; whose duration depends on the task&#46; The first stage is called the &#8220;fast stage&#44;&#8221; in which acquisition of motor skills is especially evident&#44; with efficiency improving considerably as this stage progresses&#46;</p><p id="par0015" class="elsevierStylePara elsevierViewall">Dendritic spines may display several types of plastic changes&#44; including neoformation&#44; reabsorption&#44; and geometric remodelling&#44; especially related to the translation of afferent information&#46;<a class="elsevierStyleCrossRefs" href="#bib0260"><span class="elsevierStyleSup">10&#8211;14</span></a> As PF&#8211;PC synapses are involved in modulating motor learning&#44; we studied the cytoarchitecture of distal dendritic spines of PCs in the paramedian lobule of the cerebellum of rats trained according to a motor learning paradigm&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Material and methods</span><p id="par0020" class="elsevierStylePara elsevierViewall">We used 72 adult male Sprague&#8211;Dawley rats &#40;250-300<span class="elsevierStyleHsp" style=""></span>g&#41;&#59; animals were kept in standard vivarium conditions with 12-hour light&#47;dark cycles &#40;07&#58;00-19&#58;00<span class="elsevierStyleHsp" style=""></span>h&#41;&#44; 45&#37; to 50&#37; humidity&#44; room temperature of 22<span class="elsevierStyleHsp" style=""></span>&#177;<span class="elsevierStyleHsp" style=""></span>2<span class="elsevierStyleHsp" style=""></span>&#176;C&#44; and free access to water and conventional rodent chow&#46; Our experimental protocols were approved by the research ethics committee of the National Institute of Health &#40;Mexico&#41; and were designed in accordance with the Guide for the Care and Use of Laboratory Animals &#40;NIH Publication No&#46; 8023&#44; 1996 revision&#41;&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">We established 2 groups&#58; an experimental acrobatic group &#40;EG&#44; <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>36&#41;&#44; which completed an acrobatic motor learning test on 6 consecutive days&#44; and a control group &#40;CG&#44; <span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>36&#41;&#44; which travelled the same distance as the EG but on a flat&#44; obstacle-free surface&#46; The 36 rats in each group were subdivided into 6 subgroups &#40;<span class="elsevierStyleItalic">n</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>6 per subgroup&#41;&#46; The test was performed on consecutive days&#44; from day 1 &#40;EG1&#47;CG1&#41; to day 6 &#40;EG6&#47;CG6&#41;&#44; with the number of training days increasing by subgroup &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46; According to previous studies&#44;<a class="elsevierStyleCrossRefs" href="#bib0240"><span class="elsevierStyleSup">6&#8211;8</span></a> the fast motor learning period<a class="elsevierStyleCrossRefs" href="#bib0220"><span class="elsevierStyleSup">2&#44;9</span></a> occurs during the first week of training in a spaced time paradigm&#46;<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">15</span></a></p><elsevierMultimedia ident="fig0005"></elsevierMultimedia><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Behavioural study</span><p id="par0030" class="elsevierStylePara elsevierViewall">Experimental animals were trained to traverse an elevated course &#40;4&#46;25<span class="elsevierStyleHsp" style=""></span>m at 1<span class="elsevierStyleHsp" style=""></span>m above the floor&#41; in 4 trials per day with no time limit&#44; with intervals of 60<span class="elsevierStyleHsp" style=""></span>seconds between trials&#44; between 11&#58;00 and 14&#58;00&#46; The course consisted of a steel chain &#40;50<span class="elsevierStyleHsp" style=""></span>cm length&#41;&#44; a horizontal wooden ladder &#40;10<span class="elsevierStyleHsp" style=""></span>cm width<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>50<span class="elsevierStyleHsp" style=""></span>cm length&#41; covered with straws&#44; a woven wire tube &#40;30<span class="elsevierStyleHsp" style=""></span>cm diameter<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>80<span class="elsevierStyleHsp" style=""></span>cm length&#41;&#44; a wooden staircase covered with abacus beads &#40;10<span class="elsevierStyleHsp" style=""></span>cm width<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>60<span class="elsevierStyleHsp" style=""></span>cm length&#41;&#44; parallel bars &#40;5<span class="elsevierStyleHsp" style=""></span>cm width<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>50<span class="elsevierStyleHsp" style=""></span>cm length&#41;&#44; parallel bars with a crossed truss &#40;15<span class="elsevierStyleHsp" style=""></span>cm width<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>60<span class="elsevierStyleHsp" style=""></span>cm length&#41;&#44; and a balance beam &#40;2<span class="elsevierStyleHsp" style=""></span>cm width<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>75<span class="elsevierStyleHsp" style=""></span>cm length&#41;&#46; A cage was placed at the end of the course for the animal to enter&#46;<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">7</span></a> Since rats needed motor coordination and balance to overcome the obstacles along the course&#44; we recorded both the time needed to complete the test and the number of foot faults &#40;errors&#41; in each trial&#44; as a measure of motor learning&#46; The animals in all study groups were housed in groups of 6 per cage&#44; in a room different to that used for training&#46;</p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Morphological study</span><p id="par0035" class="elsevierStylePara elsevierViewall">Immediately after their final session of behavioural training&#44; the 6 animals from the corresponding experimental and control groups were anaesthetised with intramuscular ketamine &#40;30<span class="elsevierStyleHsp" style=""></span>mg&#47;kg&#41; and intraperitoneal sodium pentobarbital &#40;50<span class="elsevierStyleHsp" style=""></span>mg&#47;kg&#41;&#46; They were immediately perfused with 200<span class="elsevierStyleHsp" style=""></span>mL of phosphate-buffered saline &#40;pH 7&#46;4&#59; 0&#46;01<span class="elsevierStyleHsp" style=""></span>M&#41; containing sodium heparin &#40;1000<span class="elsevierStyleHsp" style=""></span>IU&#47;L&#41; as an anticoagulant and procaine hydrochloride &#40;1<span class="elsevierStyleHsp" style=""></span>g&#47;L&#41; as a vasodilator&#46;<a class="elsevierStyleCrossRef" href="#bib0290"><span class="elsevierStyleSup">16</span></a> Animals were subsequently perfused with 200<span class="elsevierStyleHsp" style=""></span>mL of a phosphate-buffered 4&#37; formaldehyde fixative solution&#46; Both solutions were perfused at a flow rate of 11&#46;5<span class="elsevierStyleHsp" style=""></span>mL&#47;minutes&#46; Brains were obtained by craniectomy and were kept in 100<span class="elsevierStyleHsp" style=""></span>mL of fresh fixative solution for 48<span class="elsevierStyleHsp" style=""></span>hours&#46; A block of tissue from the left cerebellar hemisphere&#44; containing the paramedian lobule&#44;<a class="elsevierStyleCrossRef" href="#bib0295"><span class="elsevierStyleSup">17</span></a> was dissected and impregnated using a modified version of the Golgi technique&#46;<a class="elsevierStyleCrossRef" href="#bib0300"><span class="elsevierStyleSup">18</span></a> Using 75<span class="elsevierStyleHsp" style=""></span>&#956;m thick sagittal slices&#44; we performed a &#8220;blind&#8221; study of 6 clearly visible PCs from each rat&#46; In each of the 6<span class="elsevierStyleHsp" style=""></span>cells studied per rat&#44; we counted dendritic spines in a total section of 50<span class="elsevierStyleHsp" style=""></span>&#956;m from 3 to 4 terminal apical dendritic branchlets distal to the soma &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#44; left panel&#41;&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia><p id="par0040" class="elsevierStylePara elsevierViewall">We quantified the numerical and proportional density of thin&#44; mushroom&#44; stubby&#44; and wide spines&#44; according to previously established criteria<a class="elsevierStyleCrossRefs" href="#bib0265"><span class="elsevierStyleSup">11&#44;19&#8211;23</span></a> &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#44; right panel&#41;&#46; Spines were counted by direct observation at 2000&#215; using a magnification changer coupled to a light microscope and a 100&#215; Apochromat objective and an image analyser &#40;LAS 4&#46;0&#41;&#46;</p></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Statistical analysis</span><p id="par0045" class="elsevierStylePara elsevierViewall">Mean values for both the time taken to complete the course and the number of errors&#44; as well as the density and morphology of dendritic spines&#44; were calculated for the 6 animals studied each day&#59; comparisons were made between subgroups 1&#44; 2&#44; 3&#44; 4&#44; 5&#44; and 6 using two-way ANOVA &#40;group<span class="elsevierStyleHsp" style=""></span>&#215;<span class="elsevierStyleHsp" style=""></span>day&#41;&#44; followed by the <span class="elsevierStyleItalic">t</span> test for independent samples&#46;</p></span></span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0090">Results</span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0095">Motor learning</span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0100">Time</span><p id="par0050" class="elsevierStylePara elsevierViewall">Experimental animals took longer to complete the course than control animals on all training days&#58; day 1&#44; <span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;7&#46;847&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;0001&#59; day 2&#44; <span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;4&#46;847&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;001&#59; day 3&#58; <span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;4&#46;137&#59; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;002&#59; day 4&#44; <span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;5&#46;543&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;0001&#59; day 5&#44; <span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;8&#46;801&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;0001&#59; day 6&#44; <span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;11&#46;675&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;0001&#46; There were no differences in the time taken by experimental animals to complete the course on any of the 6 days of study&#46; Furthermore&#44; the control subgroups showed differences in time to complete the test &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>21&#46;614&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;0001&#41;&#59; the rats in subgroups CG2 &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;0001&#41;&#44; CG3 &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;0001&#41;&#44; CG4 &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;0001&#41;&#44; CG5 &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;0001&#41;&#44; and CG6 &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;0001&#41; travelled the required distance quicker than those in subgroup CG1&#46; No differences were observed between subgroups CG2&#44; CG3&#44; CG4&#44; CG5&#44; and CG6 &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46;</p><elsevierMultimedia ident="fig0015"></elsevierMultimedia></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0105">Errors</span><p id="par0055" class="elsevierStylePara elsevierViewall">The number of errors made by experimental animals decreased as the days of training advanced &#40;<span class="elsevierStyleItalic">F</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>20&#46;169&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;0001&#41;&#46; Compared to day 1&#44; rats made fewer errors on days 2 &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;003&#41;&#44; 3 &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;0001&#41;&#44; 4 &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;0001&#41;&#44; 5 &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;0001&#41;&#44; and 6 &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;0001&#41;&#46; Furthermore&#44; EG4 &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;004&#41;&#44; EG5 &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;004&#41;&#44; and EG6 rats &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;004&#41; made fewer errors than those in the EG2 subgroup&#44; with EG6 rats also making fewer errors than EG4 rats &#40;<span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;02&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0020">Fig&#46; 4</a>&#41;&#46;</p><elsevierMultimedia ident="fig0020"></elsevierMultimedia></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0110">Density of dendritic spines</span><p id="par0060" class="elsevierStylePara elsevierViewall">Density of dendritic spines on PCs of the paramedian lobules of animals from the EG2 &#40;<span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;3&#46;713&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;004&#41; and EG6 subgroups &#40;<span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;2&#46;577&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;02&#41; was higher than in the CG2 and CG6 subgroups &#40;<a class="elsevierStyleCrossRef" href="#fig0025">Fig&#46; 5</a>&#41;&#46;</p><elsevierMultimedia ident="fig0025"></elsevierMultimedia></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0115">Types of dendritic spines</span><p id="par0065" class="elsevierStylePara elsevierViewall">Animals in EG1&#44; EG3&#44; and EG6 subgroups had more thin spines than those in the CG1&#44; CG3&#44; and CG6 subgroups &#40;<span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;2&#46;709&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;02&#59; <span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;2&#46;223&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;05&#59; and <span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;2&#46;235&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;04&#59; respectively&#41;&#46; Furthermore&#44; the EG3 subgroup showed fewer mushroom spines than the CG3 subgroup &#40;<span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>3&#46;452&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;006&#41;&#46; Density of stubby spines was lower in EG1 rats than in CG1 rats &#40;<span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>3&#46;059&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;01&#41;&#44; whereas animals in the EG4 subgroup showed more wide spines than those in the CG4 subgroup &#40;<span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>&#8722;4&#46;902&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;001&#41;&#59; EG6 subgroup showed the same difference with regard to CG6 &#40;<span class="elsevierStyleItalic">t</span><span class="elsevierStyleHsp" style=""></span>&#61;<span class="elsevierStyleHsp" style=""></span>2&#46;976&#44; <span class="elsevierStyleItalic">P</span><span class="elsevierStyleHsp" style=""></span>&#60;<span class="elsevierStyleHsp" style=""></span>&#46;01&#41; &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia></span></span></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0120">Discussion</span><p id="par0070" class="elsevierStylePara elsevierViewall">The paramedian lobule of the cerebellum participates in the integration of information related to motor learning&#44; as has been reported in studies showing increased metabolic activity in this cerebellar region during the first days of acquisition of motor skills&#46;<a class="elsevierStyleCrossRefs" href="#bib0255"><span class="elsevierStyleSup">9&#44;24</span></a> Therefore&#44; cerebellar activity may be influenced by changes in synaptic information processing between PFs and PCs&#44;<a class="elsevierStyleCrossRefs" href="#bib0230"><span class="elsevierStyleSup">4&#8211;6</span></a> due to the remodelling of dendritic spines mediated by motor learning&#46; In line with this&#44; we observed an increase in the number of dendritic spines in PCs during the fast motor learning period&#44; corresponding to a reduction in the number of errors made as rats completed the acrobatic course&#46;</p><p id="par0075" class="elsevierStylePara elsevierViewall">Although the distance travelled by experimental and control animals was the same&#44; the time required to complete the course with obstacles was longer&#44; which could be explained by the fact that motor requirements were more complex for the experimental group&#46; Although the time taken to complete the task was not significant in comparison with day 1&#44; we did observe a downward trend&#44; which would be partially consistent with previous reports&#46;<a class="elsevierStyleCrossRefs" href="#bib0245"><span class="elsevierStyleSup">7&#44;8</span></a></p><p id="par0080" class="elsevierStylePara elsevierViewall">As reported in previous studies&#44;<a class="elsevierStyleCrossRefs" href="#bib0245"><span class="elsevierStyleSup">7&#44;8</span></a> the number of errors made by experimental rats decreased with the days of training&#46; This could be interpreted as a gradual and progressive increase in the precision and control of motor activity and demonstrates the appearance of a learning process&#46;<a class="elsevierStyleCrossRefs" href="#bib0335"><span class="elsevierStyleSup">25&#44;26</span></a> Synaptic inputs to the apical dendritic region of PCs are directly related to the organisation of the psychoneural events leading to better performance of motor skills<a class="elsevierStyleCrossRefs" href="#bib0215"><span class="elsevierStyleSup">1&#44;4&#8211;8&#44;27</span></a>&#59; according to other authors&#44;<a class="elsevierStyleCrossRef" href="#bib0350"><span class="elsevierStyleSup">28</span></a> the underlying synaptic stimulation might be related both to the potentiation and to the depression of synapses between parallel fibres and PC dendritic spines&#46; Thus&#44; the gradual increase in efficiency observed over the training period may have involved structural modifications to the synapses in the cerebellar paramedian lobule&#44;<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">15</span></a> which may correspond to plastic changes in dendritic spines&#44; as observed in our study&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">The higher number of dendritic spines reported at training days 2 and 6 suggests a higher level of presynaptic activity as a result of motor learning&#46; Several studies have associated the increased number of dendritic spines with higher presynaptic activity&#44;<a class="elsevierStyleCrossRefs" href="#bib0355"><span class="elsevierStyleSup">29&#44;30</span></a> including that related to motor learning&#46;<a class="elsevierStyleCrossRefs" href="#bib0305"><span class="elsevierStyleSup">19&#44;28&#44;31</span></a> In addition to spine density&#44; plastic changes in the types of dendritic spines may also participate in the neurobiological events underlying the processing of information related to motor learning&#46; PCs display several types of dendritic spines&#44; characterised by their shape&#59; these include the thin&#44; mushroom&#44; stubby&#44; and wide types&#46;<a class="elsevierStyleCrossRefs" href="#bib0305"><span class="elsevierStyleSup">19&#8211;21</span></a> Thin spines are associated with fast&#44; highly efficient synaptic neurotransmission&#44; the induction of long-term potentiation&#44;<a class="elsevierStyleCrossRef" href="#bib0370"><span class="elsevierStyleSup">32</span></a> and events related to information acquisition or new learning&#46;<a class="elsevierStyleCrossRefs" href="#bib0275"><span class="elsevierStyleSup">13&#44;14</span></a> Furthermore&#44; synaptic stimuli in mushroom spines are processed in the cell nucleus&#44; which has been associated with the consolidation of information previously acquired as traces of memory&#46;<a class="elsevierStyleCrossRefs" href="#bib0275"><span class="elsevierStyleSup">13&#44;14</span></a> When synaptic stimulation of neurons is sufficiently high to prevent synaptic integration&#44;<a class="elsevierStyleCrossRef" href="#bib0305"><span class="elsevierStyleSup">19</span></a> the functional activity of stubby and wide spines would participate by regulating the excitability of the postsynaptic neuron&#44;<a class="elsevierStyleCrossRefs" href="#bib0265"><span class="elsevierStyleSup">11&#44;12&#44;33</span></a> as it lacks a slender neck&#46;<a class="elsevierStyleCrossRefs" href="#bib0380"><span class="elsevierStyleSup">34&#44;35</span></a></p><p id="par0090" class="elsevierStylePara elsevierViewall">A trend towards greater abundance of thin spines was observed on all training days&#44; with the number being significant at days 1&#44; 3&#44; and 6&#46; As the animals were exposed to a new experience on the first day of training&#44; and because transmission of this new information mediated by synapses with thin spines on PCs involves fast information processing&#44;<a class="elsevierStyleCrossRef" href="#bib0390"><span class="elsevierStyleSup">36</span></a> the increase in this type of spines seems to have been functionally significant&#46; The increased density of thin spines may also be causally related to the nature of the behavioural task&#46; The volume of the heads of large spines has been demonstrated to decrease after spaced training and to change to the extent that they transform into thin spines&#44;<a class="elsevierStyleCrossRef" href="#bib0285"><span class="elsevierStyleSup">15</span></a> which may be related to long-term potentiation and depression associated with synaptic activity in the contacts between PFs and PCs&#46;<a class="elsevierStyleCrossRef" href="#bib0350"><span class="elsevierStyleSup">28</span></a> Therefore&#44; the increased density of thin spines in the long term during training may account for the increasingly accurate performance of the skills needed to resolve the behavioural task&#44; that is&#44; motor learning&#46;</p><p id="par0095" class="elsevierStylePara elsevierViewall">The density of mushroom spines was only different at training day 3&#44; with experimental animals showing lower levels than control rats&#46; As mushroom spines are related to information storage&#44;<a class="elsevierStyleCrossRefs" href="#bib0275"><span class="elsevierStyleSup">13&#44;14</span></a> this finding is relevant when considered in association with the higher number of thin spines&#46; Together&#44; these events may suggest that synaptic activity related to the information storage underlying motor performance is secondary to the acquisition of this information&#44; as reflected by the predominance of thin spines&#46; If this were the case&#44; the capacity to acquire new information would not be conditioned by consolidation of the information&#44; represented by mushroom spines&#59; this is translated into a &#8220;released&#8221; capacity to consistently acquire novel information throughout the training period&#46; This would be consistent with previous reports showing an increase in all types of spines &#40;including mushroom spines&#41; 4 weeks after the implementation of a motor learning paradigm similar to the one used in this study&#44; in which the learning curve is not modified after the first week of training&#44; following an initial stage of consistent learning&#46;<a class="elsevierStyleCrossRefs" href="#bib0230"><span class="elsevierStyleSup">4&#44;7&#44;8</span></a> This suggests that the information required to perform a task efficiently and consistently has been consolidated&#44; presumably with considerable participation of mushroom spines as mediators of the synaptic processes associated with motor learning&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">The ratio of stubby spines was lower on training day 1&#44; whereas the ratio of wide spines was higher on days 4 and 6&#46; The smaller number of stubby spines on day 1 may mean that synaptic inputs to PCs may be highly specific when correlated with the proportional increase in thin spines observed on the same day of training&#46; Furthermore&#44; the higher number of wide spines recorded in the last days of training suggests that&#44; despite active learning of motor skills&#44; the increasingly efficient performance of a task would involve functionally redundant synaptic activity&#46; This would be reflected in an increase in the proportion of spines participating in the regulation of afferent synaptic activity&#44; such as wide spines&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">This evidence suggests a close relationship between the acquisition of new motor skills and the plasticity of dendritic spines&#46; In this sense&#44; motor learning has been reported to induce &#8220;non-linear&#8221; plastic changes in dendritic spines during successive stages of training&#44;<a class="elsevierStyleCrossRef" href="#bib0395"><span class="elsevierStyleSup">37</span></a> which is clearly consistent with our findings&#46;</p><p id="par0110" class="elsevierStylePara elsevierViewall">Some other synaptic connections between neuronal elements of the cortex of the cerebellar paramedian lobule would be involved in the integration of information related to motor learning<a class="elsevierStyleCrossRefs" href="#bib0400"><span class="elsevierStyleSup">38&#8211;40</span></a>&#59; this probably also occurs in other cerebellar lobules&#46;<a class="elsevierStyleCrossRef" href="#bib0415"><span class="elsevierStyleSup">41</span></a> Furthermore&#44; possible variations in the cytoarchitecture of PCs from different areas<a class="elsevierStyleCrossRef" href="#bib0420"><span class="elsevierStyleSup">42</span></a> of the same paramedian lobule could be considered a source of plastic changes in the morphology of spines&#44; which may affect motor learning&#46; These possibilities require further study&#46;</p><p id="par0115" class="elsevierStylePara elsevierViewall">This study underscores the significance of plastic events at the synaptic level in the initial stages of motor learning&#44; favouring the acquisition of motor skills in normal or neuropsychopathological conditions&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0125">Funding</span><p id="par0120" class="elsevierStylePara elsevierViewall">This study was financed by the Health Research Fund of the <span class="elsevierStyleGrantSponsor" id="gs1">Mexican Institute of Health</span>&#44; with registry number <span class="elsevierStyleGrantNumber" refid="gs1">FIS&#47;IMSS&#47;PROT&#47;G14&#47;1336</span>&#46;</p></span><span id="sec0070" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0130">Conflicts of interest</span><p id="par0125" class="elsevierStylePara elsevierViewall">The authors have no conflicts of interest to declare&#46;</p></span></span>"
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              "titulo" => "Motor learning"
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                  "titulo" => "Density of dendritic spines"
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                  "titulo" => "Types of dendritic spines"
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    "fechaRecibido" => "2017-09-12"
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            0 => "Cerebellum"
            1 => "Purkinje cell"
            2 => "Motor activity"
            3 => "Motor learning"
            4 => "Plasticity"
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            0 => "Cerebelo"
            1 => "C&#233;lula de Purkinje"
            2 => "Actividad motora"
            3 => "Aprendizaje motor"
            4 => "Plasticidad"
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        "titulo" => "Abstract"
        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0010">Introduction</span><p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">The paramedian lobule of the cerebellum is involved in learning to correctly perform motor skills through practice&#46; Dendritic spines are dynamic structures that regulate excitatory synaptic stimulation&#46; We studied plastic changes occurring in the dendritic spines of Purkinje cells from the paramedian lobule of rats during motor learning&#46;</p></span> <span id="abst0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0015">Methods</span><p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Adult male rats were trained over a 6-day period using an acrobatic motor learning paradigm&#59; the density and type of dendritic spines were determined every day during the study period using a modified version of the Golgi method&#46;</p></span> <span id="abst0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0020">Results</span><p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">The learning curve reflected a considerable decrease in the number of errors made by rats as the training period progressed&#46; We observed more dendritic spines on days 2 and 6&#44; particularly more thin spines on days 1&#44; 3&#44; and 6&#44; fewer mushroom spines on day 3&#44; fewer stubby spines on day 1&#44; and more thick spines on days 4 and 6&#46;</p></span> <span id="abst0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Conclusion</span><p id="spar0020" class="elsevierStyleSimplePara elsevierViewall">The initial stage of motor learning may be associated with fast processing of the underlying synaptic information combined with an apparent &#8220;silencing&#8221; of memory consolidation processes&#44; based on the regulation of the neuronal excitability&#46;</p></span>"
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        "resumen" => "<span id="abst0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Introducci&#243;n</span><p id="spar0025" class="elsevierStyleSimplePara elsevierViewall">El l&#243;bulo paramediano del cerebelo est&#225; involucrado en el desempe&#241;o correcto de las habilidades motoras a trav&#233;s de la pr&#225;ctica&#46; Las espinas dendr&#237;ticas son estructuras din&#225;micas que regulan la estimulaci&#243;n sin&#225;ptica excitadora&#46; En este trabajo se estudiaron los posibles cambios pl&#225;sticos en espinas de c&#233;lulas de Purkinje del l&#243;bulo paramediano cerebelar de ratas&#44; durante el aprendizaje motor&#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 entrenaron a ratas macho adultas durante un per&#237;odo de seis d&#237;as&#44; en un paradigma de aprendizaje motor acrob&#225;tico y se cuantific&#243; tanto la densidad como los tipos de espinas dendr&#237;ticas en cada uno de los seis d&#237;as de estudio&#44; mediante una modificaci&#243;n al m&#233;todo de Golgi&#46;</p></span> <span id="abst0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Resultados</span><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">La curva de aprendizaje reflej&#243; una disminuci&#243;n consistente de los errores cometidos en el transcurso de los d&#237;as de entrenamiento&#46; As&#237; mismo&#44; se observaron m&#225;s espinas dendr&#237;ticas en los d&#237;as 2 y 6 y&#44; en particular&#44; m&#225;s espinas delgadas en los d&#237;as 1&#44; 3 y 6&#44; menos espinas en hongo el d&#237;a 3&#44; menos espinas gordas el d&#237;a 1 y m&#225;s espinas anchas los d&#237;as 4 y 6&#46;</p></span> <span id="abst0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Conclusi&#243;n</span><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">El per&#237;odo inicial de aprendizaje motor podr&#237;a estar asociado con el procesamiento r&#225;pido de la informaci&#243;n sin&#225;ptica subyacente y con un aparente &#171;silenciamiento&#187; de los procesos de consolidaci&#243;n mn&#233;mica&#44; en una base de regulaci&#243;n de la excitabilidad neuronal&#46;</p></span>"
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        "nota" => "<p class="elsevierStyleNotepara" id="npar0010">Please cite this article as&#58; Gonz&#225;lez-Tapia D&#44; Gonz&#225;lez-Ram&#237;rez MM&#44; V&#225;zquez-Hern&#225;ndez N&#44; Gonz&#225;lez-Burgos I&#46; El aprendizaje motor induce cambios pl&#225;sticos en las espinas dendr&#237;ticas de las c&#233;lulas de Purkinje del cerebelo de ratas&#46; Neurolog&#237;a&#46; 2020&#59;35&#58;451&#8211;457&#46;</p>"
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        "nota" => "<p class="elsevierStyleNotepara" id="npar0015">Part of this work was presented at the 45th Congress of the Society for Neuroscience&#46;</p>"
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Article information
ISSN: 21735808
Original language: English
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