Changes in the plastic properties of hippocampal dendritic spines underlie the attenuation of place learning in healthy aged rats

González-Ramírez, Myrna M.; Velázquez-Zamora, Dulce A.; Olvera‐Cortés, María Esther; González-Burgos, Ignacio

doi:10.1016/j.nlm.2013.11.017

Cited by 31 publications

(23 citation statements)

References 57 publications

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“…In particular, the EE effects on the morphological features of Purkinje cells (density, area, length and head diameter of spines) were evaluated in proximal and distal dendrite compartments that as known receive different inputs to elaborate. In line with the effects previously reported on neocortical and hippocampal neurons (Johansson and Belichenko 2002;Gelfo et al 2009;Mandolesi et al 2008;Rojas et al 2013;González-Ramírez et al 2014), the exposure to an enriched environment affected density, area, length and head diameter of Purkinje cell spines. In particular, spine density was higher in enriched rats than in controls on both proximal and distal dendrite compartments in the hemisphere, while it increased only on distal compartment in the vermis, suggesting that the different spinogenesis in the two dendrite compartments is the expression of the differences in the inputs they receive.…”

Section: Discussionsupporting

confidence: 87%

Activity-dependent structural plasticity of Purkinje cell spines in cerebellar vermis and hemisphere

et al. 2014

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The environmental enrichment (EE) paradigm is widely used to study experience-dependent brain plasticity. In spite of a long history of research, the EE influence on neuronal morphology has not yet been described in relation to the different regions of the cerebellum. Thus, aim of the present study was to characterize the EE effects on density and size of dendritic spines of Purkinje cell proximal and distal compartments in cerebellar vermian and hemispherical regions. Male Wistar rats were housed in an enriched or standard environment for 3.5 months from the 21st post-natal day onwards. The morphological features of Purkinje cell spines were visualized on calbindin immunofluorescence-stained cerebellar vermian and hemispherical sections. Density, area, length and head diameter of spines were manually (ImageJ) or automatically (Imaris) quantified. Results demonstrated that the Purkinje cell spine density was higher in enriched rats than in controls on both proximal and distal dendrite compartments in the hemisphere, while it increased only on distal compartment in the vermis. As for spine size, a significant increase of area, length and head diameter was found in the distal dendrites in both vermis and hemisphere. Thus, the exposure to a complex environment enhances synapse formation and plasticity either in the vermis involved in balance and locomotion and in the hemisphere involved in complex motor adaptations and acquisition of new motor strategies. These data highlight the importance of cerebellar activity-dependent structural plasticity underling the EE-related high-level performances.

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Section: Discussionsupporting

confidence: 87%

Activity-dependent structural plasticity of Purkinje cell spines in cerebellar vermis and hemisphere

et al. 2014

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“…In the current study, enriched rats trained on tasks that are highly sensitive to hippocampal lesions showed more CA1 basal spines than enriched rats that were given a comparable pseudo‐training procedure. This evidence complements previous findings that spatial training exerts an effect through these basal spines (Moser et al, ; González‐Ramírez et al, ) by providing novel support that, at least in enriched trained rats, increases in CA1 spine density are specifically related to improved spatial working memory beyond non‐specific task‐related factors.…”

Section: Discussionsupporting

confidence: 87%

“…The recovery of thin, but not mushroom spines, was an unexpected finding. Given that a selective loss of thin spine plasticity is associated with impaired spatial memory in aged rats (González‐Ramírez et al, ), a selective pattern of recovery of thin spines is consistent with the ability of enrichment to improve spatial memory after ATN lesions. In enriched rats, the effect of training as opposed to pseudo‐training also produced a substantial increase in thin spines and a far weaker effect was also evident for mushroom spines.…”

Section: Discussionmentioning

confidence: 64%

Anterior thalamic lesions reduce spine density in both hippocampal CA1 and retrosplenial cortex, but enrichment rescues CA1 spines only

et al. 2014

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Injury to the anterior thalamic nuclei (ATN) may affect both hippocampus and retrosplenial cortex thus explaining some parallels between diencephalic and medial temporal lobe amnesias. We found that standard-housed rats with ATN lesions, compared with standard-housed controls, showed reduced spine density in hippocampal CA1 neurons (basal dendrites, -11.2%; apical dendrites, -9.6%) and in retrospenial granular b cortex (Rgb) neurons (apical dendrites, -20.1%) together with spatial memory deficits on cross maze and radial-arm maze tasks. Additional rats with ATN lesions were also shown to display a severe deficit on spatial working memory in the cross-maze, but subsequent enriched housing ameliorated their performance on both this task and the radial-arm maze. These enriched rats with ATN lesions also showed recovery of both basal and apical CA1 spine density to levels comparable to that of the standard-housed controls, but no recovery of Rgb spine density. Inspection of spine types in the CA1 neurons showed that ATN lesions reduced the density of thin spines and mushroom spines, but not stubby spines; while enrichment promoted recovery of thin spines. Comparison with enriched rats that received pseudo-training, which provided comparable task-related experience, but no explicit spatial memory training, suggested that basal CA1 spine density in particular was associated with spatial learning and memory performance. Distal pathology in terms of reduced integrity of hippocampal and retrosplenial microstructure provides clear support for the influence of the ATN lesions on the extended hippocampal system. The reversal by postoperative enrichment of this deficit in the hippocampus but not the retrosplenial cortex may indicate region-specific mechanisms of recovery after ATN injury.

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“…Since the changes in dendritic spines may be a major cause of learning and memory impairment [15], [16], [17], we analyzed dendritic spine density in Golgi-stained neurons in the hippocampus and prefrontal cortex (PFC). In our study, Golgi staining was observed in the dendritic shafts and spines on secondary and tertiary dendrites of pyramidal neurons from layer II/III of the PFC (Figure 2A) and hippocampus (Figure 2B).…”

Section: Resultsmentioning

confidence: 99%

ZiBuPiYin Recipe Protects db/db Mice from Diabetes-Associated Cognitive Decline through Improving Multiple Pathological Changes

et al. 2014

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Multiple organ systems, including the brain, which undergoes changes that may increase the risk of cognitive decline, are adversely affected by diabetes mellitus (DM). Here, we demonstrate that type 2 diabetes mellitus (T2DM) db/db mice exhibited hippocampus-dependent memory impairment, which might associate with a reduction in dendritic spine density in the pyramidal neurons of brain, Aβ1-42 deposition in the prefrontal cortex (PFC) and hippocampus, and a decreased expression of neurostructural proteins including microtubule-associated protein (MAP2), a marker of dendrites, and postsynaptic density 95 (PSD95), a marker of excitatory synapses. To investigate the effects of the ZiBuPiYin recipe (ZBPYR), a traditional Chinese medicine recipe, on diabetes-related cognitive decline (DACD), db/db mice received daily administration of ZBPYR over an experimental period of 6 weeks. We then confirmed that ZBPYR rescued learning and memory performance impairments, reversed dendritic spine loss, reduced Aβ1-42 deposition and restored the expression levels of MAP2 and PSD95. The present study also revealed that ZBPYR strengthened brain leptin and insulin signaling and inhibited GSK3β overactivity, which may be the potential mechanism or underlying targets of ZBPYR. These findings conclude that ZBPYR prevents DACD, most likely by improving dendritic spine density and attenuating brain leptin and insulin signaling pathway injury. Our findings provide further evidence for the effects of ZBPYR on DACD.

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Changes in the plastic properties of hippocampal dendritic spines underlie the attenuation of place learning in healthy aged rats

Cited by 31 publications

References 57 publications

Activity-dependent structural plasticity of Purkinje cell spines in cerebellar vermis and hemisphere

Activity-dependent structural plasticity of Purkinje cell spines in cerebellar vermis and hemisphere

Anterior thalamic lesions reduce spine density in both hippocampal CA1 and retrosplenial cortex, but enrichment rescues CA1 spines only

ZiBuPiYin Recipe Protects db/db Mice from Diabetes-Associated Cognitive Decline through Improving Multiple Pathological Changes

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