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

Abstract

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.

The impact of early environmental interventions on structural plasticity of the axon initial segment in neocortex

“…Previous studies on the effects of EE on structural plasticity refer mainly to spine density and dendritic tree complexity (Berardi et al, 2015;De Bartolo, Florenzano, Burello, Gelfo, & Petrosini, 2015;Leggio et al, 2005). Here, we demonstrate that EE also affects structural plasticity of the AIS.…”

“…The positive beneficial effects of EE on brain synaptic plasticity and behavior have been known for decades (Berardi et al, ). Previous studies on the effects of EE on structural plasticity refer mainly to spine density and dendritic tree complexity (Berardi et al, ; De Bartolo, Florenzano, Burello, Gelfo, & Petrosini, ; Leggio et al, ). Here, we demonstrate that EE also affects structural plasticity of the AIS.…”

Different types of multiple‐synapse boutons in the cerebellar cortex between physically enriched and ataxic mutant mice

“…To test whether EE, a more natural brain stimulating paradigm involving motor skill acquisition, can also produce PF MSBs in the cerebellar cortex of mice, we estimated synaptic density in a series of consecutive electron microscopic images using the physical disector method. Consistent with a recent study (De Bartolo et al, ), we found a significant increase in the number of PF‐to‐Purkinje cell synapses per unit volume in enriched mice compared to control animals (Control, 0.63 ± 0.02/μm 3 ; EE, 0.83 ± 0.02/μm 3 ; Student t ‐test, p < .0001, n = 5 animals per group) (Figure c). PF‐to‐Purkinje cell synapses were further classified as SSBs contacting only one spine and MSBs contacting more than two spines.…”

“…Animals were maintained at room temperature and humidity with a 12‐h light: 12‐h dark cycle. The EE group was housed with wheels, tunnels, plastic tires, platforms, and wooden toy houses, according to the procedure specified in the previous report (De Bartolo et al, ) with a slight modification (Figure b). All animal experiments are in compliance with the guidelines for Korea University Institutional Animal Care & Use Committee (KUIACUC‐2011‐222).…”

“…A number of studies have shown that hippocampal or cortical neurons in rodents raised in an enriched environment have more synapses per neuron, higher spine density, and increased dendritic complexity compared to control animals (Leuner & Gould, 2010;Nithianantharajah & Hannan, 2006). Similarly, a recent study demonstrated that spine density and size (head diameter, length, and area) in the distal dendrites of Purkinje cells were also higher in the enriched animals (De Bartolo, Florenzano, Burello, Gelfo, & Petrosini, 2015). Despite strong evidence of PF MSB formation following motor skill training, the EE effect on MSB formation in the cerebellar cortex has not been described.…”