Elsevier

Neuroscience

Volume 199, 29 December 2011, Pages 143-152
Neuroscience

Cognitive, Behavioral, and Systems Neuroscience
Research Paper
Synapse formation in adult barrel cortex following naturalistic environmental enrichment

https://doi.org/10.1016/j.neuroscience.2011.10.040Get rights and content

Abstract

Environmental enrichment paradigms in adult laboratory animals, consisting of physical, perceptual, and social stimulation, have been shown to affect synapse and cell morphology in sensory cortex and enhance learning ability, whereas enrichment, which is in harmony with the animal's natural habitat may have even greater implications for plasticity. Previous studies in our laboratory have shown that whisker stimulation induced the formation of synapses and spines in the corresponding barrel. In the present study adult C57/Bl6J female laboratory mice at 6 weeks of age were placed during 2 months in a protected enrichment enclosure in a forest clearing at the Chisti Les Biological Station, Tvier, Russia. We analyzed neuropil ultrastructure in the C2 barrel using serial-section electron microscopy on a total of eight mice (n=4 enriched, n=4 standard cagemate controls). Quantitative analyses of volumes of neuropil showed a significant increase in excitatory and inhibitory synapses on spines and excitatory synapses on dendritic shafts in the C2 barrel in the enriched group compared with standard cagemate controls. These results demonstrate that naturalistic experience alters the synaptic circuitry in layer IV of the somatosensory cortex, the first cortical relay of sensory information, leaving a lasting trace that may guide subsequent behavior.

Graphical Abstract

Laboratory mice that were placed in a naturalistic environment for two month show signs of synapse formation in the part of the cerebral cortex where sensory stimuli from their whiskers are processed. This study provides evidence that increased sensory experience alters cortical neuronal circuits in a specific manner and underlines the dynamic nature of the adult central nervous system.

Highlights

▶We studied neuronal plasticity induced by a naturalistic environment in adult mice. ▶Synapses were analyzed at the electron microscopic level 2 months after enrichment. ▶Excitatory and inhibitory synapse densities increased in enriched versus controls. ▶Sensory activation modifies cortical circuits in the adult somatosensory cortex. ▶Naturalistic whisker stimulation alters sensory processing in barrel cortex.

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Section snippets

Animals

A total of 18, 6-week-old C57/Bl6J adult female mice were supplied by the “Stolbovaya” laboratory animal farm of the Russian Medical Academy of Sciences (RMAS). Upon arrival to the Chisti Les (“clear forest”) Biological Station (director: V.V. Pazhetnov), in Pozhnia Tvier Region in Russia, mice adapted for 1 week in standard mouse cages in the animal facility. This station is located 400 km west of Moscow and 400 km south of St. Petersburg (Lat 56.735474°; Long. 31.526772°).

Environmental enrichment

Twelve mice were

Morphometric analysis of synaptic density

For densities of excitatory and inhibitory synapses on spines and on dendritic shafts, differences in means between enriched (mean±SD: 1.887 per μm3±0.12) and control groups (mean±SD: 1.421 per μm3±0.17) were significant [MANOVA; F(4,3)=15.58, P=0.024]. The density of the total of all synapses (including excitatory and inhibitory synapses on spines and on the dendritic shaft) in the C2 barrel of the enriched group was significantly higher in the enriched group compared with the control group

Discussion

Environmental enrichment paradigms in the laboratory have been widely effective at modifying brain structure with lasting effects on synapses and spines in adult visual cortex (Connor et al., 1980, Diamond and Connor, 1983, Briones et al., 2004). In the present study, morphometric analyses performed on volumes of neuropil within the C2 barrel in adult somatosensory cortex found that the density of synapses, including inhibitory and excitatory synapses on shaft and spine, increased following an

Conclusions

In conclusion, layer IV of the somatosensory cortex is plastic not only when neurons are challenged in the laboratory (whisker stimulation, classical conditioning) but also when they are exposed to an enriched environment. Together these observations strengthen the notion that adult mice can modify their layer IV circuitry well beyond the critical period for barrel formation. Future work may study the links between whisker behavior in the natural environment, whisker cortical pathways, and

Acknowledgments

This work was supported by grants from the Swiss National Science Foundation (31003A_125379, 3100A0-108446 H.P.L.) and SCOPES 111081 to H.-P.L. and we are all very grateful to NCCR “Neural Plasticity and Repair.” We also thank Caroline Musetti, Rudolf Kraftsik, Nathalie Wenger and Christel Genoud for their valuable assistance at each step in EM, data analysis, statistics and discussion.

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