Naturalistic experience transforms sensory maps in the adult cortex of caged animals

Abstract

Much of what is known about the functional organization and plasticity of adult sensory cortex is derived from animals housed in standard laboratory cages. Here we report that the transfer of adult rats reared in standard laboratory cages to a naturalistic habitat modifies the functional and morphological organization of the facial whisker representation in the somatosensory 'barrel' cortex. Cortical whisker representations, visualized with repeated intrinsic signal optical imaging in the same animals, contracted by 46% after four to six weeks of exposure to the naturalistic habitat. Acute, multi-site extracellular recordings demonstrated suppressed evoked neuronal responses and smaller, sharper constituent receptive fields in the upper cortical layers (II/III), but not in the thalamic recipient layer (IV), of rats with naturalistic experience. Morphological plasticity of the layer IV barrel field was observed, but on a substantially smaller scale than the functional plasticity. Thus, transferring animals to an environment that promotes the expression of natural, innate behaviours induces a large-scale functional refinement of cortical sensory maps.

Plasticity in primary somatosensory cortex resulting from environmentally enriched stimulation and sensory discrimination training

“…Stimulation per se is inadequate. When appropriate conditions of behavioral context are not met, no change, or even negative changes, may be the result (Welker et al, 1992;Polley, 2004). These findings substantially differ from the changes produced by behaviorally relevant stimulation versus deprivation in our study (See Figure 3).…”

“…These results are in striking contradistinction to studies by Polley et al (2004), who recorded significant reductions in electrophysiologically recorded receptive field sizes and in the areas of cortex activated during optical imaging by stimulation of any single vibrissa, in animals that were maintained in an enriched environment with all vibrissae intact. Differences in outcomes strongly support the argument that the changes in CR that we report here were a product of competitive Hebbian network plasticity (Hebb, 1949).…”

“…By that interpretation, the dramatic enlargement of the representations of intact, behaviorally-engaged vibrissae is attributable to their competitive dominance over the inactive, surrounding short vibrissae. In the study of Polley et al (2004), vibrissae also compete for territorial domination, but with all competitors intact, the effect of behavioral engagement is the progressive refinement (not enlargement) of selective cortical representations.…”

Large-scale reorganization of the tonotopic map in mouse auditory midbrain revealed by MRI

“…Previous studies have shown that the rearing environment profoundly influences neuronal coding properties recorded in the visual, auditory, somatosensory, and olfactory cortices (1)(2)(3)(4)(5)(6)(7)(8)(9). In the central auditory pathway, most ascending projections from the lower brainstem nuclei terminate in the inferior colliculus (IC), and this structure is the principal conduit of ascending projections to the thalamus.…”

The contribution of active body movement to visual development in evolutionary robots

“…The authors showed that human subjects could develop visually-guided behavior capabilities only if they were allowed to manipulate the camera by themselves, and that if someone moves the camera for them, they just sense a noisy stream of inputs, but no "visual" perception. Furthermore, it was demonstrated that active exploration in a naturalistic environment had a powerful impact on the expression of plasticity in whisker-deprived adult rats (Polley et al, 1999(Polley et al, , 2004. These results suggest that the development of the visual system largely depends not only on the characteristics of the visual field but also on the behavior of the perceivers.…”