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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 cages1,2. 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.

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Figure 1: Chronic optical imaging of functional whisker representations through the intact skull.
Figure 2: Plasticity of functional whisker representations.
Figure 3: Receptive field plasticity in layer II/III but not IV.
Figure 4: Characterizing morphological plasticity of the layer IV barrel field.

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Acknowledgements

We would like to thank L. Sininger, J. Rickert and C. Chen-Bee for assistance with data analysis and maintaining the naturalistic habitat, and D. Simmons and P. Yahr for their histology expertise. We would like to thank S. Bao, T. Carew, M. Leon, C. Moore, F. Strata and N. Weinberger for comments on the manuscript and M. Leon for suggestions on the use of a NH. This work was supported by National Institute of Health-National Institute of Neurological Disorders and Stroke grants to R.D.F.

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Correspondence to Daniel B. Polley.

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The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Figure 1

Design of a naturalistic habitat (NH). (JPG 128 kb)

Supplementary Text (DOC 25 kb)

Supplementary Figure 2

The C2 whisker representation is obtained before and after exposure to the SC or NH. (JPG 124 kb)

Supplementary Figure 3

Analysis of receptive fields in layer II/III and IV. (JPG 172 kb)

Supplementary Figure 4

The 25 barrels comprising the PMBSF and their septal separations are represented in a schematic matrix. (JPG 89 kb)

Supplementary Text for Figure 1 (DOC 24 kb)

Supplementary Text for Figure 2 (DOC 25 kb)

Supplementary Text for Figure 3 (DOC 73 kb)

Supplementary Text for Figure 4 (DOC 52 kb)

Supplementary Legend for Figure 2 (DOC 24 kb)

Supplementary Legend for Figure 3 (DOC 25 kb)

Supplementary Legend for Figure 4 (DOC 23 kb)

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Polley, D., Kvašňák, E. & Frostig, R. Naturalistic experience transforms sensory maps in the adult cortex of caged animals. Nature 429, 67–71 (2004). https://doi.org/10.1038/nature02469

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