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

Nature volume 429, pages 67–71 (2004)Cite this article

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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References

  1. Buonomano, D. V. & Merzenich, M. M. Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci. 21, 149–186 (1998)

    Article  CAS  Google Scholar 

  2. Kaas, J. H. in The New Cognitive Neurosciences (ed. Gazzaniga, M. S.) 223–236 (MIT Press, Cambridge, Massachusetts, 2000)

    Google Scholar 

  3. Polley, D. B., Chen-Bee, C. H. & Frostig, R. D. Two directions of plasticity in the sensory-deprived adult cortex. Neuron 24, 623–637 (1999)

    Article  CAS  Google Scholar 

  4. Simons, D. J. & Land, P. W. Early experience of tactile stimulation influences organization of somatic sensory cortex. Nature 326, 694–697 (1987)

    Article  ADS  CAS  Google Scholar 

  5. Fox, K. A critical period for experience-dependent synaptic plasticity in rat barrel cortex. J. Neurosci. 12, 1826–1838 (1992)

    Article  CAS  Google Scholar 

  6. Diamond, M. E., Armstrong-James, M. & Ebner, F. F. Experience-dependent plasticity in adult rat barrel cortex. Proc. Natl Acad. Sci. USA 90, 2082–2086 (1993)

    Article  ADS  CAS  Google Scholar 

  7. Glazewski, S. & Fox, K. Time course of experience-dependent synaptic potentiation and depression in barrel cortex of adolescent rats. J. Neurophysiol. 75, 1714–1729 (1996)

    Article  CAS  Google Scholar 

  8. Kossut, M., Hand, P. J., Greenberg, J. & Hand, C. L. Single vibrissal cortical column in SI cortex of rat and its alterations in neonatal and adult vibrissa-deafferented animals: a quantitative 2DG study. J. Neurophysiol. 60, 829–852 (1988)

    Article  CAS  Google Scholar 

  9. Woolsey, T. A. & Van der Loos, H. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res. 17, 205–242 (1970)

    Article  CAS  Google Scholar 

  10. Van der Loos, H. & Woolsey, T. A. Somatosensory cortex: structural alterations following early injury to sense organs. Science 179, 395–398 (1973)

    Article  ADS  CAS  Google Scholar 

  11. Jeanmonod, D., Rice, F. L. & Van der Loos, H. Mouse somatosensory cortex: alterations in the barrel field following receptor injury at different early postnatal ages. Neuroscience 6, 1503–1535 (1981)

    Article  CAS  Google Scholar 

  12. Bennett, E. L., Diamond, M. C., Krech, D. & Rosenzweig, M. R. Chemical and anatomical plasticity of brain. Science 146, 610–619 (1964)

    Article  ADS  CAS  Google Scholar 

  13. Uylings, H. B., Kuypers, K., Diamond, M. C. & Veltman, W. A. Effects of differential environments on plasticity of dendrites of cortical pyramidal neurons in adult rats. Exp. Neurol. 62, 658–677 (1978)

    Article  CAS  Google Scholar 

  14. Green, E. J., Greenough, W. T. & Schlumpf, B. E. Effects of complex or isolated environments on cortical dendrites of middle-aged rats. Brain Res. 264, 233–240 (1983)

    Article  CAS  Google Scholar 

  15. Land, P. W. & Simons, D. J. Cytochrome oxidase staining in the rat SmI barrel cortex. J. Comp. Neurol. 238, 225–235 (1985)

    Article  CAS  Google Scholar 

  16. Fanselow, E. E. & Nicolelis, M. A. Behavioural modulation of tactile responses in the rat somatosensory system. J. Neurosci. 19, 7603–7616 (1999)

    Article  CAS  Google Scholar 

  17. Castro-Alamancos, M. A. Role of thalamocortical sensory suppression during arousal: focusing sensory inputs in neocortex. J. Neurosci. 22, 9651–9655 (2002)

    Article  CAS  Google Scholar 

  18. Castro-Alamancos, M. A. & Oldford, E. Cortical sensory suppression during arousal is due to the activity-dependent depression of thalamocortical synapses. J. Physiol. (Lond.) 541, 319–331 (2002)

    Article  CAS  Google Scholar 

  19. Beaulieu, C. & Cynader, M. Effect of the richness of the environment on neurons in cat visual cortex. I. Receptive field properties. Brain Res. Dev. Brain Res. 53, 71–81 (1990)

    Article  CAS  Google Scholar 

  20. Coq, J. O. & Xerri, C. Environmental enrichment alters organizational features of the forepaw representation in the primary somatosensory cortex of adult rats. Exp. Brain Res. 121, 191–204 (1998)

    Article  CAS  Google Scholar 

  21. Welker, E., Rao, S. B., Dorfl, J., Melzer, P. & van der Loos, H. Plasticity in the barrel cortex of the adult mouse: effects of chronic stimulation upon deoxyglucose uptake in the behaving animal. J. Neurosci. 12, 153–170 (1992)

    Article  CAS  Google Scholar 

  22. Knott, G. W., Quairiaux, C., Genoud, C. & Welker, E. Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron 34, 265–273 (2002)

    Article  CAS  Google Scholar 

  23. Prakash, N., Cohen-Cory, S. & Frostig, R. D. Rapid and opposite effects of BDNF and NGF on the functional organization of the adult cortex in vivo. Nature 381, 702–706 (1996)

    Article  ADS  CAS  Google Scholar 

  24. Stern, E. A., Maravall, M. & Svoboda, K. Rapid development and plasticity of layer 2/3 maps in rat barrel cortex in vivo. Neuron 31, 305–315 (2001)

    Article  CAS  Google Scholar 

  25. Zarzecki, P. et al. Synaptic mechanisms of cortical representational plasticity: somatosensory and corticocortical EPSPs in reorganized raccoon SI cortex. J. Neurophysiol. 69, 1422–1432 (1993)

    Article  CAS  Google Scholar 

  26. Fox, K. The cortical component of experience-dependent synaptic plasticity in the rat barrel cortex. J. Neurosci. 14, 7665–7679 (1994)

    Article  CAS  Google Scholar 

  27. Frostig, R. D., Chen-Bee, C. H. & Polley, D. B. in In Vivo Optical Imaging of Brain Function (ed. Frostig, R. D.) 21–42 (CRC Press, Boca Raton, 2002)

    Book  Google Scholar 

  28. Chen-Bee, C. H. et al. Visualizing and quantifying evoked cortical activity assessed with intrinsic signal imaging. J. Neurosci. Methods 97, 157–173 (2000)

    Article  CAS  Google Scholar 

  29. Brett-Green, B., Chen-Bee, C. H. & Frostig, R. D. Comparing the functional representations of central and border whiskers in rat primary somatosensory cortex. J. Neurosci. 21, 9944–9954 (2001)

    Article  CAS  Google Scholar 

  30. Abeles, M. Quantification, smoothing, and confidence limits for single-units' histograms. J. Neurosci. Methods 5, 317–325 (1982)

    Article  CAS  Google Scholar 

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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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Author notes

  1. Daniel B. Polley

    Present address: Keck Center for Integrative Neuroscience, University of California, San Francisco, 513 Parnassus Avenue, San Francisco, California, 94143-0732, USA

Authors and Affiliations

  1. Department of Neurobiology and Behavior, University of California, Irvine, California, 92697-4550, USA

    Daniel B. Polley, Eugen Kvašňák & Ron D. Frostig

  2. Department of Biomedical Engineering, University of California, Irvine, California, 92697-4550, USA

    Ron D. Frostig

  3. The Center for the Neurobiology of Learning and Memory, University of California, Irvine, California, 92697-4550, USA

    Ron D. Frostig

Authors
  1. Daniel B. Polley
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Corresponding author

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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