Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Prior experience enhances plasticity in adult visual cortex

Abstract

The brain has a remarkable capacity to adapt to alterations in its sensory environment, which is normally much more pronounced in juvenile animals. Here we show that in adult mice, the ability to adapt to changes can be improved profoundly if the mouse has already experienced a similar change in its sensory environment earlier in life. Using the standard model for sensory plasticity in mouse visual cortex—ocular dominance (OD) plasticity—we found that a transient shift in OD, induced by monocular deprivation (MD) earlier in life, renders the adult visual cortex highly susceptible to subsequent MD many weeks later. Irrespective of whether the first MD was experienced during the critical period (around postnatal day 28) or in adulthood, OD shifts induced by a second MD were faster, more persistent and specific to repeated deprivation of the same eye. The capacity for plasticity in the mammalian cortex can therefore be conditioned by past experience.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Retinotopic mapping of mouse binocular visual cortex using optical imaging of intrinsic signals.
Figure 2: MD during the critical period facilitates OD plasticity in adult mice.
Figure 3: OD plasticity in adult visual cortex can be assessed reliably with intrinsic signal imaging and electrophysiology.
Figure 4: Previous MD in adult mice facilitates subsequent OD plasticity.
Figure 5: Facilitatory effect of repeated MD is eye specific.

Similar content being viewed by others

References

  1. Knudsen, E.I. Instructed learning in the auditory localization pathway of the barn owl. Nature 417, 322–328 (2002).

    Article  CAS  Google Scholar 

  2. McGonigle, B.O. & Flook, J. Long-term retention of single and multistate prismatic adaptation by humans. Nature 272, 364–366 (1978).

    Article  CAS  Google Scholar 

  3. Krakauer, J.W., Ghez, C. & Ghilardi, M.F. Adaptation to visuomotor transformations: consolidation, interference, and forgetting. J. Neurosci. 25, 473–478 (2005).

    Article  CAS  Google Scholar 

  4. Kuhl, P.K. Early language acquisition: cracking the speech code. Nat. Rev. Neurosci. 5, 831–843 (2004).

    Article  CAS  Google Scholar 

  5. Knudsen, E.I. Capacity for plasticity in the adult owl auditory system expanded by juvenile experience. Science 279, 1531–1533 (1998).

    Article  CAS  Google Scholar 

  6. DeBello, W.M., Feldman, D.E. & Knudsen, E.I. Adaptive axonal remodeling in the midbrain auditory space map. J. Neurosci. 21, 3161–3174 (2001).

    Article  CAS  Google Scholar 

  7. Linkenhoker, B.A., der Ohe, C.G. & Knudsen, E.I. Anatomical traces of juvenile learning in the auditory system of adult barn owls. Nat. Neurosci. 8, 93–98 (2005).

    Article  CAS  Google Scholar 

  8. Wiesel, T.N. & Hubel, D.H. Single cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26, 1003–1017 (1963).

    Article  CAS  Google Scholar 

  9. Muir, D.W. & Mitchell, D.E. Visual resolution and experience: acuity deficits in cats following early selective visual deprivation. Science 180, 420–422 (1973).

    Article  CAS  Google Scholar 

  10. Shatz, C.J. & Stryker, M.P. Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation. J. Physiol. (Lond.) 281, 267–283 (1978).

    Article  CAS  Google Scholar 

  11. Mitchell, D.E., Cynader, M. & Movshon, J.A. Recovery from the effects of monocular deprivation in kittens. J. Comp. Neurol. 176, 53–63 (1977).

    Article  CAS  Google Scholar 

  12. Kind, P.C. et al. Correlated binocular activity guides recovery from monocular deprivation. Nature 416, 430–433 (2002).

    Article  CAS  Google Scholar 

  13. Liao, D.S., Krahe, T.E., Prusky, G.T., Medina, A.E. & Ramoa, A.S. Recovery of cortical binocularity and orientation selectivity after the critical period for ocular dominance plasticity. J. Neurophysiol. 92, 2113–2121 (2004).

    Article  Google Scholar 

  14. Dräger, U.C. Observations on monocular deprivation in mice. J. Neurophysiol. 41, 28–42 (1978).

    Article  Google Scholar 

  15. Gordon, J.A. & Stryker, M.P. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J. Neurosci. 16, 3274–3286 (1996).

    Article  CAS  Google Scholar 

  16. Grinvald, A., Lieke, E., Frostig, R.D., Gilbert, C.D. & Wiesel, T.N. Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 324, 361–364 (1986).

    Article  CAS  Google Scholar 

  17. Schuett, S., Bonhoeffer, T. & Hübener, M. Mapping retinotopic structure in mouse visual cortex with optical imaging. J. Neurosci. 22, 6549–6559 (2002).

    Article  CAS  Google Scholar 

  18. Kalatsky, V.A. & Stryker, M.P. New paradigm for optical imaging: temporally encoded maps of intrinsic signal. Neuron 38, 529–545 (2003).

    Article  CAS  Google Scholar 

  19. Frenkel, M.Y. & Bear, M.F. How monocular deprivation shifts ocular dominance in visual cortex of young mice. Neuron 44, 917–923 (2004).

    Article  CAS  Google Scholar 

  20. Sawtell, N.B. et al. NMDA receptor-dependent ocular dominance plasticity in adult visual cortex. Neuron 38, 977–985 (2003).

    Article  CAS  Google Scholar 

  21. Pham, T.A. et al. A semi-persistent adult ocular dominance plasticity in visual cortex is stabilized by activated CREB. Learn. Mem. 11, 738–747 (2004).

    Article  Google Scholar 

  22. Tagawa, Y., Kanold, P.O., Majdan, M. & Shatz, C.J. Multiple periods of functional ocular dominance plasticity in mouse visual cortex. Nat. Neurosci. 8, 380–388 (2005).

    Article  CAS  Google Scholar 

  23. Fagiolini, M. & Hensch, T.K. Inhibitory threshold for critical-period activation in primary visual cortex. Nature 404, 183–186 (2000).

    Article  CAS  Google Scholar 

  24. Yang, Y. et al. Reversible blockade of experience-dependent plasticity by calcineurin in mouse visual cortex. Nat. Neurosci. 8, 791–796 (2005).

    Article  CAS  Google Scholar 

  25. Cynader, M. & Mitchell, D.E. Prolonged sensitivity to monocular deprivation in dark-reared cats. J. Neurophysiol. 43, 1026–1040 (1980).

    Article  CAS  Google Scholar 

  26. Pizzorusso, T. et al. Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 1248–1251 (2002).

    Article  CAS  Google Scholar 

  27. Antonini, A., Fagiolini, M. & Stryker, M.P. Anatomical correlates of functional plasticity in mouse visual cortex. J. Neurosci. 19, 4388–4406 (1999).

    Article  CAS  Google Scholar 

  28. Mataga, N., Mizuguchi, Y. & Hensch, T.K. Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron 44, 1031–1041 (2004).

    Article  CAS  Google Scholar 

  29. Oray, S., Majewska, A. & Sur, M. Dendritic spine dynamics are regulated by monocular deprivation and extracellular matrix degradation. Neuron 44, 1021–1030 (2004).

    Article  CAS  Google Scholar 

  30. Hensch, T.K. Critical period regulation. Annu. Rev. Neurosci. 27, 549–579 (2004).

    Article  CAS  Google Scholar 

  31. Hübener, M. Mouse visual cortex. Curr. Opin. Neurobiol. 13, 413–420 (2003).

    Article  Google Scholar 

  32. Prusky, G.T. & Douglas, R.M. Developmental plasticity of mouse visual acuity. Eur. J. Neurosci. 17, 167–173 (2003).

    Article  Google Scholar 

Download references

Acknowledgements

We thank A. King for comments on the manuscript and M. Sperling for computing help. This work was supported by the Max Planck Society (S.B.H., T.D.M.-F., T.B. and M.H.) and the Alexander von Humboldt Foundation (T.D.M.-F.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mark Hübener.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hofer, S., Mrsic-Flogel, T., Bonhoeffer, T. et al. Prior experience enhances plasticity in adult visual cortex. Nat Neurosci 9, 127–132 (2006). https://doi.org/10.1038/nn1610

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1610

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing