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:

Cortical reorganization consistent with spike timing–but not correlation-dependent plasticity

A Corrigendum to this article was published on 01 August 2007

This article has been updated

Abstract

The receptive fields of neurons in primary visual cortex that are inactivated by retinal damage are known to 'shift' to nondamaged retinal locations, seemingly due to the plasticity of intracortical connections. We have observed in cats that these shifts occur in a pattern that is highly convergent, even among receptive fields that are separated by large distances before inactivation. Here we show, using a computational model of primary visual cortex, that the observed convergent shifts are inconsistent with the common assumption that the underlying intracortical connection plasticity is dependent on the temporal correlation of pre- and postsynaptic action potentials. The shifts are, however, consistent with the hypothesis that this plasticity is dependent on the temporal order of pre- and postsynaptic action potentials. This convergent reorganization seems to require increased neuronal gain, revealing a mechanism that networks may use to selectively facilitate the didactic transfer of neuronal response properties.

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: Measurement and modeling of retinal lesion–induced receptive field reorganization in V1.
Figure 2: Shifts in receptive field location among neurons in the cortical lesion projection zone of five cats (KR1, KR2, KR4, KR5, KL12).
Figure 3: In vivo and simulated shifts of receptive field projected onto the representation of visual space in V1 (ref.36)
Figure 4: Convergence and divergence among the shifts of in vivo and simulated receptive fields.
Figure 5: Simulated reorganization of receptive fields in a symmetric lesion projection zone, dependent on the strength of neuronal gain and use of CDP or STDP.
Figure 6: Latency of peak responses among the lesion projection zone columns of the model during and after STDP-based reorganization.

Similar content being viewed by others

Change history

  • 11 July 2007

    In the version of this article initially published, the author omitted an acknowledgement in the list of acknowledgements at the end of the article. The authors would like to acknowledge financial support contributed by the Berlin Graduate School of Mind and Brain, Germany.

Notes

  1. *NOTE: In the version of this article initially published, the author omitted an acknowledgement in the list of acknowledgements at the end of the article. The authors would like to acknowledge financial support contributed by the Berlin Graduate School of Mind and Brain, Germany.

References

  1. Hubel, D.H. & Wiesel, T.N. Binocular interaction in striate cortex of kittens reared with artificial squint. J. Neurophysiol. 28, 1041–1059 (1965)

    Article  CAS  Google Scholar 

  2. Katz, L.C. & Shatz, C.J. Synaptic activity and the construction of cortical circuits. Science 274, 1133–1138 (1996).

    Article  CAS  Google Scholar 

  3. Hebb, D.O. The Organization of Behaviour (John Wiley & Sons, New York, 1949).

    Google Scholar 

  4. Stent, G.S. A physiological mechanism for Hebb's postulate of learning. Proc. Natl. Acad. Sci. USA 70, 997–1001 (1973).

    Article  CAS  Google Scholar 

  5. Malenka, R.C. & Nicoll, R.A. NMDA receptor–dependent synaptic plasticity: multiple forms and mechanisms. Trends Neurosci. 16, 521–527 (1993).

    Article  CAS  Google Scholar 

  6. Levy, W.B. & Steward, O. Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus. Neuroscience 8, 791–797 (1983).

    Article  CAS  Google Scholar 

  7. Markram, H., Lubke, J., Frotscher, M. & Sakmann, B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275, 213–215 (1997).

    Article  CAS  Google Scholar 

  8. Song, S., Miller, K.D. & Abbott, L.F. Competitive Hebbian learning through spike-timing–dependent synaptic plasticity. Nat. Neurosci. 3, 919–926 (2000).

    Article  CAS  Google Scholar 

  9. Sjöström, P.J., Turrigiano, G.G. & Nelson, S.B. Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32, 1149–1164 (2001).

    Article  Google Scholar 

  10. Froemke, R.C. & Dan, Y. Spike-timing–dependent synaptic modification induced by natural spike trains. Nature 416, 433–438 (2002).

    Article  CAS  Google Scholar 

  11. Dan, Y. & Poo, M.-M. Spike timing–dependent plasticity of neural pircuits. Neuron 44, 23–30 (2004).

    Article  CAS  Google Scholar 

  12. Pearson, J.C., Finkel, L.H. & Edelman, G.M. Plasticity in the organization of adult cerebral cortical maps: a computer simulation based on neuronal group selection. J. Neurosci. 7, 4209–4223 (1987).

    Article  CAS  Google Scholar 

  13. Obermayer, K., Ritter, H. & Schulten, K. A principle for the formation of the spatial structure of cortical feature maps. Proc. Natl. Acad. Sci. USA 87, 8345–8349 (1990).

    Article  CAS  Google Scholar 

  14. Hirsch, J.A. & Gilbert, C.D. Long-term changes in synaptic strength along specific intrinsic pathways in the cat visual cortex. J. Physiol. (Lond.) 461, 247–262 (1993).

    Article  CAS  Google Scholar 

  15. Xing, J. & Gerstein, G.L. Networks with lateral connectivity. 3. Plasticity and reorganization of somatosensory cortex. J. Neurophysiol. 75, 217–232 (1996).

    Article  CAS  Google Scholar 

  16. Miikkulainen, R., Bednar, J.A., Choe, Y. & Sirosh, J. Self-organization, plasticity and low-level visual phenomena in a laterally connected map model of the primary visual cortex. in Psychology of Learning and Motivation: Perceptual Learning (eds. Goldstone, R.L., Schyns, P.G. & Medin, D.L.) 257–308 (Academic Press, San Diego, 1997).

    Google Scholar 

  17. Feldman, D.E. Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 27, 45–56 (2000).

    Article  CAS  Google Scholar 

  18. Song, S. & Abbott, L.F. Cortical development and remapping through spike timing–dependent plasticity. Neuron 32, 339–350 (2001).

    Article  CAS  Google Scholar 

  19. Fu, Y.X. et al. Temporal specificity in the cortical plasticity of visual space representation. Science 296, 1999–2003 (2002).

    Article  CAS  Google Scholar 

  20. Eyding, D., Schweigart, G. & Eysel, U.T. Spatio-temporal plasticity of cortical receptive fields in response to repetitive visual stimulation in the adult cat. Neuroscience 112, 195–215 (2002).

    Article  CAS  Google Scholar 

  21. Celikel, T., Szostak, V.A. & Feldman, D.E. Modulation of spike timing by sensory deprivation during induction of cortical map plasticity. Nat. Neurosci. 7, 534–541 (2004).

    Article  CAS  Google Scholar 

  22. Meliza, C.D. & Dan, Y. Receptive-field modification in rat visual cortex induced by paired visual stimulation and single-cell spiking. Neuron 49, 183–189 (2006).

    Article  CAS  Google Scholar 

  23. Pettigrew, J.D. The effect of visual experience on the development of stimulus specificity by kitten cortical neurones. J. Physiol. (Lond.) 237, 49–74 (1974).

    Article  CAS  Google Scholar 

  24. Giannikopoulos, D.V. & Eysel, U.T. Dynamics and specificity of cortical map reorganization after retinal lesions. Proc. Natl. Acad. Sci. USA 103, 10805–10810 (2006).

    Article  CAS  Google Scholar 

  25. Olson, C.R. & Freeman, R.D. Profile of the sensitive period for monocular deprivation in kittens. Exp. Brain Res. 39, 17–21 (1980).

    CAS  Google Scholar 

  26. Kaas, J.H. et al. Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. Science 248, 229–231 (1990).

    Article  CAS  Google Scholar 

  27. Chino, Y. et al. Recovery of binocular responses by cortical neurons after early monocular lesions. Nat. Neurosci. 4, 689–690 (2001).

    Article  CAS  Google Scholar 

  28. Waleszczyk, W.J. et al. Laminar differences in plasticity in cat area 17 following retinal lesions in adolescence or adulthood. Eur. J. Neurosci. 17, 2351–2368 (2003).

    Article  CAS  Google Scholar 

  29. Fitzgibbon, T., Funke, K. & Eysel, U.T. Anatomical correlations between soma size, axon diameter and intraretinal length for the α ganglion cells of the cat retina. Vis. Neurosci. 6, 159–174 (1991).

    Article  CAS  Google Scholar 

  30. Calford, M.B., Schmid, L.M. & Rosa, M.G.P. Monocular focal retinal lesions induce short-term topographic plasticity in adult cat visual cortex. Proc. Biol. Soc. 266, 499–507 (1999).

    Article  CAS  Google Scholar 

  31. Calford, M.B. et al. Plasticity in adult cat visual cortex (area 17) following circumscribed monocular lesions of all retinal layers. J. Physiol. (Lond.) 524, 587–602 (2000).

    Article  CAS  Google Scholar 

  32. Gilbert, C.D. & Wiesel, T.N. Receptive field dynamics in adult primary visual cortex. Nature 356, 150–152 (1992).

    Article  CAS  Google Scholar 

  33. Darian-Smith, C. & Gilbert, C.D. Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated. J. Neurosci. 15, 1631–1647 (1995).

    Article  CAS  Google Scholar 

  34. Calford, M.B., Wright, L.L., Metha, A.B. & Taglianetti, V. Topographic plasticity in primary visual cortex is mediated by local corticocortical connections. J. Neurosci. 23, 6434–6442 (2003).

    Article  CAS  Google Scholar 

  35. Young, J.M., Waleszczyk, W.J., Burke, W., Calford, M.B. & Dreher, B. Topographic reorganization in area 18 of adult cats following circumscribed monocular retinal lesions in adolescence. J. Physiol. (Lond.) 541, 601–612 (2002).

    Article  CAS  Google Scholar 

  36. Tusa, R.J., Palmer, L.A. & Rosenquist, A.C. The retinotopic organization of area 17 (striate cortex) in the cat. J. Comp. Neurol. 177, 213–235 (1978).

    Article  CAS  Google Scholar 

  37. Tanifuji, M., Sugiyama, T. & Murase, K. Horizontal propagation of excitation in rat visual cortical slices revealed by optical imaging. Science 266, 1057–1059 (1994).

    Article  CAS  Google Scholar 

  38. Jancke, D., Chavane, F., Naaman, S. & Grinvald, A. Imaging cortical correlates of illusion in early visual cortex. Nature 428, 423–426 (2004).

    Article  CAS  Google Scholar 

  39. Chino, Y.M., Kaas, J.H., Smith, E.L., III, Langston, A.L. & Cheng, H. Rapid reorganization of cortical maps in adult cats following restricted deafferentation in retina. Vision Res. 32, 789–796 (1992).

    Article  CAS  Google Scholar 

  40. Turrigiano, G.G., Leslie, K.R., Desai, N.S., Rutherford, L.C. & Nelson, S.B. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391, 892–896 (1998).

    Article  CAS  Google Scholar 

  41. Desai, N.S., Cudmore, R.H., Nelson, S.B. & Turrigiano, G.G. Critical periods for experience-dependent synaptic scaling in visual cortex. Nat. Neurosci. 5, 783–789 (2002).

    Article  CAS  Google Scholar 

  42. Rutherford, L.C., Nelson, S.B. & Turrigiano, G.G. BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses. Neuron 21, 521–530 (1998).

    Article  CAS  Google Scholar 

  43. Arckens, L. et al. Cooperative changes in GABA, glutamate and activity levels: the missing link in cortical plasticity. Eur. J. Neurosci. 12, 4222–4232 (2000).

    Article  CAS  Google Scholar 

  44. Darian-Smith, C. & Gilbert, C.D. Axonal sprouting accompanies functional reorganization in adult cat striate cortex. Nature 368, 737–740 (1994).

    Article  CAS  Google Scholar 

  45. Trachtenberg, J.T. & Stryker, M.P. Rapid anatomical plasticity of horizontal connections in the developing visual cortex. J. Neurosci. 21, 3476–3482 (2001).

    Article  CAS  Google Scholar 

  46. Anderson, J.S., Carandini, M. & Ferster, D. Orientation tuning of input conductance, excitation and inhibition in cat primary visual cortex. J. Neurophysiol. 84, 909–926 (2000).

    Article  CAS  Google Scholar 

  47. Yoshimura, Y. & Callaway, E.M. Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity. Nat. Neurosci. 8, 1552–1559 (2005).

    Article  CAS  Google Scholar 

  48. Bringuier, V., Chavane, F., Glaeser, L. & Frégnac, Y. Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. Science 283, 695–699 (1999).

    Article  CAS  Google Scholar 

  49. Hirsch, J.A. & Gilbert, C.D. Synaptic physiology of horizontal connections in the cat's visual cortex. J. Neurosci. 11, 1800–1809 (1991).

    Article  CAS  Google Scholar 

  50. Colman, H., Nabekura, J. & Lichtman, J.W. Alterations in synaptic strength preceding axon withdrawal. Science 275, 356–361 (1997).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank W. Burke for participating in the experimental work; J.Y. Huang for participating in the control experiments; T. Hoch for modeling advice; and K. Wimmer, E. Mukamel, L. Schwabe, T. Hoch and R. Martin for manuscript comments. Support was contributed by the Australian Research Council, the Bernstein Center for Computational Neuroscience Berlin, the German Federal Ministry of Education and Research (BMBF, grant 10025304), and the German Academic Exchange Service (DAAD).*Footnote 1

Author information

Authors and Affiliations

Authors

Contributions

J.M.Y., W.J.W., C.W. and B.D. conducted the experimental work and analyzed the collected data. M.B.C. made the retinal lesions. B.D. and M.B.C. designed the experiments. K.O. supervised the modeling project, which included providing guidance on the choice of model type and advice on the model's abstractions. J.M.Y. conceived the modeling project and conducted the modeling work, which included developing the model's novel abstractions. The manuscript was drafted primarily by J.M.Y., but all the authors were actively involved in its refinement.

Corresponding authors

Correspondence to Joshua M Young or Klaus Obermayer.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Comparison of hand-plotting and automated estimates of receptive field location. (PDF 22 kb)

Supplementary Fig. 2

The correspondence between hand-plotted and automated estimates of receptive field location relative to the distance of estimated receptive field shifts. (PDF 14 kb)

Supplementary Fig. 3

Receptive field position shifts and orientation preference among in vivo neurons within the lesion projection zone. (PDF 22 kb)

Supplementary Fig. 4

Influence of neuronal gain on receptive field reorganization in simulations using spike timing-dependent plasticity. (PDF 128 kb)

Supplementary Methods (PDF 144 kb)

Supplementary Results (PDF 95 kb)

Supplementary Video 1

KR1 (AVI 1040 kb)

Supplementary Video 2

KR2 (AVI 939 kb)

Supplementary Video 3

KR4 (AVI 1425 kb)

Supplementary Video 4

KR5 (AVI 914 kb)

Supplementary Video 5

KL12 (AVI 1486 kb)

Supplementary Videos Legend (PDF 11 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Young, J., Waleszczyk, W., Wang, C. et al. Cortical reorganization consistent with spike timing–but not correlation-dependent plasticity. Nat Neurosci 10, 887–895 (2007). https://doi.org/10.1038/nn1913

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1913

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