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Potentiation of cortical inhibition by visual deprivation

Abstract

The fine-tuning of circuits in sensory cortex requires sensory experience during an early critical period. Visual deprivation during the critical period has catastrophic effects on visual function, including loss of visual responsiveness to the deprived eye1,2,3, reduced visual acuity4, and loss of tuning to many stimulus characteristics2,5. These changes occur faster than the remodelling of thalamocortical axons6, but the intracortical plasticity mechanisms that underlie them are incompletely understood. Long-term depression of excitatory intracortical synapses has been proposed as a general candidate mechanism for the loss of cortical responsiveness after visual deprivation7,8. Alternatively (or in addition), the decreased ability of the deprived eye to activate cortical neurons could be due to enhanced intracortical inhibition9,10. Here we show that visual deprivation leaves excitatory connections in layer 4 (the primary input layer to cortex) unaffected, but markedly potentiates inhibitory feedback between fast-spiking basket cells (FS cells) and star pyramidal neurons (star pyramids). Further, a previously undescribed form of long-term potentiation of inhibition (LTPi) could be induced at synapses from FS cells to star pyramids, and was occluded by previous visual deprivation. These data suggest that potentiation of inhibition is a major cellular mechanism underlying the deprivation-induced degradation of visual function, and that this form of LTPi is important in fine-tuning cortical circuitry in response to visual experience.

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Figure 1: VD between P18 and P21 has no effect on recurrent excitatory star pyramid connections.
Figure 2: VD potentiates feedback inhibition within layer 4.
Figure 3: VD suppresses spontaneous firing of star pyramids.
Figure 4: Inhibitory LTP at FS-cell to star-pyramid synapses is occluded by previous VD.

References

  1. 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  PubMed  Google Scholar 

  2. Fagiolini, M., Pizzorusso, T., Berardi, N., Domenici, L. & Maffei, L. Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vision Res. 34, 709–720 (1994)

    Article  CAS  PubMed  Google Scholar 

  3. 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  PubMed  Google Scholar 

  4. Prusky, G. T., West, P. W. & Douglas, R. M. Experience-dependent plasticity of visual acuity in rats. Eur. J. Neurosci. 116, 135–140 (2000)

    CAS  Google Scholar 

  5. White, L. E., Coppola, D. M. & Fitzpatrick, D. The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex. Nature 411, 1049–1052 (2001)

    Article  ADS  CAS  PubMed  Google Scholar 

  6. Antonini, A. & Stryker, M. P. Plasticity of geniculocortical afferents following brief or prolonged monocular occlusion in the cat. J. Comp. Neurol. 369, 64–82 (1996)

    Article  CAS  PubMed  Google Scholar 

  7. Rittenhouse, C. D., Shouval, H. Z., Paradiso, M. A. & Bear, M. F. Monocular deprivation induces homosynaptic long-term depression in visual cortex. Nature 397, 347–350 (1999)

    Article  ADS  CAS  PubMed  Google Scholar 

  8. Kirkwood, A., Rioult, M. C. & Bear, M. F. Experience-dependent modification of synaptic plasticity in visual cortex. Nature 381, 526–528 (1996)

    Article  ADS  CAS  PubMed  Google Scholar 

  9. Duffy, F. H., Burchfield, J. L. & Conway, J. L. Bicuculline reversal of deprivation ambylopia in the cat. Nature 260, 256–257 (1976)

    Article  ADS  CAS  PubMed  Google Scholar 

  10. Sillito, A. M., Kemp, J. A. & Blakemore, C. The role of GABAergic inhibition in the cortical effects of monocular deprivation. Nature 291, 318–320 (1981)

    Article  ADS  CAS  PubMed  Google Scholar 

  11. Rauschecker, J. P. Cortical map plasticity in animals and humans. Prog. Brain Res. 138, 73–88 (2002)

    Article  PubMed  Google Scholar 

  12. Barrett, B. T., Bradley, A. & McGraw, P. V. Understanding the neural basis of amblyopia. Neuroscientist 10, 106–117 (2004)

    Article  PubMed  Google Scholar 

  13. Maffei, A., Nelson, S. B. & Turrigiano, G. G. Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nature Neurosci. 7, 1353–1359 (2004)

    Article  CAS  PubMed  Google Scholar 

  14. Egger, V., Feldmeyer, D. & Sakmann, B. Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex. Nature Neurosci. 2, 1098–1105 (1999)

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  16. Hensch, T. K. Critical period plasticity in local cortical circuits. Nature Rev. Neurosci. 6, 877–888 (2005)

    Article  CAS  Google Scholar 

  17. Thomson, A. M., Bannister, A. P., Mercer, A. & Morris, O. T. Target and temporal pattern selection at neocortical synapses. Phil. Trans. R. Soc. Lond. B 357, 1781–1791 (2002)

    Article  Google Scholar 

  18. Gaiarsa, J. L., Caillard, O. & Ben-Ari, Y. Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance. Trends Neurosci. 25, 564–570 (2002)

    Article  CAS  PubMed  Google Scholar 

  19. Woodin, M. A., Ganguly, K. & Poo, M. M. Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl- transporter activity. Neuron 39, 807–820 (2003)

    Article  CAS  PubMed  Google Scholar 

  20. Holmgren, C. D. & Zilberter, Y. Coincident spiking activity induces long-term changes in inhibition of neocortical pyramidal cells. J. Neurosci. 21, 8270–8277 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Simons, D. J. Response properties of vibrissa units in rat S1 somatosensory neocortex. J. Neurophysiol. 41, 798–820 (1978)

    Article  CAS  PubMed  Google Scholar 

  22. Contreras, D. & Palmer, L. Response to contrast of electrophysiologically defined cell classes in primary visual cortex. J. Neurosci. 23, 6936–6945 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Buzas, P., Eysel, U. T., Adorjan, P. & Kisvarday, Z. F. Axonal topography of cortical basket cells in relation to orientation, direction and ocular dominance maps. J. Comp. Neurol. 473, 259–285 (2001)

    Article  Google Scholar 

  24. Gibson, J. R., Bierlein, M. & Connors, B. W. A network of electrically coupled inhibitory neurons in neocortex. Nature 402, 75–79 (1999)

    Article  ADS  CAS  PubMed  Google Scholar 

  25. Barlow, H. B. & Levick, W. R. The mechanism of directionally selective units in rabbits' retina. J. Physiol. 178, 477–504 (1965)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Schoppa, N. E. & Urban, N. N. Dendritic processing within olfactory bulb circuits. Trends Neurosci. 26, 501–506 (2003)

    Article  CAS  PubMed  Google Scholar 

  27. Kayser, A. S. & Miller, K. D. Opponent inhibition: a developmental model of layer 4 of the neocortical circuit. Neuron 33, 131–142 (2002)

    Article  CAS  PubMed  Google Scholar 

  28. Hirsch, J. A. et al. Functionally distinct inhibitory neurons at the first stage of visual cortical processing. Nature Neurosci. 6, 1300–1308 (2003)

    Article  CAS  PubMed  Google Scholar 

  29. Jin, X., Huguenard, J. R. & Prince, D. A. Impaired Cl- extrusion in layer V pyramidal neurons of chronically injured epileptogenic neocortex. J. Neurophysiol. 93, 2117–2126 (2005)

    Article  CAS  PubMed  Google Scholar 

  30. Kilman, V., van Rossum, M. C. & Turrigiano, G. G. Activity deprivation reduces miniature IPSC amplitude by decreasing the number of postsynaptic GABAA receptors clustered at neocortical synapses. J. Neurosci. 22, 1328–1337 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank R. Pavlyuk for help with histology, and A. Fontanini for help with software and for discussions. This study was supported by the National Institutes of Health.

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Correspondence to Gina G. Turrigiano.

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Maffei, A., Nataraj, K., Nelson, S. et al. Potentiation of cortical inhibition by visual deprivation. Nature 443, 81–84 (2006). https://doi.org/10.1038/nature05079

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