Abstract
Cortical areas are generally assumed to be uniform in their capacity for adaptive changes or plasticity1,2,3,4. Here we demonstrate, however, that neurons in the cat striate cortex (V1) show pronounced adaptation-induced short-term plasticity of orientation tuning primarily at specific foci. V1 neurons are clustered according to their orientation preference in iso-orientation domains5 that converge at singularities or pinwheel centres6,7. Although neurons in pinwheel centres have similar orientation tuning and responses to those in iso-orientation domains, we find that they differ markedly in their capacity for adaptive changes. Adaptation with an oriented drifting grating stimulus alters responses of neurons located at and near pinwheel centres to a broad range of orientations, causing repulsive shifts in orientation preference and changes in response magnitude. In contrast, neurons located in iso-orientation domains show minimal changes in their tuning properties after adaptation. The anisotropy of adaptation-induced orientation plasticity is probably mediated by inhomogeneities in local intracortical interactions that are overlaid on the map of orientation preference in V1.
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References
Gilbert, C. D. & Wiesel, T. N. Receptive field dynamics in adult primary visual cortex. Nature 356, 150–152 (1992).
Wang, X., Merzenich, M. M., Sameshima, K. & Jenkins, W. M. Remodelling of hand representation in adult cortex determined by timing of tactile stimulation. Nature 378, 71–75 (1995).
Fregnac, Y. & Shulz, D. E. Activity-dependent regulation of receptive field properties of cat area 17 by supervised Hebbian learning. J. Neurobiol. 41, 69–82 (1999).
Eysel, U. T. & Schweigart, G. Increased receptive field size in the surround of chronic lesions in the adult cat visual cortex. Cereb. Cortex 9, 101–109 (1999).
Hubel, D. H. & Wiesel, T. N. Sequence regularity and geometry of orientation columns in the monkey striate cortex. J. Comp. Neurol. 158, 267–293 (1974).
Bonhoeffer, T. & Grinvald, A. Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns. Nature 353, 429–431 (1991).
Blasdel, G. G. Differential imaging of ocular dominance and orientation selectivity in monkey striate cortex. J. Neurosci. 12, 3115–3138 (1992).
Das, A. & Gilbert, C. D. Topography of contextual modulations mediated by short-range interactions in primary visual cortex. Nature 399, 655–661 (1999).
Maldonado, P. E., Godecke, I., Gray, C. M. & Bonhoeffer, T. Orientation selectivity in pinwheel centers in cat striate cortex. Science 276, 1551–1555 (1997).
Hubel, D. H. & Wiesel, T. N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. 160, 106–154 (1962).
Reid, R. C. & Alonso, J. M. Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378, 281–284 (1995).
Ferster, D., Chung, S. & Wheat, H. Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 21, 249–252 (1996).
Somers, D. C., Nelson, S. B. & Sur, M. An emergent model of orientation selectivity in cat visual cortical simple cells. J. Neurosci. 15, 5448–5465 (1995).
Dragoi, V., Sharma, J. & Sur, M. Adaptation-induced plasticity of orientation tuning in adult visual cortex. Neuron 28, 287–298 (2000).
Hammond, P., Pomfrett, C. J. & Ahmed, B. Neural motion after-effects in the cat's striate cortex: orientation selectivity. Vision Res. 29, 1671–1683 (1989).
Saul, A. B. & Cynader, M. S. Adaptation in single units in visual cortex: the tuning of aftereffects in the spatial domain. Vis. Neurosci. 2, 593–607 (1989).
Dragoi, V., Sharma, J., Miller, E. K. M. & Sur, M. Dynamics of orientation adaptation in awake monkey V1 revealed by reverse correlation. Soc. Neurosci. Abstr. 25, 1548 (1999).
Muller, J. R., Metha, A. B., Krauskopf, J. & Lennie, P. Rapid adaptation in visual cortex to the structure of images. Science 285, 1405–1408 (1999).
Hata, Y., Tsumoto, T., Sato, H. & Tamura, H. Horizontal interactions between visual cortical neurones studied by cross-correlation analysis in the cat. J. Physiol. 441, 593–614 (1991).
Weliky, M., Kandler, K., Fitzpatrick, D. & Katz, L. C. Patterns of excitation and inhibition evoked by horizontal connections in visual cortex share a common relationship to orientation columns. Neuron 15, 541–552 (1995).
Kisvarday, Z. F., Toth, E., Rausch, M. & Eysel, U. T. Orientation-specific relationship between populations of excitatory and inhibitory lateral connections in the visual cortex of the cat. Cereb. Cortex 7, 605–618 (1997).
Crair, M. C., Ruthazer, E. S., Gillespie, D. C. & Stryker, M. P. Ocular dominance peaks at pinwheel center singularities of the orientation map in cat visual cortex. J. Neurophysiol. 77, 3381–3385 (1997).
Hubener, M., Shoham, D., Grinvald, A. & Bonhoeffer, T. Spatial relationships among three columnar systems in cat area 17. J. Neurosci. 17, 9270–9284 (1997).
Isa, N. P., Trepel, C. & Stryker, M. P. Spatial frequency maps in cat visual cortex. J. Neurosci. 20, 8504–8514 (2000).
Sanchez-Vives, M. V., Nowak, L. G. & McCormick, D. A. Membrane mechanisms underlying contrast adaptation in cat area 17 in vivo. J. Neurosci. 20, 4267–4285 (2000).
Abbott, L. F., Varela, J. A., Sen, K. & Nelson, S. B. Synaptic depression and cortical gain control. Science 275, 220–224 (1997).
Dragoi, V. & Sur, M. Dynamic properties of recurrent inhibition in primary visual cortex: contrast and orientation dependence of contextual effects. J. Neurophysiol. 83, 1019–1030 (2000).
Somers, D. C., Dragoi, V. & Sur, M. in Cerebral Cortex: The Cat Primary Visual Cortex. (eds Peters, A. & Payne, B.)(Academic, San Diego, in the press).
Coppola, D. M., Purves, H. R., McCoy, A. N. & Purves, D. The distribution of oriented contours in the real world. Proc. Natl Acad. Sci. USA 95, 4002–4006 (1998).
Wörgötter, F. & Eysel, U. T. Correlations between directional and orientational tuning of cells in cat striate cortex. Exp. Brain Res. 83, 665–669 (1991).
Acknowledgements
We thank J. Schummers for discussions. This work was supported by a Merck Fellowship (V.D.) and by grants from the NIH (M.S.).
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Dragoi, V., Rivadulla, C. & Sur, M. Foci of orientation plasticity in visual cortex. Nature 411, 80–86 (2001). https://doi.org/10.1038/35075070
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DOI: https://doi.org/10.1038/35075070
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