On the anatomical basis of field size, contrast sensitivity, and orientation selectivity in macaque striate cortex: A model study
Neurons in layer 4C in macaque striate cortex show a differential change in receptive field size and achromatic contrast sensitivity with depth, and exhibit orientation selective responses in the upper 4Cα sublayer. Using a computational model we first demonstrate that the observed change in receptive field size and contrast sensitivity can arise from a differential convergence of afferents from the P and M subdivisions of the lateral geniculate nucleus onto layer 4C spiny stellate cells - if one postulates that the two anatomically identified M1 and M2 subpopulations of the M afferents differentially project to different depth in the 4Cα subdivision. Number ratios and response properties of both M subpopulations are predicted and may now be tested experimentally. We then show that realistic orientation selective responses in upper 4Cα can emerge intracortically as a result of local lateral interactions, which are anisotropic, between spiny stellate cells and inhibitory interneurons. The model assumes that orientation bias and tuning are generated by the same cortical circuits and predicts a receptive field dynamics with an initial non orientation specific response.
Unable to display preview. Download preview PDF.
- 1.G.G. Blasdel and D. Fitzpatrick. Physiological organization of layer 4 in macaque striate cortex. J. Neurosci., 4(3):880–895, 1984.Google Scholar
- 2.G.G. Blasdel and J.S. Lund. Termination of afferent axons in macaque striate cortex. J. Neurosci., 3:1389–1413, 1983.Google Scholar
- 3.U. T. Eysel, J. M. Crook, and H. F. Machemer. GABA-induced remote inactivation reveals cross-orientation inhibition in the cat striate cortex. Exp. Brain Res., 80:626–630, 1990.Google Scholar
- 4.M. J. Hawken and A. J. Parker. Contrast sensitivity and orientation selectivity in lamina iv of the striate cortex of old world monkeys. Exp. Brain. Res., 54:367–372, 1984.Google Scholar
- 5.J. S. Lund. Local circuit neurons of macaque monkey striate cortex: I. neurons of laminae 4C and 5A. J. Comp. Neurol., 257:60–92, 1987.Google Scholar
- 6.J. S. Lund, Q. Wu, P. T. Hadingham, and J. B. Levitt. Cells and circuits contributing to functional properties in area V1 macaque monkey cerebral cortex: Bases for neuroanatomically realistic models. J. Anatomy, 187:563–581, 1995.Google Scholar
- 7.S. Nelson, L. Toth, B. Sheth, and M. Sur. Orientation selectivity of cortical neurons during intracellular blockade of inhibition. Science, 265:774–777, 1994.Google Scholar
- 8.X. Pei, T. R. Vidyasagar, M. Volgushev, and O. D. Creutzfeld. Receptive field analysis and orientation selectivity of postsynaptic potentials of simple cells in cat visual cortex. J. Neurosci., 14:7130–7140, 1994.Google Scholar
- 9.H. Sato, N. Katsuyama, H. Tamura, Y. Hata, and T. Tsumoto. Mechanisms underlying orientation selectivity of neurons in the primary visual cortex of macaque. J. Physiol., 494:757–771, 1996.Google Scholar
- 10.G. Sclar and R. D. Freeman. Invariance of orientation tuning with stimulus contrast. Exp. Brain Res., 46:457–461, 1982.Google Scholar
- 11.D. C. Somers, S. B. Nelson, and M. Sur. An emergent model of orientation selectivity in cat visual cortical simple cells. J. Neurosci., 15:5448–65, 1995.Google Scholar
- 12.P.D. Spear, R.J. Moore, C.B.Y. Kim, J. Xue, and N. Tumosa. Effects on aging on primaten visual system: Spatial and temporal processing by lateral geniculate neurons in young adult and old rhesus monkeys. J. Neurophysiology, 72:402–420, 1994.Google Scholar
- 13.T. Yoshioka, J. B. Levitt, and J. S. Lund. Independence and merger of thalamocortical channels within macaque monkey primary visual cortex: anatomy of interlaminar projections. Vis. Neurosci., 11:467–489, 1994.Google Scholar