Role of feedforward geniculate inputs in the generation of orientation selectivity in the cat's primary visual cortex

Non technical summary  Neurones of the mammalian primary visual cortex have the remarkable property of being selective for the orientation of visual contours. It has been controversial whether this selectivity arises purely from mechanisms within the cortex itself, from the special way afferents from the thalamus project to the cortex or from the sharpening of a bias for orientation that already exists in the retina and the thalamus. Our experiments support the last of these three hypotheses. We used a special protocol to study both inhibitory and excitatory interactions within the cortex as well as in the thalamus and we find that the orientation selectivity may depend upon multiple mechanisms – including the thalamic biases for orientation and intracortical inhibition and excitation.

[1]  N. Logothetis,et al.  The effects of electrical microstimulation on cortical signal propagation , 2010, Nature Neuroscience.

[2]  J Bullier,et al.  Receptive-field transformations between LGN neurons and S-cells of cat-striate cortex. , 1982, Journal of neurophysiology.

[3]  T R Vidyasagar,et al.  Dynamics of the orientation tuning of postsynaptic potentials in the cat visual cortex , 1995, Visual Neuroscience.

[4]  S. Sherman,et al.  Postsynaptic potentials recorded in neurons of the cat's lateral geniculate nucleus following electrical stimulation of the optic chiasm. , 1988, Journal of neurophysiology.

[5]  K. Tanaka Cross-correlation analysis of geniculostriate neuronal relationships in cats. , 1983, Journal of neurophysiology.

[6]  Matteo Carandini,et al.  Melting the Iceberg: Contrast Invariance in Visual Cortex , 2007, Neuron.

[7]  T R Vidyasagar,et al.  Response of neurons in the cat's lateral geniculate nucleus to moving bars of different length , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  A. Sillito,et al.  A re-evaluation of the mechanisms underlying simple cell orientation selectivity , 1980, Brain Research.

[9]  O. Creutzfeldt,et al.  An intracellular analysis of visual cortical neurones to moving stimuli: Responses in a co-operative neuronal network , 2004, Experimental Brain Research.

[10]  Trichur Raman Vidyasagar,et al.  A model of striate response properties based on geniculate anisotropies , 2004, Biological Cybernetics.

[11]  R. Reid,et al.  Rules of Connectivity between Geniculate Cells and Simple Cells in Cat Primary Visual Cortex , 2001, The Journal of Neuroscience.

[12]  M. J. Friedlander,et al.  Morphology of functionally identified neurons in lateral geniculate nucleus of the cat. , 1981, Journal of neurophysiology.

[13]  J. P. Jones,et al.  The two-dimensional spatial structure of simple receptive fields in cat striate cortex. , 1987, Journal of neurophysiology.

[14]  R. Shapley,et al.  Orientation Selectivity in Macaque V1: Diversity and Laminar Dependence , 2002, The Journal of Neuroscience.

[15]  Nuno Maçarico da Costa,et al.  The proportion of synapses formed by the axons of the lateral geniculate nucleus in layer 4 of area 17 of the cat , 2009, The Journal of comparative neurology.

[16]  Trichur Raman Vidyasagar,et al.  A linear model fails to predict orientation selectivity of cells in the cat visual cortex. , 1996, The Journal of physiology.

[17]  M. Carandini,et al.  Summation and division by neurons in primate visual cortex. , 1994, Science.

[18]  R. Shapley,et al.  New perspectives on the mechanisms for orientation selectivity , 1997, Current Opinion in Neurobiology.

[19]  D. Ferster,et al.  Strength and Orientation Tuning of the Thalamic Input to Simple Cells Revealed by Electrically Evoked Cortical Suppression , 1998, Neuron.

[20]  E. Todorov,et al.  A local circuit approach to understanding integration of long-range inputs in primary visual cortex. , 1998, Cerebral cortex.

[21]  J. Alonso,et al.  Population receptive fields of ON and OFF thalamic inputs to an orientation column in visual cortex , 2011, Nature Neuroscience.

[22]  Trichur Raman Vidyasagar Subcortical mechanisms in orientation sensitivity of cat visual cortical cells , 1992, Neuroreport.

[23]  D. Whitteridge,et al.  An intracellular analysis of the visual responses of neurones in cat visual cortex. , 1991, The Journal of physiology.

[24]  R. Reid,et al.  The spatial receptive field of thalamic inputs to single cortical simple cells revealed by the interaction of visual and electrical stimulation , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Trichur Raman Vidyasagar,et al.  Geniculate orientation biases seen with moving sine wave gratings: implications for a model of simple cell afferent connectivity , 2004, Experimental Brain Research.

[26]  D. Ferster Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  M. Stryker,et al.  Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  T. Wiesel,et al.  Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  I. Ohzawa,et al.  Linear and nonlinear contributions to orientation tuning of simple cells in the cat's striate cortex , 1999, Visual Neuroscience.

[30]  W. Levick,et al.  Orientation bias of cat retinal ganglion cells , 1980, Nature.

[31]  D. Ferster,et al.  Prediction of Orientation Selectivity from Receptive Field Architecture in Simple Cells of Cat Visual Cortex , 2001, Neuron.

[32]  Dario L Ringach,et al.  You get what you get and you don't get upset , 2011, Nature Neuroscience.

[33]  P. O. Bishop,et al.  Spatial summation of responses in receptive fields of single cells in cat striate cortex , 1978, Experimental Brain Research.

[34]  Trichur Raman Vidyasagar,et al.  Receptive field analysis and orientation selectivity of postsynaptic potentials of simple cells in cat visual cortex , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  Levin Kuhlmann,et al.  A Computational Study of How Orientation Bias in the Lateral Geniculate Nucleus Can Give Rise to Orientation Selectivity in Primary Visual Cortex , 2011, Front. Syst. Neurosci..

[36]  Trichur Raman Vidyasagar,et al.  Effect of bicuculine on the length-response functions of cat striate cortical-cells. , 1985 .

[37]  Nicholas J. Priebe,et al.  The Emergence of Contrast-Invariant Orientation Tuning in Simple Cells of Cat Visual Cortex , 2007, Neuron.

[38]  Ning Qian,et al.  Comparison among some models of orientation selectivity. , 2006, Journal of neurophysiology.

[39]  U. Eysel,et al.  Evidence for a contribution of lateral inhibition to orientation tuning and direction selectivity in cat visual cortex: reversible inactivation of functionally characterized sites combined with neuroanatomical tracing techniques , 1998, The European journal of neuroscience.

[40]  B. B. Lee,et al.  The retinal input to cells in area 17 of the cat's cortex , 1977, Experimental Brain Research.

[41]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[42]  J. B. Levitt,et al.  Circuits for Local and Global Signal Integration in Primary Visual Cortex , 2002, The Journal of Neuroscience.

[43]  M. Ito,et al.  Functional synaptic organization of primary visual cortex neurones in the cat , 2004, Experimental Brain Research.

[44]  R. Reid,et al.  Specificity of monosynaptic connections from thalamus to visual cortex , 1995, Nature.

[45]  R. Shapley,et al.  Effect of stimulus size on the dynamics of orientation selectivity in Macaque V1. , 2005, Journal of neurophysiology.

[46]  A. Leventhal,et al.  Organized arrangement of orientation-sensitive relay cells in the cat's dorsal lateral geniculate nucleus , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  D. Ferster,et al.  An intracellular analysis of geniculo‐cortical connectivity in area 17 of the cat. , 1983, The Journal of physiology.

[48]  Trichur Raman Vidyasagar,et al.  Orientation sensitivity of cat LGN neurones with and without inputs from visual cortical areas 17 and 18 , 2004, Experimental Brain Research.