Receptive field size and response latency are correlated within the cat visual thalamus.

Each point in visual space is encoded at the level of the thalamus by a group of neighboring cells with overlapping receptive fields. Here we show that the receptive fields of these cells differ in size and response latency but not at random. We have found that in the cat lateral geniculate nucleus (LGN) the receptive field size and response latency of neighboring neurons are significantly correlated: the larger the receptive field, the faster the response to visual stimuli. This correlation is widespread in LGN. It is found in groups of cells belonging to the same type (e.g., Y cells), and of different types (i.e., X and Y), within a specific layer or across different layers. These results indicate that the inputs from the multiple geniculate afferents that converge onto a cortical cell (approximately 30) are likely to arrive in a sequence determined by the receptive field size of the geniculate afferents. Recent studies have shown that the peak of the spatial frequency tuning of a cortical cell shifts toward higher frequencies as the response progresses in time. Our results are consistent with the idea that these shifts in spatial frequency tuning arise from differences in the response time course of the thalamic inputs.

[1]  Jonathan Stone,et al.  Hierarchical and parallel mechanisms in the organization of visual cortex , 1979, Brain Research Reviews.

[2]  S. Sherman,et al.  Organization of visual pathways in normal and visually deprived cats. , 1982, Physiological reviews.

[3]  Mriganka Sur,et al.  Development of X- and Y-cell retinogeniculate terminations in kittens , 1984, Nature.

[4]  C. Shatz,et al.  Prenatal development of retinal ganglion cell axons: segregation into eye-specific layers within the cat's lateral geniculate nucleus , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  C. Mason Development of terminal arbors of retino-geniculate axons in the kitten—II. Electron microscopical observations , 1982, Neuroscience.

[6]  J. Stone,et al.  Properties of relay cells in cat's lateral geniculate nucleus: a comparison of W-cells with X- and Y-cells. , 1976, Journal of neurophysiology.

[7]  J. Pettigrew,et al.  Improved use of tapetal reflection for eye-position monitoring. , 1979, Investigative ophthalmology & visual science.

[8]  S. Sherman,et al.  Morphological and physiological properties of geniculate W-cells of the cat: a comparison with X- and Y-cells. , 1983, Journal of neurophysiology.

[9]  J. Lambert,et al.  Factors determining the efficacy of distal excitatory synapses in rat hippocampal CA1 pyramidal neurones , 1998, The Journal of physiology.

[10]  A. Fuchs,et al.  Spatial and temporal properties of X and Y cells in the cat lateral geniculate nucleus. , 1979, The Journal of physiology.

[11]  Detection latencies of X and Y type cells of the cat's dorsal lateral geniculate nucleus , 1987, Experimental Brain Research.

[12]  C. Enroth-Cugell,et al.  The contrast sensitivity of retinal ganglion cells of the cat , 1966, The Journal of physiology.

[13]  H. Swadlow,et al.  Receptive-field and axonal properties of neurons in the dorsal lateral geniculate nucleus of awake unparalyzed rabbits. , 1985, Journal of neurophysiology.

[14]  R C Reid,et al.  Visual physiology of the lateral geniculate nucleus in two species of New World monkey: Saimiri sciureus and Aotus trivirgatis , 2000, The Journal of physiology.

[15]  Robert Shapley,et al.  Spatial properties of X and Y cells in the lateral geniculate nucleus of the cat and conduction velocities of their inputs , 1979, Experimental Brain Research.

[16]  Nicolas J. Kerscher,et al.  State-dependent receptive-field restructuring in the visual cortex , 1998, Nature.

[17]  Robert A. Frazor,et al.  Visual cortex neurons of monkeys and cats: temporal dynamics of the spatial frequency response function. , 2004, Journal of neurophysiology.

[18]  M Sur,et al.  Linear and nonlinear W-cells in C-laminae of the cat's lateral geniculate nucleus. , 1982, Journal of neurophysiology.

[19]  J. Kremers,et al.  Influence of contrast on the responses of marmoset lateral geniculate cells to drifting gratings. , 2001, Journal of neurophysiology.

[20]  M. Sur,et al.  Morphology of physiologically identified retinogeniculate X- and Y-axons in the cat. , 1987, Journal of neurophysiology.

[21]  J. Alonso,et al.  Two different types of Y cells in the cat lateral geniculate nucleus. , 2003, Journal of neurophysiology.

[22]  A. L. Humphrey,et al.  Spatial and temporal response properties of lagged and nonlagged cells in cat lateral geniculate nucleus. , 1990, Journal of neurophysiology.

[23]  ROBERT SHAPLEY,et al.  Visual spatial summation in two classes of geniculate cells , 1975, Nature.

[24]  D. Ringach,et al.  Dynamics of Spatial Frequency Tuning in Macaque V1 , 2002, The Journal of Neuroscience.

[25]  R. Shapley,et al.  The use of m-sequences in the analysis of visual neurons: Linear receptive field properties , 1997, Visual Neuroscience.

[26]  H. Wässle,et al.  Response latency of brisk‐sustained (X) and brisk‐transient (Y) cells in the cat retina , 1982, The Journal of physiology.

[27]  B. Cleland,et al.  Visual resolution and receptive field size: examination of two kinds of cat retinal ganglion cell. , 1979, Science.

[28]  John H. R. Maunsell,et al.  Visual response latencies in striate cortex of the macaque monkey. , 1992, Journal of neurophysiology.

[29]  R. Shapley,et al.  The effect of contrast on the transfer properties of cat retinal ganglion cells. , 1978, The Journal of physiology.

[30]  R. Shapley,et al.  Quantitative analysis of retinal ganglion cell classifications. , 1976, The Journal of physiology.

[31]  J. B. Levitt,et al.  Visual response properties of neurons in the LGN of normally reared and visually deprived macaque monkeys. , 2001, Journal of neurophysiology.

[32]  J. B. Demb,et al.  Bipolar Cells Contribute to Nonlinear Spatial Summation in the Brisk-Transient (Y) Ganglion Cell in Mammalian Retina , 2001, The Journal of Neuroscience.

[33]  John H. R. Maunsell,et al.  Visual response latencies of magnocellular and parvocellular LGN neurons in macaque monkeys , 1999, Visual Neuroscience.

[34]  Stephen D. Van Hooser,et al.  Receptive field properties and laminar organization of lateral geniculate nucleus in the gray squirrel (Sciurus carolinensis). , 2003, Journal of neurophysiology.

[35]  A. B. Bonds,et al.  A comparison of koniocellular, magnocellular and parvocellular receptive field properties in the lateral geniculate nucleus of the owl monkey (Aotus trivirgatus) , 2001, The Journal of physiology.

[36]  Stephen D Van Hooser,et al.  Receptive field properties and laminar organization of lateral geniculate nucleus in the gray squirrel (Sciurus carolinensis). , 2003, Journal of neurophysiology.

[37]  A. Sestokas,et al.  Visual response latency of X- and Y-cells in the dorsal lateral geniculate nucleus of the cat , 1986, Vision Research.

[38]  L. Chalupa,et al.  The visual neurosciences , 2004 .

[39]  W. Regehr,et al.  Developmental Remodeling of the Retinogeniculate Synapse , 2000, Neuron.

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

[41]  R. Eckhorn,et al.  A new method for the insertion of multiple microprobes into neural and muscular tissue, including fiber electrodes, fine wires, needles and microsensors , 1993, Journal of Neuroscience Methods.

[42]  L. Croner,et al.  Receptive fields of P and M ganglion cells across the primate retina , 1995, Vision Research.

[43]  C. Mason Development of terminal arbors of retino-geniculate axons in the kitten—I. Light microscopical observations , 1982, Neuroscience.

[44]  P. H. Schiller,et al.  Spatial frequency and orientation tuning dynamics in area V1 , 2002, Proceedings of the National Academy of Sciences of the United States of America.