Retinotopic organization of ferret suprasylvian cortex

The retinotopic organization of striate and several extrastriate areas of ferret cortex has been established. Here we describe the representation of the visual field on the Suprasylvian visual area (Ssy). This cortical region runs mediolaterally along the posterior bank of the suprasylvian sulcus, and is distinct from adjoining areas in anatomical architecture. The Ssy lies immediately rostral to visual area 21, medial to lateral temporal areas, and lateral to posterior parietal areas. In electrophysiological experiments we made extracellular recordings in adult ferrets. We find that single and multiunit receptive fields range in size from 2 deg × 4 deg to 21 deg × 52 deg. The total visual field representation in Ssy spans over 70 deg in azimuth in the contralateral hemifield (with a small incursion into the ipsilateral hemifield), and from +36 deg to −30 deg in elevation. There are often two representations of the horizontal meridian. Furthermore, the location of the transition from upper to lower fields varies among animals. General features of topography are confirmed in anatomical experiments in which we made tracer injections into different locations in Ssy, and determined the location of retrograde label in area 17. Both isoelevation and isoazimuth lines can span substantial rostrocaudal and mediolateral distances in cortex, sometimes forming closed contours. This topography results in cortical magnifications averaging 0.07 mm/deg in elevation and 0.06 mm/deg in azimuth; however, some contours can run in such a way that it is possible to move a large distance on cortex without moving in the visual field. Because of these irregularities, Ssy contains a coarse representation of the contralateral visual field.

[1]  J. Bullier,et al.  The role of feedback connections in shaping the responses of visual cortical neurons. , 2001, Progress in brain research.

[2]  B R Payne,et al.  Evidence for visual cortical area homologs in cat and macaque monkey. , 1993, Cerebral cortex.

[3]  C. Li,et al.  Extensive integration field beyond the classical receptive field of cat's striate cortical neurons--classification and tuning properties. , 1994, Vision research.

[4]  J. Kaas,et al.  The organization of the second visual area (V II) in the owl monkey: a second order transformation of the visual hemifield. , 1974, Brain research.

[5]  S Shipp,et al.  Organization of reciprocal connections between area 17 and the lateral suprasylvian area of cat visual cortex , 1991, Visual Neuroscience.

[6]  L. Palmer,et al.  Retinotopic organization of areas 20 and 21 in the cat , 1980, The Journal of comparative neurology.

[7]  H. Sherk,et al.  A comparison of magnification functions in area 19 and the lateral suprasylvian visual area in the cat , 2004, Experimental Brain Research.

[8]  John H. R. Maunsell,et al.  The middle temporal visual area in the macaque: Myeloarchitecture, connections, functional properties and topographic organization , 1981, The Journal of comparative neurology.

[9]  Lawrence C. Sincich,et al.  Bypassing V1: a direct geniculate input to area MT , 2004, Nature Neuroscience.

[10]  H. Jones,et al.  Visual cortical mechanisms detecting focal orientation discontinuities , 1995, Nature.

[11]  L. Palmer,et al.  Retinotopic organization of areas 18 and 19 in the cat , 1979, The Journal of comparative neurology.

[12]  M. Sur,et al.  Anterograde axonal tracing with the subunit B of cholera toxin: a highly sensitive immunohistochemical protocol for revealing fine axonal morphology in adult and neonatal brains , 1996, Journal of Neuroscience Methods.

[13]  J. Kaas,et al.  Representation of the visual field in striate and adjoining cortex of the owl monkey (Aotus trivirgatus). , 1971, Brain research.

[14]  L. Palmer,et al.  The retinotopic organization of lateral suprasylvian visual areas in the cat , 1978, The Journal of comparative neurology.

[15]  J. Kaas,et al.  The dorsomedial cortical visual area: a third tier area in the occipital lobe of the owl monkey (Aotus trivirgatus). , 1975 .

[16]  J. B. Levitt,et al.  Feedback connections to ferret striate cortex: Direct evidence for visuotopic convergence of feedback inputs , 2005, The Journal of comparative neurology.

[17]  G. Henry,et al.  Physiological studies on the feedback connection to the striate cortex from cortical areas 18 and 19 of the cat , 1988, Experimental Brain Research.

[18]  J. Bullier,et al.  Reaching beyond the classical receptive field of V1 neurons: horizontal or feedback axons? , 2003, Journal of Physiology-Paris.

[19]  H. Dinse,et al.  The timing of processing along the visual pathway in the cat. , 1994, Neuroreport.

[20]  J. Movshon,et al.  Selectivity and spatial distribution of signals from the receptive field surround in macaque V1 neurons. , 2002, Journal of neurophysiology.

[21]  C. Blakemore,et al.  Characteristics of surround inhibition in cat area 17 , 1997, Experimental Brain Research.

[22]  D. C. Essen,et al.  The topographic organization of rhesus monkey prestriate cortex. , 1978, The Journal of physiology.

[23]  F. Gallyas.  Silver staining of myelin by means of physical development. , 1979, Neurological research.

[24]  Narumi Katsuyama,et al.  Lateral suprasylvian visual cortex is activated earlier than or synchronously with primary visual cortex in the cat , 1996, Neuroscience Research.

[25]  D. Hubel,et al.  Uniformity of monkey striate cortex: A parallel relationship between field size, scatter, and magnification factor , 1974, The Journal of comparative neurology.

[26]  C. Gross,et al.  Visual topography of V2 in the macaque , 1981, The Journal of comparative neurology.

[27]  R. Shapley,et al.  Visual spatial characterization of macaque V1 neurons. , 2001, Journal of neurophysiology.

[28]  K. Albus.  A quantitative study of the projection area of the central and the paracentral visual field in area 17 of the cat , 1975, Experimental brain research.

[29]  R. Vautin,et al.  Magnification factor and receptive field size in foveal striate cortex of the monkey , 2004, Experimental Brain Research.

[30]  H. Sherk,et al.  A reassessment of the lower visual field map in striate-recipient lateral suprasylvian cortex , 1993, Visual Neuroscience.

[31]  R. Desimone,et al.  Local precision of visuotopic organization in the middle temporal area (MT) of the macaque , 2004, Experimental Brain Research.

[32]  H. Sherk,et al.  Retinotopic order is surprisingly good within cell columns in the cat's lateral suprasylvian cortex , 2004, Experimental Brain Research.

[33]  John H. R. Maunsell,et al.  Topographic organization of the middle temporal visual area in the macaque monkey: Representational biases and the relationship to callosal connections and myeloarchitectonic boundaries , 1987, The Journal of comparative neurology.

[34]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  S. Zeki.  Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey , 1974, The Journal of physiology.

[36]  J. Allman,et al.  The dorsomedial cortical visual area: A third tier area in the occipital lobe of the owl monkey (aotus trivirgatus) , 1975, Brain Research.

[37]  W. B. Spatz.  Topographically organized reciprocal connections between areas 17 and MT (visual area of superior temporal sulcus) in the marmoset Callithrix jacchus , 1977, Experimental Brain Research.

[38]  D C Van Essen,et al.  Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. , 1983, Journal of neurophysiology.

[39]  K. Hoffmann,et al.  A motion-sensitive area in ferret extrastriate visual cortex: an analysis in pigmented and albino animals. , 2006, Cerebral cortex.

[40]  H. Sherk.  Coincidence of patchy inputs from the lateral geniculate complex and area 17 to the cat's clare‐bishop area , 1986, The Journal of comparative neurology.

[41]  L. Maffei,et al.  The unresponsive regions of visual cortical receptive fields , 1976, Vision Research.

[42]  I. Thompson,et al.  Retinal decussation patterns in pigmented and albino ferrets , 1987, Neuroscience.

[43]  S. Petersen,et al.  Visual response properties of neurons in four extrastriate visual areas of the owl monkey (Aotus trivirgatus): a quantitative comparison of medial, dorsomedial, dorsolateral, and middle temporal areas. , 1981, Journal of neurophysiology.

[44]  G. Orban,et al.  Response latencies of visual cells in macaque areas V1, V2 and V5 , 1989, Brain Research.

[45]  S Shipp,et al.  Visuotopic organization of the lateral suprasylvian area and of an adjacent area of the ectosylvian gyrus of cat cortex: A physioligical and connectional study , 1991, Visual Neuroscience.

[46]  Ronald P. Crick,et al.  The Representation of the Visual Field , 1983 .

[47]  T. Wiesel,et al.  The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat , 1990, Vision Research.

[48]  Italo Masiello,et al.  Architecture and callosal connections of visual areas 17, 18, 19 and 21 in the ferret (Mustela putorius). , 2002, Cerebral cortex.

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

[50]  Paul Antoine Salin,et al.  Visuotopic organization of corticocortical connections in the visual system of the cat , 1992, The Journal of comparative neurology.

[51]  C. Gross,et al.  Visuotopic organization and extent of V3 and V4 of the macaque , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  I. Ohzawa,et al.  Length and width tuning of neurons in the cat's primary visual cortex. , 1994, Journal of neurophysiology.

[53]  Giorgio M Innocenti,et al.  The representation of the visual field in three extrastriate areas of the ferret (Mustela putorius) and the relationship of retinotopy and field boundaries to callosal connectivity. , 2002, Cerebral cortex.

[54]  R Gattass,et al.  Area V4 in Cebus monkey: extent and visuotopic organization. , 1998, Cerebral cortex.

[55]  Giorgio M Innocenti,et al.  Areal organization of the posterior parietal cortex of the ferret (Mustela putorius). , 2002, Cerebral cortex.

[56]  J D Schall,et al.  Morphology, central projections, and dendritic field orientation of retinal ganglion cells in the ferret , 1985, The Journal of comparative neurology.

[57]  D. V. van Essen,et al.  Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. , 1992, Journal of neurophysiology.

[58]  Dezhe Z. Jin,et al.  The Coordinated Mapping of Visual Space and Response Features in Visual Cortex , 2005, Neuron.

[59]  M. Wong-Riley.  Reciprocal connections between striate and prestriate cortex in squirrel monkey as demonstrated by combined peroxidase histochemistry and autoradiography , 1978, Brain Research.

[60]  M. Law,et al.  Organization of primary visual cortex (area 17) in the ferret , 1988, The Journal of comparative neurology.

[61]  I. Ohzawa,et al.  Asymmetric Suppression Outside the Classical Receptive Field of the Visual Cortex , 1999, The Journal of Neuroscience.

[62]  Giorgio M Innocenti,et al.  Visual areas in the lateral temporal cortex of the ferret (Mustela putorius). , 2004, Cerebral cortex.

[63]  J. Tigges,et al.  Reciprocal point‐to‐point connections between parastriate and striate cortex in the squirrel monkey (Saimiri) , 1973, The Journal of comparative neurology.

[64]  C. Gross,et al.  Visual topography of striate projection zone (MT) in posterior superior temporal sulcus of the macaque. , 1981, Journal of neurophysiology.

[65]  J. B. Levitt,et al.  Contrast dependence of contextual effects in primate visual cortex , 1997, nature.

[66]  D. Whitteridge,et al.  The representation of the visual field on the cerebral cortex in monkeys , 1961, The Journal of physiology.

[67]  H. Sherk,et al.  The retinotopic match between area 17 and its targets in visual suprasylvian cortex , 2004, Experimental Brain Research.

[68]  J. J. Koenderink,et al.  Inhomogeneity and anisotropies for motion detection in the monocular visual field of human observers , 1993, Vision Research.

[69]  F. Sanides,et al.  Cyto- and myeloarchitecture of the visual cortex of the cat and of the surrounding integration cortices. , 1969, Journal fur Hirnforschung.

[70]  Z. Henderson.  Distribution of ganglion cells in the retina of adult pigmented ferret , 1985, Brain Research.

[71]  D. Tolhurst,et al.  Spatial‐frequency tuning and geniculocortical projections in the visual cortex (areas 17 and 18) of the pigmented ferret , 1998, The European journal of neuroscience.

[72]  W. Burke,et al.  Areas PMLS and 21a of cat visual cortex: two functionally distinct areas. , 1996, Cerebral cortex.

[73]  L. Palmer,et al.  The retinotopic organization of area 17 (striate cortex) in the cat , 1978, The Journal of comparative neurology.

[74]  M. Clare,et al.  Responses from an association area secondarily activated from optic cortex. , 1954, Journal of neurophysiology.

[75]  R Gattass,et al.  Visual area MT in the Cebus monkey: Location, visuotopic organization, and variability , 1989, The Journal of comparative neurology.