Maps of Central Visual Space in Ferret V1 and V2 Lack Matching Inputs from the Two Eyes

In the visual cortex, the representation of central visual space is supplied by matching geniculate inputs that are driven exclusively by one eye or the other. In layer 4 of early visual areas (V1 in primates and V1 and V2 in cat), these inputs form a nearly uniform array of small ocular dominance domains, while preserving overall topographic order within the cortical map. In ferret, however, ocular dominance domains in different regions of the visual cortex are strikingly irregular in size and shape. The exceptionally large size of domains in some regions implies a departure from the usual visuotopic matching of inputs from the two eyes. Using optical-imaging, electrophysiological, and anatomical techniques, we show that this regional variation is attributable to exclusively monocular maps of the central portions of the ipsilateral visual field in V1 and the contralateral visual field in V2. In addition, we document a complex interdigitation of V1 and V2 that entails a discontinuity in the mapping of visual space and fragmentation of V2 into isolated cortical territories. We suggest that both the monocularity of these cortical maps and the visuotopic discontinuity along the V1–V2 border derive from asymmetries in the crossed and uncrossed retinal pathways.

[1]  John Edward Lennard-Jones,et al.  The determination of molecular orbitals , 1949, Proceedings of the Royal Society of London. Series A. Mathematical and Physical Sciences.

[2]  C W LANGE,et al.  Visual development. , 1950, The Optometric weekly.

[3]  D. Hubel,et al.  Aberrant visual projections in the Siamese cat , 1971, The Journal of physiology.

[4]  R W Guillery,et al.  A study of normal and congenitally abnormal retinogeniculate projections in cats , 1971, The Journal of comparative neurology.

[5]  R. Guillery,et al.  The transfer of abnormal visual field representations from the dorsal lateral geniculate nucleus to the visual cortex in Siamese cats. , 1973, Brain research.

[6]  D. Hubel,et al.  Ferrier lecture - Functional architecture of macaque monkey visual cortex , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[7]  C. Shatz,et al.  A comparison of visual pathways in Boston and Midwestern Siamese cats , 1977, The Journal of comparative neurology.

[8]  D. Whitteridge,et al.  The nature of the boundary between cortical visual areas II and III in the cat , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[9]  M. Mesulam,et al.  Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. , 1978, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[10]  D. V. van Essen,et al.  Visual areas of the mammalian cerebral cortex. , 1979, Annual review of neuroscience.

[11]  J. Pettigrew,et al.  The decussation of the retinothalamic pathway in the cat, with a note on the major meridians of the cat's eye , 1979, The Journal of comparative neurology.

[12]  J. Pettigrew,et al.  The retinothalamic pathways in Siamese cats , 1979, The Journal of comparative neurology.

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

[14]  K. Albus,et al.  Second and third visual areas of the cat: interindividual variability in retinotopic arrangement and cortical location , 1980, The Journal of physiology.

[15]  R. Guillery,et al.  The dorsal lateral geniculate nucleus of the normal ferret and its postnatal development , 1981, The Journal of comparative neurology.

[16]  H. Wässle,et al.  The retinal projection to the thalamus in the cat: A quantitative investigation and a comparison with the retinotectal pathway , 1981, The Journal of comparative neurology.

[17]  D. Whitteridge,et al.  Ipsilateral visual field represented in the cat's visual cortex , 1982, Neuroscience.

[18]  A Hughes,et al.  The organization of binocular cortex in the primary visual area of the rabbit , 1982, The Journal of comparative neurology.

[19]  V S Ramachandran,et al.  Some neural connections subserving binocular vision in ungulates. , 1984, Brain, behavior and evolution.

[20]  J. Malpeli,et al.  Cat medial interlaminar nucleus: retinotopy, relation to tapetum and implications for scotopic vision. , 1984, Journal of neurophysiology.

[21]  Jeff W. Lichtman,et al.  Principles of neural development , 1985 .

[22]  M P Stryker,et al.  The projection of the visual field onto the lateral geniculate nucleus of the ferret , 1985, The Journal of comparative neurology.

[23]  K. Rockland.  Anatomical organization of primary visual cortex (area 17) in the ferret , 1985, The Journal of comparative neurology.

[24]  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.

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

[26]  J. Pettigrew,et al.  Parallel processing of binocular disparity in the cat’s retinogeniculocortical pathways , 1987, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[27]  R. C. Van Sluyters,et al.  The overall pattern of ocular dominance bands in cat visual cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  J. Schall,et al.  Experimental induction of an abnormal ipsilateral visual field representation in the geniculocortical pathway of normally pigmented cats , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[30]  D. Ts'o,et al.  Functional organization of primate visual cortex revealed by high resolution optical imaging. , 1990, Science.

[31]  M Diksic,et al.  Functional organization in the ferret visual cortex: a double-label 2- deoxyglucose study , 1990, Journal of Neuroscience.

[32]  B. Payne,et al.  Representation of the ipsilateral visual field in the transition zone between areas 17 and 18 of the cat's cerebral cortex , 1990, Visual Neuroscience.

[33]  Richard Durbin,et al.  A dimension reduction framework for understanding cortical maps , 1990, Nature.

[34]  I. Thompson,et al.  Albino gene dosage and retinal decussation patterns in the pigmented ferrret , 1991, Visual Neuroscience.

[35]  J. Cucchiaro.  Early development of the retinal line of decussation in normal and albino ferrets , 1991, The Journal of comparative neurology.

[36]  B R Payne,et al.  Visual-field map in the callosal recipient zone at the border between areas 17 and 18 in the cat , 1991, Visual Neuroscience.

[37]  Bogdan Dreher,et al.  Neuroanatomy of the Visual Pathways and Their Development , 1991 .

[38]  I. Thompson,et al.  Lucifer yellow, retrograde tracers, and fractal analysis characterise adult ferret retinal ganglion cells , 1992, The Journal of comparative neurology.

[39]  B. Reese,et al.  Chiasmatic course of temporal retinal axons in the developing ferret , 1993, The Journal of comparative neurology.

[40]  I. Thompson,et al.  The Development of Retinal Ganglion Cell Decussation Patterns in Postnatal Pigmented and Albino Ferrets , 1993, The European journal of neuroscience.

[41]  A. Leventhal,et al.  Abnormal ipsilateral visual field representation in areas 17 and 18 of hypopigmented cats , 1995, The Journal of comparative neurology.

[42]  J. Horton,et al.  Intrinsic Variability of Ocular Dominance Column Periodicity in Normal Macaque Monkeys , 1996, The Journal of Neuroscience.

[43]  I. Thompson,et al.  Soma and axon diameter distributions and central projections of ferret retinal ganglion cells , 1996, Visual Neuroscience.

[44]  N. Swindale.  The development of topography in the visual cortex: a review of models. , 1996, Network.

[45]  M. Rosa.  Visuotopic Organization of Primate Extrastriate Cortex , 1997 .

[46]  K. Miller,et al.  Correlation-Based Development of Ocularly Matched Orientation and Ocular Dominance Maps: Determination of Required Input Activities , 1998, The Journal of Neuroscience.