Deletion of Ten-m3 induces the formation of eye dominance domains in mouse visual cortex.

The visual system is characterized by precise retinotopic mapping of each eye, together with exquisitely matched binocular projections. In many species, the inputs that represent the eyes are segregated into ocular dominance columns in primary visual cortex (V1), whereas in rodents, this does not occur. Ten-m3, a member of the Ten-m/Odz/Teneurin family, regulates axonal guidance in the retinogeniculate pathway. Significantly, ipsilateral projections are expanded in the dorsal lateral geniculate nucleus and are not aligned with contralateral projections in Ten-m3 knockout (KO) mice. Here, we demonstrate the impact of altered retinogeniculate mapping on the organization and function of V1. Transneuronal tracing and c-fos immunohistochemistry demonstrate that the subcortical expansion of ipsilateral input is conveyed to V1 in Ten-m3 KOs: Ipsilateral inputs are widely distributed across V1 and are interdigitated with contralateral inputs into eye dominance domains. Segregation is confirmed by optical imaging of intrinsic signals. Single-unit recording shows ipsilateral, and contralateral inputs are mismatched at the level of single V1 neurons, and binocular stimulation leads to functional suppression of these cells. These findings indicate that the medial expansion of the binocular zone together with an interocular mismatch is sufficient to induce novel structural features, such as eye dominance domains in rodent visual cortex.

[1]  Mriganka Sur,et al.  Structural Dynamics of Synapses in Vivo Correlate with Functional Changes during Experience-Dependent Plasticity in Visual Cortex , 2010, The Journal of Neuroscience.

[2]  M. Sur,et al.  Loss of Arc renders the visual cortex impervious to the effects of sensory experience or deprivation , 2010, Nature Neuroscience.

[3]  C. Mason,et al.  Switching Retinogeniculate Axon Laterality Leads to Normal Targeting but Abnormal Eye-Specific Segregation That Is Activity Dependent , 2009, The Journal of Neuroscience.

[4]  Gabriel Kreiman,et al.  Differential Gene Expression in the Developing Lateral Geniculate Nucleus and Medial Geniculate Nucleus Reveals Novel Roles for Zic4 and Foxp2 in Visual and Auditory Pathway Development , 2009, The Journal of Neuroscience.

[5]  Michael P. Stryker,et al.  Retinal Input Instructs Alignment of Visual Topographic Maps , 2009, Cell.

[6]  K. Miller,et al.  Equalization of Ocular Dominance Columns Induced by an Activity-Dependent Learning Rule and the Maturation of Inhibition , 2009, The Journal of Neuroscience.

[7]  M. Sur,et al.  Intrinsic patterning and experience-dependent mechanisms that generate eye-specific projections and binocular circuits in the visual pathway , 2009, Current Opinion in Neurobiology.

[8]  Nathan R. Wilson,et al.  Partial reversal of Rett Syndrome-like symptoms in MeCP2 mutant mice , 2009, Proceedings of the National Academy of Sciences.

[9]  Jonathan C Horton,et al.  Ocular Dominance Columns: Enigmas and Challenges , 2009, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[10]  L. Chalupa,et al.  Molecular Correlates of Laminar Differences in the Macaque Dorsal Lateral Geniculate Nucleus , 2008, The Journal of Neuroscience.

[11]  Michael P Stryker,et al.  Roles of Ephrin-As and Structured Activity in the Development of Functional Maps in the Superior Colliculus , 2008, The Journal of Neuroscience.

[12]  W. M. Keck,et al.  Highly Selective Receptive Fields in Mouse Visual Cortex , 2008, The Journal of Neuroscience.

[13]  M. Feller,et al.  Mechanisms underlying development of visual maps and receptive fields. , 2008, Annual review of neuroscience.

[14]  G. Goodhill Contributions of Theoretical Modeling to the Understanding of Neural Map Development , 2007, Neuron.

[15]  M. Sur,et al.  Ten_m3 Regulates Eye-Specific Patterning in the Mammalian Visual Pathway and Is Required for Binocular Vision , 2007, PLoS biology.

[16]  Quanxin Wang,et al.  Area map of mouse visual cortex , 2007, The Journal of comparative neurology.

[17]  M. Sur,et al.  Differential gene expression between sensory neocortical areas: potential roles for Ten_m3 and Bcl6 in patterning visual and somatosensory pathways. , 2007, Cerebral cortex.

[18]  A. Huberman,et al.  Spontaneous Retinal Activity Mediates Development of Ocular Dominance Columns and Binocular Receptive Fields in V1 , 2006, Neuron.

[19]  D. O'Leary,et al.  Potential target genes of EMX2 include Odz/Ten-M and other gene families with implications for cortical patterning , 2006, Molecular and Cellular Neuroscience.

[20]  T. Hensch Critical period plasticity in local cortical circuits , 2005, Nature Reviews Neuroscience.

[21]  John G Flanagan,et al.  Ephrin-As and neural activity are required for eye-specific patterning during retinogeniculate mapping , 2005, Nature Neuroscience.

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

[23]  Tadashi Hamasaki,et al.  EMX2 Regulates Sizes and Positioning of the Primary Sensory and Motor Areas in Neocortex by Direct Specification of Cortical Progenitors , 2004, Neuron.

[24]  Andreas Burkhalter,et al.  Paucity of horizontal connections for binocular vision in V1 of naturally strabismic macaques: Cytochrome oxidase compartment specificity , 2004, The Journal of comparative neurology.

[25]  S. Nelson,et al.  Homeostatic plasticity in the developing nervous system , 2004, Nature Reviews Neuroscience.

[26]  Matthew S. Grubb,et al.  Abnormal Functional Organization in the Dorsal Lateral Geniculate Nucleus of Mice Lacking the β2 Subunit of the Nicotinic Acetylcholine Receptor , 2003, Neuron.

[27]  Michael P. Stryker,et al.  New Paradigm for Optical Imaging Temporally Encoded Maps of Intrinsic Signal , 2003, Neuron.

[28]  S. Hirakawa,et al.  All Four Members of the Ten-m/Odz Family of Transmembrane Proteins Form Dimers* , 2002, The Journal of Biological Chemistry.

[29]  L. C. Katz,et al.  Early development of ocular dominance columns. , 2000, Science.

[30]  D. O'Leary,et al.  Regulation of area identity in the mammalian neocortex by Emx2 and Pax6. , 2000, Science.

[31]  M. Fagiolini,et al.  Inhibitory threshold for critical-period activation in primary visual cortex , 2000, Nature.

[32]  L. C. Katz,et al.  Development of ocular dominance columns in the absence of retinal input , 1999, Nature Neuroscience.

[33]  Michael P. Stryker,et al.  Anatomical Correlates of Functional Plasticity in Mouse Visual Cortex , 1999, The Journal of Neuroscience.

[34]  R. Fässler,et al.  Mouse Ten-m/Odz Is a New Family of Dimeric Type II Transmembrane Proteins Expressed in Many Tissues , 1999, The Journal of cell biology.

[35]  M. Stryker,et al.  The role of visual experience in the development of columns in cat visual cortex. , 1998, Science.

[36]  C. Shatz,et al.  Synaptic Activity and the Construction of Cortical Circuits , 1996, Science.

[37]  M P Stryker,et al.  Experience-Dependent Plasticity of Binocular Responses in the Primary Visual Cortex of the Mouse , 1996, The Journal of Neuroscience.

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

[39]  S Löwel,et al.  Ocular dominance column development: strabismus changes the spacing of adjacent columns in cat visual cortex. , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  H. Ritter,et al.  A principle for the formation of the spatial structure of cortical feature maps. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[41]  W. Singer,et al.  Blockade of "NMDA" receptors disrupts experience-dependent plasticity of kitten striate cortex. , 1987, Science.

[42]  E. Debski,et al.  N-methyl-D-aspartate receptor antagonist desegregates eye-specific stripes. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[43]  M. Stryker,et al.  Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  S. Levay,et al.  The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  J. Cucchiaro,et al.  The development of the retinogeniculate pathways in normal and albino ferrets , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[46]  J. Schmidt,et al.  Activity and the formation of ocular dominance patches in dually innervated tectum of goldfish , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  D. Hubel,et al.  Specificity of intrinsic connections in primate primary visual cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  B. Reese,et al.  Crossed and uncrossed visual topography in dorsal lateral geniculate nucleus of the pigmented rat. , 1983, Journal of neurophysiology.

[49]  U. Dräger,et al.  Origins of crossed and uncrossed retinal projections in pigmented and albino mice , 1980, The Journal of comparative neurology.

[50]  S. Levay,et al.  Siamese cat: altered connections of visual cortex. , 1979, Science.

[51]  M. Law,et al.  Eye-specific termination bands in tecta of three-eyed frogs. , 1978, Science.

[52]  S. Levay,et al.  Ocular dominance columns and their development in layer IV of the cat's visual cortex: A quantitative study , 1978, The Journal of comparative neurology.

[53]  J. Schmidt,et al.  Retinal fibers alter tectal positional markers during the expansion of the half retinal projection in goldfish , 1978, The Journal of comparative neurology.

[54]  T. Wiesel,et al.  The distribution of afferents representing the right and left eyes in the cat's visual cortex , 1977, Brain Research.

[55]  D. Hubel,et al.  Plasticity of ocular dominance columns in monkey striate cortex. , 1977, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[56]  P. Rakic Prenatal genesis of connections subserving ocular dominance in the rhesus monkey , 1976, Nature.

[57]  J. Malpeli,et al.  The representation of the visual field in the lateral geniculate nucleus of Macaca mulatta , 1975, The Journal of comparative neurology.

[58]  U. Dräger,et al.  Receptive fields of single cells and topography in mouse visual cortex , 1975, The Journal of comparative neurology.

[59]  D H Hubel,et al.  Autoradiographic demonstration of ocular-dominance columns in the monkey striate cortex by means of transneuronal transport. , 1974, Brain research.

[60]  D. Hubel,et al.  Laminar and columnar distribution of geniculo‐cortical fibers in the macaque monkey , 1972, The Journal of comparative neurology.

[61]  R. Guillery An abnormal retinogeniculate projection in Siamese cats. , 1969, Brain research.

[62]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[63]  B. Dreher,et al.  Comparative Survey of the Mammalian Visual System with Reference to the Mouse , 2008 .

[64]  Robert W. Williams,et al.  Eye, retina, and visual system of the mouse , 2008 .

[65]  L. C. Katz,et al.  Development of cortical circuits: Lessons from ocular dominance columns , 2002, Nature Reviews Neuroscience.

[66]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

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