Remapping for visual stability

Visual perception is based on both incoming sensory signals and information about ongoing actions. Recordings from single neurons have shown that corollary discharge signals can influence visual representations in parietal, frontal and extrastriate visual cortex, as well as the superior colliculus (SC). In each of these areas, visual representations are remapped in conjunction with eye movements. Remapping provides a mechanism for creating a stable, eye-centred map of salient locations. Temporal and spatial aspects of remapping are highly variable from cell to cell and area to area. Most neurons in the lateral intraparietal area remap stimulus traces, as do many neurons in closely allied areas such as the frontal eye fields the SC and extrastriate area V3A. Remapping is not purely a cortical phenomenon. Stimulus traces are remapped from one hemifield to the other even when direct cortico-cortical connections are removed. The neural circuitry that produces remapping is distinguished by significant plasticity, suggesting that updating of salient stimuli is fundamental for spatial stability and visuospatial behaviour. These findings provide new evidence that a unified and stable representation of visual space is constructed by redundant circuitry, comprising cortical and subcortical pathways, with a remarkable capacity for reorganization.

[1]  R. Wurtz,et al.  Activity of superior colliculus in behaving monkey. I. Visual receptive fields of single neurons. , 1972, Journal of neurophysiology.

[2]  R. Wurtz,et al.  Activity of superior colliculus in behaving monkey. 3. Cells discharging before eye movements. , 1972, Journal of neurophysiology.

[3]  M. Cynader,et al.  Response characteristics of single cells in the monkey superior colliculus following ablation or cooling of visual cortex. , 1974, Journal of neurophysiology.

[4]  B L Finlay,et al.  Quantitative studies of single-cell properties in monkey striate cortex. IV. Corticotectal cells. , 1976, Journal of neurophysiology.

[5]  L. Benevento,et al.  The cortical projections of the inferior pulvinar and adjacent lateral pulvinar in the rhesus monkey (macaca mulatta): An autoradiographic study , 1976, Brain Research.

[6]  P. E. Hallett,et al.  Saccadic eye movements to flashed targets , 1976, Vision Research.

[7]  L E Mays,et al.  Saccades are spatially, not retinocentrically, coded. , 1980, Science.

[8]  J. E. Albano,et al.  Visual-motor function of the primate superior colliculus. , 1980, Annual review of neuroscience.

[9]  D. Sparks,et al.  Corollary discharge provides accurate eye position information to the oculomotor system. , 1983, Science.

[10]  H. Vanegas,et al.  Comparative neurology of the optic tectum , 1984 .

[11]  W. Fries Cortical projections to the superior colliculus in the macaque monkey: A retrograde study using horseradish peroxidase , 1984, The Journal of comparative neurology.

[12]  D. Pandya,et al.  Projections to the frontal cortex from the posterior parietal region in the rhesus monkey , 1984, The Journal of comparative neurology.

[13]  J. K. Harting,et al.  The Mammalian Superior Colliculus: Studies of Its Morphology and Connections , 1984 .

[14]  C. Bruce,et al.  Primate frontal eye fields. I. Single neurons discharging before saccades. , 1985, Journal of neurophysiology.

[15]  M. Goldberg,et al.  Functional properties of corticotectal neurons in the monkey's frontal eye field. , 1987, Journal of neurophysiology.

[16]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

[17]  D. B. Bender,et al.  Comparison of saccadic eye movements in humans and macaques to single-step and double-step target movements , 1989, Vision Research.

[18]  C. Bruce,et al.  Primate frontal eye fields. III. Maintenance of a spatially accurate saccade signal. , 1990, Journal of neurophysiology.

[19]  R. M. Siegel,et al.  Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule , 1990, The Journal of comparative neurology.

[20]  R. Andersen,et al.  Visual receptive field organization and cortico‐cortical connections of the lateral intraparietal area (area LIP) in the macaque , 1990, The Journal of comparative neurology.

[21]  Leslie G. Ungerleider,et al.  Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  R. Andersen,et al.  Saccade-related activity in the lateral intraparietal area. I. Temporal properties; comparison with area 7a. , 1991, Journal of neurophysiology.

[23]  M. Goldberg,et al.  Saccadic dysmetria in a patient with a right frontoparietal lesion. The importance of corollary discharge for accurate spatial behaviour. , 1992, Brain : a journal of neurology.

[24]  J R Duhamel,et al.  The updating of the representation of visual space in parietal cortex by intended eye movements. , 1992, Science.

[25]  A. Cowey,et al.  Patterns of inter- and intralaminar GABAergic connections distinguish striate (V1) and extrastriate (V2, V4) visual cortices and their functionally specialized subdivisions in the rhesus monkey , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  J. Schall,et al.  Saccade target selection in frontal eye field of macaque. I. Visual and premovement activation , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  J. Bullier,et al.  Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  M. Goldberg,et al.  Neurons in the monkey superior colliculus predict the visual result of impending saccadic eye movements. , 1995, Journal of neurophysiology.

[29]  C. Bruce,et al.  Topography of projections to posterior cortical areas from the macaque frontal eye fields , 1995, The Journal of comparative neurology.

[30]  W. Heide,et al.  Cortical control of double‐step saccades: Implications for spatial orientation , 1995, Annals of neurology.

[31]  C. Gilbert,et al.  Spatial integration and cortical dynamics. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[32]  J. Bullier,et al.  Functional streams in occipito-frontal connections in the monkey , 1996, Behavioural Brain Research.

[33]  R. Wurtz,et al.  Monkey posterior parietal cortex neurons antidromically activated from superior colliculus. , 1997, Journal of neurophysiology.

[34]  M. Goldberg,et al.  Spatial processing in the monkey frontal eye field. I. Predictive visual responses. , 1997, Journal of neurophysiology.

[35]  W. Heide,et al.  Combined deficits of saccades and visuo-spatial orientation after cortical lesions , 1998, Experimental Brain Research.

[36]  C. Colby Action-Oriented Spatial Reference Frames in Cortex , 1998, Neuron.

[37]  P. Goldman-Rakic,et al.  Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. , 1998, Journal of neurophysiology.

[38]  M. Goldberg,et al.  Space and attention in parietal cortex. , 1999, Annual review of neuroscience.

[39]  D. V. van Essen,et al.  Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey , 2000, The Journal of comparative neurology.

[40]  P. Goldman-Rakic,et al.  Inactivation of parietal and prefrontal cortex reveals interdependence of neural activity during memory-guided saccades. , 2000, Journal of neurophysiology.

[41]  Dottie M. Clower,et al.  The Inferior Parietal Lobule Is the Target of Output from the Superior Colliculus, Hippocampus, and Cerebellum , 2001, The Journal of Neuroscience.

[42]  K. Hoffmann,et al.  Cortical input to the nucleus of the optic tract and dorsal terminal nucleus (NOT-DTN) in macaques: a retrograde tracing study. , 2001, Cerebral cortex.

[43]  R. Andersen,et al.  Inactivation of macaque lateral intraparietal area delays initiation of the second saccade predominantly from contralesional eye positions in a double-saccade task , 2001, Experimental Brain Research.

[44]  M. Goldberg,et al.  Spatial processing in the monkey frontal eye field. II. Memory responses. , 2001, Journal of neurophysiology.

[45]  G. Leichnetz Connections of the medial posterior parietal cortex (area 7m) in the monkey , 2001, The Anatomical record.

[46]  D. Burr,et al.  Changes in visual perception at the time of saccades , 2001, Trends in Neurosciences.

[47]  R. Wurtz,et al.  Progression in neuronal processing for saccadic eye movements from parietal cortex area lip to superior colliculus. , 2001, Journal of neurophysiology.

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

[49]  Kae Nakamura,et al.  Updating of the visual representation in monkey striate and extrastriate cortex during saccades , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[50]  R. Wurtz,et al.  Comparison of cortico-cortical and cortico-collicular signals for the generation of saccadic eye movements. , 2002, Journal of neurophysiology.

[51]  R. Wurtz,et al.  A Pathway in Primate Brain for Internal Monitoring of Movements , 2002, Science.

[52]  Jean Bennett,et al.  Lateral Connectivity and Contextual Interactions in Macaque Primary Visual Cortex , 2002, Neuron.

[53]  C. Genovese,et al.  Spatial Updating in Human Parietal Cortex , 2003, Neuron.

[54]  M. Goldberg,et al.  The time course of perisaccadic receptive field shifts in the lateral intraparietal area of the monkey. , 2003, Journal of neurophysiology.

[55]  T. Vilis,et al.  Gaze-Centered Updating of Visual Space in Human Parietal Cortex , 2003, The Journal of Neuroscience.

[56]  R. Andersen,et al.  Memory related motor planning activity in posterior parietal cortex of macaque , 1988, Experimental Brain Research.

[57]  P. Schiller,et al.  Interactions between visually and electrically elicited saccades before and after superior colliculus and frontal eye field ablations in the rhesus monkey , 2004, Experimental Brain Research.

[58]  R. Ram-Tsur,et al.  The Saccadic system more readily co-processes orthogonal than co-linear saccades , 2004, Experimental Brain Research.

[59]  J. Lynch,et al.  Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport , 2004, Experimental Brain Research.

[60]  A. Murthy,et al.  Programming of double-step saccade sequences: Modulation by cognitive control , 2004, Vision Research.

[61]  M. Schlag-Rey,et al.  The frontal eye field provides the goal of saccadic eye movement , 2004, Experimental Brain Research.

[62]  R. Berman,et al.  Dynamic circuitry for updating spatial representations. I. Behavioral evidence for interhemispheric transfer in the split-brain macaque. , 2005, Journal of neurophysiology.

[63]  R. Berman,et al.  Corollary discharge and spatial updating: when the brain is split, is space still unified? , 2004, Progress in brain research.

[64]  R. Berman,et al.  Dynamic circuitry for updating spatial representations. II. Physiological evidence for interhemispheric transfer in area LIP of the split-brain macaque. , 2005, Journal of neurophysiology.

[65]  C. Colby,et al.  Spatial updating in area LIP is independent of saccade direction. , 2006, Journal of neurophysiology.

[66]  T. Vilis,et al.  Directional selectivity of BOLD activity in human posterior parietal cortex for memory-guided double-step saccades. , 2006, Journal of neurophysiology.

[67]  J. Lynch,et al.  Cortico-cortical networks and cortico-subcortical loops for the higher control of eye movements. , 2006, Progress in brain research.

[68]  P. May The mammalian superior colliculus: laminar structure and connections. , 2006, Progress in brain research.

[69]  Robert H. Wurtz,et al.  Influence of the thalamus on spatial visual processing in frontal cortex , 2006, Nature.

[70]  R. Berman,et al.  Dynamic circuitry for updating spatial representations. III. From neurons to behavior. , 2007, Journal of neurophysiology.

[71]  D. Melcher Predictive remapping of visual features precedes saccadic eye movements , 2007, Nature Neuroscience.

[72]  M. Goldberg,et al.  Rhesus monkeys mislocalize saccade targets flashed for 100ms around the time of a saccade , 2007, Vision Research.

[73]  Christopher D Chambers,et al.  Parietal stimulation destabilizes spatial updating across saccadic eye movements , 2007, Proceedings of the National Academy of Sciences.

[74]  C. Genovese,et al.  Remapping in human visual cortex. , 2007, Journal of neurophysiology.

[75]  M. Sommer,et al.  Corollary discharge across the animal kingdom , 2008, Nature Reviews Neuroscience.

[76]  C. Colby,et al.  Trans-saccadic perception , 2008, Trends in Cognitive Sciences.

[77]  M. Sommer,et al.  Frontal Eye Field Neurons with Spatial Representations Predicted by Their Subcortical Input , 2009, The Journal of Neuroscience.

[78]  C. Colby,et al.  Spatial updating in monkey superior colliculus in the absence of the forebrain commissures: dissociation between superficial and intermediate layers. , 2010, Journal of neurophysiology.