Neural representation during visually guided reaching in macaque posterior parietal cortex.

Visually guided hand movements in primates require an interconnected network of various cortical areas. Single unit firing rate from area 7a and dorsal prelunate (DP) neurons of macaque posterior parietal cortex (PPC) was recorded during reaching movements to targets at variable locations and under different eye position conditions. In the eye position-varied task, the reach target was always foveated; thus eye position varied with reach target location. In the retinal-varied task, the monkey reached to targets at variable retinotopic locations while eye position was kept constant in the center. Spatial tuning was examined with respect to temporal (task epoch) and contextual (task condition) aspects, and response fields were compared. The analysis showed distinct tuning types. The majority of neurons changed their gain field tuning and retinotopic tuning between different phases of the task. Between the onset of visual stimulation and the preparatory phase (before the go signal), about one half the neurons altered their firing rate significantly. Spatial response fields during preparation and initiation epochs were strongly influenced by the task condition (eye position varied vs. retinal varied), supporting a strong role of eye position during visually guided reaching. DP neurons, classically considered visual, showed reach related modulation similar to 7a neurons. This study shows that both area 7a and DP are modulated during reaching behavior in primates. The various tuning types in both areas suggest distinct populations recruiting different circuits during visually guided reaching.

[1]  Y. Rossetti,et al.  Optic ataxia and the function of the dorsal stream: Contributions to perception and action , 2009, Neuropsychologia.

[2]  C. Galletti,et al.  Reaching activity in parietal area V6A of macaque: eye influence on arm activity or retinocentric coding of reaching movements? , 2008, The European journal of neuroscience.

[3]  S. Scott,et al.  Reaching movements with similar hand paths but different arm orientations. II. Activity of individual cells in dorsal premotor cortex and parietal area 5. , 1997, Journal of neurophysiology.

[4]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. I. Relations between single cell discharge and direction of movement , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  H. Tanaka,et al.  The protective effects of vitamin E on microcephaly in rats X-irradiated in utero: DNA, lipid peroxide and confronting cisternae. , 1986, Brain research.

[6]  G. Sheean,et al.  Upper Motor Neurone Syndrome and Spasticity: Neurophysiology of spasticity , 2008 .

[7]  C. Prablanc,et al.  Vectorial coding of movement: vision, proprioception, or both? , 1995, Journal of neurophysiology.

[8]  B. C. Motter,et al.  The functional properties of the light-sensitive neurons of the posterior parietal cortex studied in waking monkeys: foveal sparing and opponent vector organization , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  F. Lacquaniti,et al.  Parieto-frontal coding of reaching: an integrated framework , 1999, Experimental Brain Research.

[10]  E. Batschelet Circular statistics in biology , 1981 .

[11]  R. Andersen,et al.  Intention-related activity in the posterior parietal cortex: a review , 2000, Vision Research.

[12]  R. Andersen,et al.  Cortical Local Field Potential Encodes Movement Intentions in the Posterior Parietal Cortex , 2005, Neuron.

[13]  S. Scott,et al.  Reaching movements with similar hand paths but different arm orientations. I. Activity of individual cells in motor cortex. , 1997, Journal of neurophysiology.

[14]  D. Y. P. Henriques,et al.  Direction-dependent distortions of retinocentric space in the visuomotor transformation for pointing , 2000, Experimental Brain Research.

[15]  Simona Monaco,et al.  Visual, somatosensory, and bimodal activities in the macaque parietal area PEc. , 2008, Cerebral cortex.

[16]  R. Caminiti,et al.  Cortical mechanisms for online control of hand movement trajectory: the role of the posterior parietal cortex. , 2009, Cerebral cortex.

[17]  Scott T. Grafton,et al.  Role of the posterior parietal cortex in updating reaching movements to a visual target , 1999, Nature Neuroscience.

[18]  R Caminiti,et al.  Early coding of visuomanual coordination during reaching in parietal area PEc. , 2001, Journal of neurophysiology.

[19]  T. Sejnowski,et al.  Book Review: Gain Modulation in the Central Nervous System: Where Behavior, Neurophysiology, and Computation Meet , 2001, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[20]  R. M. Siegel,et al.  Encoding of spatial location by posterior parietal neurons. , 1985, Science.

[21]  R. Andersen,et al.  The parietal reach region codes the next planned movement in a sequential reach task. , 2001, Journal of neurophysiology.

[22]  Eiji Hoshi,et al.  Movement-related neuronal activity reflecting the transformation of coordinates in the ventral premotor cortex of monkeys. , 2002, Journal of neurophysiology.

[23]  R. M. Siegel,et al.  Functional architecture of retinotopy in visual association cortex of behaving monkey. , 2005, Cerebral cortex.

[24]  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.

[25]  A P Batista,et al.  Reach plans in eye-centered coordinates. , 1999, Science.

[26]  J. Bogousslavsky,et al.  Parietal kinetic ataxia without proprioceptive deficit. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[27]  Dr. Juhani Hyvärinen The Parietal Cortex of Monkey and Man , 1982, Studies of Brain Function.

[28]  P. Bédard,et al.  On-line vs. off-line utilization of peripheral visual afferent information to ensure spatial accuracy of goal-directed movements , 2004, Experimental Brain Research.

[29]  K. Hoffmann,et al.  Eye position effects in monkey cortex. II. Pursuit- and fixation-related activity in posterior parietal areas LIP and 7A. , 1997, Journal of neurophysiology.

[30]  C. Galletti,et al.  Spatial tuning of reaching activity in the medial parieto‐occipital cortex (area V6A) of macaque monkey , 2005, The European journal of neuroscience.

[31]  S. Grossberg,et al.  Cortical networks for control of voluntary arm movements under variable force conditions. , 1998, Cerebral cortex.

[32]  I. Toni,et al.  Integration of target and effector information in the human brain during reach planning. , 2007, Journal of neurophysiology.

[33]  Ferdinando A Mussa-Ivaldi,et al.  Interaction of visual and proprioceptive feedback during adaptation of human reaching movements. , 2005, Journal of neurophysiology.

[34]  Hansjörg Scherberger,et al.  Target selection for reaching and saccades share a similar behavioral reference frame in the macaque. , 2003, Journal of neurophysiology.

[35]  R. M. Siegel,et al.  Analysis of optic flow in the monkey parietal area 7a. , 1997, Cerebral cortex.

[36]  R. M. Siegel,et al.  Attentional modulation of receptive field structure in area 7a of the behaving monkey. , 2007, Cerebral cortex.

[37]  H. Kennedy,et al.  How Humans Reach: Distinct Cortical Systems for Central and Peripheral Vision , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[38]  F. Lacquaniti,et al.  Visual Control of Hand‐reaching Movement: Activity in Parietal Area 7m , 1997, The European journal of neuroscience.

[39]  Reza Shadmehr,et al.  The Computational Neurobiology of Reaching and Pointing: A Foundation for Motor Learning , 2004 .

[40]  Laurel J Buxbaum,et al.  SPATIO-MOTOR REPRESENTATIONS IN REACHING: EVIDENCE FOR SUBTYPES OF OPTIC ATAXIA. , 1998, Cognitive neuropsychology.

[41]  R Caminiti,et al.  Eye-hand coordination during reaching. II. An analysis of the relationships between visuomanual signals in parietal cortex and parieto-frontal association projections. , 2001, Cerebral cortex.

[42]  R. Andersen,et al.  Target Selection Signals for Arm Reaching in the Posterior Parietal Cortex , 2007, The Journal of Neuroscience.

[43]  J. Kaas,et al.  Reappraisal of DL / V 4 Boundaries Based on Connectivity Patterns of Dorsolateral Visual Cortex in Macaques Iwona Stepniewska , 2005 .

[44]  Timothy J Ebner,et al.  What Do Complex Spikes Signal about Limb Movements? , 2002, Annals of the New York Academy of Sciences.

[45]  B. Blum Manipulation reach and visual reach neurons in the inferior parietal lobule of the rhesus monkey , 1985, Behavioural Brain Research.

[46]  B. Fischer,et al.  Selection of visual targets activates prelunate cortical cells in trained rhesus monkey , 2004, Experimental Brain Research.

[47]  Scott T. Grafton,et al.  Forward modeling allows feedback control for fast reaching movements , 2000, Trends in Cognitive Sciences.

[48]  M. A. Steinmetz,et al.  Neurophysiological evidence for a role of posterior parietal cortex in redirecting visual attention. , 1995, Cerebral cortex.

[49]  Byron M. Yu,et al.  Reference frames for reach planning in macaque dorsal premotor cortex. , 2007, Journal of neurophysiology.

[50]  R. M. Siegel,et al.  Modulation of responses to optic flow in area 7a by retinotopic and oculomotor cues in monkey. , 1997, Cerebral cortex.

[51]  R. M. Siegel,et al.  Cerebral Cortex doi:10.1093/cercor/bhj155 Spatiotemporal Dynamics of the Functional Architecture for Gain Fields in Inferior Parietal Lobule of Behaving Monkey , 2022 .

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

[53]  Emiliano Brunamonti,et al.  The over-representation of contralateral space in parietal cortex: a positive image of directional motor components of neglect? , 2005, Cerebral cortex.

[54]  C. Gielen,et al.  Gaze affects pointing toward remembered visual targets after a self-initiated step. , 2004, Journal of neurophysiology.

[55]  Gopal Santhanam,et al.  Preparatory activity in premotor and motor cortex reflects the speed of the upcoming reach. , 2006, Journal of neurophysiology.

[56]  C. Connor,et al.  Covert attention suppresses neuronal responses in area 7a of the posterior parietal cortex. , 1994, Journal of neurophysiology.

[57]  R. M. Siegel,et al.  Functional architecture of eye position gain fields in visual association cortex of behaving monkey. , 2003, Journal of neurophysiology.

[58]  V. Mountcastle,et al.  Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. , 1975, Journal of neurophysiology.

[59]  Lawrence H Snyder,et al.  Idiosyncratic and systematic aspects of spatial representations in the macaque parietal cortex , 2010, Proceedings of the National Academy of Sciences.

[60]  D. Robinson,et al.  Behavioral enhancement of visual responses in monkey cerebral cortex. I. Modulation in posterior parietal cortex related to selective visual attention. , 1981, Journal of neurophysiology.

[61]  B. C. Motter,et al.  The influence of attentive fixation upon the excitability of the light- sensitive neurons of the posterior parietal cortex , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[62]  G. Rizzolatti,et al.  Functional Organization of Inferior Parietal Lobule Convexity in the Macaque Monkey: Electrophysiological Characterization of Motor, Sensory and Mirror Responses and Their Correlation with Cytoarchitectonic Areas , 2022 .

[63]  M. A. Steinmetz,et al.  Neuronal responses in area 7a to multiple-stimulus displays: I. neurons encode the location of the salient stimulus. , 2001, Cerebral cortex.

[64]  G. Magenes,et al.  Eye-head-hand coordination in pointing at visual targets: spatial and temporal analysis , 2004, Experimental Brain Research.

[65]  Claude Prablanc,et al.  Two modes of error processing in reaching , 2009, Experimental Brain Research.

[66]  M. Tanaka,et al.  Visual properties and spatial distribution of neurones in the visual association area on the prelunate gyrus of the awake monkey , 2004, Experimental Brain Research.

[67]  R. M. Siegel,et al.  Foundations of Cognitive Science , 1990, Journal of Cognitive Neuroscience.

[68]  Ralph M. Siegel,et al.  Optic Flow Selectivity in the Anterior Superior Temporal Polysensory Area, STPa, of the Behaving Monkey , 1999, The Journal of Neuroscience.

[69]  M. Goldberg,et al.  The Role of the Lateral Intraparietal Area of the Monkey in the Generation of Saccades and Visuospatial Attention , 2002, Annals of the New York Academy of Sciences.

[70]  M. Goodale,et al.  Visual control of reaching movements without vision of the limb , 2004, Experimental Brain Research.

[71]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[72]  E Guigon,et al.  Recoding arm position to learn visuomotor transformations. , 2001, Cerebral cortex.

[73]  D. B. Bender,et al.  Vertical meridian representation on the prelunate gyrus in area V4 of macaque , 2001, Brain Research Bulletin.

[74]  R. E. Passingham,et al.  Parietal cortex and movement I. Movement selection and reaching , 1997, Experimental Brain Research.

[75]  D. Pélisson,et al.  From Eye to Hand: Planning Goal-directed Movements , 1998, Neuroscience & Biobehavioral Reviews.

[76]  L. Fogassi,et al.  Eye position effects on visual, memory, and saccade-related activity in areas LIP and 7a of macaque , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[77]  R. Andersen,et al.  The influence of the angle of gaze upon the excitability of the light- sensitive neurons of the posterior parietal cortex , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[78]  Yq Liu,et al.  Intention and Attention: Different functional roles for LIPd and LIPv , 2010, Nature Neuroscience.

[79]  J. Kalaska The representation of arm movements in postcentral and parietal cortex. , 1988, Canadian journal of physiology and pharmacology.

[80]  J. Wann,et al.  How active gaze informs the hand in sequential pointing movements , 2006, Experimental Brain Research.

[81]  R. Andersen,et al.  Dorsal Premotor Neurons Encode the Relative Position of the Hand, Eye, and Goal during Reach Planning , 2006, Neuron.

[82]  A B Schwartz,et al.  Motor cortical representation of speed and direction during reaching. , 1999, Journal of neurophysiology.

[83]  M. Desmurget,et al.  An ‘automatic pilot’ for the hand in human posterior parietal cortex: toward reinterpreting optic ataxia , 2000, Nature Neuroscience.

[84]  A. Milner,et al.  Reaching errors in optic ataxia are linked to eye position rather than head or body position , 2006, Neuropsychologia.

[85]  Anthony R. Dickinson,et al.  Non-spatial, motor-specific activation in posterior parietal cortex , 2002, Nature Neuroscience.

[86]  A P Georgopoulos,et al.  Effects of optic flow in motor cortex and area 7a. , 2001, Journal of neurophysiology.

[87]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. II. Coding of the direction of movement by a neuronal population , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[88]  W A MacKay,et al.  Properties of reach-related neuronal activity in cortical area 7A. , 1992, Journal of neurophysiology.

[89]  M. Husain,et al.  Control over Conflict during Movement Preparation: Role of Posterior Parietal Cortex , 2008, Neuron.

[90]  D. B. Bender,et al.  Effect of attentive fixation in macaque thalamus and cortex. , 2001, Journal of neurophysiology.

[91]  R. Andersen,et al.  Change in motor plan, without a change in the spatial locus of attention, modulates activity in posterior parietal cortex. , 1998, Journal of neurophysiology.

[92]  R. M. Siegel,et al.  Functional Architecture of Spatial Attention in the Parietal Cortex of the Behaving Monkey , 2005, The Journal of Neuroscience.

[93]  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.

[94]  M. Mascaro,et al.  Temporal evolution and strength of neural activity in parietal cortex during eye and hand movements. , 2007, Cerebral cortex.

[95]  Jessie Chen,et al.  Neural representation of hand kinematics during prehension in posterior parietal cortex of the macaque monkey. , 2009, Journal of neurophysiology.

[96]  Anthony R. Dickinson,et al.  Preparatory Delay Activity in the Monkey Parietal Reach Region Predicts Reach Reaction Times , 2006, The Journal of Neuroscience.

[97]  B. Fischer,et al.  Enhanced activation of neurons in prelunate cortex before visually guided saccades of trained rhesus monkeys , 2004, Experimental Brain Research.

[98]  Paul B. Johnson,et al.  Cortical networks for visual reaching: physiological and anatomical organization of frontal and parietal lobe arm regions. , 1996, Cerebral cortex.

[99]  R A Andersen,et al.  Multimodal integration for the representation of space in the posterior parietal cortex. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[100]  R F Lewis,et al.  Efference copy provides the eye position information required for visually guided reaching. , 1998, Journal of neurophysiology.

[101]  R. Andersen,et al.  Coding of intention in the posterior parietal cortex , 1997, Nature.

[102]  Jessie Chen,et al.  Neurophysiology of prehension. I. Posterior parietal cortex and object-oriented hand behaviors. , 2007, Journal of neurophysiology.

[103]  Michela Gamberini,et al.  ‘Arm‐reaching’ neurons in the parietal area V6A of the macaque monkey , 2001, The European journal of neuroscience.

[104]  Christophe Jouffrais,et al.  Neuronal activity related to eye-hand coordination in the primate premotor cortex , 1999, Experimental Brain Research.

[105]  J D Crawford,et al.  Proprioceptive guidance of saccades in eye-hand coordination. , 2006, Journal of neurophysiology.

[106]  B. C. Motter,et al.  Common and differential effects of attentive fixation on the excitability of parietal and prestriate (V4) cortical visual neurons in the macaque monkey , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[107]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections , 1989, The Journal of comparative neurology.

[108]  G. Luppino,et al.  Cortical connections of the inferior parietal cortical convexity of the macaque monkey. , 2006, Cerebral cortex.

[109]  Lauretta Passarelli,et al.  Somatosensory Cells in Area PEc of Macaque Posterior Parietal Cortex , 2006, The Journal of Neuroscience.

[110]  J. Kalaska,et al.  Proprioceptive activity in primate primary somatosensory cortex during active arm reaching movements. , 1994, Journal of neurophysiology.

[111]  R. Andersen,et al.  Multimodal representation of space in the posterior parietal cortex and its use in planning movements. , 1997, Annual review of neuroscience.

[112]  H. Sakata,et al.  Neural mechanisms of visual guidance of hand action in the parietal cortex of the monkey. , 1995, Cerebral cortex.

[113]  H. Bekkering,et al.  Gaze anchoring to a pointing target is present during the entire pointing movement and is driven by a non-visual signal. , 2001, Journal of neurophysiology.

[114]  W. Maguire,et al.  Visuotopic organization of the prelunate gyrus in rhesus monkey , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[115]  Christopher A. Buneo,et al.  Direct visuomotor transformations for reaching , 2002, Nature.

[116]  J. Crawford,et al.  Gaze-Centered Remapping of Remembered Visual Space in an Open-Loop Pointing Task , 1998, The Journal of Neuroscience.