Multiple levels of representation of reaching in the parieto-frontal network.

In daily life, hand and eye movements occur in different contexts. Hand movements can be made to a visual target shortly after its presentation, or after a longer delay; alternatively, they can be made to a memorized target location. In both instances, the hand can move in a visually structured scene under normal illumination, which allows visual monitoring of its trajectory, or in darkness. Across these conditions, movement can be directed to points in space already foveated, or to extrafoveal ones, thus requiring different forms of eye-hand coordination. The ability to adapt to these different contexts by providing successful answers to their demands probably resides in the high degree of flexibility of the operations that govern cognitive visuomotor behavior. The neurophysiological substrates of these processes include, among others, the context-dependent nature of neural activity, and a transitory, or task-dependent, affiliation of neurons to the assemblies underlying different forms of sensorimotor behavior. Moreover, the ability to make independent or combined eye and hand movements in the appropriate order and time sequence must reside in a process that encodes retinal-, eye- and hand-related inputs in a spatially congruent fashion. This process, in fact, requires exact knowledge of where the eye and the hand are at any given time, although we have no or little conscious experience of where they stay at any instant. How this information is reflected in the activity of cortical neurons remains a central question to understanding the mechanisms underlying the planning of eye-hand movement in the cerebral cortex. In the last 10 years, psychophysical analyses in humans, as well as neurophysiological studies in monkeys, have provided new insights on the mechanisms of different forms of oculo-manual actions. These studies have also offered preliminary hints as to the cortical substrates of eye-hand coordination. In this review, we will highlight some of the results obtained as well as some of the questions raised, focusing on the role of eye- and hand-tuning signals in cortical neural activity. This choice rests on the crucial role this information exerts in the specification of movement, and coordinate transformation.

[1]  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.

[2]  A. B. Mayer,et al.  Visuomotor transformations: early cortical mechanisms of reaching , 1998, Current Opinion in Neurobiology.

[3]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  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.

[5]  Stephen H. Scott,et al.  Overlap of internal models in motor cortex for mechanical loads during reaching , 2002, Nature.

[6]  J. Vercher,et al.  The role of ocular muscle proprioception in visual localization of targets. , 1990, Science.

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

[8]  Klaus-Peter Hoffmann,et al.  Temporal relation of population activity in visual areas MT/MST and in primary motor cortex during visually guided tracking movements. , 2002, Cerebral cortex.

[9]  D. Sparks,et al.  Combined eye-head gaze shifts produced by electrical stimulation of the superior colliculus in rhesus monkeys. , 1996, Journal of neurophysiology.

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

[11]  F. Bremmer,et al.  Spatial invariance of visual receptive fields in parietal cortex neurons , 1997, Nature.

[12]  F. Lacquaniti,et al.  Combination of hand and gaze signals during reaching: activity in parietal area 7 m of the monkey. , 1997, Journal of neurophysiology.

[13]  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.

[14]  L H Snyder,et al.  Saccade-related activity in the parietal reach region. , 2000, Journal of neurophysiology.

[15]  Alexandra Battaglia-Mayer,et al.  Optic ataxia as a result of the breakdown of the global tuning fields of parietal neurones. , 2002, Brain : a journal of neurology.

[16]  C Ghez,et al.  Learning of Visuomotor Transformations for Vectorial Planning of Reaching Trajectories , 2000, The Journal of Neuroscience.

[17]  A. Georgopoulos Higher order motor control. , 1991, Annual review of neuroscience.

[18]  J. F. Soechting,et al.  Sensorimotor representations for pointing to targets in three-dimensional space. , 1989, Journal of neurophysiology.

[19]  L. Snyder Coordinate transformations for eye and arm movements in the brain , 2000, Current Opinion in Neurobiology.

[20]  J. Kalaska,et al.  Simultaneous encoding of multiple potential reach directions in dorsal premotor cortex. , 2002, Journal of neurophysiology.

[21]  T. Ebner,et al.  Neuronal specification of direction and distance during reaching movements in the superior precentral premotor area and primary motor cortex of monkeys. , 1993, Journal of neurophysiology.

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

[23]  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.

[24]  Francesco Lacquaniti,et al.  Cognitive allocentric representations of visual space shape pointing errors , 2002, Experimental Brain Research.

[25]  Driss Boussaoud,et al.  Effects of gaze on apparent visual responses of frontal cortex neurons , 2004, Experimental Brain Research.

[26]  H. Sakata,et al.  From Three-Dimensional Space Vision to Prehensile Hand Movements: The Lateral Intraparietal Area Links the Area V3A and the Anterior Intraparietal Area in Macaques , 2001, The Journal of Neuroscience.

[27]  S. Scott,et al.  Dissociation between hand motion and population vectors from neural activity in motor cortex , 2022 .

[28]  F. Lacquaniti,et al.  Short-Term Memory for Reaching to Visual Targets: Psychophysical Evidence for Body-Centered Reference Frames , 1998, The Journal of Neuroscience.

[29]  J. F. Soechting,et al.  Transformation from Head- to Shoulder-Centered Representation of Target Direction in Arm Movements , 1990, Journal of Cognitive Neuroscience.

[30]  D. Amit,et al.  The eye and the hand: neural mechanisms and network models for oculomanual coordination in parietal cortex. , 2003, Cerebral cortex.

[31]  B. Bridgeman,et al.  Interaction of cognitive and sensorimotor maps of visual space , 1997, Perception & psychophysics.

[32]  Robert L. Sainburg,et al.  Spatial representations and internal models of limb dynamics in motor learning , 1999 .

[33]  F. Duffy,et al.  Somatosensory System: Organizational Hierarchy from Single Units in Monkey Area 5 , 1971, Science.

[34]  L E Mays,et al.  Neurons in monkey parietal area LIP are tuned for eye-movement parameters in three-dimensional space. , 1995, Journal of neurophysiology.

[35]  Paul B. Johnson,et al.  Visuomotor transformations underlying arm movements toward visual targets: a neural network model of cerebral cortical operations , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  F. Lacquaniti,et al.  Viewer-centered and body-centered frames of reference in direct visuomotor transformations , 1999, Experimental Brain Research.

[37]  R. Johansson,et al.  Eye–Hand Coordination in Object Manipulation , 2001, The Journal of Neuroscience.

[38]  Paul B. Johnson,et al.  Making arm movements within different parts of space: dynamic aspects in the primate motor cortex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  U Salvolini,et al.  Mechanical noxious stimuli cause bilateral activation of parietal operculum in callosotomized subjects. , 2002, Cerebral cortex.

[40]  J. Kalaska,et al.  Differential relation of discharge in primary motor cortex and premotor cortex to movements versus actively maintained postures during a reaching task , 1996, Experimental Brain Research.

[41]  J. F. Soechting,et al.  Early stages in a sensorimotor transformation , 1992, Behavioral and Brain Sciences.

[42]  L. Bianchi,et al.  Posterior parietal cortex: functional properties of neurons in area 5 during an instructed-delay reaching task within different parts of space , 2004, Experimental Brain Research.

[43]  R. Andersen,et al.  Head position signals used by parietal neurons to encode locations of visual stimuli , 1995, Nature.

[44]  C R Olson,et al.  Object-centered direction selectivity in the macaque supplementary eye field , 1995, Science.

[45]  Paul B. Johnson,et al.  Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. , 1997, Annual review of neuroscience.

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

[47]  D. Wolpert,et al.  Evidence for an eye-centered spherical representation of the visuomotor map. , 1999, Journal of neurophysiology.

[48]  F Bremmer,et al.  Eye position effects on the neuronal activity of dorsal premotor cortex in the macaque monkey. , 1998, Journal of neurophysiology.

[49]  E. Bizzi,et al.  Neuronal Correlates of Motor Performance and Motor Learning in the Primary Motor Cortex of Monkeys Adapting to an External Force Field , 2001, Neuron.

[50]  R. Andersen,et al.  Models of the Posterior Parietal Cortex Which Perform Multimodal Integration and Represent Space in Several Coordinate Frames , 2000, Journal of Cognitive Neuroscience.

[51]  Francesco Lacquaniti,et al.  Early motor influences on visuomotor transformations for reaching: a positive image of optic ataxia , 1998, Experimental Brain Research.

[52]  J. F. Soechting,et al.  Errors in pointing are due to approximations in sensorimotor transformations. , 1989, Journal of neurophysiology.

[53]  A. P. Georgopoulos,et al.  Primate motor cortex and free arm movements to visual targets in three- dimensional space. III. Positional gradients and population coding of movement direction from various movement origins , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[55]  P. P. Battaglini,et al.  Parietal neurons encoding spatial locations in craniotopic coordinates , 2004, Experimental Brain Research.

[56]  A B Schwartz,et al.  Direct cortical representation of drawing. , 1994, Science.

[57]  C R Olson,et al.  Macaque SEF neurons encode object-centered directions of eye movements regardless of the visual attributes of instructional cues. , 1999, Journal of neurophysiology.

[58]  Yale E. Cohen,et al.  A common reference frame for movement plans in the posterior parietal cortex , 2002, Nature Reviews Neuroscience.

[59]  Carolyn R. Mason,et al.  Central processes for the multiparametric control of arm movements in primates , 2001, Current Opinion in Neurobiology.

[60]  L. Abbott,et al.  A model of multiplicative neural responses in parietal cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[61]  Alexandre Pouget,et al.  A computational perspective on the neural basis of multisensory spatial representations , 2002, Nature Reviews Neuroscience.

[62]  A. Georgopoulos Cognitive motor control: spatial and temporal aspects , 2002, Current Opinion in Neurobiology.

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

[64]  F. Lacquaniti,et al.  Viewer-centered frame of reference for pointing to memorized targets in three-dimensional space. , 1997, Journal of neurophysiology.

[65]  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.

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

[67]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[68]  Jacques Droulez,et al.  Analysis of Pointing Errors Reveals Properties of Data Representations and Coordinate Transformations Within the Central Nervous System , 2000, Neural Computation.

[69]  A. Pouget,et al.  Efficient computation and cue integration with noisy population codes , 2001, Nature Neuroscience.

[70]  F. Lacquaniti,et al.  Representing spatial information for limb movement: role of area 5 in the monkey. , 1995, Cerebral cortex.

[71]  J. F. Soechting,et al.  Similarity in the response of smooth pursuit and manual tracking to a change in the direction of target motion. , 2000, Journal of neurophysiology.

[72]  Richard A. Andersen,et al.  A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons , 1988, Nature.

[73]  A. P. Georgopoulos,et al.  Movement parameters and neural activity in motor cortex and area 5. , 1994, Cerebral cortex.

[74]  Alexandre Pouget,et al.  Computational approaches to sensorimotor transformations , 2000, Nature Neuroscience.

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

[76]  G. Rizzolatti,et al.  The organization of the cortical motor system: new concepts. , 1998, Electroencephalography and clinical neurophysiology.

[77]  J. Simpson The accessory optic system. , 1984, Annual review of neuroscience.

[78]  F. Lacquaniti,et al.  Early coding of reaching in the parietooccipital cortex. , 2000, Journal of neurophysiology.

[79]  A. Georgopoulos,et al.  Static spatial effects in motor cortex and area 5: Quantitative relations in a two-dimensional space , 1984, Experimental Brain Research.

[80]  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.

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

[82]  H. Bekkering,et al.  Ocular gaze is anchored to the target of an ongoing pointing movement. , 2000, Journal of neurophysiology.

[83]  J. Kalaska,et al.  Tactile activity in primate primary somatosensory cortex during active arm movements: correlation with receptive field properties. , 1994, Journal of neurophysiology.

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

[85]  R Caminiti,et al.  Making arm movements within different parts of space: the premotor and motor cortical representation of a coordinate system for reaching to visual targets , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[86]  C. Galletti,et al.  Eye Position Influence on the Parieto‐occipital Area PO (V6) of the Macaque Monkey , 1995, The European journal of neuroscience.

[87]  H. Sakata,et al.  Parietal control of hand action , 1994, Current Opinion in Neurobiology.

[88]  D. Rosenbaum Human movement initiation: specification of arm, direction, and extent. , 1980, Journal of experimental psychology. General.

[89]  J. T. Enright,et al.  The non-visual impact of eye orientation on eye—hand coordination , 1995, Vision Research.

[90]  J W Gnadt,et al.  Eye movements in depth: What does the monkey's parietal cortex tell the superior colliculus? , 1998, Neuroreport.

[91]  A. P. Georgopoulos,et al.  Cortical mechanisms related to the direction of two-dimensional arm movements: relations in parietal area 5 and comparison with motor cortex , 1983, Experimental Brain Research.

[92]  F. Lacquaniti,et al.  Eye-hand coordination during reaching. I. Anatomical relationships between parietal and frontal cortex. , 2001, Cerebral cortex.

[93]  H. Sakata,et al.  Spatial properties of visual fixation neurons in posterior parietal association cortex of the monkey. , 1980, Journal of neurophysiology.

[94]  R. Wurtz,et al.  Signal transformations from cerebral cortex to superior colliculus for the generation of saccades , 2001, Vision Research.

[95]  T. Ebner,et al.  Temporal encoding of movement kinematics in the discharge of primate primary motor and premotor neurons. , 1995, Journal of neurophysiology.

[96]  M. Jeannerod,et al.  The coordination of eye, head, and arm movements during reaching at a single visual target , 2004, Experimental Brain Research.

[97]  D. Hoffman,et al.  Muscle and movement representations in the primary motor cortex. , 1999, Science.

[98]  O. Bock,et al.  Contribution of retinal versus extraretinal signals towards visual localization in goal-directed movements , 2004, Experimental Brain Research.

[99]  Paul Cisek,et al.  Modest gaze-related discharge modulation in monkey dorsal premotor cortex during a reaching task performed with free fixation. , 2002, Journal of neurophysiology.

[100]  P Viviani,et al.  Pointing to Kinesthetic Targets in Space , 1998, The Journal of Neuroscience.

[101]  D. Boussaoud,et al.  Gaze effects in the cerebral cortex: reference frames for space coding and action , 1999, Experimental Brain Research.

[102]  M. Land,et al.  The Roles of Vision and Eye Movements in the Control of Activities of Daily Living , 1998, Perception.

[103]  R H Wurtz,et al.  Disparity sensitivity of frontal eye field neurons. , 2000, Journal of neurophysiology.

[104]  J F Soechting,et al.  Moving in three-dimensional space: frames of reference, vectors, and coordinate systems. , 1992, Annual review of neuroscience.

[105]  G C DeAngelis,et al.  The physiology of stereopsis. , 2001, Annual review of neuroscience.

[106]  C. Galletti,et al.  Functional Demarcation of a Border Between Areas V6 and V6A in the Superior Parietal Gyrus of the Macaque Monkey , 1996, The European journal of neuroscience.

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

[108]  V B Mountcastle,et al.  The parietal system and some higher brain functions. , 1995, Cerebral cortex.

[109]  J. Soechting,et al.  Somatosensory cortical activity in relation to arm posture: nonuniform spatial tuning. , 1996, Journal of neurophysiology.

[110]  D L Sparks,et al.  Activity of cells in the deeper layers of the superior colliculus of the rhesus monkey: evidence for a gaze displacement command. , 1997, Journal of neurophysiology.

[111]  Anthony R. Dickinson,et al.  Eye-hand coordination: saccades are faster when accompanied by a coordinated arm movement. , 2002, Journal of neurophysiology.

[112]  H. Sakata,et al.  The TINS Lecture The parietal association cortex in depth perception and visual control of hand action , 1997, Trends in Neurosciences.

[113]  C Galletti,et al.  Superior area 6 afferents from the superior parietal lobule in the macaque monkey , 1998, The Journal of comparative neurology.

[114]  R. Andersen,et al.  Intentional maps in posterior parietal cortex. , 2002, Annual review of neuroscience.

[115]  John F. Kalaska,et al.  Spatial coding of movement: A hypothesis concerning the coding of movement direction by motor cortical populations , 1983 .

[116]  Paul B. Johnson,et al.  The sources of visual information to the primate frontal lobe: a novel role for the superior parietal lobule. , 1996, Cerebral cortex.

[117]  D. Boussaoud Primate premotor cortex: modulation of preparatory neuronal activity by gaze angle. , 1995, Journal of neurophysiology.

[118]  C. Prablanc,et al.  Automatic control during hand reaching at undetected two-dimensional target displacements. , 1992, Journal of neurophysiology.

[119]  D M Wolpert,et al.  Context estimation for sensorimotor control. , 2000, Journal of neurophysiology.

[120]  T. Sejnowski,et al.  Spatial Transformations in the Parietal Cortex Using Basis Functions , 1997, Journal of Cognitive Neuroscience.

[121]  D. Hoffman,et al.  Direction of action is represented in the ventral premotor cortex , 2001, Nature Neuroscience.

[122]  F Lacquaniti,et al.  A hybrid frame of reference for visuo-manual coordination. , 1994, Neuroreport.

[123]  R. Gellman,et al.  The contribution of retinal and extraretinal signals to manual tracking movements , 2004, Experimental Brain Research.

[124]  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.

[125]  R. Caminiti,et al.  Cortical networks for visual reaching , 2004, Experimental Brain Research.

[126]  H. Sakata,et al.  Somatosensory properties of neurons in the superior parietal cortex (area 5) of the rhesus monkey. , 1973, Brain research.

[127]  J. Tanji,et al.  Rostrocaudal distinction of the dorsal premotor area based on oculomotor involvement. , 2000, Journal of neurophysiology.

[128]  O J Grüsser,et al.  Localization and responses of neurones in the parieto‐insular vestibular cortex of awake monkeys (Macaca fascicularis). , 1990, The Journal of physiology.