Integration of target and hand position signals in the posterior parietal cortex: effects of workspace and hand vision.

Previous findings suggest the posterior parietal cortex (PPC) contributes to arm movement planning by transforming target and limb position signals into a desired reach vector. However, the neural mechanisms underlying this transformation remain unclear. In the present study we examined the responses of 109 PPC neurons as movements were planned and executed to visual targets presented over a large portion of the reaching workspace. In contrast to previous studies, movements were made without concurrent visual and somatic cues about the starting position of the hand. For comparison, a subset of neurons was also examined with concurrent visual and somatic hand position cues. We found that single cells integrated target and limb position information in a very consistent manner across the reaching workspace. Approximately two-thirds of the neurons with significantly tuned activity (42/61 and 30/46 for left and right workspaces, respectively) coded targets and initial hand positions separably, indicating no hand-centered encoding, whereas the remaining one-third coded targets and hand positions inseparably, in a manner more consistent with the influence of hand-centered coordinates. The responses of both types of neurons were largely invariant with respect to the presence or absence of visual hand position cues, suggesting their corresponding coordinate frames and gain effects were unaffected by cue integration. The results suggest that the PPC uses a consistent scheme for computing reach vectors in different parts of the workspace that is robust to changes in the availability of somatic and visual cues about hand position.

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

[2]  Christopher A. Buneo,et al.  Time-invariant reference frames for parietal reach activity , 2008, Experimental Brain Research.

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

[4]  Christopher A. Buneo,et al.  Analyzing neural responses with vector fields , 2011, Journal of Neuroscience Methods.

[5]  R. Andersen,et al.  Reaches to Sounds Encoded in an Eye-Centered Reference Frame , 2000, Neuron.

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

[7]  W Pieter Medendorp,et al.  Behavioral reference frames for planning human reaching movements. , 2006, Journal of neurophysiology.

[8]  Philip N. Sabes,et al.  Sensory transformations and the use of multiple reference frames for reach planning , 2009, Nature Neuroscience.

[9]  G. DeAngelis,et al.  Multisensory integration: psychophysics, neurophysiology, and computation , 2009, Current Opinion in Neurobiology.

[10]  R. Andersen,et al.  The posterior parietal cortex: Sensorimotor interface for the planning and online control of visually guided movements , 2006, Neuropsychologia.

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

[12]  R. Andersen,et al.  Eye-centered, head-centered, and intermediate coding of remembered sound locations in area LIP. , 1996, Journal of neurophysiology.

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

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

[15]  Philip N. Sabes,et al.  Heterogeneous Representations in the Superior Parietal Lobule Are Common across Reaches to Visual and Proprioceptive Targets , 2011, The Journal of Neuroscience.

[16]  G. Binsted,et al.  Visuomotor representation decay: influence on motor systems , 2006, Experimental Brain Research.

[17]  Xiaogang Yan,et al.  Transcranial magnetic stimulation over human dorsal-lateral posterior parietal cortex disrupts integration of hand position signals into the reach plan. , 2008, Journal of neurophysiology.

[18]  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.

[19]  Kenji Matsuura,et al.  Vector Correlation: Review, Exposition, and Geographic Application , 1992 .

[20]  Philippe Souères,et al.  Eye-centered vs body-centered reaching control: A robotics insight into the neuroscience debate , 2009, 2009 IEEE International Conference on Robotics and Biomimetics (ROBIO).

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

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

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

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

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

[26]  Y. Petrov,et al.  Crowding is directed to the fovea and preserves only feature contrast. , 2007, Journal of vision.

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

[28]  M S Graziano,et al.  Coding the location of the arm by sight. , 2000, Science.

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

[30]  J D Crawford,et al.  Spatial transformations for eye-hand coordination. , 2004, Journal of neurophysiology.

[31]  Michael I. Jordan,et al.  An internal model for sensorimotor integration. , 1995, Science.

[32]  M Konishi,et al.  Auditory Spatial Receptive Fields Created by Multiplication , 2001, Science.

[33]  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.

[34]  Steve W. C. Chang,et al.  Using a Compound Gain Field to Compute a Reach Plan , 2009, Neuron.

[35]  Emiliano Brunamonti,et al.  Reaching in Depth: Hand Position Dominates over Binocular Eye Position in the Rostral Superior Parietal Lobule , 2009, The Journal of Neuroscience.

[36]  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.

[37]  Y Agid,et al.  Temporal limits of spatial working memory in humans , 1998, The European journal of neuroscience.

[38]  Konrad Paul Kording,et al.  Bayesian integration in sensorimotor learning , 2004, Nature.

[39]  Philip N. Sabes,et al.  Multisensory Integration during Motor Planning , 2003, The Journal of Neuroscience.

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

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

[42]  Bijan Pesaran,et al.  A Relative Position Code for Saccades in Dorsal Premotor Cortex , 2010, The Journal of Neuroscience.

[43]  Philip N. Sabes,et al.  Flexible strategies for sensory integration during motor planning , 2005, Nature Neuroscience.

[44]  I. Toni,et al.  Reference frames for reach planning in human parietofrontal cortex. , 2010, Journal of neurophysiology.

[45]  Dylan F. Cooke,et al.  Distribution of hand location in monkeys during spontaneous behavior , 2004, Experimental Brain Research.

[46]  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.

[47]  Gunnar Blohm,et al.  Influence of initial hand and target position on reach errors in optic ataxic and normal subjects. , 2007, Journal of vision.