Transformations for Goal-Directed Action

Much of the central nervous system is involved in visuomotor transformations for goal-directed gaze and reach movements. These transformations are often described in terms of stimulus location, gaze fixation, and reach endpoints, as viewed through the lens of translational geometry. Here, we argue that the intrinsic (primarily rotational) 3-D geometry of the eye-head-reach systems determines the spatial relationship between extrinsic goals and effector commands, and therefore the required transformations. This approach provides a common theoretical framework for understanding both gaze and reach control. Combined with an assessment of the behavioral, neurophysiological, imaging, and neuropsychological literature, this framework leads us to conclude that (a) the internal representation and updating of visual goals are dominated by gaze-centered mechanisms, but (b) these representations must then be transformed as a function of eye and head orientation signals into effector-specific 3-D movement commands.

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

[2]  J Douglas Crawford,et al.  Cue reliability and a landmark stability heuristic determine relative weighting between egocentric and allocentric visual information in memory-guided reach. , 2010, Journal of neurophysiology.

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

[4]  Hiroshi Ono,et al.  The cyclopean eye in vision: the new and old data continue to hit you right between the eyes , 2002, Vision Research.

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

[6]  C R Olson,et al.  Macaque supplementary eye field neurons encode object-centered locations relative to both continuous and discontinuous objects. , 2000, Journal of neurophysiology.

[7]  J. Demer,et al.  Human gaze stabilization during natural activities: translation, rotation, magnification, and target distance effects. , 1997, Journal of neurophysiology.

[8]  H. Gomi Implicit online corrections of reaching movements , 2008, Current Opinion in Neurobiology.

[9]  M. Goodale,et al.  Frames of Reference for Perception and Action in the Human Visual System , 1998, Neuroscience & Biobehavioral Reviews.

[10]  Scott T. Grafton,et al.  Human Posterior Parietal Cortex Flexibly Determines Reference Frames for Reaching Based on Sensory Context , 2010, Neuron.

[11]  Y. Rossetti,et al.  Optic ataxia is not only ‘optic’: Impaired spatial integration of proprioceptive information , 2007, NeuroImage.

[12]  S. Wise,et al.  Visuospatial versus visuomotor activity in the premotor and prefrontal cortex of a primate , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  C. Galletti,et al.  Gaze-dependent visual neurons in area V3A of monkey prestriate cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  Carl R Olson,et al.  Brain representation of object-centered space , 1996, Current Opinion in Neurobiology.

[15]  M. Graziano,et al.  Complex Movements Evoked by Microstimulation of Precentral Cortex , 2002, Neuron.

[16]  Dora E. Angelaki,et al.  Do Motoneurons Encode the Noncommutativity of Ocular Rotations? , 2005, Neuron.

[17]  R. Douglas,et al.  Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades , 2004, Experimental Brain Research.

[18]  Dora E Angelaki,et al.  Three-Dimensional Kinematics at the Level of the Oculomotor Plant , 2006, The Journal of Neuroscience.

[19]  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.

[20]  Michael A Smith,et al.  Distributed population mechanism for the 3-D oculomotor reference frame transformation. , 2005, Journal of neurophysiology.

[21]  K. Hepp,et al.  Smooth pursuit eye movements obey Listing's law in the monkey , 2004, Experimental Brain Research.

[22]  Alexandre Pouget,et al.  Basis Functions for Object-Centered Representations , 2003, Neuron.

[23]  J M Groh,et al.  Saccades to somatosensory targets. III. eye-position-dependent somatosensory activity in primate superior colliculus. , 1996, Journal of neurophysiology.

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

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

[26]  T Vilis,et al.  Symmetry of oculomotor burst neuron coordinates about Listing's plane. , 1992, Journal of neurophysiology.

[27]  H. Collewijn,et al.  A direct test of Listing's law—I. Human ocular torsion measured in static tertiary positions , 1987, Vision Research.

[28]  A. Fuchs,et al.  Activity of brain stem neurons during eye movements of alert monkeys. , 1972, Journal of neurophysiology.

[29]  T Raphan,et al.  Modeling control of eye orientation in three dimensions. I. Role of muscle pulleys in determining saccadic trajectory. , 1998, Journal of neurophysiology.

[30]  Aldo Genovesio,et al.  Integration of retinal disparity and fixation-distance related signals toward an egocentric coding of distance in the posterior parietal cortex of primates. , 2004, Journal of neurophysiology.

[31]  Joseph L Demer,et al.  Current concepts of mechanical and neural factors in ocular motility , 2006, Current opinion in neurology.

[32]  Thomas Schmidt,et al.  Immediate spatial distortions of pointing movements induced by visual landmarks , 2004, Perception & psychophysics.

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

[34]  Carol L Colby,et al.  Oculomotor control and spatial processing , 1992, Current Biology.

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

[36]  George E Stelmach,et al.  Pointing to an allocentric and egocentric remembered target. , 2004, Motor control.

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

[38]  Dora E Angelaki,et al.  Neural Correlates of Forward and Inverse Models for Eye Movements: Evidence from Three-Dimensional Kinematics , 2008, The Journal of Neuroscience.

[39]  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.

[40]  Gerald P. Keith,et al.  Saccade-related remapping of target representations between topographic maps: a neural network study , 2008, Journal of Computational Neuroscience.

[41]  R. Andersen,et al.  Neural Dynamics in Monkey Parietal Reach Region Reflect Context-Specific Sensorimotor Transformations , 2006, The Journal of Neuroscience.

[42]  Eliana M. Klier,et al.  The superior colliculus encodes gaze commands in retinal coordinates , 2001, Nature Neuroscience.

[43]  Francesco Lacquaniti,et al.  Multiple levels of representation of reaching in the parieto-frontal network. , 2003, Cerebral cortex.

[44]  J M Groh,et al.  Saccades to somatosensory targets. II. motor convergence in primate superior colliculus. , 1996, Journal of neurophysiology.

[45]  Pascal Fries,et al.  Neuronal Synchronization in Human Posterior Parietal Cortex during Reach Planning , 2010, The Journal of Neuroscience.

[46]  T Vilis,et al.  Three-dimensional eye, head, and chest orientations after large gaze shifts and the underlying neural strategies. , 1994, Journal of neurophysiology.

[47]  D Tweed,et al.  Implications of rotational kinematics for the oculomotor system in three dimensions. , 1987, Journal of neurophysiology.

[48]  Tony Ro,et al.  Maintenance of Visual Stability in the Human Posterior Parietal Cortex , 2007, Journal of Cognitive Neuroscience.

[49]  U. Büttner,et al.  Saccade-related burst neurons with torsional and vertical on-directions in the interstitial nucleus of Cajal of the alert monkey , 2004, Experimental Brain Research.

[50]  W Pieter Medendorp,et al.  Motion Parallax Is Computed in the Updating of Human Spatial Memory , 2003, The Journal of Neuroscience.

[51]  Melvyn A. Goodale,et al.  The effects of landmarks on the performance of delayed and real-time pointing movements , 2005, Experimental Brain Research.

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

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

[54]  Gunnar Blohm,et al.  Depth estimation from retinal disparity requires eye and head orientation signals. , 2008, Journal of vision.

[55]  D S Zee,et al.  Three-dimensional kinematics of ocular drift in humans with cerebellar atrophy. , 2000, Journal of neurophysiology.

[56]  L M Optican,et al.  Superior colliculus neurons mediate the dynamic characteristics of saccades. , 1991, Journal of neurophysiology.

[57]  James Danckert,et al.  Attention for action? Examining the link between attention and visuomotor control deficits in a patient with optic ataxia , 2009, Neuropsychologia.

[58]  Pascal Fries,et al.  Gamma-Band Activity in Human Posterior Parietal Cortex Encodes the Motor Goal during Delayed Prosaccades and Antisaccades , 2008, The Journal of Neuroscience.

[59]  Joseph L Demer,et al.  Evidence supporting extraocular muscle pulleys: refuting the platygean view of extraocular muscle mechanics. , 2006, Journal of pediatric ophthalmology and strabismus.

[60]  S. Coren,et al.  The dominant eye. , 1976, Psychological bulletin.

[61]  D Guitton,et al.  Human head-free gaze saccades to targets flashed before gaze-pursuit are spatially accurate. , 1998, Journal of neurophysiology.

[62]  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.

[63]  Hongying Wang,et al.  Electrical stimulation of the supplementary eye fields in the head-free macaque evokes kinematically normal gaze shifts. , 2003, Journal of neurophysiology.

[64]  Kenneth F. Valyear,et al.  Human parietal cortex in action , 2006, Current Opinion in Neurobiology.

[65]  M. Graziano,et al.  Probing cortical function with electrical stimulation , 2002, Nature Neuroscience.

[66]  P. Dixon,et al.  A step and a hop on the Müller-Lyer: illusion effects on lower-limb movements , 2004, Experimental Brain Research.

[67]  J D Crawford,et al.  Curvature of Visual Space Under Vertical Eye Rotation: Implications for Spatial Vision and Visuomotor Control , 2000, The Journal of Neuroscience.

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

[69]  Emiliano Brunamonti,et al.  Postsaccadic Activities in the Posterior Parietal Cortex of Primates Are Influenced by both Eye Movement Vectors and Eye Position , 2007, The Journal of Neuroscience.

[70]  Denise Y P Henriques,et al.  Reference frame conversions for repeated arm movements. , 2008, Journal of neurophysiology.

[71]  Gunnar Blohm,et al.  Decoding the cortical transformations for visually guided reaching in 3D space. , 2009, Cerebral cortex.

[72]  Nuo Li,et al.  Updating Visual Space during Motion in Depth , 2005, Neuron.

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

[74]  Michael Petrides,et al.  Anatomical organization of the eye fields in the human and non-human primate frontal cortex , 2009, Progress in Neurobiology.

[75]  D. Heeger,et al.  Topographic organization for delayed saccades in human posterior parietal cortex. , 2005, Journal of neurophysiology.

[76]  T Vilis,et al.  Violations of Listing's law after large eye and head gaze shifts. , 1992, Journal of neurophysiology.

[77]  Madeleine Schlag-Rey,et al.  Frames of reference for saccadic command tested by saccade collision in the supplementary eye field. , 2006, Journal of neurophysiology.

[78]  D. Heeger,et al.  Specificity of Human Cortical Areas for Reaches and Saccades , 2007, The Journal of Neuroscience.

[79]  Gunnar Blohm,et al.  Computations for geometrically accurate visually guided reaching in 3-D space. , 2007, Journal of vision.

[80]  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.

[81]  Jacqueline Gottlieb,et al.  The lateral intraparietal area as a salience map: the representation of abrupt onset, stimulus motion, and task relevance , 2000, Vision Research.

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

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

[84]  T. Flash,et al.  Intrinsic joint kinematic planning. II: Hand-path predictions based on a Listing’s plane constraint , 2006, Experimental Brain Research.

[85]  T. Vilis,et al.  Generation of torsional and vertical eye position signals by the interstitial nucleus of Cajal , 1991, Science.

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

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

[88]  K. P. Krommenhoek,et al.  Evidence for nonretinal feedback in combined version-vergence eye movements , 2004, Experimental Brain Research.

[89]  D. Munoz,et al.  Look away: the anti-saccade task and the voluntary control of eye movement , 2004, Nature Reviews Neuroscience.

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

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

[92]  Denise Y P Henriques,et al.  Updating visual memory across eye movements for ocular and arm motor control. , 2008, Journal of neurophysiology.

[93]  Tandra Ghose,et al.  Relative image size, not eye position, determines eye dominance switches , 2004, Vision Research.

[94]  Gunnar Blohm,et al.  A model that integrates eye velocity commands to keep track of smooth eye displacements , 2006, Journal of Computational Neuroscience.

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

[96]  Y. Rossetti,et al.  Optic ataxia errors depend on remapped, not viewed, target location , 2005, Nature Neuroscience.

[97]  M. Schlag-Rey,et al.  Saccades can be aimed at the spatial location of targets flashed during pursuit. , 1990, Journal of neurophysiology.

[98]  G. Baylis,et al.  Visually misguided reaching in Balint's syndrome , 2001, Neuropsychologia.

[99]  A. Pouget,et al.  Reference frames for representing visual and tactile locations in parietal cortex , 2005, Nature Neuroscience.

[100]  W Pieter Medendorp,et al.  Rotational Remapping in Human Spatial Memory during Eye and Head Motion , 2002, The Journal of Neuroscience.

[101]  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.

[102]  Laure Pisella,et al.  The contribution of spatial remapping impairments to unilateral visual neglect , 2004, Neuroscience & Biobehavioral Reviews.

[103]  W. Graf,et al.  Functional anatomy of the head-neck movement system of quadrupedal and bipedal mammals. , 1995, Journal of anatomy.

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

[105]  F. Tremblay,et al.  Cortico-motor excitability of the lower limb motor representation: a comparative study in Parkinson's disease and healthy controls , 2002, Clinical Neurophysiology.

[106]  Tutis Vilis,et al.  Human parietal "reach region" primarily encodes intrinsic visual direction, not extrinsic movement direction, in a visual motor dissociation task. , 2007, Cerebral cortex.

[107]  J D Crawford,et al.  Frames of reference for gaze saccades evoked during stimulation of lateral intraparietal cortex. , 2007, Journal of neurophysiology.

[108]  Kikuro Fukushima,et al.  The interstitial nucleus of Cajal in the midbrain reticular formation and vertical eye movement , 1991, Neuroscience Research.

[109]  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.

[110]  Bruno B Averbeck,et al.  Neural Ensemble Decoding Reveals a Correlate of Viewer- to Object-Centered Spatial Transformation in Monkey Parietal Cortex , 2008, The Journal of Neuroscience.

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

[112]  J. Crawford,et al.  The oculomotor neural integrator uses a behavior-related coordinate system , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[113]  E. M. Klier,et al.  Human oculomotor system accounts for 3-D eye orientation in the visual-motor transformation for saccades. , 1998, Journal of neurophysiology.

[114]  M. Sereno,et al.  Mapping of Contralateral Space in Retinotopic Coordinates by a Parietal Cortical Area in Humans , 2001, Science.

[115]  D. Sparks,et al.  Eye-head coordination during head-unrestrained gaze shifts in rhesus monkeys. , 1997, Journal of neurophysiology.

[116]  P. E. Hallett,et al.  Primary and secondary saccades to goals defined by instructions , 1978, Vision Research.

[117]  Yale E Cohen,et al.  Motor-related signals in the intraparietal cortex encode locations in a hybrid, rather than eye-centered reference frame. , 2009, Cerebral cortex.

[118]  P. Goldman-Rakic Working memory and the mind. , 1992, Scientific American.

[119]  Richard A Andersen,et al.  Parietal reach region encodes reach depth using retinal disparity and vergence angle signals. , 2009, Journal of neurophysiology.

[120]  Dora E Angelaki,et al.  Do Visual Cues Contribute to the Neural Estimate of Viewing Distance Used by the Oculomotor System? , 2003, The Journal of Neuroscience.

[121]  Laurette Hay,et al.  Response delay and spatial representation in pointing movements , 2006, Neuroscience Letters.

[122]  Zoubin Ghahramani,et al.  Computational principles of movement neuroscience , 2000, Nature Neuroscience.

[123]  Stefan Schaal,et al.  Forward models in visuomotor control. , 2002, Journal of neurophysiology.

[124]  T Vilis,et al.  Rapid eye movement generation in the primate. Physiology, pathophysiology, and clinical implications. , 1989, Revue neurologique.

[125]  Eliana M. Klier,et al.  Midbrain Control of Three-Dimensional Head Orientation , 2002, Science.

[126]  J. Tanji,et al.  Differential roles of neuronal activity in the supplementary and presupplementary motor areas: from information retrieval to motor planning and execution. , 2004, Journal of neurophysiology.

[127]  W Pieter Medendorp,et al.  Updating target distance across eye movements in depth. , 2008, Journal of neurophysiology.

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

[129]  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.

[130]  T. Schenk,et al.  An allocentric rather than perceptual deficit in patient D.F. , 2006, Nature Neuroscience.

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

[132]  Lawrence H Snyder,et al.  Spatial memory following shifts of gaze. I. Saccades to memorized world-fixed and gaze-fixed targets. , 2003, Journal of neurophysiology.

[133]  W P Medendorp,et al.  Visuospatial memory computations during whole-body rotations in roll. , 2005, Journal of neurophysiology.

[134]  W P Medendorp,et al.  Donders' law in torticollis. , 1999, Journal of neurophysiology.

[135]  T. Vilis,et al.  Remapping the remembered target location for anti-saccades in human posterior parietal cortex. , 2005, Journal of neurophysiology.

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

[137]  W P Medendorp,et al.  Context compensation in the vestibuloocular reflex during active head rotations. , 2000, Journal of neurophysiology.

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

[139]  S. Scott The role of primary motor cortex in goal-directed movements: insights from neurophysiological studies on non-human primates , 2003, Current Opinion in Neurobiology.

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

[141]  C. Gielen,et al.  Geometric computations underlying eye-hand coordination: orientations of the two eyes and the head , 2003, Experimental Brain Research.

[142]  Dora E Angelaki,et al.  Foveal Versus Full-Field Visual Stabilization Strategies for Translational and Rotational Head Movements , 2003, The Journal of Neuroscience.

[143]  Jonathan D. Nelson,et al.  Multiple Parietal Reach Regions in Humans: Cortical Representations for Visual and Proprioceptive Feedback during On-Line Reaching , 2009, The Journal of Neuroscience.

[144]  Shinsuke Shimojo,et al.  Extrinsic Cues Suppress the Encoding of Intrinsic Cues , 2004, Journal of Cognitive Neuroscience.

[145]  D Guitton,et al.  Visual-motor transformations required for accurate and kinematically correct saccades. , 1997, Journal of neurophysiology.

[146]  Yves Rossetti,et al.  Impairment of gaze-centered updating of reach targets in bilateral parietal-occipital damaged patients. , 2005, Cerebral cortex.

[147]  P. Medendorp,et al.  Visuospatial updating of reaching targets in near and far space , 2002, Neuroreport.

[148]  K Hepp,et al.  Two- rather than three-dimensional representation of saccades in monkey superior colliculus. , 1991, Science.

[149]  J. Schall,et al.  Neural selection and control of visually guided eye movements. , 1999, Annual review of neuroscience.

[150]  Matthew Heath,et al.  Background visual cues and memory-guided reaching. , 2004, Human movement science.

[151]  J D Crawford,et al.  Implications of ocular kinematics for the internal updating of visual space. , 2001, Journal of neurophysiology.

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

[153]  R. Shadmehr,et al.  Why Does the Brain Predict Sensory Consequences of Oculomotor Commands? Optimal Integration of the Predicted and the Actual Sensory Feedback , 2006, The Journal of Neuroscience.

[154]  Philip N. Sabes,et al.  Parietal representation of object-based saccades. , 2002, Journal of neurophysiology.

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

[156]  Dora E Angelaki,et al.  Roles of gravitational cues and efference copy signals in the rotational updating of memory saccades. , 2005, Journal of neurophysiology.

[157]  J. Kalaska,et al.  Neural mechanisms for interacting with a world full of action choices. , 2010, Annual review of neuroscience.

[158]  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.

[159]  A. G. Feldman Once More on the Equilibrium-Point Hypothesis (λ Model) for Motor Control , 1986 .

[160]  R. Johansson,et al.  Gaze behavior when reaching to remembered targets. , 2008, Journal of neurophysiology.

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

[162]  Xiaogang Yan,et al.  Specificity of Human Parietal Saccade and Reach Regions during Transcranial Magnetic Stimulation , 2010, The Journal of Neuroscience.

[163]  Gunnar Blohm,et al.  Processing of retinal and extraretinal signals for memory-guided saccades during smooth pursuit. , 2005, Journal of neurophysiology.

[164]  Casper J. Erkelens,et al.  Binocular Visual Direction , 1994, Vision Research.

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

[166]  A. V. van den Berg,et al.  Representation of heading direction in far and near head space , 2003, Experimental Brain Research.

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

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

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

[170]  P. E. Hallett,et al.  Saccadic eye movements towards stimuli triggered by prior saccades , 1976, Vision Research.

[171]  Aldo Genovesio,et al.  Parietal encoding of action in depth , 2009, Neuropsychologia.

[172]  L. Optican,et al.  Commutative saccadic generator is sufficient to control a 3-D ocular plant with pulleys. , 1998, Journal of neurophysiology.

[173]  S. Highstein,et al.  The anatomy and physiology of primate neurons that control rapid eye movements. , 1994, Annual review of neuroscience.

[174]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[175]  Dora E Angelaki,et al.  Human visuospatial updating after noncommutative rotations. , 2007, Journal of neurophysiology.

[176]  Mingsha Zhang,et al.  Neuronal switching of sensorimotor transformations for antisaccades , 2000, Nature.

[177]  H Misslisch,et al.  Neural and mechanical factors in eye control. , 2001, Journal of neurophysiology.

[178]  A John Van Opstal,et al.  Gaze orienting in dynamic visual double steps. , 2005, Journal of neurophysiology.

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

[180]  Denise Y. P. Henriques,et al.  Memory for proprioceptive and multisensory targets is partially coded relative to gaze , 2010, Neuropsychologia.

[181]  Ian P. Howard,et al.  Binocular Vision and Stereopsis , 1996 .

[182]  Dora E Angelaki,et al.  Human visuospatial updating after passive translations in three-dimensional space. , 2008, Journal of neurophysiology.

[183]  I. Toni,et al.  Spatial and effector processing in the human parietofrontal network for reaches and saccades. , 2009, Journal of neurophysiology.

[184]  Hongying Wang,et al.  Contribution of head movement to gaze command coding in monkey frontal cortex and superior colliculus. , 2003, Journal of neurophysiology.

[185]  G. S. Russo,et al.  Supplementary eye field: representation of saccades and relationship between neural response fields and elicited eye movements. , 2000, Journal of neurophysiology.

[186]  K Hepp,et al.  Monkey superior colliculus represents rapid eye movements in a two-dimensional motor map. , 1993, Journal of neurophysiology.

[187]  P. Viviani,et al.  Error parsing in visuomotor pointing reveals independent processing of amplitude and direction. , 2005, Journal of neurophysiology.

[188]  R. Shadmehr,et al.  A Real-Time State Predictor in Motor Control: Study of Saccadic Eye Movements during Unseen Reaching Movements , 2002, The Journal of Neuroscience.

[189]  Hongying Wang,et al.  Three-dimensional eye-head coordination is implemented downstream from the superior colliculus. , 2003, Journal of neurophysiology.

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

[191]  Peter Dayan,et al.  Doubly Distributional Population Codes: Simultaneous Representation of Uncertainty and Multiplicity , 2003, Neural Computation.

[192]  T. Vilis,et al.  Computing three-dimensional eye position quaternions and eye velocity from search coil signals , 1990, Vision Research.

[193]  W Pieter Medendorp,et al.  Gaze-centered updating of remembered visual space during active whole-body translations. , 2007, Journal of neurophysiology.

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

[195]  Dora E Angelaki,et al.  Primate memory saccade amplitude after intervened motion depends on target distance. , 2005, Journal of neurophysiology.

[196]  Sabine Kastner,et al.  Topographic maps in human frontal cortex revealed in memory-guided saccade and spatial working-memory tasks. , 2007, Journal of neurophysiology.

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

[198]  A. Opstal,et al.  Influence of eye position on activity in monkey superior colliculus. , 1995, Journal of neurophysiology.

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

[200]  J D Crawford,et al.  Role of eye, head, and shoulder geometry in the planning of accurate arm movements. , 2002, Journal of neurophysiology.

[201]  Christian Quaia,et al.  The maintenance of spatial accuracy by the perisaccadic remapping of visual receptive fields , 1998, Neural Networks.

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

[203]  Julio Martinez-Trujillo,et al.  Electrical stimulation of the frontal eye fields in the head-free macaque evokes kinematically normal 3D gaze shifts. , 2010, Journal of neurophysiology.

[204]  P. Strick,et al.  Imaging the premotor areas , 2001, Current Opinion in Neurobiology.

[205]  R. Wurtz,et al.  Brain circuits for the internal monitoring of movements. , 2008, Annual review of neuroscience.

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

[207]  G Blohm,et al.  Saccadic compensation for smooth eye and head movements during head-unrestrained two-dimensional tracking. , 2010, Journal of neurophysiology.