The encoding of saccadic eye movements within human posterior parietal cortex

Over the last few years, several functionally distinct subregions of the posterior parietal cortex (PPC) have been shown to subserve oculomotor control. Since these areas seem to overlap with regions whose activation is related to attention, we used functional magnetic resonance imaging to compare the cerebral activation pattern evoked by eye movements with different attentional loads, i.e., oscillatory saccades with different frequencies, as well as predictable, and unpredictable saccades. Our results show activation in largely overlapping networks with differing strength of activity and symmetry of involved areas. Predictable saccades having the shortest saccadic latency led to the most pronounced cerebral activity both in terms of cortical areas involved and signal intensity. Predictable and unpredictable saccades were dominated by activation within the right hemisphere, whereas oscillatory saccades showing the longest saccadic latency were dominated by activation within the left hemisphere. In all tasks, the centers of gravity of activation occurred within the posterior part of the intraparietal sulcus (IPS), while the predictable saccades additionally activated its anterior part. The enhanced activity during the execution of predictable saccades was probably related to top-down processing and/or the preparation of the upcoming eye movement. The hemispheric difference could arise from a predominant role of the right PPC for shifting spatial attention and the left PPC for shifting temporal attention. The differential encoding of saccadic eye movements within IPS indicates that the PPC splits up into different functional modules related to the particular demands of a saccade.

[1]  Stephen M. Rao,et al.  The evolution of brain activation during temporal processing , 2001, Nature Neuroscience.

[2]  J Tanji,et al.  An oculomotor representation area within the ventral premotor cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[3]  T. Kimura,et al.  Mental navigation in humans is processed in the anterior bank of the parieto-occipital sulcus , 2002, Neuroscience Letters.

[4]  R. P. Maguire,et al.  Event-related fMRI responses in the human frontal eye fields in a randomized pro- and antisaccade task , 2001, NeuroImage.

[5]  W. Schultz,et al.  Role of primate basal ganglia and frontal cortex in the internal generation of movements , 2004, Experimental Brain Research.

[6]  R. Passingham,et al.  The left parietal cortex and motor attention , 1997, Neuropsychologia.

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

[8]  D P Munoz,et al.  Saccadic reaction time in the monkey: advanced preparation of oculomotor programs is primarily responsible for express saccade occurrence. , 1996, Journal of neurophysiology.

[9]  Leslie G. Ungerleider,et al.  Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation , 1999, Neuron.

[10]  Richard S. J. Frackowiak,et al.  Functional localization of the system for visuospatial attention using positron emission tomography. , 1997, Brain : a journal of neurology.

[11]  A. Berthoz,et al.  Functional Anatomy of a Prelearned Sequence of Horizontal Saccades in Humans , 1996, The Journal of Neuroscience.

[12]  R. Andersen,et al.  Saccade-related activity in the lateral intraparietal area. II. Spatial properties. , 1991, Journal of neurophysiology.

[13]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[14]  M. Preul The Human Brain: Surface, Blood Supply, and Three-Dimensional Sectional Anatomy , 2001 .

[15]  Volkmar Glauche,et al.  Functional properties and interaction of the anterior and posterior intraparietal areas in humans , 2003, The European journal of neuroscience.

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

[17]  Karl J. Friston,et al.  The functional anatomy of attention to visual motion. A functional MRI study. , 1998, Brain : a journal of neurology.

[18]  B. J. McCurtain,et al.  Dorsal cortical regions subserving visually guided saccades in humans: an fMRI study. , 1998, Cerebral cortex.

[19]  Ravi S. Menon,et al.  Human fMRI evidence for the neural correlates of preparatory set , 2002, Nature Neuroscience.

[20]  A. Nobre,et al.  Where and When to Pay Attention: The Neural Systems for Directing Attention to Spatial Locations and to Time Intervals as Revealed by Both PET and fMRI , 1998, The Journal of Neuroscience.

[21]  M. Goldberg,et al.  Representation of visuomotor space in the parietal lobe of the monkey. , 1990, Cold Spring Harbor symposia on quantitative biology.

[22]  M. Schlag-Rey,et al.  Evidence for a supplementary eye field. , 1987, Journal of neurophysiology.

[23]  T. Paus Location and function of the human frontal eye-field: A selective review , 1996, Neuropsychologia.

[24]  T. Mergner,et al.  Relationship between saccadic eye movements and cortical activity as measured by fMRI: quantitative and qualitative aspects , 2001, Experimental Brain Research.

[25]  C. Pierrot-Deseilligny,et al.  Cerebral ocular motor signs , 1997, Journal of Neurology.

[26]  M. Corbetta,et al.  Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  M. Corbetta,et al.  A PET study of visuospatial attention , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  Gregory S. Berns,et al.  The Context of Uncertainty Modulates the Subcortical Response to Predictability , 2001, Journal of Cognitive Neuroscience.

[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]  A. Nobre,et al.  Orienting attention in time: behavioural and neuroanatomical distinction between exogenous and endogenous shifts , 2000, Neuropsychologia.

[31]  J. T. Murphy,et al.  The role of the basal ganglia in controlling a movement initiated by a visually presented cue , 1980, Brain Research.

[32]  A. Fuchs Saccadic and smooth pursuit eye movements in the monkey , 1967, The Journal of physiology.

[33]  Robert M. McPeek,et al.  What neural pathways mediate express saccades? , 1993, Behavioral and Brain Sciences.

[34]  M. Goldberg,et al.  Neuronal Activity in the Lateral Intraparietal Area and Spatial Attention , 2003, Science.

[35]  Alan C. Evans,et al.  Functional neuroanatomy of smooth pursuit and predictive saccades , 2000, Neuroreport.

[36]  J. Hopfield,et al.  Electrical microstimulation suggests two different forms of representation of head-centered space in the intraparietal sulcus of rhesus monkeys. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Dieter Jaeger,et al.  Neuronal activity in the striatum and pallidum of primates related to the execution of externally cued reaching movements , 1995, Brain Research.

[38]  M Corbetta,et al.  Frontoparietal cortical networks for directing attention and the eye to visual locations: identical, independent, or overlapping neural systems? , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[39]  E A Cabanis,et al.  Location of the human posterior eye field with functional magnetic resonance imaging. , 1996, Journal of neurology, neurosurgery, and psychiatry.

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

[41]  S Clare,et al.  Functional magnetic resonance imaging of single motor events reveals human presupplementary motor area , 1997, Annals of neurology.

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

[43]  G. Rizzolatti,et al.  Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention , 1987, Neuropsychologia.

[44]  Charles G. Gross,et al.  Visual responses with and without fixation: neurons in premotor cortex encode spatial locations independently of eye position , 1998, Experimental Brain Research.

[45]  E. Stein,et al.  Right hemispheric dominance of inhibitory control: an event-related functional MRI study. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Leslie G. Ungerleider,et al.  The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[48]  J. Haxby,et al.  Functional anatomy of pursuit eye movements in humans as revealed by fMRI. , 1999, Journal of neurophysiology.

[49]  A. Berthoz,et al.  An anatomical landmark for the supplementary eye fields in human revealed with functional magnetic resonance imaging. , 1999, Cerebral cortex.

[50]  M. Mintun,et al.  Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. , 1996, Journal of neurophysiology.

[51]  R. Carpenter,et al.  Movements of the Eyes , 1978 .

[52]  N. Kanwisher,et al.  Covert visual attention modulates face-specific activity in the human fusiform gyrus: fMRI study. , 1998, Journal of neurophysiology.

[53]  D. Levy,et al.  Functional neuroanatomy of antisaccade eye movements investigated with positron emission tomography. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[54]  G. Mangun,et al.  The neural mechanisms of top-down attentional control , 2000, Nature Neuroscience.

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

[56]  Anna C. Nobre,et al.  Cortical Activation in the Human Brain during Lateral Saccades Using EPISTAR Functional Magnetic Resonance Imaging , 1996, NeuroImage.

[57]  Christopher Kennard,et al.  Differential cortical activation during voluntary and reflexive saccades in man , 2003, NeuroImage.

[58]  Richard S. J. Frackowiak,et al.  Cortical control of saccades and fixation in man. A PET study. , 1994, Brain : a journal of neurology.

[59]  M. Corbetta,et al.  A Common Network of Functional Areas for Attention and Eye Movements , 1998, Neuron.

[60]  R. J. Seitz,et al.  Activation of frontoparietal cortices during memorized triple‐step sequences of saccadic eye movements: an fMRI study , 2001, The European journal of neuroscience.

[61]  Matthew F. S. Rushworth,et al.  The left hemisphere and the selection of learned actions , 1998, Neuropsychologia.

[62]  J. R. Augustine Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.

[63]  J. Lynch,et al.  Corticocortical input to the smooth and saccadic eye movement subregions of the frontal eye field in Cebus monkeys. , 1996, Journal of neurophysiology.

[64]  R. Wurtz,et al.  Role of the rostral superior colliculus in active visual fixation and execution of express saccades. , 1992, Journal of neurophysiology.

[65]  C. Pierrot-Deseilligny,et al.  Neurology of saccades and smooth pursuit. , 1999, Current opinion in neurology.

[66]  M. Corbetta,et al.  Areas Involved in Encoding and Applying Directional Expectations to Moving Objects , 1999, The Journal of Neuroscience.

[67]  S. Ben Hamed,et al.  Representation of the visual field in the lateral intraparietal area of macaque monkeys: a quantitative receptive field analysis , 2001, Experimental Brain Research.

[68]  A. Berthoz,et al.  PET study of voluntary saccadic eye movements in humans: basal ganglia-thalamocortical system and cingulate cortex involvement. , 1993, Journal of neurophysiology.

[69]  Edward E. Smith,et al.  Spatial working memory in humans as revealed by PET , 1993, Nature.

[70]  M. Petrides,et al.  The effect of spatial and temporal information on saccades and neural activity in oculomotor structures. , 2002, Brain : a journal of neurology.

[71]  David Ferrier,et al.  The localization of function in the brain , 1874, Proceedings of the Royal Society of London.

[72]  S. Dehaene,et al.  Topographical Layout of Hand, Eye, Calculation, and Language-Related Areas in the Human Parietal Lobe , 2002, Neuron.

[73]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[74]  J. Assad,et al.  Dynamic coding of behaviourally relevant stimuli in parietal cortex , 2002, Nature.

[75]  S. Zeki,et al.  The neurology of saccades and covert shifts in spatial attention: an event-related fMRI study. , 2000, Brain : a journal of neurology.

[76]  D. Gitelman,et al.  Covert Visual Spatial Orienting and Saccades: Overlapping Neural Systems , 2000, NeuroImage.

[77]  Y. Agid,et al.  Saccade disturbances after bilateral lentiform nucleus lesions in humans. , 1996, Journal of neurology, neurosurgery, and psychiatry.

[78]  M. Goldberg,et al.  Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. , 1996, Journal of neurophysiology.

[79]  M. Goldberg,et al.  The representation of visual salience in monkey parietal cortex , 1998, Nature.

[80]  K. Zilles,et al.  Crossmodal Processing of Object Features in Human Anterior Intraparietal Cortex An fMRI Study Implies Equivalencies between Humans and Monkeys , 2002, Neuron.

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

[82]  G. d'Ydewalle,et al.  Presaccadic attention allocation and express saccades , 1996, Psychological research.

[83]  Ferdinand Binkofski,et al.  Modular organization of parietal lobe functions as revealed by functional activation studies. , 2003, Advances in neurology.

[84]  J Schlag,et al.  Interaction of the two frontal eye fields before saccade onset. , 1998, Journal of neurophysiology.

[85]  Driss Boussaoud,et al.  Role of the primate striatum in attention and sensorimotor processes: comparison with premotor cortex. , 1995 .

[86]  Joel R. Meyer,et al.  A large-scale distributed network for covert spatial attention: further anatomical delineation based on stringent behavioural and cognitive controls. , 1999, Brain : a journal of neurology.

[87]  M. Kimura The role of primate putamen neurons in the association of sensory stimuli with movement , 1986, Neuroscience Research.

[88]  R. Andersen,et al.  Evidence for the lateral intraparietal area as the parietal eye field , 1992, Current Opinion in Neurobiology.

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

[90]  P. H. Schiller,et al.  The effects of frontal eye field and dorsomedial frontal cortex lesions on visually guided eye movements , 1998, Nature Neuroscience.

[91]  M. Mesulam,et al.  Right cerebral dominance in spatial attention. Further evidence based on ipsilateral neglect. , 1987, Archives of neurology.

[92]  M. Mesulam A cortical network for directed attention and unilateral neglect , 1981, Annals of neurology.

[93]  W. Eddy,et al.  Pursuit and saccadic eye movement subregions in human frontal eye field: a high-resolution fMRI investigation. , 2002, Cerebral cortex.

[94]  C. Pierrot-Deseilligny,et al.  Cortical control of saccades , 1998, Experimental Brain Research.