Target Selection by the Frontal Cortex during Coordinated Saccadic and Smooth Pursuit Eye Movements

Oculomotor tracking of moving objects is an important component of visually based cognition and planning. Such tracking is achieved by a combination of saccades and smooth-pursuit eye movements. In particular, the saccadic and smooth-pursuit systems interact to often choose the same target, and to maximize its visibility through time. How do multiple brain regions interact, including frontal cortical areas, to decide the choice of a target among several competing moving stimuli? How is target selection information that is created by a bias (e.g., electrical stimulation) transferred from one movement system to another? These saccade–pursuit interactions are clarified by a new computational neural model, which describes interactions between motion processing areas: the middle temporal area, the middle superior temporal area, the frontal pursuit area, and the dorsal lateral pontine nucleus; saccade specification, selection, and planning areas: the lateral intraparietal area, the frontal eye fields, the substantia nigra pars reticulata, and the superior colliculus; the saccadic generator in the brain stem; and the cerebellum. Model simulations explain a broad range of neuroanatomical and neurophysiological data. These results are in contrast with the simplest parallel model with no interactions between saccades and pursuit other than common-target selection and recruitment of shared motoneurons. Actual tracking episodes in primates reveal multiple systematic deviations from predictions of the simplest parallel model, which are explained by the current model.

[1]  R J Krauzlis,et al.  Discharge properties of neurons in the rostral superior colliculus of the monkey during smooth-pursuit eye movements. , 2000, Journal of neurophysiology.

[2]  R D Yee,et al.  Smooth pursuitlike eye movements evoked by microstimulation in macaque nucleus reticularis tegmenti pontis. , 1996, Journal of neurophysiology.

[3]  Xiao-Jing Wang,et al.  Cortico–basal ganglia circuit mechanism for a decision threshold in reaction time tasks , 2006, Nature Neuroscience.

[4]  A Treisman,et al.  Feature analysis in early vision: evidence from search asymmetries. , 1988, Psychological review.

[5]  E. Keller,et al.  Saccade target selection in the superior colliculus during a visual search task. , 2002, Journal of neurophysiology.

[6]  S. Grossberg,et al.  Normal and amnesic learning, recognition and memory by a neural model of cortico-hippocampal interactions , 1993, Trends in Neurosciences.

[7]  J. Maunsell,et al.  Effects of Attention on the Processing of Motion in Macaque Middle Temporal and Medial Superior Temporal Visual Cortical Areas , 1999, The Journal of Neuroscience.

[8]  David C Lyon,et al.  Distribution across cortical areas of neurons projecting to the superior colliculus in new world monkeys. , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[9]  J. Schall,et al.  Saccade target selection in frontal eye field of macaque. I. Visual and premovement activation , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[11]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  W. Hodos,et al.  Comparative Vertebrate Neuroanatomy: Evolution and Adaptation , 2005 .

[13]  C. Bruce,et al.  Deficits in smooth-pursuit eye movements after muscimol inactivation within the primate's frontal eye field. , 1998, Journal of neurophysiology.

[14]  A. Berthoz,et al.  From brainstem to cortex: Computational models of saccade generation circuitry , 2005, Progress in Neurobiology.

[15]  J. Gold,et al.  Representation of a perceptual decision in developing oculomotor commands , 2000, Nature.

[16]  S. Lisberger,et al.  Role of arcuate frontal cortex of monkeys in smooth pursuit eye movements. II. Relation to vector averaging pursuit. , 2002, Journal of neurophysiology.

[17]  S. Lisberger,et al.  Enhancement of multiple components of pursuit eye movement by microstimulation in the arcuate frontal pursuit area in monkeys. , 2002, Journal of neurophysiology.

[18]  R. Wurtz,et al.  Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus. , 2000, Journal of neurophysiology.

[19]  Vallabh E Das,et al.  Gaze-related response properties of DLPN and NRTP neurons in the rhesus macaque. , 2004, Journal of neurophysiology.

[20]  Robert M. McPeek,et al.  Deficits in saccade target selection after inactivation of superior colliculus , 2004, Nature Neuroscience.

[21]  R. Krauzlis,et al.  Neural activity in the frontal pursuit area does not underlie pursuit target selection , 2011, Vision Research.

[22]  T. Albright Direction and orientation selectivity of neurons in visual area MT of the macaque. , 1984, Journal of neurophysiology.

[23]  J. Duhamel,et al.  Saccadic Target Selection Deficits after Lateral Intraparietal Area Inactivation in Monkeys , 2002, The Journal of Neuroscience.

[24]  Stephen G. Lisberger,et al.  Serial linkage of target selection for orienting and tracking eye movements , 2002, Nature Neuroscience.

[25]  F. A. Miles,et al.  Target Selection for Pursuit and Saccadic Eye Movements in Humans , 1999, Journal of Cognitive Neuroscience.

[26]  J. Penney,et al.  The functional anatomy of basal ganglia disorders , 1989, Trends in Neurosciences.

[27]  H. Noda,et al.  Eye movements evoked by microstimulation in the flocculus of the alert macaque , 2004, Experimental Brain Research.

[28]  Masaki Tanaka,et al.  Smooth Pursuit Eye Movements , 2018 .

[29]  Stephen G Lisberger,et al.  Signals that modulate gain control for smooth pursuit eye movements in monkeys. , 2004, Journal of neurophysiology.

[30]  E. G. Keating,et al.  Ablation of the pursuit area in the frontal cortex of the primate degrades foveal but not optokinetic smooth eye movements. , 1996, Journal of neurophysiology.

[31]  Christopher C. Pack,et al.  A Neural Model of Smooth Pursuit Control and Motion Perception by Cortical Area MST , 2001, Journal of Cognitive Neuroscience.

[32]  Justin L. Gardner,et al.  Linked Target Selection for Saccadic and Smooth Pursuit Eye Movements , 2001, The Journal of Neuroscience.

[33]  S. Lisberger,et al.  Role of arcuate frontal cortex of monkeys in smooth pursuit eye movements. I. Basic response properties to retinal image motion and position. , 2002, Journal of neurophysiology.

[34]  R. Wurtz,et al.  Role of the basal ganglia in the initiation of saccadic eye movements. , 1986, Progress in brain research.

[35]  Christopher D. Carello,et al.  Target selection and the superior colliculus: goals, choices and hypotheses , 2004, Vision Research.

[36]  E. Seidemann,et al.  Effect of spatial attention on the responses of area MT neurons. , 1999, Journal of neurophysiology.

[37]  J. Lynch,et al.  Subcortical Input to the Smooth and Saccadic Eye Movement Subregions of the Frontal Eye Field in Cebus Monkey , 1997, The Journal of Neuroscience.

[38]  L A Krubitzer,et al.  Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. cortical connections , 1986, The Journal of comparative neurology.

[39]  Richard J Krauzlis,et al.  Primacy of spatial information in guiding target selection for pursuit and saccades. , 2002, Journal of vision.

[40]  Stephen Grossberg,et al.  How laminar frontal cortex and basal ganglia circuits interact to control planned and reactive saccades , 2004, Neural Networks.

[41]  Stephen Grossberg,et al.  How do children learn to follow gaze , share joint attention , imitate their teachers , and use tools during social interactions ? , 2010 .

[42]  R. Wurtz,et al.  Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. , 1993, Journal of neurophysiology.

[43]  R. Iansek,et al.  Inaccuracy and instability of sequential movements in Parkinson's disease , 2004, Experimental Brain Research.

[44]  Peter H Schiller,et al.  Neural mechanisms underlying target selection with saccadic eye movements. , 2005, Progress in brain research.

[45]  D. B. Bender,et al.  Selectivity for relative motion in the monkey superior colliculus. , 1991, Journal of neurophysiology.

[46]  J. Lynch,et al.  Pursuit subregion of the frontal eye field projects to the caudate nucleus in monkeys. , 2003, Journal of neurophysiology.

[47]  A M Graybiel,et al.  The differential projection of two cytoarchitectonic subregions of the inferior parietal lobule of macaque upon the deep layers of the superior colliculus , 1985, The Journal of comparative neurology.

[48]  Joel L. Davis,et al.  Adaptive Critics and the Basal Ganglia , 1995 .

[49]  R D Yee,et al.  Smooth-pursuit eye-movement deficits with chemical lesions in macaque nucleus reticularis tegmenti pontis. , 1999, Journal of neurophysiology.

[50]  D. Zee,et al.  Effects of ablation of flocculus and paraflocculus of eye movements in primate. , 1981, Journal of neurophysiology.

[51]  C. Bruce,et al.  Frontal eye field efferents in the macaque monkey: II. Topography of terminal fields in midbrain and pons , 1988, The Journal of comparative neurology.

[52]  M. A. Basso,et al.  Neuronal Activity in Substantia Nigra Pars Reticulata during Target Selection , 2002, The Journal of Neuroscience.

[53]  J. Lynch,et al.  Functionally defined smooth and saccadic eye movement subregions in the frontal eye field of Cebus monkeys. , 1996, Journal of neurophysiology.

[54]  S. Grossberg,et al.  A neural model of motion processing and visual navigation by cortical area MST. , 1999, Cerebral cortex.

[55]  J. Tigges,et al.  Studies on the visual area MT in primates. II. Projection fibers to subcortical structures. , 1973, Brain research.

[56]  Peter L. Strick,et al.  Macro-organization of the circuits connecting the basal ganglia with the cortical motor areas , 1995 .

[57]  S. Grossberg,et al.  A Neural Model of Multimodal Adaptive Saccadic Eye Movement Control by Superior Colliculus , 1997, The Journal of Neuroscience.

[58]  A. Hodgkin,et al.  The Ionic Basis of Nervous Conduction , 1964, Science.

[59]  D C Van Essen,et al.  Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. , 1983, Journal of neurophysiology.

[60]  A. Fuchs,et al.  Brainstem control of saccadic eye movements. , 1985, Annual review of neuroscience.

[61]  K. Tanaka,et al.  Analysis of object motion in the ventral part of the medial superior temporal area of the macaque visual cortex. , 1993, Journal of neurophysiology.

[62]  Vincent P Ferrera,et al.  Coordination of smooth pursuit and saccade target selection in monkeys. , 2007, Journal of neurophysiology.

[63]  P H Schiller,et al.  Look and see: how the brain moves your eyes about. , 2001, Progress in brain research.

[64]  W. Smeets,et al.  Evolution of the basal ganglia in tetrapods: a new perspective based on recent studies in amphibians , 1998, Trends in Neurosciences.

[65]  S. Scott,et al.  Discharge properties of monkey tectoreticular neurons. , 2006, Journal of neurophysiology.

[66]  Stefan Treue,et al.  Seeing multiple directions of motion—physiology and psychophysics , 2000, Nature Neuroscience.

[67]  Joel L. Davis,et al.  Macro-organization of the Circuits Connecting the Basal Ganglia with the Cortical Motor Areas , 1994 .

[68]  H. Komatsu,et al.  Modulation of pursuit eye movements by stimulation of cortical areas MT and MST. , 1989, Journal of neurophysiology.

[69]  D. Munoz,et al.  On your mark, get set: Brainstem circuitry underlying saccadic initiation , 2000 .

[70]  N. J. Gandhi,et al.  Spatial distribution and discharge characteristics of superior colliculus neurons antidromically activated from the omnipause region in monkey. , 1997, Journal of neurophysiology.

[71]  Peter H Schiller,et al.  Cortical inhibitory circuits in eye‐movement generation , 2003, The European journal of neuroscience.

[72]  R. Wurtz,et al.  Fixation cells in monkey superior colliculus. II. Reversible activation and deactivation. , 1993, Journal of neurophysiology.

[73]  R. Wurtz,et al.  Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. , 1983, Journal of neurophysiology.

[74]  L. Goldstein The frontal lobes and voluntary action , 1996 .

[75]  D. Guitton,et al.  The fixation area of the cat superior colliculus: effects of electrical stimulation and direct connection with brainstem omnipause neurons , 2004, Experimental Brain Research.

[76]  W T Newsome,et al.  Target selection for saccadic eye movements: direction-selective visual responses in the superior colliculus. , 2001, Journal of neurophysiology.

[77]  R J Krauzlis,et al.  Shared motor error for multiple eye movements. , 1997, Science.

[78]  S. Grossberg How does the cerebral cortex work? Development, learning, attention, and 3-D vision by laminar circuits of visual cortex. , 2003, Behavioral and cognitive neuroscience reviews.

[79]  R. Wurtz,et al.  What the brain stem tells the frontal cortex. I. Oculomotor signals sent from superior colliculus to frontal eye field via mediodorsal thalamus. , 2004, Journal of neurophysiology.

[80]  M Missal,et al.  Common inhibitory mechanism for saccades and smooth-pursuit eye movements. , 2002, Journal of neurophysiology.

[81]  Daniel Bullock,et al.  Computational perspectives on forebrain microcircuits implicated in reinforcement learning, action selection, and cognitive control , 2009, Neural Networks.

[82]  Stephen Grossberg,et al.  Studies of mind and brain , 1982 .

[83]  N. P. Bichot,et al.  Dissociation of visual discrimination from saccade programming in macaque frontal eye field. , 1997, Journal of neurophysiology.

[84]  J. Bullier,et al.  Topography of visual cortex connections with frontal eye field in macaque: convergence and segregation of processing streams , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[85]  S. Lisberger,et al.  Attention and target selection for smooth pursuit eye movements , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[86]  F. Ottes,et al.  Metrics of saccade responses to visual double stimuli: Two different modes , 1984, Vision Research.

[87]  E. L. Keller,et al.  Visual signals in the dorsolateral pontine nucleus of the alert monkey: Their relationship to smooth-pursuit eye movements , 2004, Experimental Brain Research.

[88]  S. Grossberg Contour Enhancement , Short Term Memory , and Constancies in Reverberating Neural Networks , 1973 .

[89]  C. Bruce,et al.  Smooth eye movements elicited by microstimulation in the primate frontal eye field. , 1993, Journal of neurophysiology.

[90]  Stephen G Lisberger,et al.  Directional Cuing of Target Choice in Human Smooth Pursuit Eye Movements , 2006, The Journal of Neuroscience.

[91]  S. Grossberg Biological competition: Decision rules, pattern formation, and oscillations. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[92]  R. Wurtz,et al.  Saccade-related activity in monkey superior colliculus. II. Spread of activity during saccades. , 1995, Journal of neurophysiology.

[93]  N. P. Bichot,et al.  Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search. , 1996, Journal of neurophysiology.

[94]  Peter Thier,et al.  The neural basis of smooth pursuit eye movements in the rhesus monkey brain , 2008, Brain and Cognition.

[95]  M. Shadlen,et al.  Response of Neurons in the Lateral Intraparietal Area during a Combined Visual Discrimination Reaction Time Task , 2002, The Journal of Neuroscience.

[96]  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.

[97]  R. Krauzlis The Control of Voluntary Eye Movements: New Perspectives , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[98]  J. Gold,et al.  Neural computations that underlie decisions about sensory stimuli , 2001, Trends in Cognitive Sciences.

[99]  D. Zee,et al.  Effects of lesions of the oculomotor vermis on eye movements in primate: saccades. , 1998, Journal of neurophysiology.

[100]  Praveen K. Pilly,et al.  Temporal dynamics of decision-making during motion perception in the visual cortex , 2008, Vision Research.

[101]  R J Krauzlis,et al.  Activation and inactivation of rostral superior colliculus neurons during smooth-pursuit eye movements in monkeys. , 2000, Journal of neurophysiology.

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

[103]  Christopher D. Carello,et al.  Manipulating Intent Evidence for a Causal Role of the Superior Colliculus in Target Selection , 2004, Neuron.

[104]  M. Paré,et al.  Temporal processing of saccade targets in parietal cortex area LIP during visual search. , 2007, Journal of neurophysiology.

[105]  S. Grossberg The complementary brain: unifying brain dynamics and modularity , 2000, Trends in Cognitive Sciences.

[106]  D. Munoz,et al.  Comparison of the discharge characteristics of brain stem omnipause neurons and superior colliculus fixation neurons in monkey: implications for control of fixation and saccade behavior. , 1998, Journal of neurophysiology.

[107]  R. Wurtz,et al.  Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. , 1995, Journal of neurophysiology.

[108]  W. Newsome,et al.  Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. , 2001, Journal of neurophysiology.

[109]  L A Krubitzer,et al.  Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. cortical connections , 1986, The Journal of comparative neurology.

[110]  U Büttner,et al.  Present concepts of oculomotor organization. , 1988, Reviews of oculomotor research.

[111]  B. Cohen,et al.  Projections from the superior colliculus motor map to omnipause neurons in monkey , 1999, The Journal of comparative neurology.

[112]  J. Kaas,et al.  Cortical and subcortical projections of the middle temporal area (MT) and adjacent cortex in galagos , 1982, The Journal of comparative neurology.

[113]  G H Recanzone,et al.  Shift in smooth pursuit initiation and MT and MST neuronal activity under different stimulus conditions. , 1999, Journal of neurophysiology.

[114]  S. Squatrito,et al.  Projections from cortical visual areas of the superior temporal sulcus to the superior colliculus, in macaque monkeys. , 1992, Archives italiennes de biologie.

[115]  J. Lynch,et al.  Cortico-cortical networks and cortico-subcortical loops for the higher control of eye movements. , 2006, Progress in brain research.

[116]  M. Mustari,et al.  Modeling of smooth pursuit-related neuronal responses in the DLPN and NRTP of the rhesus macaque. , 2005, Journal of neurophysiology.

[117]  Robert M. McPeek,et al.  Properties of saccadic responses in monkey when multiple competing visual stimuli are present. , 2004, Journal of neurophysiology.

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

[119]  A. Fuchs,et al.  Response properties of dorsolateral pontine units during smooth pursuit in the rhesus macaque. , 1988, Journal of neurophysiology.

[120]  Stephen G. Lisberger,et al.  Regulation of the gain of visually guided smooth-pursuit eye movements by frontal cortex , 2001, Nature.

[121]  Dottie M. Clower,et al.  The Inferior Parietal Lobule Is the Target of Output from the Superior Colliculus, Hippocampus, and Cerebellum , 2001, The Journal of Neuroscience.

[122]  S. Grossberg,et al.  A neural model of saccadic eye movement control explains task-specific adaptation , 1999, Vision Research.

[123]  P. Brodal,et al.  The cortical projection to the nucleus reticularis tegmenti pontis in the rhesus monkey , 2004, Experimental Brain Research.

[124]  D. A. Suzuki,et al.  Cortical and subcortical afferents to the nucleus reticularis tegmenti pontis and basal pontine nuclei in the macaque monkey , 2001, Visual Neuroscience.