Hierarchical control of two-dimensional gaze saccades

Coordinating the movements of different body parts is a challenging process for the central nervous system because of several problems. Four of these main difficulties are: first, moving one part can move others; second, the parts can have different dynamics; third, some parts can have different motor goals; and fourth, some parts may be perturbed by outside forces. Here, we propose a novel approach for the control of linked systems with feedback loops for each part. The proximal parts have separate goals, but critically the most distal part has only the common goal. We apply this new control policy to eye-head coordination in two-dimensions, specifically head-unrestrained gaze saccades. Paradoxically, the hierarchical structure has controllers for the gaze and the head, but not for the eye (the most distal part). Our simulations demonstrate that the proposed control structure reproduces much of the published empirical data about gaze movements, e.g., it compensates for perturbations, accurately reaches goals for gaze and head from arbitrary initial positions, simulates the nine relationships of the head-unrestrained main sequence, and reproduces observations from lesion and single-unit recording experiments. We conclude by showing how our model can be easily extended to control structures with more linked segments, such as the control of coordinated eye on head on trunk movements.

[1]  A. Opstal,et al.  Human eye-head coordination in two dimensions under different sensorimotor conditions , 1997, Experimental Brain Research.

[2]  J. Findlay,et al.  Using the eye–movement system to control the head , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[3]  Kathleen E Cullen,et al.  Time course of vestibuloocular reflex suppression during gaze shifts. , 2004, Journal of neurophysiology.

[4]  D. Munoz,et al.  Neck muscle responses to stimulation of monkey superior colliculus. II. Gaze shift initiation and volitional head movements. , 2002, Journal of neurophysiology.

[5]  Eye-head gaze shifts , 2011 .

[6]  Daniel M. Wolpert,et al.  Signal-dependent noise determines motor planning , 1998, Nature.

[7]  A. Fuchs,et al.  Discharge patterns in nucleus prepositus hypoglossi and adjacent medial vestibular nucleus during horizontal eye movement in behaving macaques. , 1992, Journal of neurophysiology.

[8]  D. Guitton,et al.  Tectospinal neurons in the cat have discharges coding gaze position error , 1985, Brain Research.

[9]  Lance M. Optican,et al.  Recovery of saccadic dysmetria following localized lesions in monkey superior colliculus , 2004, Experimental Brain Research.

[10]  J M Findlay,et al.  Saccades without eye movements , 1997, Nature.

[11]  Adonis K Moschovakis,et al.  Optimal Control of Gaze Shifts , 2009, The Journal of Neuroscience.

[12]  Neeraj J Gandhi,et al.  Effect of reversible inactivation of superior colliculus on head movements. , 2008, Journal of neurophysiology.

[13]  A. Grantyn,et al.  Neural network simulations of the primate oculomotor system. V. Eye–head gaze shifts , 2010, Biological Cybernetics.

[14]  D. Munoz,et al.  Gaze control in the cat: studies and modeling of the coupling between orienting eye and head movements in different behavioral tasks. , 1990, Journal of neurophysiology.

[15]  H. Noda,et al.  Discharges of Purkinje cells and mossy fibres in the cerebellar vermis of the monkey during saccadic eye movements and fixation , 1980, The Journal of physiology.

[16]  R. Tomlinson,et al.  Combined eye-head gaze shifts in the primate. I. Metrics. , 1986, Journal of neurophysiology.

[17]  E. Bizzi,et al.  Eye-Head Coordination in Monkeys: Evidence for Centrally Patterned Organization , 1971, Science.

[18]  D. Guitton Control of eye—head coordination during orienting gaze shifts , 1992, Trends in Neurosciences.

[19]  R. Tomlinson Combined eye-head gaze shifts in the primate. III. Contributions to the accuracy of gaze saccades. , 1990, Journal of neurophysiology.

[20]  Edward G. Freedman,et al.  Coordination of the eyes and head: movement kinematics , 2000, Experimental Brain Research.

[21]  D Guitton,et al.  Central Organization and Modeling of Eye‐Head Coordination during Orienting Gaze Shifts a , 1992, Annals of the New York Academy of Sciences.

[22]  D. Guitton,et al.  Gaze control in humans: eye-head coordination during orienting movements to targets within and beyond the oculomotor range. , 1987, Journal of neurophysiology.

[23]  D. Pélisson,et al.  Orienting gaze shifts during muscimol inactivation of caudal fastigial nucleus in the cat. I. Gaze dysmetria. , 1998, Journal of neurophysiology.

[24]  E. Keller Participation of medial pontine reticular formation in eye movement generation in monkey. , 1974, Journal of neurophysiology.

[25]  D. Munoz,et al.  Presaccadic burst discharges of tecto-reticulo-spinal neurons in the alert head-free and -fixed cat , 1986, Brain Research.

[26]  Jefferson E. Roy,et al.  A neural correlate for vestibulo-ocular reflex suppression during voluntary eye–head gaze shifts , 1998, Nature Neuroscience.

[27]  Mario Prsa,et al.  Visual-vestibular interaction hypothesis for the control of orienting gaze shifts by brain stem omnipause neurons. , 2007, Journal of neurophysiology.

[28]  D Pélisson,et al.  Orienting gaze shifts during muscimol inactivation of caudal fastigial nucleus in the cat. II. Dynamics and eye-head coupling. , 1998, Journal of Neurophysiology.

[29]  J. Corriou Process Control: Theory and Applications , 2010 .

[30]  E Bizzi,et al.  Strategies of eye-head coordination. , 1979, Progress in brain research.

[31]  D. Tweed,et al.  Three-dimensional model of the human eye-head saccadic system. , 1997, Journal of neurophysiology.

[32]  R J Leigh,et al.  Properties of horizontal saccades accompanied by blinks. , 1998, Journal of neurophysiology.

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

[34]  D Pélisson,et al.  Compensation for gaze perturbation during inactivation of the caudal fastigial nucleus in the head-unrestrained cat. , 1998, Journal of neurophysiology.

[35]  D. Robinson,et al.  Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey. , 1987, Journal of neurophysiology.

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

[37]  Daniel Guitton,et al.  Responses of Collicular Fixation Neurons to Gaze Shift Perturbations in Head-Unrestrained Monkey Reveal Gaze Feedback Control , 2006, Neuron.

[38]  E. Freedman Coordination of the eyes and head during visual orienting , 2008, Experimental Brain Research.

[39]  Lance M Optican,et al.  Sensorimotor Transformation for Visually Guided Saccades , 2005, Annals of the New York Academy of Sciences.

[40]  Kathleen E Cullen,et al.  Premotor Correlates of Integrated Feedback Control for Eye–Head Gaze Shifts , 2006, The Journal of Neuroscience.

[41]  Kathleen E Cullen,et al.  The nucleus prepositus predominantly outputs eye movement-related information during passive and active self-motion. , 2013, Journal of neurophysiology.

[42]  N. J. Gandhi,et al.  Matching the oculomotor drive during head-restrained and head-unrestrained gaze shifts in monkey. , 2010, Journal of neurophysiology.

[43]  Michael A. Arbib,et al.  A model of the cerebellum in adaptive control of saccadic gain , 1996, Biological Cybernetics.

[44]  B. W. Peterson,et al.  A dynamical model for reflex activated head movements in the horizontal plane , 1996, Biological Cybernetics.

[45]  Neeraj J. Gandhi Interactions between gaze-evoked blinks and gaze shifts in monkeys , 2011, Experimental Brain Research.

[46]  D. Guitton,et al.  Brain stem omnipause neurons and the control of combined eye-head gaze saccades in the alert cat. , 1998, Journal of neurophysiology.

[47]  L. Stark,et al.  Simulation of head movement trajectories: model and fit to main sequence , 2004, Biological Cybernetics.

[48]  L. Optican,et al.  Cerebellar-dependent adaptive control of primate saccadic system. , 1980, Journal of neurophysiology.

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

[50]  D. Guitton,et al.  Compensatory eye and head movements generated by the cat following stimulation-induced perturbations in gaze position , 2004, Experimental Brain Research.

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

[52]  Michael F. Land,et al.  The coordination of rotations of the eyes, head and trunk in saccadic turns produced in natural situations , 2004, Experimental Brain Research.

[53]  D. Robinson,et al.  The vestibulo‐ocular reflex during human saccadic eye movements. , 1986, The Journal of physiology.

[54]  M. Desmurget,et al.  Mapping motor representations in the human cerebellum. , 2013, Brain : a journal of neurology.

[55]  H. Galiana,et al.  A bilateral model for central neural pathways in vestibuloocular reflex. , 1984, Journal of neurophysiology.

[56]  R. Tomlinson,et al.  Combined eye-head gaze shifts in the primate. II. Interactions between saccades and the vestibuloocular reflex. , 1986, Journal of neurophysiology.

[57]  A. K. Moschovakis,et al.  Neural network simulations of the primate oculomotor system , 2004, Biological Cybernetics.

[58]  R. Wurtz,et al.  Reversible inactivation of monkey superior colliculus. II. Maps of saccadic deficits. , 1998, Journal of neurophysiology.

[59]  Philippe Lefèvre,et al.  Dynamic feedback to the superior colliculus in a neural network model of the gaze control system , 1992, Neural Networks.

[60]  Yanning H Han,et al.  Comparison of Velocity Waveforms of Eye and Head Saccades , 2005, Annals of the New York Academy of Sciences.

[61]  L. M. Optican,et al.  Oculomotor System: Models , 2009 .

[62]  A. Bronstein,et al.  Gaze displacement and inter-segmental coordination during large whole body voluntary rotations , 2009, Experimental Brain Research.

[63]  A. Fuchs,et al.  The brainstem burst generator for saccadic eye movements , 2002, Experimental Brain Research.

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

[65]  Artem V. Belopolsky,et al.  I. Curvature of Saccadic Trajectory Reversible Inactivation of Monkey Superior Colliculus. , 2015 .

[66]  A. Berthoz,et al.  Burst activity of identified tecto-reticulo-spinal neurons in the alert cat , 2004, Experimental Brain Research.

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

[68]  Christian Quaia,et al.  Distributed Model of Collicular and Cerebellar Function during Saccades , 2002, Annals of the New York Academy of Sciences.

[69]  Denis Pélisson,et al.  On-line compensation of gaze shifts perturbed by micro-stimulation of the superior colliculus in the cat with unrestrained head , 2004, Experimental Brain Research.

[70]  D. Pélisson,et al.  Contribution of the rostral fastigial nucleus to the control of orienting gaze shifts in the head-unrestrained cat. , 1998, Journal of neurophysiology.

[71]  Daniel Guitton,et al.  Human eye-head gaze shifts preserve their accuracy and spatiotemporal trajectory profiles despite long-duration torque perturbations that assist or oppose head motion. , 2012, Journal of neurophysiology.

[72]  R. Wurtz,et al.  Reversible inactivation of monkey superior colliculus. I. Curvature of saccadic trajectory. , 1998, Journal of neurophysiology.

[73]  Jefferson E. Roy,et al.  Signal processing in the vestibular system during active versus passive head movements. , 2004, Journal of neurophysiology.

[74]  Edward G. Freedman,et al.  Interactions between eye and head control signals can account for movement kinematics , 2001, Biological Cybernetics.

[75]  Philippe Lefèvre,et al.  Experimental study and modeling of vestibulo-ocular reflex modulation during large shifts of gaze in humans , 2004, Experimental Brain Research.

[76]  Hongying Wang,et al.  Three-dimensional eye-head coordination after injection of muscimol into the interstitial nucleus of Cajal (INC). , 2007, Journal of neurophysiology.

[77]  Tadashi Isa,et al.  Brainstem control of head movements during orienting; organization of the premotor circuits , 2002, Progress in Neurobiology.

[78]  L. Stark,et al.  The main sequence, a tool for studying human eye movements , 1975 .

[79]  J. Fuller,et al.  Head movement propensity , 2004, Experimental Brain Research.

[80]  H. Kornhuber,et al.  Natural and drug-induced variations of velocity and duration of human saccadic eye movements: Evidence for a control of the neural pulse generator by local feedback , 2004, Biological Cybernetics.

[81]  Christian Quaia,et al.  Distributed model of control of saccades by superior colliculus and cerebellum , 1998, Neural Networks.

[82]  G. Cheron,et al.  Disabling of the oculomotor neural integrator by kainic acid injections in the prepositus‐vestibular complex of the cat. , 1987, The Journal of physiology.

[83]  J. L. Conway,et al.  Deficits in eye movements following frontal eye-field and superior colliculus ablations. , 1980, Journal of neurophysiology.

[84]  G. Barnes,et al.  Independent control of head and gaze movements during head‐free pursuit in humans , 1999, The Journal of physiology.

[85]  D Pélisson,et al.  Gaze shifts evoked by electrical stimulation of the superior colliculus in the head‐unrestrained cat. II. Effect of muscimol inactivation of the caudal fastigial nucleus , 2001, The European journal of neuroscience.

[86]  A. K. Moschovakis,et al.  The local loop of the saccadic system closes downstream of the superior colliculus , 2006, Neuroscience.

[87]  R P Travis,et al.  Firing patterns of reticular formation neurons during horizontal eye movements. , 1971, Brain research.

[88]  Neeraj J Gandhi,et al.  Dissociation of eye and head components of gaze shifts by stimulation of the omnipause neuron region. , 2007, Journal of neurophysiology.

[89]  D. A. Robinson,et al.  A model of quick phase generation in the vestibuloocular reflex , 1978, Biological Cybernetics.

[90]  M. Land Vision, eye movements, and natural behavior , 2009, Visual Neuroscience.

[91]  Werner Haustein,et al.  Considerations on Listing's Law and the primary position by means of a matrix description of eye position control , 1989, Biological Cybernetics.

[92]  Masahiko Fujita,et al.  Feed-forward associative learning for volitional movement control , 2005, Neuroscience Research.

[93]  J. L. Conway,et al.  Effects of frontal eye field and superior colliculus ablations on eye movements. , 1979, Science.

[94]  A. Berthoz,et al.  Dynamics of the head-neck system in response to small perturbations: Analysis and modeling in the frequency domain , 1975, Biological Cybernetics.

[95]  A. Fuchs,et al.  Role of the caudal fastigial nucleus in saccade generation. II. Effects of muscimol inactivation. , 1993, Journal of neurophysiology.

[96]  L. Optican,et al.  Model of the control of saccades by superior colliculus and cerebellum. , 1999, Journal of neurophysiology.

[97]  Denis Pélisson,et al.  Visuo-motor deficits induced by fastigial nucleus inactivation , 2008, The Cerebellum.