Kinematic redundancy and variance of eye, head and trunk displacements during large horizontal gaze reorientations in standing humans

Shifting the direction of the line of sight in everyday life often involves rotations not only of the eyes and head but also of the trunk. Here, we investigated covariation patterns of eye-in-orbit, head-on-trunk and trunk-in-space angular horizontal displacements during whole-body rotations to targets of up to 180° eccentricity performed by standing healthy human subjects. The spatial covariation was quantified statistically across various behavioral task conditions (unpredictable, memory driven predictable, visual feedback) and constraints (accuracy) by principal components (PC) analysis. Overall, the combined movement was stereotyped such that the first two PCs accounted for essentially the whole data variance of combined gaze transfers up to about 400 ms, suggesting that the three mechanical degrees of freedom under consideration are reduced to two kinematic degrees of freedom. Moreover, quantification of segment velocity variability across repetitions showed that velocities of eye-in-space and head-in-space (i.e. ‘end-point’ velocity) were less variable than those of the elemental variables composing them. In contrast, three statistically significant PCs accounted for the covariation of the three segments during presumably vestibularly mediated nystagmic transfers, suggesting control by a separate driving circuit. We conclude that progression of the line of sight is initially stereotypic and fulfills criteria defining a motor synergy.

[1]  J. Foley The co-ordination and regulation of movements , 1968 .

[2]  A. Grantyn,et al.  Axonal patterns and sites of termination of cat superior colliculus neurons projecting in the tecto-bulbo-spinal tract , 2004, Experimental Brain Research.

[3]  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.

[4]  Michael F. Land,et al.  Predictable eye-head coordination during driving , 1992, Nature.

[5]  P. Morasso,et al.  Adjustment of saccade characteristics during head movements , 1973, Experimental Brain Research.

[6]  R. Hassler Die zentralen Apparate der Wendebewegungen , 1956, Archiv für Psychiatrie und Nervenkrankheiten.

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

[8]  L. Stark,et al.  Gaze latency: Variable interactions of head and eye latency , 1982, Experimental Neurology.

[9]  E. J. Tehovnik Head and body movements evoked electrically from the caudal superior colliculus of rats: Pulse frequency effects , 1989, Behavioural Brain Research.

[10]  P. Stanzione,et al.  Bilateral deep brain stimulation of the pedunculopontine and subthalamic nuclei in severe Parkinson's disease. , 2007, Brain : a journal of neurology.

[11]  W. Zangemeister,et al.  Preview control of gaze saccades: efficacy of prediction modulates eye-head interaction during human gaze saccades. , 1993, Neurological research.

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

[13]  J. Massion,et al.  Axial synergies during human upper trunk bending , 1998, Experimental Brain Research.

[14]  Y. Shinoda,et al.  Long descending motor tract axons and their control of neck and axial muscles. , 2006, Progress in brain research.

[15]  N. Mizuno,et al.  Direct projections from the entopeduncular nucleus to the lower brainstem in the rat , 1994, The Journal of comparative neurology.

[16]  Xianggui Qu,et al.  Multivariate Data Analysis , 2007, Technometrics.

[17]  P. Morasso,et al.  Mechanisms underlying recovery of eye-head coordination following bilateral labyrinthectomy in monkeys , 1973, Experimental Brain Research.

[18]  D. Pélisson,et al.  Vestibuloocular reflex inhibition and gaze saccade control characteristics during eye-head orientation in humans. , 1988, Journal of neurophysiology.

[19]  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.

[20]  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.

[21]  F. Richmond,et al.  Control of head movement , 1988 .

[22]  F. Baldissera,et al.  Anticipatory postural adjustments in arm muscles associated with movements of the contralateral limb and their possible role in interlimb coordination , 2008, Experimental Brain Research.

[23]  Kathleen E Cullen,et al.  Eye, head, and body coordination during large gaze shifts in rhesus monkeys: movement kinematics and the influence of posture. , 2007, Journal of neurophysiology.

[24]  L. Stark,et al.  Types of gaze movement: Variable interactions of eye and head movements , 1982, Experimental Neurology.

[25]  J. Stein,et al.  The role of the pedunculopontine region in basal-ganglia mechanisms of akinesia , 1999, Experimental Brain Research.

[26]  G. Barnes Vestibulo‐ocular function during co‐ordinated head and eye movements to acquire visual targets. , 1979, The Journal of physiology.

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

[28]  Lena H Ting,et al.  Neuromechanics of muscle synergies for posture and movement , 2007, Current Opinion in Neurobiology.

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

[30]  C D Mah,et al.  Quantitative analysis of human movement synergies: constructive pattern analysis for gait. , 1994, Journal of motor behavior.

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

[32]  A. Berthoz,et al.  Reticulo-spinal neurons participating in the control of synergic eye and head movements during orienting in the cat , 1987, Experimental Brain Research.

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

[34]  L. Rocchi,et al.  Dependence of anticipatory postural adjustments for step initiation on task movement features: a study based on dynamometric and accelerometric data , 2006, 2006 International Conference of the IEEE Engineering in Medicine and Biology Society.

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

[36]  J. Siegel,et al.  Behavioral organization of reticular formation: studies in the unrestrained cat. I. Cells related to axial, limb, eye, and other movements. , 1983, Journal of neurophysiology.