Monocular and Binocular Contributions to Oculomotor Plasticity

Most eye movements in the real-world redirect the foveae to objects at a new depth and thus require the co-ordination of monocular saccade amplitudes and binocular vergence eye movements. Additionally to maintain the accuracy of these oculomotor control processes across the lifespan, ongoing calibration is required to compensate for errors in foveal landing positions. Such oculomotor plasticity has generally been studied under conditions in which both eyes receive a common error signal, which cannot resolve the long-standing debate regarding whether both eyes are innervated by a common cortical signal or by a separate signal for each eye. Here we examine oculomotor plasticity when error signals are independently manipulated in each eye, which can occur naturally owing to aging changes in each eye’s orbit and extra-ocular muscles, or in oculomotor dysfunctions. We find that both rapid saccades and slow vergence eye movements are continuously recalibrated independently of one another and corrections can occur in opposite directions in each eye. Whereas existing models assume a single cortical representation of space employed for the control of both eyes, our findings provide evidence for independent monoculomotor and binoculomotor plasticities and dissociable spatial mapping for each eye.

[1]  Bruce Bridgeman,et al.  Failure to detect displacement of the visual world during saccadic eye movements , 1975, Vision Research.

[2]  S. C. Mclaughlin Parametric adjustment in saccadic eye movements , 1967 .

[3]  Shinya Saida,et al.  Methodological caveats for monitoring binocular eye position with Nonius stimuli , 1998, Vision Research.

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

[5]  Daniel R Saunders,et al.  Direct measurement of the system latency of gaze-contingent displays , 2013, Behavior Research Methods.

[6]  V. Della-Maggiore,et al.  Sensorimotor Adaptation , 2015, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[7]  W. King,et al.  Dynamics and efficacy of saccade-facilitated vergence eye movements in monkeys. , 1992, Journal of neurophysiology.

[8]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[9]  Thérèse Collins,et al.  The relative importance of retinal error and prediction in saccadic adaptation. , 2012, Journal of neurophysiology.

[10]  D. Pélisson,et al.  Sensorimotor adaptation of saccadic eye movements , 2010, Neuroscience & Biobehavioral Reviews.

[11]  J. A. Gisbergen,et al.  Specificity of saccadic adaptation in three-dimensional space , 1997, Vision Research.

[12]  H. Helmholtz Handbuch der physiologischen Optik , 2015 .

[13]  S. Salvi,et al.  Ageing changes in the eye , 2006, Postgraduate Medical Journal.

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

[15]  B. Bridgeman,et al.  Postsaccadic target blanking prevents saccadic suppression of image displacement , 1996, Vision Research.

[16]  Kathleen E Cullen,et al.  The brain stem saccadic burst generator encodes gaze in three-dimensional space. , 2008, Journal of neurophysiology.

[17]  W. King,et al.  Binocular coordination of eye movements – Hering’s Law of equal innervation or uniocular control? , 2011, The European journal of neuroscience.

[18]  J. Pokorny,et al.  Temporal dynamics of early light adaptation. , 2003, Journal of vision.

[19]  CASPER J ERKELENS,et al.  Trajectories of the Human Binocular Fixation Point during Conjugate and Non-conjugate Gaze-shifts , 1997, Vision Research.

[20]  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.

[21]  Heiner Deubel,et al.  Transsaccadic memory of position and form. , 2002, Progress in brain research.

[22]  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.

[23]  R. Leigh,et al.  Tests of two hypotheses to account for different-sized saccades during disjunctive gaze shifts , 1999, Experimental Brain Research.

[24]  Wu Zhou,et al.  Premotor commands encode monocular eye movements , 1998, Nature.

[25]  B. Bridgeman,et al.  Immediate post-saccadic information mediates space constancy , 1998, Vision Research.

[26]  Frans W Cornelissen,et al.  The Eyelink Toolbox: Eye tracking with MATLAB and the Psychophysics Toolbox , 2002, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[27]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[28]  F C VOLKMANN,et al.  Vision during voluntary saccadic eye movements. , 1962, Journal of the Optical Society of America.

[29]  A. Fuchs,et al.  The characteristics and neuronal substrate of saccadic eye movement plasticity , 2004, Progress in Neurobiology.

[30]  T. Vilis,et al.  Monocular adaptation of the saccadic system and vestibulo-ocular reflex. , 1988, Investigative ophthalmology & visual science.

[31]  M. Raichle,et al.  The role of cerebral cortex in the generation of voluntary saccades: a positron emission tomographic study. , 1985, Journal of neurophysiology.

[32]  P. Bex,et al.  Peri-Saccadic Natural Vision , 2013, The Journal of Neuroscience.

[33]  W. King,et al.  Neural Basis of Disjunctive Eye Movements , 2002, Annals of the New York Academy of Sciences.

[34]  S. Pensiero,et al.  Saccadic eye movement conjugation in children , 1995, Vision Research.

[35]  J. Demer,et al.  Effect of aging on human rectus extraocular muscle paths demonstrated by magnetic resonance imaging. , 2002, American journal of ophthalmology.

[36]  T Usui,et al.  Adaptive changes in dynamic properties of human disparity-induced vergence. , 2001, Investigative ophthalmology & visual science.

[37]  M. Clarke,et al.  Amblyopia , 2006, The Lancet.

[38]  Z. Kapoula,et al.  Binocular coordination of saccades at far and at near in children and in adults. , 2003, Journal of vision.

[39]  J. T. Enright The remarkable saccades of asymmetrical vergence , 1992, Vision Research.

[40]  C Busettini,et al.  Short-term saccadic adaptation in the macaque monkey: a binocular mechanism. , 2013, Journal of neurophysiology.

[41]  Olivier A Coubard,et al.  Saccade and vergence eye movements: a review of motor and premotor commands , 2013, The European journal of neuroscience.

[42]  Robert B Shaw,et al.  Aging of the Facial Skeleton: Aesthetic Implications and Rejuvenation Strategies , 2011, Plastic and reconstructive surgery.

[43]  G. B. Wetherill,et al.  SEQUENTIAL ESTIMATION OF POINTS ON A PSYCHOMETRIC FUNCTION. , 1965, The British journal of mathematical and statistical psychology.

[44]  J. E. Albano,et al.  Binocular interactions in rapid saccadic adaptation , 1995, Vision Research.