Short-latency disparity vergence in humans.

Eye movement recordings from humans indicated that brief exposures (200 ms) to horizontal disparity steps applied to large random-dot patterns elicit horizontal vergence at short latencies (80.9 +/- 3.9 ms, mean +/- SD; n = 7). Disparity tuning curves, describing the dependence of the initial vergence responses (measured over the period 90-157 ms after the step) on the magnitude of the steps, resembled the derivative of a Gaussian, with nonzero asymptotes and a roughly linear servo region that extended only a degree or two on either side of zero disparity. Responses showed transient postsaccadic enhancement: disparity steps applied in the immediate wake of saccadic eye movements yielded higher vergence accelerations than did the same steps applied some time later (mean time constant of the decay, 200 ms). This enhancement seemed to be dependent, at least in part, on the visual reafference associated with the prior saccade because similar enhancement was observed when the disparity steps were applied in the wake of saccadelike shifts of the textured pattern. Vertical vergence responses to vertical disparity steps were qualitatively similar: latencies were longer (on average, by 3 ms), disparity tuning curves had the same general form but were narrower (by approximately 20%), and their peak-to-peak amplitudes were smaller (by approximately 70%). Initial vergence responses usually had directional errors (orthogonal components) with a very systematic dependence on step size that often approximated an exponential decay to a nonzero asymptote (mean space constant +/- SD, 1.18 +/- 0.66 degrees ). Based on the asymptotes of these orthogonal responses, horizontal errors (with vertical steps) were on average more than three times greater than vertical errors (with horizontal steps). Disparity steps >7 degrees generated "default" responses that were independent of the direction of the step, idiosyncratic, and generally had both horizontal and vertical components. We suggest that the responses depend on detectors that sense local disparity matches, and that orthogonal and "default" responses result from globally "false" matches. Recordings from three monkeys, using identical disparity stimuli, confirmed that monkeys also show short-latency disparity vergence responses (latency approximately 25 ms shorter than that of humans), and further indicated that these responses show all of the major features seen in humans, the differences between the two species being solely quantitative. Based on these data and those of others implying that foveal images normally take precedence, we suggest that the mechanisms under study here ordinarily serve to correct small vergence errors, automatically, especially after saccades.

[1]  W. Newsome,et al.  Motion selectivity in macaque visual cortex. I. Mechanisms of direction and speed selectivity in extrastriate area MT. , 1986, Journal of neurophysiology.

[2]  R. Leigh,et al.  The neurology of eye movements , 1984 .

[3]  M W Greenlee,et al.  Human cortical areas underlying the perception of optic flow: brain imaging studies. , 2000, International review of neurobiology.

[4]  S Thorpe,et al.  Neural processing of stereopsis as a function of viewing distance in primate visual cortical area V1. , 1993, Journal of neurophysiology.

[5]  Leslie G. Ungerleider,et al.  Subcortical connections of visual areas MST and FST in macaques , 1992, Visual Neuroscience.

[6]  Nick Fogt,et al.  The Neurology of Eye Movements, 3rd ed. , 2000 .

[7]  G. DeAngelis,et al.  Cortical area MT and the perception of stereoscopic depth , 1998, Nature.

[8]  S. Zeki,et al.  The cerebral activity related to the visual perception of forward motion in depth. , 1994, Brain : a journal of neurology.

[9]  Poggio Gf Cortical neural mechanisms of stereopsis studied with dynamic random-dot stereograms. , 1990 .

[10]  G. Leichnetz,et al.  Cortical projections to the paramedian tegmental and basilar pons in the monkey , 1984, The Journal of comparative neurology.

[11]  John M. Findlay,et al.  The area of spatial integration for initial horizontal disparity vergence , 1998, Vision Research.

[12]  B G Cumming,et al.  Disparity Detection in Anticorrelated Stereograms , 1998, Perception.

[13]  D. J. Felleman,et al.  Receptive field properties of neurons in area V3 of macaque monkey extrastriate cortex. , 1987, Journal of neurophysiology.

[14]  Brian D. Ripley,et al.  Non-linear Models , 1999 .

[15]  P. O. Bishop,et al.  Binocular interaction fields of single units in the cat striate cortex , 1971, The Journal of physiology.

[16]  M. C. Jones,et al.  Spline Smoothing and Nonparametric Regression. , 1989 .

[17]  Paul D. Gamlin,et al.  Single-unit activity in the primate nucleus reticularis tegmenti pontis related to vergence and ocular accommodation. , 1995, Journal of neurophysiology.

[18]  M. Glickstein,et al.  Corticopontine projection in the rat: The distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei , 1989, The Journal of comparative neurology.

[19]  D. V. van Essen,et al.  Processing of color, form and disparity information in visual areas VP and V2 of ventral extrastriate cortex in the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  R. Jennrich,et al.  Application of Stepwise Regression to Non-Linear Estimation , 1968 .

[21]  D. Mitchell,et al.  Properties of stimuli eliciting vergence eye movements and stereopsis. , 1970, Vision research.

[22]  S. Thorpe,et al.  Neural processing of stereopsis as a function of viewing distance in primate visual cortical area V1 , 1996 .

[23]  F A Miles,et al.  Short latency ocular-following responses in man , 1990, Visual Neuroscience.

[24]  R H Wurtz,et al.  Disparity sensitivity of frontal eye field neurons. , 2000, Journal of neurophysiology.

[25]  J. V. Van Gisbergen,et al.  Stimulation in the rostral pole of monkey superior colliculus: effects on vergence eye movements , 2000, Experimental Brain Research.

[26]  D. B. Bender,et al.  Distribution of corticotectal cells in macaque , 2003, Experimental Brain Research.

[27]  D. Ferster A comparison of binocular depth mechanisms in areas 17 and 18 of the cat visual cortex , 1981, The Journal of physiology.

[28]  F. A. Miles,et al.  Vergence eye movements in response to binocular disparity without depth perception , 1997, Nature.

[29]  G. Poggio,et al.  Binocular interaction and depth sensitivity in striate and prestriate cortex of behaving rhesus monkey. , 1977, Journal of neurophysiology.

[30]  B. Yandell Spline smoothing and nonparametric regression , 1989 .

[31]  R. Andersen,et al.  Integration of motion and stereopsis in middle temporal cortical area of macaques , 1995, Nature.

[32]  G C DeAngelis,et al.  The physiology of stereopsis. , 2001, Annual review of neuroscience.

[33]  W. P. Dixon,et al.  BMPD statistical software manual , 1988 .

[34]  A. Gibson,et al.  Corticopontine visual projections in macaque monkeys , 1980, The Journal of comparative neurology.

[35]  G. DeAngelis,et al.  Organization of Disparity-Selective Neurons in Macaque Area MT , 1999, The Journal of Neuroscience.

[36]  D. Robinson,et al.  A METHOD OF MEASURING EYE MOVEMENT USING A SCLERAL SEARCH COIL IN A MAGNETIC FIELD. , 1963, IEEE transactions on bio-medical engineering.

[37]  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.

[38]  I. P. Howard,et al.  Effects of stimulus size and eccentricity on horizontal and vertical vergence , 2000, Experimental Brain Research.

[39]  Cortical neural mechanisms of stereopsis studied with dynamic random-dot stereograms. , 1990, Cold Spring Harbor symposia on quantitative biology.

[40]  Richard S. J. Frackowiak,et al.  Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. , 1993, Cerebral cortex.

[41]  G. Poggio,et al.  Mechanisms of static and dynamic stereopsis in foveal cortex of the rhesus monkey , 1981, The Journal of physiology.

[42]  N. Shimizu [Neurology of eye movements]. , 2000, Rinsho shinkeigaku = Clinical neurology.

[43]  G. Poggio,et al.  Stereoscopic mechanisms in monkey visual cortex: binocular correlation and disparity selectivity , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  G. Westheimer,et al.  Disjunctive eye movements , 1961, The Journal of physiology.

[45]  Paul D. Gamlin,et al.  The role of cerebro-ponto-cerebellar pathways in the control of vergence eye movements , 1996, Eye.

[46]  Andrew J. Parker,et al.  Local Disparity Not Perceived Depth Is Signaled by Binocular Neurons in Cortical Area V1 of the Macaque , 2000, The Journal of Neuroscience.

[47]  Scott B Stevenson,et al.  The effect of target size and eccentricity on reflex disparity vergence , 1999, Vision Research.

[48]  A. Parker,et al.  Binocular Neurons in V1 of Awake Monkeys Are Selective for Absolute, Not Relative, Disparity , 1999, The Journal of Neuroscience.

[49]  DH Hubel,et al.  Segregation of form, color, and stereopsis in primate area 18 , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[50]  S. Stevenson,et al.  The influence of subject instruction on horizontal and vertical vergence tracking , 1997, Vision Research.

[51]  D. Hubel,et al.  Stereoscopic Vision in Macaque Monkey: Cells sensitive to Binocular Depth in Area 18 of the Macaque Monkey Cortex , 1970, Nature.

[52]  J. Lund,et al.  Sensory processing in the mammalian brain : neural substrates and experimental strategies , 1989 .

[53]  H. Sakata,et al.  Functional properties of visual tracking neurons in posterior parietal association cortex of the monkey. , 1983, Journal of neurophysiology.

[54]  R Jones,et al.  Fusional vergence: sustained and transient components. , 1980, American journal of optometry and physiological optics.

[55]  Eileen Kowler,et al.  The effect of expectations on slow oculomotor control—II. Single target displacements , 1979, Vision Research.

[56]  J W Gnadt,et al.  Eye movements in depth: What does the monkey's parietal cortex tell the superior colliculus? , 1998, Neuroreport.

[57]  R. Wurtz,et al.  Response to motion in extrastriate area MSTl: disparity sensitivity. , 1999, Journal of neurophysiology.

[58]  Eileen Kowler,et al.  The effect of expectations on slow oculomotor control—I. Periodic target steps , 1979, Vision Research.

[59]  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.

[60]  R. Andersen,et al.  Center–Surround Antagonism Based on Disparity in Primate Area MT , 1998, The Journal of Neuroscience.

[61]  H. Collewijn,et al.  Precise recording of human eye movements , 1975, Vision Research.

[62]  F. Krause,et al.  Binocular matching in monkey visual cortex: Single cell responses to correlated and uncorrelated dynamic random dot stereograms , 1993, Neuroscience.

[63]  L E Mays,et al.  Neurons in monkey parietal area LIP are tuned for eye-movement parameters in three-dimensional space. , 1995, Journal of neurophysiology.

[64]  Robert S. Allison,et al.  The dynamics of vertical vergence , 1997, Experimental Brain Research.

[65]  F A Miles,et al.  Short-latency ocular following responses of monkey. II. Dependence on a prior saccadic eye movement. , 1986, Journal of neurophysiology.

[66]  C. Schor,et al.  Negative feedback control model of proximal convergence and accommodation , 1992, Ophthalmic & physiological optics : the journal of the British College of Ophthalmic Opticians.

[67]  S G Lisberger,et al.  Postsaccadic enhancement of initiation of smooth pursuit eye movements in monkeys. , 1998, Journal of neurophysiology.

[68]  Lance M. Optican,et al.  Unix-based multiple-process system, for real-time data acquisition and control , 1982 .

[69]  W. Newsome,et al.  Motion selectivity in macaque visual cortex. II. Spatiotemporal range of directional interactions in MT and V1. , 1986, Journal of neurophysiology.

[70]  W. Newsome,et al.  Motion selectivity in macaque visual cortex. III. Psychophysics and physiology of apparent motion. , 1986, Journal of neurophysiology.

[71]  Paul D. Gamlin Subcortical neural circuits for ocular accommodation and vergence in primates , 1999, Ophthalmic & physiological optics.

[72]  A. Parker,et al.  The Precision of Single Neuron Responses in Cortical Area V1 during Stereoscopic Depth Judgments , 2000, The Journal of Neuroscience.

[73]  H Collewijn,et al.  Binocular eye movements and the perception of depth. , 1990, Reviews of oculomotor research.

[74]  F A Miles,et al.  The neural processing of 3‐D visual information: evidence from eye movements , 1998, The European journal of neuroscience.

[75]  B. G. Cumming,et al.  Responses of primary visual cortical neurons to binocular disparity without depth perception , 1997, Nature.

[76]  Paul D. Gamlin,et al.  An area for vergence eye movement in primate frontal cortex , 2000, Nature.

[77]  C. Busettini,et al.  A role for stereoscopic depth cues in the rapid visual stabilization of the eyes , 1996, Nature.

[78]  Karl J. Friston,et al.  A direct demonstration of functional specialization in human visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[79]  Y. Chino,et al.  Binocular combination of contrast signals by striate cortical neurons in the monkey. , 1997, Journal of neurophysiology.

[80]  G WESTHEIMER,et al.  Eye movement responses to convergence stimuli. , 1956, A.M.A. archives of ophthalmology.

[81]  L F Dell'Osso,et al.  Enhancement of the vestibulo-ocular reflex by prior eye movements. , 1999, Journal of neurophysiology.

[82]  John H. R. Maunsell,et al.  Functional properties of neurons in middle temporal visual area of the macaque monkey. II. Binocular interactions and sensitivity to binocular disparity. , 1983, Journal of neurophysiology.

[83]  R. Jones,et al.  Anomalies of disparity detection in the human visual system. , 1977, The Journal of physiology.

[84]  F A Miles,et al.  Short-latency disparity vergence responses and their dependence on a prior saccadic eye movement. , 1996, Journal of neurophysiology.

[85]  R. Andersen,et al.  Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[86]  Alexander I. Cogan,et al.  Depth in anticorrelated stereograms: Effects of spatial density and interocular delay , 1993, Vision Research.

[87]  H. Komatsu,et al.  Disparity sensitivity of neurons in monkey extrastriate area MST , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.