Deficits in Short-Latency Tracking Eye Movements after Chemical Lesions in Monkey Cortical Areas MT and MST

Past work has suggested that the medial superior temporal area (MST) is involved in the initiation of three kinds of eye movements at short latency by large-field visual stimuli. These eye movements consist of (1) version elicited by linear motion (the ocular following response), (2) vergence elicited by binocular parallax (the disparity vergence response), and (3) vergence elicited by global motion toward or away from the fovea (the radial-flow vergence response). We investigated this hypothesis by recording the effects of ibotenic acid injections in the superior temporal sulcus (STS) of both hemispheres in five monkeys. After the injections, all three kinds of eye movements were significantly impaired, with the magnitude of the impairments often showing a strong correlation with the extent of the morphological damage in the three subregions of the STS: dorsal MST on the anterior bank, lateral MST and middle temporal area on the posterior bank. However, the extent of the lesions in the three subregions often covaried, rendering it difficult to assess their relative contributions to the various deficits. The effects of the lesions on other aspects of oculomotor behavior that are known to be important for the normal functioning of the three tracking mechanisms (e.g., ocular stability, fixation disparity) were judged to be generally minor and to contribute little to the impairments. We conclude that, insofar as MST sustained significant damage in all injected hemispheres, our findings are consistent with the hypothesis that MST is a primary site for initiating all three visual tracking eye movements at ultra-short latencies.

[1]  F A Miles,et al.  Optokinetic response in monkey: underlying mechanisms and their sensitivity to long-term adaptive changes in vestibuloocular reflex. , 1981, Journal of neurophysiology.

[2]  G. Sperling,et al.  Full-wave and half-wave rectification in second-order motion perception , 1994, Vision Research.

[3]  F. A. Miles,et al.  Dependence of short-latency ocular following and associated activity in the medial superior temporal area (MST) on ocular vergence , 1998, Experimental Brain Research.

[4]  Aya Takemura,et al.  Neuronal responses in MST reflect the post-saccadic enhancement of short-latency ocular following responses , 2006, Experimental Brain Research.

[5]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[6]  C Busettini,et al.  Short-latency disparity vergence in humans. , 2001, Journal of neurophysiology.

[7]  B. Cohen,et al.  Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after‐nystagmus , 1977, The Journal of physiology.

[8]  John H. R. Maunsell,et al.  Coding of image contrast in central visual pathways of the macaque monkey , 1990, Vision Research.

[9]  D. G. Albrecht,et al.  Striate cortex of monkey and cat: contrast response function. , 1982, Journal of neurophysiology.

[10]  Eric Castet,et al.  Parallel Motion Processing for the Initiation of Short-Latency Ocular Following in Humans , 2002, The Journal of Neuroscience.

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

[12]  J. Maunsell,et al.  Two‐dimensional maps of the cerebral cortex , 1980, The Journal of comparative neurology.

[13]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. I. Localization and visual properties of neurons. , 1988, Journal of neurophysiology.

[14]  F A Miles,et al.  Ocular responses to translation and their dependence on viewing distance. I. Motion of the observer. , 1991, Journal of neurophysiology.

[15]  T D Albright,et al.  Form-cue invariant motion processing in primate visual cortex. , 1992, Science.

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

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

[18]  Jan Churan,et al.  Motion perception without explicit activity in areas MT and MST. , 2004, Journal of neurophysiology.

[19]  F. A. Miles,et al.  Short-latency ocular following responses of monkey. I. Dependence on temporospatial properties of visual input. , 1986, Journal of neurophysiology.

[20]  Robert A. Frazor,et al.  Visual cortex neurons of monkeys and cats: temporal dynamics of the contrast response function. , 2002, Journal of neurophysiology.

[21]  S. Yamane,et al.  Neural activity in cortical area MST of alert monkey during ocular following responses. , 1994, Journal of neurophysiology.

[22]  K. Tanaka,et al.  Analysis of motion of the visual field by direction, expansion/contraction, and rotation cells clustered in the dorsal part of the medial superior temporal area of the macaque monkey. , 1989, Journal of neurophysiology.

[23]  B. Cumming,et al.  Testing quantitative models of binocular disparity selectivity in primary visual cortex. , 2003, Journal of neurophysiology.

[24]  A. Takemura,et al.  The effect of disparity on the very earliest ocular following responses and the initial neuronal activity in monkey cortical area MST , 2000, Neuroscience Research.

[25]  John H. R. Maunsell,et al.  The middle temporal visual area in the macaque: Myeloarchitecture, connections, functional properties and topographic organization , 1981, The Journal of comparative neurology.

[26]  C. Busettini,et al.  Human ocular responses to translation of the observer and of the scene: dependence on viewing distance , 1994, Experimental Brain Research.

[27]  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.

[28]  K. Kawano,et al.  Role of Purkinje cells in the ventral paraflocculus in short-latency ocular following responses , 2004, Experimental Brain Research.

[29]  Allan Pantle,et al.  Visual resolution of motion ambiguity with periodic luminance- and contrast-domain stimuli , 1992, Vision Research.

[30]  Frederick A. Miles,et al.  Short-latency eye movements: evidence for rapid, parallel processing of optic flow , 2004 .

[31]  C. Busettini,et al.  Radial optic flow induces vergence eye movements with ultra-short latencies , 1997, Nature.

[32]  S. Nishida Spatiotemporal properties of motion perception for random-check contrast modulations , 1993, Vision Research.

[33]  Z L Lu,et al.  Three-systems theory of human visual motion perception: review and update. , 2001, Journal of the Optical Society of America. A, Optics, image science, and vision.

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

[35]  P J Benson,et al.  Stages in motion processing revealed by the ocular following response. , 1999, Neuroreport.

[36]  F. A. Miles,et al.  Single-unit activity in cortical area MST associated with disparity-vergence eye movements: evidence for population coding. , 2001, Journal of neurophysiology.

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

[38]  E. Fitzgibbon,et al.  Short-latency vergence eye movements induced by radial optic flow in humans: dependence on ambient vergence level. , 1999, Journal of neurophysiology.

[39]  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.

[40]  A. T. Smith,et al.  Transparent motion from feature- and luminance-based processes , 1993, Vision Research.

[41]  Leslie G. Ungerleider,et al.  Cortical connections of visual area MT in the macaque , 1986, The Journal of comparative neurology.

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

[43]  Leslie G. Ungerleider,et al.  Multiple visual areas in the caudal superior temporal sulcus of the macaque , 1986, The Journal of comparative neurology.

[44]  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.

[45]  W. Newsome,et al.  Deficits in visual motion processing following ibotenic acid lesions of the middle temporal visual area of the macaque monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  A. Takemura,et al.  Short-latency vergence eye movements elicited by looming step in monkeys , 1998, Neurosciences research.

[47]  Aya Takemura,et al.  Visually Driven Eye Movements Elicited at Ultra‐short Latency Are Severely Impaired by MST Lesions , 2002, Annals of the New York Academy of Sciences.

[48]  K. Tanaka,et al.  Analysis of local and wide-field movements in the superior temporal visual areas of the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  Aya Takemura,et al.  Ocular tracking of moving targets: effects of perturbing the background. , 2004, Journal of neurophysiology.

[50]  F. Gallyas Silver staining of myelin by means of physical development. , 1979, Neurological research.

[51]  Sheng He,et al.  Visual motion of missing-fundamental patterns: motion energy versus feature correspondence , 2000, Vision Research.

[52]  F A Miles,et al.  Ocular responses to translation and their dependence on viewing distance. II. Motion of the scene. , 1991, Journal of neurophysiology.

[53]  R. Wurtz,et al.  The role of disparity-sensitive cortical neurons in signalling the direction of self-motion , 1990, Nature.

[54]  L. P. O'Keefe,et al.  Processing of first- and second-order motion signals by neurons in area MT of the macaque monkey , 1998, Visual Neuroscience.

[55]  C Busettini,et al.  Short-latency ocular following in humans: sensitivity to binocular disparity , 2001, Vision Research.

[56]  R. Wurtz,et al.  Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. , 1991, Journal of neurophysiology.

[57]  A. T. Smith,et al.  Correspondence-based and energy-based detection of second-order motion in human vision. , 1994, Journal of the Optical Society of America. A, Optics, image science, and vision.

[58]  W. Newsome,et al.  Directional pursuit deficits following lesions of the foveal representation within the superior temporal sulcus of the macaque monkey. , 1987, Journal of neurophysiology.

[59]  Mark A. Georgeson,et al.  Monocular motion sensing, binocular motion perception , 1989, Vision Research.

[60]  F. A. Miles,et al.  Population Coding in Cortical Area MST , 2002, Annals of the New York Academy of Sciences.

[61]  Mark A. Georgeson,et al.  The temporal range of motion sensing and motion perception , 1990, Vision Research.

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

[63]  Vision Research , 1961, Nature.

[64]  F A Miles,et al.  Initial Ocular Following in Humans Depends Critically on the Fourier Components of the Motion Stimulus , 2005, Annals of the New York Academy of Sciences.

[65]  R. Wurtz,et al.  Pursuit and optokinetic deficits following chemical lesions of cortical areas MT and MST. , 1988, Journal of neurophysiology.

[66]  F. Miles,et al.  Short-latency ocular following in humans is dependent on absolute (rather than relative) binocular disparity , 2003, Vision Research.

[67]  F. A. Miles,et al.  The role of MST neurons during ocular tracking in 3D space. , 2000, International review of neurobiology.

[68]  A. Fuchs,et al.  A method for measuring horizontal and vertical eye movement chronically in the monkey. , 1966, Journal of applied physiology.

[69]  K. H. Britten,et al.  Contrast dependence of response normalization in area MT of the rhesus macaque. , 2002, Journal of neurophysiology.

[70]  F. A. Miles,et al.  Initial ocular following in humans: A response to first-order motion energy , 2005, Vision Research.

[71]  K. Naka,et al.  S‐potentials from colour units in the retina of fish (Cyprinidae) , 1966, The Journal of physiology.

[72]  F A Miles,et al.  Short-latency ocular following responses of monkey. III. Plasticity. , 1986, Journal of neurophysiology.

[73]  E H Adelson,et al.  Spatiotemporal energy models for the perception of motion. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[74]  R. Wurtz,et al.  Recovery of function after lesions in the superior temporal sulcus in the monkey. , 1991, Journal of neurophysiology.

[75]  John A. Baro,et al.  Apparent motion can be perceived between patterns with dissimilar spatial frequencies , 1988, Vision Research.

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

[77]  B. Sheliga,et al.  Short‐Latency Disparity Vergence in Humans: Evidence for Early Spatial Filtering , 2005, Annals of the New York Academy of Sciences.

[78]  K. D. Valois,et al.  Motion-reversal Reveals Two Motion Mechanisms Functioning in Scotopic Vision , 1997, Vision Research.

[79]  G. Sperling,et al.  The functional architecture of human visual motion perception , 1995, Vision Research.

[80]  R. Wurtz Visual receptive fields of striate cortex neurons in awake monkeys. , 1969, Journal of neurophysiology.