Short-latency eye movements: evidence for rapid, parallel processing of optic flow

As we go about our daily activities we view the world from a constantly shifting platform and some visual functions are compromised if the images on the retina are not reasonably stable. For example, visual acuity begins to deteriorate when retinal image speeds exceed a few degrees per second (Westheimer & McKee, 1975). There are a number of visual reflexes that help to stabilize our gaze on particular objects of interest by generating eye movements to offset our head movements. However, it is important to remember that these visual mechanisms normally operate in close synergy with vestibuloocular reflexes that rely on two types of end-organ embedded in the base of the skull: the semicircular canals, which are selectively sensitive to angular accelerations of the head, and the otolith organs, which are selectively sensitive to linear accelerations (Goldberg & Fernandez, 1975). Thus, the vestibular end-organs decompose head movements into their angular and linear components and support two quite independent reflexes, the RVOR and TVOR, that compensate selectively for rotational and translational disturbances of the head respectively with latencies <10 msec. These vestibular reflexes operate open-loop—because their output, eye movement, does not influence their input, head movement—and neither is perfect, hence motion of the observer must often be associated with some residual retinal image motion and this is where the visual stabilization mechanisms become involved. However, the visual end-organs — the two retinas — see all visual disturbances, regardless of whether they result from rotation and/or translation of gaze so that if any visual decomposition is to be done it must be by signal processing in the central nervous system (CNS). It is our contention that the visual system does attempt to perform such decomposition, using visual filters to sense the pattern of optic flow and thereby infer the observer’s motion and the eye movements that best compensate for that motion.

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

[2]  Ian P. Howard,et al.  Human optokinetic nystagmus in response to moving binocularly disparate stimuli , 1987, Vision Research.

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

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

[5]  I. P. Howard,et al.  Human optokinetic nystagmus is linked to the stereoscopic system , 2004, Experimental Brain Research.

[6]  F A Miles,et al.  Ocular responses to linear motion are inversely proportional to viewing distance. , 1989, Science.

[7]  Frederick A. Miles,et al.  The Sensing of Optic Flow by the Primate Optokinetic System , 1995 .

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

[9]  Frederick A. Miles,et al.  The parsing of optic flow by the primate oculomotor system , 1991 .

[10]  G. Orban,et al.  Responses of macaque STS neurons to optic flow components: a comparison of areas MT and MST. , 1994, Journal of neurophysiology.

[11]  H. Collewijn,et al.  Optokinetic reactions in man elicited by localized retinal motion stimuli , 1979, Vision Research.

[12]  R. Wurtz,et al.  Sensitivity of MST neurons to optic flow stimuli. II. Mechanisms of response selectivity revealed by small-field stimuli. , 1991, Journal of neurophysiology.

[13]  Frederick A. Miles,et al.  Decoding of Optic Flow by the Primate Optokinetic System , 1992 .

[14]  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.

[15]  D. R MESTRE,et al.  Ocular Responses to Motion Parallax Stimuli: The Role of Perceptual and Attentional Factors , 1997, Vision Research.

[16]  A. Berthoz,et al.  Adaptive mechanisms in gaze control : facts and theories , 1985 .

[17]  I. P. Howard,et al.  Up-down asymmetry in human vertical optokinetic nystagmus and afternystagmus: contributions of the central and peripheral retinae , 2004, Experimental Brain Research.

[18]  C J Duffy,et al.  Optic flow analysis for self-movement perception. , 2000, International review of neurobiology.

[19]  F A Miles,et al.  Effects of stationary textured backgrounds on the initiation of pursuit eye movements in monkeys. , 1992, Journal of neurophysiology.

[20]  K. Hoffmann,et al.  Optic flow and eye movements. , 2000, International review of neurobiology.

[21]  K. Hoffmann,et al.  Ocular responses to radial optic flow and single accelerated targets in humans , 1999, Vision Research.

[22]  F. Miles,et al.  Visual stabilization of the eyes in primates , 1997, Current Opinion in Neurobiology.

[23]  Robert H. Wurtz,et al.  Multiple temporal components of optic flow responses in MST neurons , 1997, Experimental Brain Research.

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

[25]  F. A. Miles,et al.  Reversed short-latency ocular following , 2002, Vision Research.

[26]  R. Wurtz,et al.  Medial Superior Temporal Area Neurons Respond to Speed Patterns in Optic Flow , 1997, The Journal of Neuroscience.

[27]  G. D. Paige,et al.  The influence of target distance on eye movement responses during vertical linear motion , 2004, Experimental Brain Research.

[28]  R. Wurtz,et al.  Planar directional contributions to optic flow responses in MST neurons. , 1997, Journal of neurophysiology.

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

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

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

[32]  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.

[33]  H. Collewijn,et al.  Motion perception during dichoptic viewing of moving random-dot stereograms , 1985, Vision Research.

[34]  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.

[35]  F. A. Miles,et al.  Visual Motion and Its Role in the Stabilization of Gaze , 1992 .

[36]  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.

[37]  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.

[38]  Masao Ohmi,et al.  The efficiency of the central and peripheral retina in driving human optokinetic nystagmus , 1984, Vision Research.

[39]  D Regan,et al.  Human ocular vergence movements induced by changing size and disparity. , 1986, The Journal of physiology.

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

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

[42]  Keiji Tanaka,et al.  Integration of direction signals of image motion in the superior temporal sulcus of the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  A. Borst,et al.  Detecting visual motion: theory and models. , 1993, Reviews of oculomotor research.

[44]  D. Regan,et al.  Necessary conditions for the perception of motion in depth. , 1986, Investigative ophthalmology & visual science.

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

[46]  K. Hoffmann,et al.  Optokinetic eye movements elicited by radial optic flow in the macaque monkey. , 1998, Journal of neurophysiology.

[47]  F. A. Miles,et al.  Role of primate medial vestibular nucleus in long-term adaptive plasticity of vestibuloocular reflex. , 1980, Journal of neurophysiology.

[48]  F A Miles,et al.  Long-term adaptive changes in primate vestibuloocular reflex. I. Behavioral observations. , 1980, Journal of neurophysiology.

[49]  J. Goldberg,et al.  Responses of peripheral vestibular neurons to angular and linear accelerations in the squirrel monkey. , 1975, Acta oto-laryngologica.

[50]  S. McKee,et al.  Visual acuity in the presence of retinal-image motion. , 1975, Journal of the Optical Society of America.

[51]  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.

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

[53]  J. Simpson The accessory optic system. , 1984, Annual review of neuroscience.

[54]  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.

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

[56]  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.

[57]  G. Paige,et al.  Eye movement responses to linear head motion in the squirrel monkey. I. Basic characteristics. , 1991, Journal of neurophysiology.

[58]  J I Simpson,et al.  The selection of reference frames by nature and its investigators. , 1985, Reviews of oculomotor research.

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

[60]  F. A. Miles,et al.  The Role of Inertial and Visual Mechanisms in the Stabilization of Gaze in Natural and Artificial Systems , 2001 .

[61]  Alain Berthoz,et al.  The Head-neck sensory motor system , 1992 .

[62]  J. Gibson The Senses Considered As Perceptual Systems , 1967 .

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

[64]  J. Perrone,et al.  A model of self-motion estimation within primate extrastriate visual cortex , 1994, Vision Research.

[65]  F. A. Miles,et al.  Adaptive plasticity in the vestibulo-ocular responses of the rhesus monkey. , 1974, Brain research.

[66]  E. Adelson,et al.  The analysis of moving visual patterns , 1985 .

[67]  R. Wurtz,et al.  Response of monkey MST neurons to optic flow stimuli with shifted centers of motion , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[68]  J A Perrone,et al.  Emulating the Visual Receptive-Field Properties of MST Neurons with a Template Model of Heading Estimation , 1998, The Journal of Neuroscience.

[69]  E. Castet,et al.  Temporal dynamics of motion integration for the initiation of tracking eye movements at ultra-short latencies , 2000, Visual Neuroscience.

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

[71]  H. Collewijn,et al.  Eye movements and stereopsis during dichoptic viewing of moving random-dot stereograms , 1985, Vision Research.

[72]  E. L. Keller,et al.  Smooth-pursuit initiation in the presence of a textured background in monkey , 1986, Vision Research.

[73]  Charles G. Gross,et al.  Pattern recognition mechanisms , 1985 .

[74]  J. Gibson The perception of the visual world , 1951 .