How Is a Sensory Map Read Out? Effects of Microstimulation in Visual Area MT on Saccades and Smooth Pursuit Eye Movements

To generate behavioral responses based on sensory input, motor areas of the brain must interpret, or “read out,” signals from sensory maps. Our experiments tested several algorithms for how the motor systems for smooth pursuit and saccadic eye movements might extract a usable signal of target velocity from the distributed representation of velocity in the middle temporal visual area (MT or V5). Using microstimulation, we attempted to manipulate the velocity information within MT while monkeys tracked a moving visual stimulus. We examined the effects of the microstimulation on smooth pursuit and on the compensation for target velocity shown by saccadic eye movements. Microstimulation could alter both the speed and direction of the motion estimates of both types of eye movements and could also cause monkeys to generate pursuit even when the visual target was actually stationary. The pattern of alterations suggests that microstimulation can introduce an additional velocity signal into MT and that the pursuit and saccadic systems usually compute a vector average of the visually evoked and microstimulation-induced velocity signals (pursuit, 55 of 122 experiments; saccades, 70 of 122). Microstimulation effects in a few experiments were consistent with vector summation of these two signals (pursuit, 6 of 122; saccades, 2 of 122). In the remainder of the experiments, microstimulation caused either an apparent impairment in motion processing (pursuit, 47 of 122; saccades, 41 of 122) or had no effect (pursuit, 14 of 122; saccades, 9 of 122). Within individual experiments, the effects on pursuit and saccades were usually similar, but the occasional striking exception suggests that the two eye movement systems may perform motion computations somewhat independently.

[1]  W. Becker,et al.  An analysis of the saccadic system by means of double step stimuli , 1979, Vision Research.

[2]  W. Newsome,et al.  Microstimulation in visual area MT: effects on direction discrimination performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  R. Larsen An introduction to mathematical statistics and its applications / Richard J. Larsen, Morris L. Marx , 1986 .

[4]  A Grinvald,et al.  Optical imaging reveals the functional architecture of neurons processing shape and motion in owl monkey area MT , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[5]  S. Zeki,et al.  Response properties and receptive fields of cells in an anatomically defined region of the superior temporal sulcus in the monkey. , 1971, Brain research.

[6]  D C Van Essen,et al.  Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. , 1983, Journal of neurophysiology.

[7]  D. Sparks,et al.  Population coding of saccadic eye movements by neurons in the superior colliculus , 1988, Nature.

[8]  S G Lisberger,et al.  Vector Averaging for Smooth Pursuit Eye Movements Initiated by Two Moving Targets in Monkeys , 1997, The Journal of Neuroscience.

[9]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  W. Newsome,et al.  Microstimulation in visual area MT: effects of varying pulse amplitude and frequency , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  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.

[12]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  Jacques Droulez,et al.  Target velocity based prediction in saccadic vector programming , 1989, Vision Research.

[14]  William T. Newsome,et al.  Cortical microstimulation influences perceptual judgements of motion direction , 1990, Nature.

[15]  A. Fuchs,et al.  Eye movements evoked by stimulation of frontal eye fields. , 1969, Journal of neurophysiology.

[16]  J. D. Mollon,et al.  Control of eye movements , 1977, Nature.

[17]  Peter H. Schiller,et al.  Paired stimulation of the frontal eye fields and the superior colliculus of the rhesus monkey , 1979, Brain Research.

[18]  T. Albright Direction and orientation selectivity of neurons in visual area MT of the macaque. , 1984, Journal of neurophysiology.

[19]  N. L. Johnson,et al.  Multivariate Analysis , 1958, Nature.

[20]  K. Duncker,et al.  Über induzierte Bewegung , 1929 .

[21]  John H. R. Maunsell,et al.  Physiological Evidence for Two Visual Subsystems , 1987 .

[22]  Simon Heywood,et al.  Saccades to step-ramp stimuli , 1981, Vision Research.

[23]  N J Gandhi,et al.  Discharge of superior collicular neurons during saccades made to moving targets. , 1996, Journal of neurophysiology.

[24]  C. Rashbass,et al.  The relationship between saccadic and smooth tracking eye movements , 1961, The Journal of physiology.

[25]  E. J. Morris,et al.  Visual motion processing and sensory-motor integration for smooth pursuit eye movements. , 1987, Annual review of neuroscience.

[26]  R. Wurtz,et al.  Probing visual cortical function with discrete chemical lesions , 1988, Trends in Neurosciences.

[27]  G. Orban,et al.  Response to movement of neurons in areas 17 and 18 of the cat: velocity sensitivity. , 1981, Journal of neurophysiology.

[28]  S. Lisberger,et al.  Attention and target selection for smooth pursuit eye movements , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  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.

[30]  K. H. Britten,et al.  A relationship between behavioral choice and the visual responses of neurons in macaque MT , 1996, Visual Neuroscience.

[31]  J. Findlay Global visual processing for saccadic eye movements , 1982, Vision Research.

[32]  T D Albright,et al.  Cortical processing of visual motion. , 1993, Reviews of oculomotor research.

[33]  H. Komatsu,et al.  Modulation of pursuit eye movements by stimulation of cortical areas MT and MST. , 1989, Journal of neurophysiology.

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

[35]  J. Finn A General Model for Multivariate Analysis , 1978 .

[36]  J. Movshon The velocity tuning of single units in cat striate cortex. , 1975, The Journal of physiology.

[37]  S. Zeki Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey , 1974, The Journal of physiology.

[38]  D. Robinson Control of eye movements , 1981 .

[39]  D. Robinson Eye movements evoked by collicular stimulation in the alert monkey. , 1972, Vision research.

[40]  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.

[41]  G. Orban,et al.  Response latencies of visual cells in macaque areas V1, V2 and V5 , 1989, Brain Research.

[42]  C D Salzman,et al.  Neural mechanisms for forming a perceptual decision. , 1994, Science.

[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]  R. Desimone,et al.  Columnar organization of directionally selective cells in visual area MT of the macaque. , 1984, Journal of neurophysiology.

[45]  J T McIlwain,et al.  Distributed spatial coding in the superior colliculus: A review , 1991, Visual Neuroscience.

[46]  P H Schiller,et al.  The effects of lateral geniculate nucleus, area V4, and middle temporal (MT) lesions on visually guided eye movements , 1994, Visual Neuroscience.

[47]  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.