Functions of the nucleus of the optic tract (NOT).

Abstract. Ocular pursuit in monkeys, elicited by sinusoidal and triangular (constant velocity) stimuli, was studied before and after lesions of the nucleus of the optic tract (NOT). Before NOT lesions, pursuit gains (eye velocity/target velocity) were close to unity for sinusoidal and constant-velocity stimuli at frequencies up to 1 Hz. In this range, retinal slip was less than 2°. Electrode tracks made to identify the location of NOT caused deficits in ipsilateral pursuit, which later recovered. Small electrolytic lesions of NOT reduced ipsilateral pursuit gains to below 0.5 in all tested conditions. Pursuit was better, however, when the eyes moved from the contralateral side toward the center (centripetal pursuit) than from the center ipsilaterally (centrifugal pursuit), although the eyes remained in close proximity to the target with saccadic tracking. Effects of lesions on ipsilateral pursuit were not permanent, and pursuit gains had generally recovered to 60–80% of baseline after about 2 weeks. One animal had bilateral NOT lesions and lost pursuit for 4 days. Thereafter, it had a centrifugal pursuit deficit that lasted for more than 2 months. Vertical pursuit and visually guided saccades were not affected by the bilateral NOT lesions in this animal. We also compared effects of these and similar NOT lesions on optokinetic nystagmus (OKN) and optokinetic after-nystagmus (OKAN). Correlation of functional deficits with NOT lesions from this and previous studies showed that rostral lesions of NOT in and around the pretectal olivary nucleus, which interrupted cortical input through the brachium of the superior colliculus (BSC), affected both smooth pursuit and OKN. In two animals in which it was tested, NOT lesions that caused a deficit in pursuit also decreased the rapid and slow components of OKN slow-phase velocity and affected OKAN. It was previously shown that slightly more caudal NOT lesions were more effective in altering gain adaptation of the angular vestibulo-ocular relfex (aVOR). The present findings suggest that cortical pathways through rostral NOT play an important role in maintenance of ipsilateral ocular pursuit. Since lesions that affected ocular pursuit had similar effects on ipsilateral OKN, processing for these two functions is probably closely linked in NOT, as it is elsewhere.

[1]  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.

[2]  S. Lisberger,et al.  Neural basis for motor learning in the vestibuloocular reflex of primates. I. Changes in the responses of brain stem neurons. , 1994, Journal of neurophysiology.

[3]  J. Simpson,et al.  Climbing fiber responses evoked in vestibulocerebellum of rabbit from visual system. , 1973, Journal of neurophysiology.

[4]  A. Fuchs,et al.  Visual Signals in the Nucleus of the Optic Tract and Their Brain Stem Destinations a , 1992, Annals of the New York Academy of Sciences.

[5]  N. Shimizu,et al.  Optokinetic response and adaptation of the vestibulo-ocular reflex (VOR) in a patient with chronic cortical blindness. , 1991, Acta oto-laryngologica. Supplementum.

[6]  J. Simpson,et al.  Climbing fiber activation of Purkinje cells in the flocculus by impulses transferred through the visual pathway. , 1972, Brain research.

[7]  Y. Zhang,et al.  Properties of superior vestibular nucleus flocculus target neurons in the squirrel monkey. I. General properties in comparison with flocculus projecting neurons. , 1995, Journal of neurophysiology.

[8]  S. Lisberger,et al.  Neural basis for motor learning in the vestibuloocular reflex of primates. II. Changes in the responses of horizontal gaze velocity Purkinje cells in the cerebellar flocculus and ventral paraflocculus. , 1994, Journal of neurophysiology.

[9]  B. N. Cardozo,et al.  GABAergic and non‐GABAergic neurons in the nucleus of the optic tract project to the superior colliculus: An ultrastructural retrograde tracer and immunocytochemical study in the rabbit , 1994, The Journal of comparative neurology.

[10]  S G Lisberger,et al.  Vestibular signals carried by pathways subserving plasticity of the vestibulo-ocular reflex in monkeys , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  M. Glickstein,et al.  Visual pontocerebellar projections in the macaque , 1994, The Journal of comparative neurology.

[12]  G. Jones,et al.  Extreme vestibulo‐ocular adaptation induced by prolonged optical reversal of vision , 1976, The Journal of physiology.

[13]  K. Hoffmann,et al.  Functional projections from striate cortex and superior temporal sulcus to the nucleus of the optic tract (NOT) and dorsal terminal nucleus of the accessory optic tract (DTN) of macaque monkeys , 1991, The Journal of comparative neurology.

[14]  I B Kozlovskaya,et al.  Changes in monkey horizontal semicircular canal afferent responses after spaceflight. , 1992, Journal of applied physiology.

[15]  Y. Zhang,et al.  Dorsal Y group in the squirrel monkey. II. Contribution of the cerebellar flocculus to neuronal responses in normal and adapted animals. , 1995, Journal of neurophysiology.

[16]  Tadashi Kawasaki,et al.  Role of the nucleus of the optic tract in monkeys in relation to optokinetic nystagmus , 1986, Brain Research.

[17]  I. Kato,et al.  Role of the nucleus of the optic tract of monkeys in optokinetic nystagmus and optokinetic after-nystagmus , 1988, Brain Research.

[18]  K. Hoffmann,et al.  Responses of monkey nucleus of the optic tract neurons during pursuit and fixation , 1991, Neuroscience Research.

[19]  M. Bentivoglio,et al.  Independent efferent populations in the nucleus of the optic tract: An anatomical and physiological study in rat and cat , 1995, The Journal of comparative neurology.

[20]  A. Fuchs,et al.  Anatomical connections of the primate pretectal nucleus of the optic tract , 1994, The Journal of comparative neurology.

[21]  A. Schoppmann,et al.  A direct afferent visual pathway from the nucleus of the optic tract to the inferior olive in the cat , 1976, Brain Research.

[22]  A. Fuchs,et al.  Discharge patterns of neurons in the pretectal nucleus of the optic tract (NOT) in the behaving primate. , 1990, Journal of neurophysiology.

[23]  M. Sirota,et al.  The role of the motor cortex in the control of accuracy of locomotor movements in the cat. , 1993, The Journal of physiology.

[24]  J. Simpson,et al.  The accessory optic system of rabbit. I. Basic visual response properties. , 1988, Journal of neurophysiology.

[25]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. , 1988, Journal of neurophysiology.

[26]  K. Hoffmann,et al.  Responses of Neurons of the Nucleus of the Optic Tract and the Dorsal Terminal Nucleus of the Accessory Optic Tract in the Awake Monkey , 1996, The European journal of neuroscience.

[27]  K. Hoffmann,et al.  Quantitative analysis of visual receptive fields of neurons in nucleus of the optic tract and dorsal terminal nucleus of the accessory optic tract in macaque monkey. , 1989, Journal of neurophysiology.

[28]  S. Lisberger Neural basis for motor learning in the vestibuloocular reflex of primates. III. Computational and behavioral analysis of the sites of learning. , 1994, Journal of neurophysiology.

[29]  J. T. Weber,et al.  The efferent projections of the pretectal complex: an autoradiographic and horseradish peroxidase analysis , 1980, Brain Research.

[30]  J. Büttner-Ennever,et al.  Pretectal projections to the oculomotor complex of the monkey and their role in eye movements , 1996, The Journal of comparative neurology.

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

[32]  K. Hoffmann,et al.  The Contribution of GABA‐mediated Inhibition to Response Properties of Neurons in the Nucleus of the Optic Tract in the Rat , 1994, The European journal of neuroscience.

[33]  D A Robinson,et al.  Effects of reversible lesions and stimulation of olivocerebellar system on vestibuloocular reflex plasticity. , 1982, Journal of neurophysiology.

[34]  J. Movshon,et al.  Selectivity for orientation and direction of motion of single neurons in cat striate and extrastriate visual cortex. , 1990, Journal of neurophysiology.

[35]  F. A. Miles,et al.  Plasticity in the vestibulo-ocular reflex: a new hypothesis. , 1981, Annual review of neuroscience.

[36]  T. Okada,et al.  Retinal Ganglion Cells Projecting to the Nucleus of the Optic Tract in the Cat , 1993 .

[37]  J. Yokota,et al.  The Nucleus of the Optic Tract a : Its Function in Gaze Stabilization and Control of Visual‐Vestibular Interaction , 1992, Annals of the New York Academy of Sciences.

[38]  D. Robinson The mechanics of human smooth pursuit eye movement. , 1965, The Journal of physiology.

[39]  R. Blanks,et al.  Projections of the nucleus of the optic tract to the nucleus reticularis tegmenti pontis and prepositus hypoglossi nucleus in the pigmented rat as demonstrated by anterograde and retrograde transport methods , 1989, Visual Neuroscience.

[40]  Harry J. Wyatt,et al.  Target position and velocity: The stimuli for smooth pursuit eye movements , 1980, Vision Research.

[41]  Role of the Y-group of the vestibular nuclei and flocculus of the cerebellum in motor learning of the vertical vestibulo-ocular reflex. , 1997, Progress in brain research.

[42]  Michael E. Goldberg,et al.  Effect of stimulus position and velocity upon the maintenance of smooth pursuit eye velocity , 1994, Vision Research.

[43]  C. Togt,et al.  Inhibition of Neuronal Activity in the Nucleus of the Optic Tract due to Electrical Stimulation of the Medial Terminal Nucleus in the Rat , 1994, The European journal of neuroscience.

[44]  S. Onodera,et al.  Olivary projections from the pretectal region in the cat studied with horseradish peroxidase and tritiated amino acids axonal transport. , 1984, Archives italiennes de biologie.

[45]  J. Fallon,et al.  GABAergic and non‐GABAergic projections of accessory optic nuclei, including the visual tegmental relay zone, to the nucleus of the optic tract and dorsal terminal accessory optic nucleus in rat , 1992, The Journal of comparative neurology.

[46]  D. A. Suzuki,et al.  Visual motion response properties of neurons in dorsolateral pontine nucleus of alert monkey. , 1990, Journal of neurophysiology.

[47]  Blank Rh,et al.  The pretectal nuclear complex and the accessory optic system. , 1988 .

[48]  D. Zee,et al.  Effects of ablation of flocculus and paraflocculus of eye movements in primate. , 1981, Journal of neurophysiology.

[49]  R. Blanks Afferents to the cerebellar flocculus in cat with special reference to pathways conveying vestibular, visual (optokinetic) and oculomotor signals , 1990, Journal of neurocytology.

[50]  K. Hoffmann,et al.  Retinal Projections to the Pretectum, Accessory Optic System and Superior Colliculus in Pigmented and Albino Ferrets , 1993, The European journal of neuroscience.

[51]  G. Melvill Jones,et al.  Adaptation of cat vestibulo-ocular reflex to 200 days of optically reversed vision , 1976, Brain Research.

[52]  P. Brodal,et al.  The corticopontine projection in the rhesus monkey. Origin and principles of organization. , 1978, Brain : a journal of neurology.

[53]  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.

[54]  W. Precht,et al.  Anatomical studies on the nucleus reticularis tegmenti pontis in the pigmented rat. II. Subcortical afferents demonstrated by the retrograde transport of horseradish peroxidase , 1986, The Journal of comparative neurology.

[55]  J L Demer,et al.  Cortical areas involved in OKN and VOR in cats: cortical lesions , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  B. Cohen,et al.  Efferent pathways of the nucleus of the optic tract in monkey and their role in eye movements , 1996, The Journal of comparative neurology.

[57]  Division on Earth Guide for the Care and Use of Laboratory Animals , 1996 .

[58]  K. Maekawa,et al.  Electrophysiological study of the nucleus of the optic tract that transfers optic signals to the nucleus reticularis tegmenti pontis—the visual mossy fiber pathway to the cerebellar flocculus , 1981, Brain Research.

[59]  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.

[60]  E. J. Morris,et al.  Different responses to small visual errors during initiation and maintenance of smooth-pursuit eye movements in monkeys. , 1987, Journal of neurophysiology.

[61]  L. Young,et al.  Pursuit eye tracking movements , 1971 .

[62]  Y. Miyashita,et al.  Contribution of cerebellar intracortical inhibition to Purkinje cell response during vestibulo‐ocular reflex of alert rabbits. , 1984, The Journal of physiology.

[63]  Frank Bremmer,et al.  Optokinetic and pursuit system: A case report , 1993, Behavioural Brain Research.

[64]  D. A. Suzuki,et al.  Smooth-pursuit eye movement deficits with chemical lesions in the dorsolateral pontine nucleus of the monkey. , 1988, Journal of neurophysiology.

[65]  U. Büttner The role of the cerebellum in smooth pursuit eye movements and optokinetic nystagmus in primates. , 1989, Revue neurologique.

[66]  Per Brodal,et al.  Principles of organization of the monkey corticopontine projection , 1978, Brain Research.

[67]  K. Hoffmann,et al.  Combined GABA-immunocytochemistry and TMB-HRP histochemistry of pretectal nuclei projecting to the inferior olive in rats, cats and monkeys , 1987, Brain Research.

[68]  K. Hoffmann Control of the optokinetic reflex by the nucleus of the optic tract in primates. , 1989, Progress in brain research.

[69]  F. A. Miles,et al.  Long-term adaptive changes in primate vestibuloocular reflex. IV. Electrophysiological observations in flocculus of adapted monkeys. , 1980, Journal of neurophysiology.

[70]  H. Collewijn Direction-selective units in the rabbit's nucleus of the optic tract , 1975, Brain Research.

[71]  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.

[72]  S. Highstein,et al.  Properties of superior vestibular nucleus flocculus target neurons in the squirrel monkey. II. Signal components revealed by reversible flocculus inactivation. , 1995, Journal of neurophysiology.

[73]  M. Pu,et al.  Dendritic morphologies of retinal ganglion cells projecting to the nucleus of the optic tract in the rabbit , 1990, The Journal of comparative neurology.

[74]  D S Zee,et al.  Effects of occipital lobectomy upon eye movements in primate. , 1987, Journal of neurophysiology.

[75]  G. Jones,et al.  Short‐term adaptive changes in the human vestibulo‐ocular reflex arc , 1976, The Journal of physiology.

[76]  Jones Gm Adaptive modulation of VOR parameters by vision. , 1985 .

[77]  Yasushi Miyashita,et al.  The Effects of Chronic Destruction of the Inferior Olive upon Visual Modification of the Horizontal Vestibulo-Ocular Reflex of Rabbits , 1975 .

[78]  S G Lisberger,et al.  Responses during eye movements of brain stem neurons that receive monosynaptic inhibition from the flocculus and ventral paraflocculus in monkeys. , 1994, Journal of neurophysiology.

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

[80]  M Fetter,et al.  Effect of lack of vision and of occipital lobectomy upon recovery from unilateral labyrinthectomy in rhesus monkey. , 1988, Journal of neurophysiology.

[81]  A. Fuchs,et al.  Response properties of dorsolateral pontine units during smooth pursuit in the rhesus macaque. , 1988, Journal of neurophysiology.

[82]  M. Glickstein,et al.  Corticopontine projection in the macaque: The distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei , 1985, The Journal of comparative neurology.

[83]  R M Steinman,et al.  Compensatory eye movements during active and passive head movements: fast adaptation to changes in visual magnification. , 1983, The Journal of physiology.

[84]  S. Lisberger,et al.  Neural Learning Rules for the Vestibulo-Ocular Reflex , 1998, The Journal of Neuroscience.

[85]  C. van der Togt,et al.  Medial terminal nucleus terminals in the nucleus of the optic tract contain GABA: An electron microscopical study with immunocytochemical double labeling of GABA and PHA‐L , 1991, The Journal of comparative neurology.

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

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

[88]  A. Fuchs,et al.  Role of the caudal fastigial nucleus in saccade generation. II. Effects of muscimol inactivation. , 1993, Journal of neurophysiology.

[89]  B Cohen,et al.  Semicircular canal contributions to the three-dimensional vestibuloocular reflex: a model-based approach. , 1995, Journal of neurophysiology.

[90]  F A Miles,et al.  Frequency-selective adaptation: evidence for channels in the vestibulo- ocular reflex? , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[91]  M. Norita,et al.  Pretectofugal fibers from the nucleus of the optic tract in monkeys , 1995, Brain Research.

[92]  J. T. Weber,et al.  The pretectal complex of the monkey: A reinvestigation of the morphology and retinal terminations , 1985, The Journal of comparative neurology.

[93]  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.

[94]  K. Kawamura,et al.  An HRP study in the monkey of olivary projections from the mesodiencephalic structures with particular reference to pretecto-olivary neurons. , 1985, Archives italiennes de biologie.

[95]  A. Fuchs,et al.  Response properties of single units in the lateral terminal nucleus of the accessory optic system in the behaving primate. , 1989, Journal of neurophysiology.

[96]  E. Keller,et al.  Neuronal responses to optokinetic stimuli in pontine nuclei of behaving monkey. , 1983, Journal of neurophysiology.

[97]  M Ito,et al.  Neurophysiological aspects of the cerebellar motor control system. , 1970, International journal of neurology.

[98]  A. Fuchs,et al.  Afferents to the flocculus of the cerebellum in the rhesus macaque as revealed by retrograde transport of horseradish peroxidase , 1985, The Journal of comparative neurology.

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

[100]  M. Ito Cerebellar control of the vestibulo-ocular reflex--around the flocculus hypothesis. , 1982, Annual review of neuroscience.

[101]  I Kato,et al.  Retinal ganglion cells related to optokinetic nystagmus in the rat. , 1992, Acta oto-laryngologica.

[102]  M. Ito,et al.  Neural design of the cerebellar motor control system. , 1972, Brain research.

[103]  P. Brodal,et al.  Further observations on the cerebellar projections from the pontine nuclei and the nucleus reticularis tegmenti pontis in the rhesus monkey , 1982, The Journal of comparative neurology.

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

[105]  H Collewijn,et al.  Oculomotor areas in the rabbits midbrain and pretectum. , 1975, Journal of neurobiology.