Extraretinal signals in MSTd neurons related to volitional smooth pursuit.

Smooth pursuit (SP)-related neurons in the dorsal-medial part of medial superior temporal cortex (MSTd) carry extraretinal signals that may play a role in maintenance of SP once eye velocity matches target velocity. For example, it has not been determined whether the extraretinal signals reflect volitional SP commands or proprioception. The aim of this study was to test some potential sources of extraretinal signals in MSTd pursuit neurons. We tested 40 MSTd neurons during step-ramp SP with target blink conditions to show that they carried an extraretinal signal. To examine potential contributions from eye movements that might reflect proprioceptive feedback from eye muscles, we tested MSTd neurons during rotational vestibular ocular reflex in complete darkness (VORd). Vestibular stimulation was delivered in the earth horizontal plane to elicit reflex driven smooth eye movements that matched the speed and frequency of volitional SP. We also tested VOR in the light (VOR x 1) and cancellation of the VOR (VOR x 0). Our neurons were modulated during both SP and cancellation of the VOR. In contrast, MSTd smooth pursuit neurons with extraretinal signals were not significantly modulated during VORd (sensitivity < or = 0.10 spike/s/ degrees /s). This combination of properties is compatible with classifying these neurons as gaze-velocity related. Absence of modulation during VORd testing could be caused by cancellation of head and eye movement sensitivity or dependence of neuronal firing on volitional SP commands. Our results support the suggestion that modulation of SP-related MSTd neurons reflects volitional SP commands rather then eye movements generated by reflex pathways.

[1]  A. Fuchs,et al.  Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smooth-pursuit eye movements and passive head rotation. , 1978, Journal of neurophysiology.

[2]  R. Wurtz,et al.  What the brain stem tells the frontal cortex. II. Role of the SC-MD-FEF pathway in corollary discharge. , 2004, Journal of neurophysiology.

[3]  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.

[4]  M. Mustari,et al.  Modeling of smooth pursuit-related neuronal responses in the DLPN and NRTP of the rhesus macaque. , 2005, Journal of neurophysiology.

[5]  S. Lisberger,et al.  Enhancement of multiple components of pursuit eye movement by microstimulation in the arcuate frontal pursuit area in monkeys. , 2002, Journal of neurophysiology.

[6]  A. Fuchs,et al.  Gaze-stabilizing deficits and latent nystagmus in monkeys with early-onset visual deprivation: role of the pretectal not. , 2001, Journal of neurophysiology.

[7]  M. Mustari,et al.  Information processing by parafoveal cells in the primate nucleus of the optic tract , 2001, Experimental Brain Research.

[8]  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.

[9]  K. Kawano,et al.  Response properties of neurons in posterior parietal cortex of monkey during visual-vestibular stimulation. I. Visual tracking neurons. , 1984, Journal of neurophysiology.

[10]  T. Sato,et al.  Activity of smooth pursuit-related neurons in the monkey periarcuate cortex during pursuit and passive whole-body rotation. , 2000, Journal of neurophysiology.

[11]  P. Thier,et al.  Visual tracking neurons in primate area MST are activated by smooth-pursuit eye movements of an "imaginary" target. , 2003, Journal of neurophysiology.

[12]  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.

[13]  A. Churchland,et al.  Relationship between extraretinal component of firing rate and eye speed in area MST of macaque monkeys. , 2005, Journal of neurophysiology.

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

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

[16]  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.

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

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

[19]  P. Thier,et al.  Posterior Parietal Cortex Neurons Encode Target Motion in World-Centered Coordinates , 2004, Neuron.

[20]  R. Tusa,et al.  Role of the Dorsolateral Pontine Nucleus in Visual‐Vestibular Behavior , 2003, Annals of the New York Academy of Sciences.

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

[22]  M. Tanaka,et al.  Neuronal responses related to smooth pursuit eye movements in the periarcuate cortical area of monkeys. , 1998, Journal of neurophysiology.

[23]  A. Fuchs,et al.  Response properties of pretectal omnidirectional pause neurons in the behaving primate. , 1997, Journal of neurophysiology.

[24]  H. Spitzer,et al.  Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. I. Response characteristics. , 1987, Journal of neurophysiology.

[25]  Vallabh E Das,et al.  Role of the dorsolateral pontine nucleus in short-term adaptation of the horizontal vestibuloocular reflex. , 2003, Journal of neurophysiology.

[26]  Kikuro Fukushima,et al.  Discharge characteristics of pursuit neurons in MST during vergence eye movements. , 2005, Journal of neurophysiology.

[27]  Vallabh E Das,et al.  Gaze-related response properties of DLPN and NRTP neurons in the rhesus macaque. , 2004, Journal of neurophysiology.

[28]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

[29]  R. McCrea,et al.  Role of the cerebellar flocculus region in cancellation of the VOR during passive whole body rotation. , 2000, Journal of neurophysiology.

[30]  Dora E Angelaki,et al.  Visual and Nonvisual Contributions to Three-Dimensional Heading Selectivity in the Medial Superior Temporal Area , 2006, The Journal of Neuroscience.