scholarly journals Neuronal control of fixation and fixational eye movements

2017 ◽  
Vol 372 (1718) ◽  
pp. 20160205 ◽  
Author(s):  
Richard J. Krauzlis ◽  
Laurent Goffart ◽  
Ziad M. Hafed
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Brain Structures ◽  
Eye Position ◽  
Smooth Pursuit Eye Movements ◽  
Ocular Fixation ◽  
Pursuit Eye Movements ◽  
Fixational Eye Movements ◽  
Neuronal Control ◽  
Neuronal Mechanisms

Ocular fixation is a dynamic process that is actively controlled by many of the same brain structures involved in the control of eye movements, including the superior colliculus, cerebellum and reticular formation. In this article, we review several aspects of this active control. First, the decision to move the eyes not only depends on target-related signals from the peripheral visual field, but also on signals from the currently fixated target at the fovea, and involves mechanisms that are shared between saccades and smooth pursuit. Second, eye position during fixation is actively controlled and depends on bilateral activity in the superior colliculi and medio-posterior cerebellum; disruption of activity in these circuits causes systematic deviations in eye position during both fixation and smooth pursuit eye movements. Third, the eyes are not completely still during fixation but make continuous miniature movements, including ocular drift and microsaccades, which are controlled by the same neuronal mechanisms that generate larger saccades. Finally, fixational eye movements have large effects on visual perception. Ocular drift transforms the visual input in ways that increase spatial acuity; microsaccades not only improve vision by relocating the fovea but also cause momentary changes in vision analogous to those caused by larger saccades. This article is part of the themed issue ‘Movement suppression: brain mechanisms for stopping and stillness’.

Neuronal Responses Related to Smooth Pursuit Eye Movements in the Periarcuate Cortical Area of Monkeys

1998 ◽  
Vol 80 (1) ◽  
pp. 28-47 ◽  
Author(s):  
Masaki Tanaka ◽  
Kikuro Fukushima
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Cortical Area ◽  
Eye Position ◽  
Smooth Pursuit Eye Movements ◽  
Neuronal Responses ◽  
Stationary Target ◽  
Pursuit Eye Movements ◽  
Preferred Direction ◽  
Eye Velocity

Tanaka, Masaki and Kikuro Fukushima. Neuronal responses related to smooth pursuit eye movements in the periarcuate cortical area of monkeys. J. Neurophysiol. 80: 28–47, 1998. To examine how the periarcuate area is involved in the control of smooth pursuit eye movements, we recorded 177 single neurons while monkeys pursued a moving target in the dark. The majority (52%, 92/177) of task-related neurons responded to pursuit but had little or no response to saccades. Histological reconstructions showed that these neurons were located mainly in the posterior bank of the arcuate sulcus near the sulcal spur. Twenty-seven percent (48/177) changed their activity at the onset of saccades. Of these, 36 (75%) showed presaccadic burst activity with strong preference for contraversive saccades. Eighteen (10%, 18/177) were classified as eye-position–related neurons, and 11% (19/177) were related to other aspects of the stimuli or response. Among the 92 neurons that responded to pursuit, 85 (92%) were strongly directional with uniformly distributed preferred directions. Further analyses were performed in these directionally sensitive pursuit-related neurons. For 59 neurons that showed distinct changes in activity around the initiation of pursuit, the median latency from target motion was 96 ms and that preceding pursuit was −12 ms, indicating that these neuron can influence the initiation of pursuit. We tested some neurons by briefly extinguishing the tracking target ( n = 39) or controlling its movement with the eye position signal ( n = 24). The distribution of the change in pursuit-related activity was similar to previous data for the dorsomedial part of the medial superior temporal neurons ( Newsome et al. 1988) , indicating that pursuit-related neurons in the periarcuate area also carry extraretinal signals. For 22 neurons, we examined the responses when the animals reversed pursuit direction to distinguish the effects of eye acceleration in the preferred direction from oppositely directed eye velocity. Almost all neurons discharged before eye velocity reached zero, however, only nine neurons discharged before the eyes were accelerated in the preferred direction. The delay in neuronal responses relative to the onset of eye acceleration in these trials might be caused by suppression from oppositely directed pursuit velocity. The results suggest that the periarcuate neurons do not participate in the earliest stage of eye acceleration during the change in pursuit direction, although most of them may participate in the early stages of pursuit initiation in the ordinary step-ramp pursuit trials. Some neurons changed their activity when the animals fixated a stationary target, and this activity could be distinguished easily from the strong pursuit-related responses. Our results suggest that the periarcuate pursuit area carries extraretinal signals and affects the premotor circuitry for smooth pursuit.

Smooth pursuitlike eye movements evoked by microstimulation in macaque nucleus reticularis tegmenti pontis

1996 ◽  
Vol 76 (5) ◽  
pp. 3313-3324 ◽  
Author(s):  
T. Yamada ◽  
D. A. Suzuki ◽  
R. D. Yee
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Current Intensity ◽  
Image Motion ◽  
Eye Position ◽  
Smooth Pursuit Eye Movements ◽  
Pontine Nucleus ◽  
Nucleus Reticularis Tegmenti Pontis ◽  
Pursuit Eye Movements ◽  
Nucleus Reticularis

1. Smooth pursuitlike eye movements were evoked with low current microstimulation delivered to rostral portions of the nucleus reticularis tegmenti pontis (rNRTP) in alert macaques. Microstimulation sites were selected by the observation of modulations in single-cell firing rates that were correlated with periodic smoothpursuit eye movements. Current intensities ranged from 10 to 120 microA and were routinely < 40 microA. Microstimulation was delivered either in the dark with no fixation, 100 ms after a fixation target was extinguished, or during maintained fixation of a stationary or moving target. Evoked eye movements also were studied under open-loop conditions with the target image stabilized on the retina. 2. Eye movements evoked in the absence of a target rapidly accelerated to a constant velocity that was maintained for the duration of the microstimulation. Evoked eye speeds ranged from 3.7 to 23 deg/s and averaged 11 deg/s. Evoked eye speed appeared to be linearly related to initial eye position with a sensitivity to initial eye position that averaged 0.23 deg.s-1.deg-1. While some horizontal and oblique smooth eye movements were elicited, microstimulation resulted in upward eye movements in 89% of the sites. 3. Evoked eye speed was found to be dependent on microstimulation pulse frequency and current intensity. Within limits, evoked eye speed increased with increases in stimulation frequency or current intensity. For stimulation frequencies < 300–400 Hz, only smooth pursuit-like eye movements were evoked. At higher stimulation frequencies, accompanying saccades consistently were elicited. 4. Feedback of retinal image motion interacted with the evoked eye movements to decrease eye speed if the visual motion was in the opposite direction as the evoked, pursuit-like eye movements. 5. The results implicate rNRTP as part of the neuronal substrate that controls smooth-pursuit eye movements. NRTP appears to be divided functionally into a rostral, pursuit-related portion and a caudal, saccade-related area. rNRTP is a component of a corticopontocerebellar circuit that presumably involves the pursuit area of the frontal eye field and that parallels the middle and medial superior temporal cerebral cortical/dorsalateral pontine nucleus (MT/MST-DLPN-cerebellum) pathway known to be involved also with regulating smooth-pursuit eye movements.

Similar Kinematic Properties for Ocular Following and Smooth Pursuit Eye Movements

2005 ◽  
Vol 93 (3) ◽  
pp. 1710-1717 ◽  
Author(s):  
Babatunde Adeyemo ◽  
Dora E. Angelaki
Keyword(s):  
Steady State ◽  
Eye Movements ◽  
Smooth Pursuit ◽  
Eye Position ◽  
Vestibuloocular Reflex ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements ◽  
Initial Fixation ◽  
Ocular Following ◽  
Kinematic Properties

Ocular following (OFR) is a short-latency visual stabilization response to the optic flow experienced during self-motion. It has been proposed that it represents the early component of optokinetic nystagmus (OKN) and that it is functionally linked to the vestibularly driven stabilization reflex during translation (translational vestibuloocular reflex, TVOR). Because no single eye movement can eliminate slip from the whole retina during translation, the OFR and the TVOR appear to be functionally related to maintaining visual acuity on the fovea. Other foveal-specific eye movements, like smooth pursuit and saccades, exhibit an eye-position-dependent torsional component, as dictated by what is known as the “half-angle rule” of Listing's law. In contrast, eye movements that stabilize images on the whole retina, such as the rotational vestibuloocular reflex (RVOR) and steady-state OKN do not. Consistent with the foveal stabilization hypothesis, it was recently shown that the TVOR is indeed characterized by an eye-position-dependent torsion, similar to pursuit eye movements. Here we have investigated whether the OFR exhibits three-dimensional kinematic properties consistent with a foveal response (i.e., similar to the TVOR and smooth pursuit eye movements) or with a whole-field stabilization function (similar to steady-state OKN). The OFR was elicited using 100-ms ramp motion of a full-field random dot pattern that moved horizontally at 20, 62, or 83°/s. To study if an eye-position-dependent torsion is generated during the OFR, we varied the initial fixation position vertically within a range of ±20°. As a control, horizontal smooth pursuit eye movements were also elicited using step-ramp target motion (10, 20, or 30°/s) at similar eccentric positions. We found that the OFR followed kinematic properties similar to those seen in pursuit and the TVOR with the eye-position-dependent torsional tilt of eye velocity having slopes that averaged 0.73 ± 0.16 for OFR and 0.57 ± 0.12 (means ± SD) for pursuit. These findings support the notion that the OFR, like the TVOR and pursuit, are foveal image stabilization systems.

Visuomotor Velocity Transformations for Smooth Pursuit Eye Movements

2010 ◽  
Vol 104 (4) ◽  
pp. 2103-2115 ◽  
Author(s):  
Gunnar Blohm ◽  
Philippe Lefèvre
Keyword(s):  
Eye Movements ◽  
Reference Frame ◽  
Smooth Pursuit ◽  
Eye Position ◽  
Smooth Pursuit Eye Movements ◽  
Velocity Transformation ◽  
Pursuit Eye Movements ◽  
Pursuit Initiation ◽  
Retinal Motion ◽  
Frame Transformation

Smooth pursuit eye movements are driven by retinal motion signals. These retinal motion signals are converted into motor commands that obey Listing's law (i.e., no accumulation of ocular torsion). The fact that smooth pursuit follows Listing's law is often taken as evidence that no explicit reference frame transformation between the retinal velocity input and the head-centered motor command is required. Such eye-position-dependent reference frame transformations between eye- and head-centered coordinates have been well-described for saccades to static targets. Here we suggest that such an eye (and head)-position-dependent reference frame transformation is also required for target motion (i.e., velocity) driving smooth pursuit eye movements. Therefore we tested smooth pursuit initiation under different three-dimensional eye positions and compared human performance to model simulations. We specifically tested if the ocular rotation axis changed with vertical eye position, if the misalignment of the spatial and retinal axes during oblique fixations was taken into account, and if ocular torsion (due to head roll) was compensated for. If no eye-position-dependent velocity transformation was used, the pursuit initiation should follow the retinal direction, independently of eye position; in contrast, a correct visuomotor velocity transformation would result in spatially correct pursuit initiation. Overall subjects accounted for all three components of the visuomotor velocity transformation, but we did observe differences in the compensatory gains between individual subjects. We concluded that the brain does perform a visuomotor velocity transformation but that this transformation was prone to noise and inaccuracies of the internal model.

Different extraretinal neuronal mechanisms of smooth pursuit eye movements in schizophrenia: An fMRI study

NeuroImage ◽  
2007 ◽  
Vol 34 (1) ◽  
pp. 300-309 ◽  
Author(s):  
Matthias Nagel ◽  
Andreas Sprenger ◽  
Matthias Nitschke ◽  
Silke Zapf ◽  
Wolfgang Heide ◽  
...  
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements ◽  
Fmri Study ◽  
Neuronal Mechanisms

Firing behavior of brain stem neurons during voluntary cancellation of the horizontal vestibuloocular reflex. II. Eye movement related neurons

1993 ◽  
Vol 70 (2) ◽  
pp. 844-856 ◽  
Author(s):  
K. E. Cullen ◽  
C. Chen-Huang ◽  
R. A. McCrea
Keyword(s):  
Eye Movements ◽  
Firing Rate ◽  
Smooth Pursuit ◽  
Vestibular Nucleus ◽  
Medial Vestibular Nucleus ◽  
Eye Position ◽  
Smooth Pursuit Eye Movements ◽  
Stationary Target ◽  
Pursuit Eye Movements ◽  
Eye Velocity

1. The single-unit activity of neurons in the vestibular nucleus, the prepositus nucleus, and the abducens nucleus, whose activity was primarily related to horizontal eye movements, was recorded in alert squirrel monkeys that were trained to track a small visual target by generating smooth pursuit eye movements and to cancel their horizontal vestibuloocular reflex (VOR) by fixating a head stationary target. 2. The spiking behavior of each cell was recorded during 1) spontaneous eye movements, 2) horizontal smooth pursuit of a target that was moved sinusoidally +/- 20 degrees/s at 0.5 Hz, 3) horizontal VOR evoked by 0.5-Hz sinusoidal turntable rotations +/- 40 degrees/s (VORs), and 4) voluntary cancellation of the VOR by fixation of a head-stationary target during 0.5-Hz sinusoidal turntable rotation at +/- 40 degrees/s (VORCs). The responses of most (28/42) of the units were recorded during unpredictable 100-ms steps in head acceleration (400 degrees/s2) that were generated while the monkey was fixating a target light. The acceleration steps were generated either when the monkey was stationary or when the turntable was already rotating (VORt trials), and the monkey was canceling its VOR (VORCt trials). 3. The firing behavior of all 12 of the abducens neurons recorded was closely related to horizontal eye position and eye velocity during all of the behavioral paradigms used, although there was a small but significant increase in the eye position sensitivity of many of these units when the eye was moving (smooth pursuit) versus when the eye was stationary (fixation). 4. Many neurons in the prepositus nucleus and the medial vestibular nucleus (n = 15) were similar to abducens neurons, in that their firing rate was related primarily to horizontal eye position and eye velocity, regardless of the behavioral paradigm used. These cells were, on average, more sensitive to eye position and smooth pursuit eye velocity than were abducens neurons. 5. The firing rate of 15 other neurons in the prepositus and medial vestibular nucleus was related primarily to horizontal smooth pursuit eye movements. The tonic firing rate of all of these smooth pursuit (SP) cells was related to horizontal eye position, and the majority generated bursts of spikes during saccades in all directions but their off direction. Six of the SP neurons fired in phase with ipsilateral eye movements, whereas the remaining nine were sensitive to eye movements in the opposite direction.(ABSTRACT TRUNCATED AT 400 WORDS)

Smooth-Pursuit Eye-Movement-Related Neuronal Activity in Macaque Nucleus Reticularis Tegmenti Pontis

2003 ◽  
Vol 89 (4) ◽  
pp. 2146-2158 ◽  
Author(s):  
David A. Suzuki ◽  
Tetsuto Yamada ◽  
Robert D. Yee
Keyword(s):  
Eye Movements ◽  
Smooth Pursuit ◽  
Response Amplitude ◽  
Eye Position ◽  
Smooth Pursuit Eye Movements ◽  
Average Sensitivity ◽  
Nucleus Reticularis Tegmenti Pontis ◽  
Pursuit Eye Movements ◽  
Nucleus Reticularis ◽  
Eye Velocity

Neuronal responses that were observed during smooth-pursuit eye movements were recorded from cells in rostral portions of the nucleus reticularis tegmenti pontis (rNRTP). The responses were categorized as smooth-pursuit eye velocity (78%) or eye acceleration (22%). A separate population of rNRTP cells encoded static eye position. The sensitivity to pursuit eye velocity averaged 0.81 spikes/s per °/s, whereas the average sensitivity to pursuit eye acceleration was 0.20 spikes/s per °/s2. Of the eye-velocity cells with horizontal preferences for pursuit responses, 56% were optimally responsive to contraversive smooth-pursuit eye movements and 44% preferred ipsiversive pursuit. For cells with vertical pursuit preferences, 61% preferred upward pursuit and 39% preferred downward pursuit. The direction selectivity was broad with 50% of the maximal response amplitude observed for directions of smooth pursuit up to ±85° away from the optimal direction. The activities of some rNRTP cells were linearly related to eye position with an average sensitivity of 2.1 spikes/s per deg. In some cells, the magnitude of the response during smooth-pursuit eye movements was affected by the position of the eyes even though these cells did not encode eye position. On average, pursuit centered to one side of screen center elicited a response that was 73% of the response amplitude obtained with tracking centered at screen center. For pursuit centered on the opposite side, the average response was 127% of the response obtained at screen center. The results provide a neuronal rationale for the slow, pursuit-like eye movements evoked with rNRTP microstimulation and for the deficits in smooth-pursuit eye movements observed with ibotenic acid injection into rNRTP. More globally, the results support the notion of a frontal and supplementary eye field-rNRTP-cerebellum pathway involved with controlling smooth-pursuit eye movements.

Visual Tracking Neurons in Primate Area MST Are Activated by Smooth-Pursuit Eye Movements of an “Imaginary” Target

2003 ◽  
Vol 90 (3) ◽  
pp. 1489-1502 ◽  
Author(s):  
Uwe J. Ilg ◽  
Peter Thier
Keyword(s):  
Eye Movements ◽  
Visual Field ◽  
Eye Movement ◽  
Visual Tracking ◽  
Smooth Pursuit ◽  
Rhesus Monkeys ◽  
Image Motion ◽  
Eye Position ◽  
Smooth Pursuit Eye Movements ◽  
Pursuit Eye Movements

Because smooth-pursuit eye movements (SPEM) can be executed only in the presence of a moving target, it has been difficult to attribute the neuronal activity observed during the execution of these eye movements to either sensory processing or to motor preparation or execution. Previously, we showed that rhesus monkeys can be trained to perform SPEM directed toward an “imaginary” target defined by visual cues confined to the periphery of the visual field. The pursuit of an “imaginary” target provides the opportunity to elicit SPEM without stimulating visual receptive fields confined to the center of the visual field. Here, we report that a subset of neurons [85 “ imaginary” visual tracking (iVT)-neurons] in area MST of 3 rhesus monkeys were identically activated during pursuit of a conventional, foveal dot target and the “imaginary” target. Because iVT-neurons did not respond to the presentation of a moving “imaginary” target during fixation of a stationary dot, we are able to exclude that responses to pursuit of the “imaginary” target were artifacts of stimulation of the visual field periphery. Neurons recorded from the representation of the central parts of the visual field in neighboring area MT, usually vigorously discharging during pursuit of foveal targets, in no case responded to pursuit of the “imaginary” target. This dissociation between MT and MST neurons supports the view that pursuit responses of MT neurons are the result of target image motion, whereas those of iVT-neurons in area MST reflect an eye movement–related signal that is nonretinal in origin. iVT-neurons fell into two groups, depending on the properties of the eye movement–related signal. Whereas most of them (71%) encoded eye velocity, a minority showed responses determined by eye position, irrespective of whether eye position was changed by smooth pursuit or by saccades. Only the former group exhibited responses that led the eye movement, which is a prerequisite for a causal role in the generation of SPEM.

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