Saccades along spatial neural circuit discontinuities

Spatial Coordinates ◽

Discontinuity Problem

AbstractSaccades are realized by six extraocular muscles that define the final reference frame for eyeball rotations. However, upstream of the nuclei innervating the eye muscles, eye movement commands are represented in two-dimensional retinocentric coordinates, as is the case in the superior colliculus (SC). In such spatial coordinates, the horizontal and vertical visual field meridians, relative to the line of sight, are associated with neural tissue discontinuities due to routing of binocular retinal outputs when forming retinotopic sensory-motor maps. At the level of the SC, a functional discontinuity along the horizontal meridian was additionally discovered, beyond the structural vertical discontinuity associated with hemifield lateralization. How do such neural circuit discontinuities influence purely cardinal saccades? Using thousands of saccades from 3 rhesus macaque monkeys and 14 human subjects, we show how the likelihood of purely horizontal or vertical saccades is infinitesimally small, nulling a discontinuity problem. This does not mean that saccades are sloppy. On the contrary, saccades exhibit remarkable direction and amplitude corrections to account for small initial eye position deviations due to fixational variability: “purely” cardinal saccades can deviate, with an orthogonal component of as little as 0.03 deg, to correct for tiny target position deviations from initial eye position. In humans, probing perceptual target localization additionally revealed that saccades show different biases from perception when targets deviate slightly from purely cardinal directions. These results demonstrate a new functional role for fixational eye movements in visually-guided behavior, and they motivate further neurophysiological investigations of saccade trajectory control in the brainstem.New and NoteworthyPurely cardinal saccades are often characterized as being straight. We show how a small amount of curvature is inevitable, alleviating an implementational problem of dealing with neural circuit discontinuities in the representations of the visual meridians. The small curvature functionally corrects for minute variability in initial eye position due to fixational eye movements. Saccades are far from sloppy; they deviate by as little as <1% of the total vector size to adjust their landing position.

Abnormal fixational eye movements in strabismus

British Journal of Ophthalmology ◽

10.1136/bjophthalmol-2017-310346 ◽

2017 ◽

Vol 102 (2) ◽

pp. 253-259 ◽

Cited By ~ 8

Author(s):

Fatema F Ghasia ◽

Jorge Otero-Millan ◽

Aasef G Shaikh

Keyword(s):

Eye Movements ◽

Large Angle ◽

Fine Tuning ◽

Eye Position ◽

Visually Guided ◽

Binocular Fusion ◽

The Gaze ◽

The Stability ◽

Fixational Saccades

IntroductionFixational saccades are miniature eye movements that constantly change the gaze during attempted visual fixation. Visually guided saccades and fixational saccades represent an oculomotor continuum and are produced by common neural machinery. Patients with strabismus have disconjugate binocular horizontal saccades. We examined the stability and variability of eye position during fixation in patients with strabismus and correlated the severity of fixational instability with strabismus angle and binocular vision.MethodsEye movements were measured in 13 patients with strabismus and 16 controls during fixation and visually guided saccades under monocular viewing conditions. Fixational saccades and intersaccadic drifts were analysed in the viewing and non-viewing eye of patients with strabismus and controls.ResultsWe found an increase in fixational instability in patients with strabismus compared with controls. We also found an increase in the disconjugacy of fixational saccades and intrasaccadic ocular drift in patients with strabismus compared with controls. The disconjugacy was worse in patients with large-angle strabismus and absent stereopsis. There was an increase in eye position variance during drifts in patients with strabismus. Our findings suggest that both fixational saccades and intersaccadic drifts are abnormal and likely contribute to the fixational instability in patients with strabismus.DiscussionFixational instability could be a useful tool for mass screenings of children to diagnose strabismus in the absence of amblyopia and latent nystagmus. The increased disconjugacy of fixational eye movements and visually guided saccades in patients with strabismus reflects the disruption of the fine-tuning of the motor and visual systems responsible for achieving binocular fusion in these patients.

Eye Position Compensation Improves Estimates of Response Magnitude and Receptive Field Geometry in Alert Monkeys

10.1152/jn.00881.2006 ◽

2007 ◽

Vol 97 (5) ◽

pp. 3439-3448 ◽

Cited By ~ 12

Author(s):

Yamei Tang ◽

Alan Saul ◽

Moshe Gur ◽

Stephanie Goei ◽

Elsie Wong ◽

...

Keyword(s):

Eye Movements ◽

Receptive Field ◽

Receptive Fields ◽

Eye Position ◽

Stimulus Position ◽

Field Geometry ◽

Receptive Field Subregions ◽

Movement Compensation ◽

Definition Of

Studies of visual function in behaving subjects require that stimuli be positioned reliably on the retina in the presence of eye movements. Fixational eye movements scatter stimuli about the retina, inflating estimates of receptive field dimensions, reducing estimates of peak responses, and blurring maps of receptive field subregions. Scleral search coils are frequently used to measure eye position, but their utility for correcting the effects of fixational eye movements on receptive field maps has been questioned. Using eye coils sutured to the sclera and preamplifiers configured to minimize cable artifacts, we reexamined this issue in two rhesus monkeys. During repeated fixation trials, the eye position signal was used to adjust the stimulus position, compensating for eye movements and correcting the stimulus position to place it at the desired location on the retina. Estimates of response magnitudes and receptive field characteristics in V1 and in LGN were obtained in both compensated and uncompensated conditions. Receptive fields were narrower, with steeper borders, and response amplitudes were higher when eye movement compensation was used. In sum, compensating for eye movements facilitated more precise definition of the receptive field. We also monitored horizontal vergence over long sequences of fixation trials and found the variability to be low, as expected for this precise behavior. Our results imply that eye coil signals can be highly accurate and useful for optimizing visual physiology when rigorous precautions are observed.

Local Feedback Signals Are Not Distorted By Prior Eye Movements: Evidence From Visually Evoked Double Saccades

10.1152/jn.1997.78.1.533 ◽

1997 ◽

Vol 78 (1) ◽

pp. 533-538 ◽

Cited By ~ 31

Author(s):

H.H.L.M. Goossens ◽

A. J. Van Opstal

Keyword(s):

Eye Movements ◽

Feedback Control ◽

Time Constant ◽

Feedback Loop ◽

Eye Position ◽

Visually Guided ◽

Double Step ◽

Local Feedback ◽

Reset Time ◽

Saccadic Responses

Goossens, H.H.L.M. and A. J. Van Opstal. Local feedback signals are not distorted by prior eye movements: evidence from visually evoked double saccades. J. Neurophysiol. 78: 533–538, 1997. Recent experiments have shown that the amplitude and direction of saccades evoked by microstimulation of the monkey superior colliculus depend systematically on the amplitude and direction of preceding visually guided saccades as well as on the postsaccade stimulation interval. The data are consistent with the hypothesis that an eye displacement integrator in the local feedback loop of the saccadic burst generator is gradually reset with a time constant of ∼45 ms. If this is true, similar effects should occur during naturally evoked saccade sequences, causing systematic interval-dependent errors. To test this prediction in humans, saccades toward visual single- and double-step stimuli were elicited, and the properties of the second saccades were investigated as a function of the intersaccadic interval (ISI). In 15–20% of the saccadic responses, ISIs fell well below 100 ms. The errors of the second saccades were not systematically affected by the preceding primary saccade, irrespective of the ISI. Only a slight increase in the endpoint variability of second saccades was observed for the shortest ISIs. These results are at odds with the hypothesis that the putative eye displacement integrator has a reset time constant >10 ms. Instead, it is concluded that the signals involved in the internal feedback control of the saccadic burst generator reflect eye position and/or eye displacement accurately, irrespective of preceding eye movements.

Primate Translational Vestibuloocular Reflexes. I. High-Frequency Dynamics and Three-Dimensional Properties During Lateral Motion

10.1152/jn.2000.83.3.1637 ◽

2000 ◽

Vol 83 (3) ◽

pp. 1637-1647 ◽

Cited By ~ 39

Author(s):

Dora E. Angelaki ◽

M. Quinn McHenry ◽

Bernhard J. M. Hess

Keyword(s):

Eye Movements ◽

High Frequency ◽

Three Dimensional ◽

Eye Position ◽

Lateral Motion ◽

Visually Guided ◽

Torsional Response ◽

Target Eccentricity ◽

Eye Velocity ◽

Tilt Response

The dynamics and three-dimensional (3-D) properties of the primate translational vestibuloocular reflex (trVOR) for high-frequency (4–12 Hz, ±0.3–0.4 g) lateral motion were investigated during near-target viewing at center and eccentric targets. Horizontal response gains increased with frequency and depended on target eccentricity. The larger the horizontal and vertical target eccentricity, the steeper the dependence of horizontal response gain on frequency. In addition to horizontal eye movements, robust torsional response components also were present at all frequencies. During center-target fixation, torsional response phase was opposite (anticompensatory) to that expected for an “apparent” tilt response. Instead torsional response components depended systematically on vertical-target eccentricity, increasing in amplitude when looking down and reversing phase when looking up. As a result the trVOR eye velocity vector systematically tilted away from a purely horizontal direction, through an angle that increased with vertical eccentricity with a slope of ∼0.7. This systematic dependence of torsional eye velocity tilt on vertical eye position suggests that the trVOR might follow the 3-D kinematic requirements that have been shown to govern visually guided eye movements and near-target fixation.

Effects of eye position on electrically evoked saccades: a theoretical note

Visual Neuroscience ◽

10.1017/s0952523800001498 ◽

1988 ◽

Vol 1 (2) ◽

pp. 239-244 ◽

Cited By ~ 8

Author(s):

James T. McIlwain

Keyword(s):

Eye Movements ◽

Internal Representation ◽

Target Position ◽

Saccadic Eye Movements ◽

Brain Structures ◽

Initial Position ◽

Eye Position ◽

Saccadic System ◽

Early Processing ◽

The Difference

AbstractThe trajectories of saccadic eye movements evoked electrically from many brain structures are dependent to some degree on the initial position of the eye. Under certain conditions, likely to occur in stimulation experiments, local feedback models of the saccadic system can yield eye movements which behave in this way. The models in question assume that an early processing stage adds an internal representation of eye position to retinal error to yield a signal representing target position with respect to the head. The saccadic system is driven by the difference between this signal and one representing the current position of the eye. Albano & Wurtz (1982) pointed out that lesions perturbing the computation of eye position with respect to the head can result in initial position dependence of visually evoked saccades. It is shown here that position-dependent saccades will also result if electrical stimulation evokes a signal equivalent to retinal error but fails to effect a complete addition of eye position to this signal. Also, when multiple or staircase saccades are produced, as during long stimulus trains, they will have identical directions but decrease progressively in amplitude by a factor related to the fraction of added eye position.

Memory-guided microsaccades

10.1101/539205 ◽

2019 ◽

Author(s):

Konstantin-Friedrich Willeke ◽

Xiaoguang Tian ◽

Antimo Buonocore ◽

Joachim Bellet ◽

Araceli Ramirez-Cardenas ◽

...

Keyword(s):

Eye Movements ◽

Superior Colliculus ◽

Human Subjects ◽

Visual Performance ◽

Visually Guided ◽

Related Activity ◽

Visual Guidance ◽

On Demand ◽

Visually Guided Movements ◽

Superior Colliculus Neurons

AbstractMicrosaccades are overwhelmingly described as involuntary eye movements. Here we show in both human subjects and monkeys that individual microsaccades of any direction can easily be triggered: (1) “on demand”, based on an arbitrary instruction, (2) without any special training, (3) without visual guidance by a stimulus, and (4) in a spatially and temporally accurate manner. Subjects voluntarily generated instructed “memory-guided” microsaccades readily, and similarly to how they made normal visually-guided ones. In two monkeys, we also observed midbrain superior colliculus neurons that exhibited movement-related activity bursts exclusively for memory-guided microsaccades, but not for similarly-sized visually-guided movements. Our results demonstrate behavioral and neural evidence for voluntary control over individual microsaccades, supporting recently discovered functional contributions of individual microsaccade generation to visual performance alterations and covert visual selection.

Mice Make Targeted Saccades

10.1101/2021.02.10.430669 ◽

2021 ◽

Author(s):

Sebastian H. Zahler ◽

David E. Taylor ◽

Julia M. Adams ◽

Evan H. Feinberg

Keyword(s):

Eye Movements ◽

Visual Field ◽

Visual System ◽

Neural Circuit ◽

Saccadic Eye Movements ◽

Eye Position ◽

Innate Behavior ◽

High Acuity ◽

Early Origin ◽

Innate Ability

AbstractHumans read text, recognize faces, and process emotions using targeted saccadic eye movements. In the textbook model, this innate ability to make targeted saccades evolved in species with foveae or similar high-acuity retinal specializations that enable scrutiny of salient stimuli. According to the model, saccades made by species without retinal specializations (such as mice) are never targeted and serve only to reset the eyes after gaze-stabilizing movements. Here we show that mice innately make touch-evoked targeted saccades. Optogenetic manipulations revealed the neural circuit mechanisms underlying targeted saccades are conserved. Saccade probability is a U-shaped function of current eye position relative to the target, mirroring the simulated relationship between an object’s location within the visual field and the probability its next movement carries it out of view. Thus, a cardinal sophistication of our visual system may have had an unexpectedly early origin as an innate behavior that keeps stimuli in view.

Measuring V1 Receptive Fields Despite Eye Movements in Awake Monkeys

10.1152/jn.01068.2002 ◽

2003 ◽

Vol 90 (2) ◽

pp. 946-960 ◽

Cited By ~ 13

Author(s):

Jenny C. A. Read ◽

Bruce G. Cumming

Keyword(s):

Eye Movements ◽

Receptive Field ◽

Time Course ◽

Receptive Fields ◽

Field Measurements ◽

Field Structure ◽

Eye Position ◽

Stimulus Position ◽

The Difference

One difficulty with measuring receptive fields in the awake monkey is that even well-trained animals make small eye movements during fixation. These complicate the measurement of receptive fields by blurring out the region where a response is observed, causing underestimates of the ability of individual neurons to signal changes in stimulus position. In simple cells, this blurring may severely disrupt estimates of receptive field structure. An accurate measurement of eye movements would allow correction of this blurring. Scleral search coils have been used to provide such measurements, although little is known about their accuracy. We have devised a range of approaches to address this issue: implanting two coils into a single eye, exploiting the small size of V1 receptive fields and developing maximum-likelihood fitting techniques to extract receptive field parameters in the presence of eye movements. All our investigations lead to the same conclusion: our scleral search coils (which were not sutured to the globe) are subject to an error of approximately the same magnitude as the small eye movements which occur during fixation: SD ∼ 0.1°. This error is large enough to explain the SD of measured vergence in the absence of any real changes in vergence state. This, and a variety of other arguments, indicate that the real variation in vergence is much smaller than coil measurements suggest. These results suggest that monkeys, like humans, maintain very stable vergence. The error has a slower time course than fixational eye movements so that search coils report the difference in eye position between two consecutive trials more accurately than the eye position itself on either trial. Receptive field estimates are unlikely to be improved by assuming the coil record is veridical and correcting for eye position accordingly. However, receptive field parameters can reliably be determined by a fitting technique that allows for eye movements. It is possible that suturing coils to the globe reduces the artifacts, but no method has been available to demonstrate this. These receptive field measurements provide a general means by which the reliability of eye-position measurements can be assessed.

Neuronal control of fixation and fixational eye movements

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2016.0205 ◽

2017 ◽

Vol 372 (1718) ◽

pp. 20160205 ◽

Cited By ~ 59

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 ◽

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’.

Human smooth pursuit: stimulus-dependent responses

10.1152/jn.1987.57.5.1446 ◽

1987 ◽

Vol 57 (5) ◽

pp. 1446-1463 ◽

Cited By ~ 216

Author(s):

J. R. Carl ◽

R. S. Gellman

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Retinal Image ◽

Human Subjects ◽

Target Position ◽

Stimulus Presentation ◽

Target Motion ◽

Target Velocity ◽

Target Movement ◽

Lower Velocity

We studied pursuit eye movements in seven normal human subjects with the scleral search-coil technique. The initial eye movements in response to unpredictable changes in target motion were analyzed to determine the effect of target velocity and position on the latency and acceleration of the response. By restricting our analysis to the presaccadic portion of the response we were able to eliminate any saccadic interactions, and the randomized stimulus presentation minimized anticipatory responses. This approach has allowed us to characterize a part of the smooth-pursuit system that is dependent primarily on retinal image properties. The latency of the smooth-pursuit response was very consistent, with a mean of 100 +/- 5 ms to targets moving 5 degrees/s or faster. The responses were the same whether the velocity step was presented when the target was initially stationary or after tracking was established. The latency did increase for lower velocity targets; this increase was well described by a latency model requiring a minimum target movement of 0.028 degrees, in addition to a fixed processing time of 98 ms. The presaccadic accelerations were fairly low, and increased with target velocity until an acceleration of about 50 degrees/s2 was reached for target velocities of 10 degrees/s. Higher velocities produced only a slight increase in eye acceleration. When the target motion was adjusted so that the retinal image slip occurred at increasing distances from the fovea, the accelerations declined until no presaccadic response was measurable when the image slip started 15 degrees from the fovea. The smooth-pursuit response to a step of target position was a brief acceleration; this response occurred even when an oppositely directed velocity stimulus was present. The latency of the pursuit response to such a step was also approximately 100 ms. This result seems consistent with the idea that sensory pathways act as a low-pass spatiotemporal filter of the retinal input, effectively converting position steps into briefly moving stimuli. There was a large asymmetry in the responses to position steps: the accelerations were much greater when the position step of the target was away from the direction of tracking, compared with steps in the direction of tracking. The asymmetry may be due to the addition of a fixed slowing of the eyes whenever the target image disappears from the foveal region. When saccades were delayed by step-ramp stimuli, eye accelerations increased markedly approximately 200 ms after stimulus onset.(ABSTRACT TRUNCATED AT 400 WORDS)