scholarly journals Voluntary Control of Multisaccade Gaze Shifts During Movement Preparation and Execution

2010 ◽  
Vol 103 (5) ◽  
pp. 2400-2416 ◽  
Author(s):  
Arjun Ramakrishnan ◽  
Snehal Chokhandre ◽  
Aditya Murthy
Keyword(s):  
Race Model ◽  
Oculomotor System ◽  
Gaze Control ◽  
Inhibitory Process ◽  
Gaze Shifts ◽  
Motor Error ◽  
Average Latency ◽  
Corrective Response ◽  
Different Levels ◽  
Initial Target

Although the nature of gaze control regulating single saccades is relatively well documented, how such control is implemented to regulate multisaccade gaze shifts is not known. We used highly eccentric targets to elicit multisaccade gaze shifts and tested the ability of subjects to control the saccade sequence by presenting a second target on random trials. Their response allowed us to test the nature of control at many levels: before, during, and between saccades. Although the saccade sequence could be inhibited before it began, we observed clear signs of truncation of the first saccade, which confirmed that it could be inhibited in midflight as well. Using a race model that explains the control of single saccades, we estimated that it took about 100 ms to inhibit a planned saccade but took about 150 ms to inhibit a saccade during its execution. Although the time taken to inhibit was different, the high subject-wise correlation suggests a unitary inhibitory control acting at different levels in the oculomotor system. We also frequently observed responses that consisted of hypometric initial saccades, followed by secondary saccades to the initial target. Given the estimates of the inhibitory process provided by the model that also took into account the variances of the processes as well, the secondary saccades (average latency ∼215 ms) should have been inhibited. Failure to inhibit the secondary saccade suggests that the intersaccadic interval in a multisaccade response is a ballistic stage. Collectively, these data indicate that the oculomotor system can control a response until a very late stage in its execution. However, if the response consists of multiple movements then the preparation of the second movement becomes refractory to new visual input, either because it is part of a preprogrammed sequence or as a consequence of being a corrective response to a motor error.

Visual-Vestibular Interaction Hypothesis for the Control of Orienting Gaze Shifts by Brain Stem Omnipause Neurons

2007 ◽  
Vol 97 (2) ◽  
pp. 1149-1162 ◽  
Author(s):  
Mario Prsa ◽  
Henrietta L. Galiana
Keyword(s):  
Brain Stem ◽  
Head Movements ◽  
Gaze Control ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Switching Mechanism ◽  
Interaction Hypothesis ◽  
Visual Vestibular Interaction ◽  
Motor Error ◽  
Gaze Position

Models of combined eye-head gaze shifts all aim to realistically simulate behaviorally observed movement dynamics. One of the most problematic features of such models is their inability to determine when a saccadic gaze shift should be initiated and when it should be ended. This is commonly referred to as the switching mechanism mediated by omni-directional pause neurons (OPNs) in the brain stem. Proposed switching strategies implemented in existing gaze control models all rely on a sensory error between instantaneous gaze position and the spatial target. Accordingly, gaze saccades are initiated after presentation of an eccentric visual target and subsequently terminated when an internal estimate of gaze position becomes nearly equal to that of the target. Based on behavioral observations, we demonstrate that such a switching mechanism is insufficient and is unable to explain certain types of movements. We propose an improved hypothesis for how the OPNs control gaze shifts based on a visual-vestibular interaction of signals known to be carried on anatomical projections to the OPN area. The approach is justified by the analysis of recorded gaze shifts interrupted by a head brake in animal subjects and is demonstrated by implementing the switching mechanism in an anatomically based gaze control model. Simulated performance reveals that a weighted sum of three signals: gaze motor error, head velocity, and eye velocity, hypothesized as inputs to OPNs, successfully reproduces diverse behaviorally observed eye-head movements that no other existing model can account for.

Brain Stem Omnipause Neurons and the Control of CombinedEye-Head Gaze Saccades in the Alert Cat

1998 ◽  
Vol 79 (6) ◽  
pp. 3060-3076 ◽  
Author(s):  
Martin Paré ◽  
Daniel Guitton
Keyword(s):  
Gaze Control ◽  
Error Signal ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Alert Cat ◽  
Motor Error ◽  
Omnipause Neurons ◽  
Gaze Saccades ◽  
Stimulation Of

Paré, Martin and Daniel Guitton. Brain stem omnipause neurons and the control of combined eye-head gaze saccades in the alert cat. J. Neurophysiol. 79: 3060–3076, 1998. When the head is unrestrained, rapid displacements of the visual axis—gaze shifts (eye-re-space)—are made by coordinated movements of the eyes (eye-re-head) and head (head-re-space). To address the problem of the neural control of gaze shifts, we studied and contrasted the discharges of omnipause neurons (OPNs) during a variety of combined eye-head gaze shifts and head-fixed eye saccades executed by alert cats. OPNs discharged tonically during intersaccadic intervals and at a reduced level during slow perisaccadic gaze movements sometimes accompanying saccades. Their activity ceased for the duration of the saccadic gaze shifts the animal executed, either by head-fixed eye saccades alone or by combined eye-head movements. This was true for all types of gaze shifts studied: active movements to visual targets; passive movements induced by whole-body rotation or by head rotation about stationary body; and electrically evoked movements by stimulation of the caudal part of the superior colliculus (SC), a central structure for gaze control. For combined eye-head gaze shifts, the OPN pause was therefore not correlated to the eye-in-head trajectory. For instance, in active gaze movements, the end of the pause was better correlated with the gaze end than with either the eye saccade end or the time of eye counterrotation. The hypothesis that cat OPNs participate in controlling gaze shifts is supported by these results, and also by the observation that the movements of both the eyes and the head were transiently interrupted by stimulation of OPNs during gaze shifts. However, we found that the OPN pause could be dissociated from the gaze-motor-error signal producing the gaze shift. First, OPNs resumed discharging when perturbation of head motion briefly interrupted a gaze shift before its intended amplitude was attained. Second, stimulation of caudal SC sites in head-free cat elicited large head-free gaze shifts consistent with the creation of a large gaze-motor-error signal. However, stimulation of the same sites in head-fixed cat produced small “goal-directed” eye saccades, and OPNs paused only for the duration of the latter; neither a pause nor an eye movement occurred when the same stimulation was applied with the eyes at the goal location. We conclude that OPNs can be controlled by neither a simple eye control system nor an absolute gaze control system. Our data cannot be accounted for by existing models describing the control of combined eye-head gaze shifts and therefore put new constraints on future models, which will have to incorporate all the various signals that act synergistically to control gaze shifts.

scholarly journals Role of Frontal Eye Fields in Countermanding Saccades: Visual, Movement, and Fixation Activity

1998 ◽  
Vol 79 (2) ◽  
pp. 817-834 ◽  
Author(s):  
Doug P. Hanes ◽  
Warren F. Patterson ◽  
Jeffrey D. Schall
Keyword(s):  
Single Cells ◽  
Race Model ◽  
Stop Signal ◽  
Frontal Eye Fields ◽  
Gaze Control ◽  
Related Activity ◽  
Gaze Shifts ◽  
Visual Movement ◽  
Fixation Activity

Hanes, Doug P., Warren F. Patterson II, and Jeffrey D. Schall. Role of frontal eye fields in countermanding saccades: visual, movement, and fixation activity. J. Neurophysiol. 79: 817–834, 1998. A new approach was developed to investigate the role of visual-, movement-, and fixation-related neural activity in gaze control. We recorded unit activity in the frontal eye fields (FEF), an area in frontal cortex that plays a central role in the production of purposeful eye movements, of monkeys ( Macaca mulatta) performing visually and memory-guided saccades. The countermanding paradigm was employed to assess whether single cells generate signals sufficient to control movement production. The countermanding paradigm consists of a task that manipulates the monkeys' ability to withhold planned saccades combined with an analysis based on a race model that provides an estimate of the time needed to cancel the movement that is being prepared. We obtained clear evidence that FEF neurons with eye movement-related activity generate signals sufficient to control the production of gaze shifts. Movement-related activity, which was growing toward a trigger threshold as the saccades were prepared, decayed in response to the stop signal within the time required to cancel the saccade. Neurons with fixation-related activity were less common, but during the countermanding paradigm, these neurons exhibited an equally clear gaze-control signal. Fixation cells that had a pause in firing before a saccade exhibited elevated activity in response to the stop signal within the time that the saccade was cancelled. In contrast to cells with movement or fixation activity, neurons with only visually evoked activity exhibited no evidence of signals sufficient to control the production of gaze shifts. However, a fraction of tonic visual cells exhibited a reduction of activity once a saccade command had been cancelled even though the visual target was still present in the receptive field. These findings demonstrate the use of the countermanding paradigm in identifying neural signatures of motor control and provide new information about the fine balance between gaze shifting and gaze holding mechanisms.

scholarly journals Countermanding Eye-Head Gaze Shifts in Humans: Marching Orders Are Delivered to the Head First

2005 ◽  
Vol 94 (1) ◽  
pp. 883-895 ◽  
Author(s):  
Brian D. Corneil ◽  
James K. Elsley
Keyword(s):  
Head Movement ◽  
Reaction Times ◽  
Race Model ◽  
Saccadic Eye Movements ◽  
Oculomotor System ◽  
Stop Signal ◽  
Head Movements ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Countermanding Task

The countermanding task requires subjects to cancel a planned movement on appearance of a stop signal, providing insights into response generation and suppression. Here, we studied human eye-head gaze shifts in a countermanding task with targets located beyond the horizontal oculomotor range. Consistent with head-restrained saccadic countermanding studies, the proportion of gaze shifts on stop trials increased the longer the stop signal was delayed after target presentation, and gaze shift stop-signal reaction times (SSRTs: a derived statistic measuring how long it takes to cancel a movement) averaged ∼120 ms across seven subjects. We also observed a marked proportion of trials (13% of all stop trials) during which gaze remained stable but the head moved toward the target. Such head movements were more common at intermediate stop signal delays. We never observed the converse sequence wherein gaze moved while the head remained stable. SSRTs for head movements averaged ∼190 ms or ∼70–75 ms longer than gaze SSRTs. Although our findings are inconsistent with a single race to threshold as proposed for controlling saccadic eye movements, movement parameters on stop trials attested to interactions consistent with a race model architecture. To explain our data, we tested two extensions to the saccadic race model. The first assumed that gaze shifts and head movements are controlled by parallel but independent races. The second model assumed that gaze shifts and head movements are controlled by a single race, preceded by terminal ballistic intervals not under inhibitory control, and that the head-movement branch is activated at a lower threshold. Although simulations of both models produced acceptable fits to the empirical data, we favor the second alternative as it is more parsimonious with recent findings in the oculomotor system. Using the second model, estimates for gaze and head ballistic intervals were ∼25 and 90 ms, respectively, consistent with the known physiology of the final motor paths. Further, the threshold of the head movement branch was estimated to be 85% of that required to activate gaze shifts. From these results, we conclude that a commitment to a head movement is made in advance of gaze shifts and that the comparative SSRT differences result primarily from biomechanical differences inherent to eye and head motion.

scholarly journals Corrective response times in a coordinated eye-head-arm countermanding task

2018 ◽  
Vol 119 (6) ◽  
pp. 2036-2051 ◽  
Author(s):  
Gordon Tao ◽  
Aarlenne Z. Khan ◽  
Gunnar Blohm
Keyword(s):  
Reaction Time ◽  
Response Times ◽  
Residual Effect ◽  
Race Model ◽  
Information Criteria ◽  
Decision Processes ◽  
Decision Threshold ◽  
Corrective Response ◽  
Motor Initiation ◽  
Countermanding Task

Inhibition of motor responses has been described as a race between two competing decision processes of motor initiation and inhibition, which manifest as the reaction time (RT) and the stop signal reaction time (SSRT); in the case where motor initiation wins out over inhibition, an erroneous movement occurs that usually needs to be corrected, leading to corrective response times (CRTs). Here we used a combined eye-head-arm movement countermanding task to investigate the mechanisms governing multiple effector coordination and the timing of corrective responses. We found a high degree of correlation between effector response times for RT, SSRT, and CRT, suggesting that decision processes are strongly dependent across effectors. To gain further insight into the mechanisms underlying CRTs, we tested multiple models to describe the distribution of RTs, SSRTs, and CRTs. The best-ranked model (according to 3 information criteria) extends the LATER race model governing RTs and SSRTs, whereby a second motor initiation process triggers the corrective response (CRT) only after the inhibition process completes in an expedited fashion. Our model suggests that the neural processing underpinning a failed decision has a residual effect on subsequent actions. NEW & NOTEWORTHY Failure to inhibit erroneous movements typically results in corrective movements. For coordinated eye-head-hand movements we show that corrective movements are only initiated after the erroneous movement cancellation signal has reached a decision threshold in an accelerated fashion.

Analysis of Primate IBN Spike Trains Using System Identification Techniques. III. Relationship to Motor Error During Head-Fixed Saccades and Head-Free Gaze Shifts

1997 ◽  
Vol 78 (6) ◽  
pp. 3307-3322 ◽  
Author(s):  
Kathleen E. Cullen ◽  
Daniel Guitton
Keyword(s):  
System Identification ◽  
Eye Movement ◽  
Spike Trains ◽  
Eye Position ◽  
Error Signal ◽  
Gaze Shifts ◽  
Movement Dynamics ◽  
Motor Error ◽  
Identification Techniques ◽  
Better Than

Cullen, Kathleen E. and Daniel Guitton. Analysis of primate IBN spike trains using system identification techniques. III. Relationship to motor error during head-fixed saccades and head-free gaze shifts. J. Neurophysiol. 78: 3307–3322, 1997. The classic model of saccade generation assumes that the burst generator is driven by a motor-error signal, the difference between the actual eye position and the final “desired” eye position in the orbit. Here we evaluate objectively, using system identification techniques, the dynamic relationship between motor-error signals and primate inhibitory burst neuron (IBN) discharges (upstream analysis). The IBNs presented here are the same neurons whose downstream relationships were characterized during head-fixed saccades and head-free gaze shifts in our companion papers. In our analysis of head-fixed saccades we determined how well IBN discharges encode eye motor error (εe) compared with downstream saccadic eye movement dynamics and whether long-lead IBN (LLIBN) discharges encode εe better than short-lead IBNs (SLIBNs), given that it is commonly assumed that short-lead burst neurons (BNs) are closer than long-lead BNs to the motor output and thus further from the εe signal. In the εe-based models tested, IBN firing frequency B( t) was represented by one of the following: 1) model 1u, a nonlinear function of εe; 2) model 2u, a linear function of εe [ B( t) = r k + a 1εe( t)] where the bias term r k was estimated separately for each saccade; 3) model 3u, a version of model 2u wherein the bias term was a function of saccade amplitude; or 4) model 4u, a linear function of εe with an added pole term (the derivative of firing rate). Models based on εe consistently produced worse predictions of IBN activity than models of comparable complexity based on eye movement dynamics (e.g., eye velocity). Hence, the simple two parameter downstream model 2d [ B( t) = r + b 1E˙( t)] was much better than any upstream (εe-based) model with a comparable number of parameters. The link between B( t) and εe is due primarily to the correlation between the declining phases of B( t) and εe; motor-error models did not predict well the rising phase of the discharge. We could improve substantially the performance of upstream models by adding an ε˙e term. Because ε˙e = − E˙, this process was equivalent to incorporating E˙ terms into upstream models thereby erasing the distinction between upstream and downstream analyses. Adding an ε˙e term to the upstream models made them as good as downstream ones in predicting B( t). However, the εe term now became redundant because its removal did not affect model accuracy. Thus, when E˙ is available as a parameter, εe becomes irrelevant. In the head-free monkey the ability of upstream models to predict IBN firing during head-free gaze shifts when gaze, eye, or head motor-error signals were model inputs was poor and similar to the upstream analysis of the head-fixed condition. We conclude that during saccades (head-fixed) or gaze shifts (head-free) the activity of both SLIBNs and LLIBNs is more closely linked to downstream events (i.e., the dynamics of ongoing movements) than to the coincident upstream motor-error signal. Furthermore, SLIBNs and LLIBNs do not differ in their characteristics; the latter are not, as is usually hypothesized, closer to a motor-error signal than the former.

Human eye-head gaze shifts preserve their accuracy and spatiotemporal trajectory profiles despite long-duration torque perturbations that assist or oppose head motion

2012 ◽  
Vol 108 (1) ◽  
pp. 39-56 ◽  
Author(s):  
Mathieu Boulanger ◽  
Henrietta L. Galiana ◽  
Daniel Guitton
Keyword(s):  
Control System ◽  
Sensory Information ◽  
Head Motion ◽  
Gaze Control ◽  
Gaze Shifts ◽  
The Gaze ◽  
Moving Platforms ◽  
Long Duration ◽  
Random Direction ◽  
Horizontal Gaze

Humans routinely use coordinated eye-head gaze saccades to rapidly and accurately redirect the line of sight (Land MF. Vis Neurosci 26: 51–62, 2009). With a fixed body, the gaze control system combines visual, vestibular, and neck proprioceptive sensory information and coordinates two moving platforms, the eyes and head. Classic engineering tools have investigated the structure of motor systems by testing their ability to compensate for perturbations. When a reaching movement of the hand is subjected to an unexpected force field of random direction and strength, the trajectory is deviated and its final position is inaccurate. Here, we found that the gaze control system behaves differently. We perturbed horizontal gaze shifts with long-duration torques applied to the head that unpredictably either assisted or opposed head motion and very significantly altered the intended head trajectory. We found, as others have with brief head perturbations, that gaze accuracy was preserved. Unexpectedly, we found also that the eye compensated well—with saccadic and rollback movements—for long-duration head perturbations such that resulting gaze trajectories remained close to that when the head was not perturbed. However, the ocular compensation was best when torques assisted, compared with opposed, head motion. If the vestibuloocular reflex (VOR) is suppressed during gaze shifts, as currently thought, what caused invariant gaze trajectories and accuracy, early eye-direction reversals, and asymmetric compensations? We propose three mechanisms: a gaze feedback loop that generates a gaze-position error signal; a vestibular-to-oculomotor signal that dissociates self-generated from passively imposed head motion; and a saturation element that limits orbital eye excursion.

scholarly journals Coding of interceptive saccades in parietal cortex of macaque monkeys

2021 ◽  
Author(s):  
Jan Churan ◽  
Andre Kaminiarz ◽  
Jakob C.B. Schwenk ◽  
Frank Bremmer
Keyword(s):  
Oculomotor System ◽  
Saccade Target ◽  
Frontal Eye Field ◽  
Moving Target ◽  
Gaze Control ◽  
Moving Targets ◽  
Macaque Monkeys ◽  
Parietal Area ◽  
Eye Field ◽  
Target Selecting

The oculomotor system can initiate remarkably accurate saccades towards moving targets (interceptive saccades) the processing of which is still under debate. The generation of these saccades requires the oculomotor centers to have information about the motion parameters of the target that then must be extrapolated to bridge the inherent processing delays. We investigated to what degree the information about motion of a saccade target is available in the lateral intra-parietal area (area LIP) of macaque monkeys for generation of accurate interceptive saccades. When a multi-layer neural network was trained based on neural discharges from area LIP around the time of saccades towards stationary targets it was also able to predict the end points of saccades directed towards moving targets. This prediction, however, lagged behind the actual post-saccadic position of the moving target by ~80 ms when the whole neuronal sample of 105 neurons was used. We further found that single neurons differentially code for the motion of the target. Selecting neurons with the strongest representation of target motion reduced this lag to ~30 ms which represents the position of the moving target approximately at the onset of the interceptive saccade. We conclude that - similarly to recent findings from the Superior Colliculus (Goffart et al., 2017) - there is a continuum of contributions of individual LIP neurons to the accuracy of interceptive saccades. A contribution of other gaze control centers (like the cerebellum or the frontal eye field) that further increase the saccadic accuracy is, however, likely.

scholarly journals Independent and conjugate eye movements during optokinesis in teleost fish

2002 ◽  
Vol 205 (9) ◽  
pp. 1241-1252 ◽  
Author(s):  
Kerstin A. Fritsches ◽  
N. Justin Marshall
Keyword(s):  
Eye Movements ◽  
Visual Field ◽  
Teleost Fish ◽  
Optokinetic Nystagmus ◽  
Oculomotor System ◽  
Visual Input ◽  
Comparative Approach ◽  
Optokinetic Response ◽  
Different Levels

SUMMARYIn response to movements involving a large part of the visual field, the eyes of vertebrates typically show an optokinetic nystagmus, a response in which both eyes are tightly yoked. Using a comparative approach, this study sets out to establish whether fish with independent spontaneous eye movements show independent optokinetic nystagmus in each eye. Two fish with independent spontaneous eye movements, the pipefish Corythoichthyes intestinalisand the sandlance Limnichthyes fasciatus were compared with the butterflyfish Chaetodon rainfordi, which exhibits tightly yoked eye movements. In the butterflyfish a single whole-field stimulus elicits conjugate optokinesis, whereas the sandlance and pipefish show asynchronous optokinetic movements. In a split drum experiment, when both eyes were stimulated in opposite directions with different speeds, both the sandlance and the pipefish compensated independently with each eye. The optokinetic response in the butterflyfish showed some disconjugacy but was generally confused. When one eye was occluded, the seeing eye was capable of driving the occluded eye in both the butterflyfish and the pipefish but not in the sandlance. Monocular occlusion therefore unmasks a link between the two eyes in the pipefish, which is overridden when both eyes receive visual input. The sandlance never showed any correlation between the eyes during optokinesis in all stimulus conditions. This suggests that there are different levels of linkage between the two eyes in the oculomotor system of teleosts, depending on the visual input.

scholarly journals Coding of interceptive saccades in parietal cortex of macaque monkeys

2021 ◽  
Author(s):  
Jan Churan ◽  
Andre Kaminiarz ◽  
Jakob C. B. Schwenk ◽  
Frank Bremmer
Keyword(s):  
Oculomotor System ◽  
Saccade Target ◽  
Frontal Eye Field ◽  
Moving Target ◽  
Gaze Control ◽  
Moving Targets ◽  
Macaque Monkeys ◽  
Parietal Area ◽  
Eye Field ◽  
Target Selecting

AbstractThe oculomotor system can initiate remarkably accurate saccades towards moving targets (interceptive saccades) the processing of which is still under debate. The generation of these saccades requires the oculomotor centers to have information about the motion parameters of the target that then must be extrapolated to bridge the inherent processing delays. We investigated to what degree the information about motion of a saccade target is available in the lateral intra-parietal area (area LIP) of macaque monkeys for generation of accurate interceptive saccades. When a multi-layer neural network was trained based on neural discharges from area LIP around the time of saccades towards stationary targets, it was also able to predict the end points of saccades directed towards moving targets. This prediction, however, lagged behind the actual post-saccadic position of the moving target by ~ 80 ms when the whole neuronal sample of 105 neurons was used. We further found that single neurons differentially code for the motion of the target. Selecting neurons with the strongest representation of target motion reduced this lag to ~ 30 ms which represents the position of the moving target approximately at the onset of the interceptive saccade. We conclude that—similarly to recent findings from the Superior Colliculus (Goffart et al. J Neurophysiol 118(5):2890–2901)—there is a continuum of contributions of individual LIP neurons to the accuracy of interceptive saccades. A contribution of other gaze control centers (like the cerebellum or the frontal eye field) that further increase the saccadic accuracy is, however, likely.

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