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1.
Sci Rep ; 14(1): 9082, 2024 04 20.
Article in English | MEDLINE | ID: mdl-38643273

ABSTRACT

Studying the oculomotor system provides a unique window to assess brain health and function in various clinical populations. Although the use of detailed oculomotor parameters in clinical research has been limited due to the scalability of the required equipment, the development of novel tablet-based technologies has created opportunities for fast, easy, cost-effective, and reliable eye tracking. Oculomotor measures captured via a mobile tablet-based technology have previously been shown to reliably discriminate between Parkinson's Disease (PD) patients and healthy controls. Here we further investigate the use of oculomotor measures from tablet-based eye-tracking to inform on various cognitive abilities and disease severity in PD patients. When combined using partial least square regression, the extracted oculomotor parameters can explain up to 71% of the variance in cognitive test scores (e.g. Trail Making Test). Moreover, using a receiver operating characteristics (ROC) analysis we show that eye-tracking parameters can be used in a support vector classifier to discriminate between individuals with mild PD from those with moderate PD (based on UPDRS cut-off scores) with an accuracy of 90%. Taken together, our findings highlight the potential usefulness of mobile tablet-based technology to rapidly scale eye-tracking use and usefulness in both research and clinical settings by informing on disease stage and cognitive outcomes.


Subject(s)
Parkinson Disease , Humans , Eye Movements , Cognition , Movement , Patient Acuity
2.
Front Neurol ; 14: 1243594, 2023.
Article in English | MEDLINE | ID: mdl-37745656

ABSTRACT

A growing body of evidence supports the link between eye movement anomalies and brain health. Indeed, the oculomotor system is composed of a diverse network of cortical and subcortical structures and circuits that are susceptible to a variety of degenerative processes. Here we show preliminary findings from the baseline measurements of an ongoing longitudinal cohort study in MS participants, designed to determine if disease and cognitive status can be estimated and tracked with high accuracy based on eye movement parameters alone. Using a novel gaze-tracking technology that can reliably and accurately track eye movements with good precision without the need for infrared cameras, using only an iPad Pro embedded camera, we show in this cross-sectional study that several eye movement parameters significantly correlated with clinical outcome measures of interest. Eye movement parameters were extracted from fixation, pro-saccade, anti-saccade, and smooth pursuit visual tasks, whereas the clinical outcome measures were the scores of several disease assessment tools and standard cognitive tests such as the Expanded Disability Status Scale (EDSS), Brief International Cognitive Assessment for MS (BICAMS), the Multiple Sclerosis Functional Composite (MSFC) and the Symbol Digit Modalities Test (SDMT). Furthermore, partial least squares regression analyses show that a small set of oculomotor parameters can explain up to 84% of the variance of the clinical outcome measures. Taken together, these findings not only replicate previously known associations between eye movement parameters and clinical scores, this time using a novel mobile-based technology, but also the notion that interrogating the oculomotor system with a novel eye-tracking technology can inform us of disease severity, as well as the cognitive status of MS participants.

3.
Front Neurol ; 14: 1204733, 2023.
Article in English | MEDLINE | ID: mdl-37396780

ABSTRACT

The idea that eye movements can reflect certain aspects of brain function and inform on the presence of neurodegeneration is not a new one. Indeed, a growing body of research has shown that several neurodegenerative disorders, such as Alzheimer's and Parkinson's Disease, present characteristic eye movement anomalies and that specific gaze and eye movement parameters correlate with disease severity. The use of detailed eye movement recordings in research and clinical settings, however, has been limited due to the expensive nature and limited scalability of the required equipment. Here we test a novel technology that can track and measure eye movement parameters using the embedded camera of a mobile tablet. We show that using this technology can replicate several well-known findings regarding oculomotor anomalies in Parkinson's disease (PD), and furthermore show that several parameters significantly correlate with disease severity as assessed with the MDS-UPDRS motor subscale. A logistic regression classifier was able to accurately distinguish PD patients from healthy controls on the basis of six eye movement parameters with a sensitivity of 0.93 and specificity of 0.86. This tablet-based tool has the potential to accelerate eye movement research via affordable and scalable eye-tracking and aid with the identification of disease status and monitoring of disease progression in clinical settings.

4.
Rev Neurosci ; 31(5): 505-520, 2020 Jul 28.
Article in English | MEDLINE | ID: mdl-32242834

ABSTRACT

About 25 years ago, the discovery of receptive field (RF) remapping in the parietal cortex of nonhuman primates revealed that visual RFs, widely assumed to have a fixed retinotopic organization, can change position before every saccade. Measuring such changes can be deceptively difficult. As a result, studies that followed have generated a fascinating but somewhat confusing picture of the phenomenon. In this review, we describe how observations of RF remapping depend on the spatial and temporal sampling of visual RFs and saccade directions. Further, we summarize some of the theories of how remapping might occur in neural circuitry. Finally, based on neurophysiological and psychophysical observations, we discuss the ways in which remapping information might facilitate computations in downstream brain areas.


Subject(s)
Attention/physiology , Brain/physiology , Perception/physiology , Saccades/physiology , Visual Perception/physiology , Animals , Humans , Photic Stimulation/methods
5.
Proc Natl Acad Sci U S A ; 117(14): 8203-8211, 2020 04 07.
Article in English | MEDLINE | ID: mdl-32209663

ABSTRACT

Most people easily learn to recognize new faces and places, and with more extensive practice they can become experts at visual tasks as complex as radiological diagnosis and action video games. Such perceptual plasticity has been thoroughly studied in the context of training paradigms that require constant fixation. In contrast, when observers learn under more natural conditions, they make frequent saccadic eye movements. Here we show that such eye movements can play an important role in visual learning. Observers performed a task in which they executed a saccade while discriminating the motion of a cued visual stimulus. Additional stimuli, presented simultaneously with the cued one, permitted an assessment of the perceptual integration of information across visual space. Consistent with previous results on perisaccadic remapping [M. Szinte, D. Jonikaitis, M. Rolfs, P. Cavanagh, H. Deubel, J. Neurophysiol. 116, 1592-1602 (2016)], most observers preferentially integrated information from locations representing the presaccadic and postsaccadic retinal positions of the cue. With extensive training on the saccade task, these observers gradually acquired the ability to perform similar motion integration without making eye movements. Importantly, the newly acquired pattern of spatial integration was determined by the metrics of the saccades made during training. These results suggest that oculomotor influences on visual processing, long thought to subserve the function of perceptual stability, also play a role in visual plasticity.


Subject(s)
Saccades/physiology , Spatial Learning/physiology , Visual Perception/physiology , Adult , Cues , Female , Humans , Male , Photic Stimulation/methods , Young Adult
6.
Cortex ; 111: 127-133, 2019 02.
Article in English | MEDLINE | ID: mdl-30472384

ABSTRACT

A critical question in neurology is how the brain reorganizes its structure and function following injury. Here, we consider oculomotor control following a massive brain lesion, a hemispherectomy. We used the oblique anti-saccade task which requires the suppression of a saccade towards a visual cue, flashed anywhere in a patient's seeing hemifield, and the generation, in the dark, of an anti-saccade to a task-dependent location in the opposite blind hemifield; inverting either the horizontal or both horizontal and vertical components. Anti-saccades require a visuo-motor vector inversion that normally involves bilateral interactions between frontal, parietal and subcortical structures across both hemispheres. Here, oblique anti-saccades presented a major challenge to the patient's single hemisphere, requiring one site in visual cortex to communicate with an instruction-dependent site in oculomotor cortex. Patients with discrete frontal lobe damage can be strongly impaired in anti-saccades. By contrast, hemispherectomy patients performed oblique anti-saccades normally, contrasting with their permanent contralesional hemianopia and severe hemiparesis.


Subject(s)
Eye Movements/physiology , Hemispherectomy , Neuronal Plasticity/physiology , Visual Fields/physiology , Adult , Cerebral Cortex/physiopathology , Female , Frontal Lobe/physiopathology , Humans , Male , Middle Aged , Photic Stimulation , Reaction Time/physiology
7.
Proc Natl Acad Sci U S A ; 114(29): E5979-E5985, 2017 07 18.
Article in English | MEDLINE | ID: mdl-28673993

ABSTRACT

Oscillations are ubiquitous in the brain, and they can powerfully influence neural coding. In particular, when oscillations at distinct sites are coherent, they provide a means of gating the flow of neural signals between different cortical regions. Coherent oscillations also occur within individual brain regions, although the purpose of this coherence is not well understood. Here, we report that within a single brain region, coherent alpha oscillations link stimulus representations as they change in space and time. Specifically, in primate cortical area V4, alpha coherence links sites that encode the retinal location of a visual stimulus before and after a saccade. These coherence changes exhibit properties similar to those of receptive field remapping, a phenomenon in which individual neurons change their receptive fields according to the metrics of each saccade. In particular, alpha coherence, like remapping, is highly dependent on the saccade vector and the spatial arrangement of current and future receptive fields. Moreover, although visual stimulation plays a modulatory role, it is neither necessary nor sufficient to elicit alpha coherence. Indeed, a similar pattern of coherence is observed even when saccades are made in darkness. Together, these results show that the pattern of alpha coherence across the retinotopic map in V4 matches many of the properties of receptive field remapping. Thus, oscillatory coherence might play a role in constructing the stable representation of visual space that is an essential aspect of conscious perception.


Subject(s)
Saccades/physiology , Visual Cortex/physiology , Animals , Darkness , Female , Macaca fascicularis , Neurons/physiology , Photic Stimulation
8.
J Neurosci ; 36(35): 9227-39, 2016 08 31.
Article in English | MEDLINE | ID: mdl-27581462

ABSTRACT

UNLABELLED: Psychophysical studies have shown that subjects are often unaware of visual stimuli presented around the time of an eye movement. This saccadic suppression is thought to be a mechanism for maintaining perceptual stability. The brain might accomplish saccadic suppression by reducing the gain of visual responses to specific stimuli or by simply suppressing firing uniformly for all stimuli. Moreover, the suppression might be identical across the visual field or concentrated at specific points. To evaluate these possibilities, we recorded from individual neurons in cortical area V4 of nonhuman primates trained to execute saccadic eye movements. We found that both modes of suppression were evident in the visual responses of these neurons and that the two modes showed different spatial and temporal profiles: while gain changes started earlier and were more widely distributed across visual space, nonspecific suppression was found more often in the peripheral visual field, after the completion of the saccade. Peripheral suppression was also associated with increased noise correlations and stronger local field potential oscillations in the α frequency band. This pattern of results suggests that saccadic suppression shares some of the circuitry responsible for allocating voluntary attention. SIGNIFICANCE STATEMENT: We explore our surroundings by looking at things, but each eye movement that we make causes an abrupt shift of the visual input. Why doesn't the world look like a film recorded on a shaky camera? The answer in part is a brain mechanism called saccadic suppression, which reduces the responses of visual neurons around the time of each eye movement. Here we reveal several new properties of the underlying mechanisms. First, the suppression operates differently in the central and peripheral visual fields. Second, it appears to be controlled by oscillations in the local field potentials at frequencies traditionally associated with attention. These results suggest that saccadic suppression shares the brain circuits responsible for actively ignoring irrelevant stimuli.


Subject(s)
Neurons/physiology , Saccades/physiology , Visual Cortex/cytology , Visual Cortex/physiology , Visual Fields/physiology , Visual Perception/physiology , Action Potentials/physiology , Animals , Attention/physiology , Evoked Potentials, Visual/physiology , Female , Fourier Analysis , Macaca mulatta , Male , Photic Stimulation , Reaction Time/physiology , Statistics, Nonparametric
9.
J Neurophysiol ; 116(4): 1956-1985, 2016 10 01.
Article in English | MEDLINE | ID: mdl-27440248

ABSTRACT

During gaze shifts, the eyes and head collaborate to rapidly capture a target (saccade) and fixate it. Accordingly, models of gaze shift control should embed both saccadic and fixation modes and a mechanism for switching between them. We demonstrate a model in which the eye and head platforms are driven by a shared gaze error signal. To limit the number of free parameters, we implement a model reduction approach in which steady-state cerebellar effects at each of their projection sites are lumped with the parameter of that site. The model topology is consistent with anatomy and neurophysiology, and can replicate eye-head responses observed in multiple experimental contexts: 1) observed gaze characteristics across species and subjects can emerge from this structure with minor parametric changes; 2) gaze can move to a goal while in the fixation mode; 3) ocular compensation for head perturbations during saccades could rely on vestibular-only cells in the vestibular nuclei with postulated projections to burst neurons; 4) two nonlinearities suffice, i.e., the experimentally-determined mapping of tectoreticular cells onto brain stem targets and the increased recruitment of the head for larger target eccentricities; 5) the effects of initial conditions on eye/head trajectories are due to neural circuit dynamics, not planning; and 6) "compensatory" ocular slow phases exist even after semicircular canal plugging, because of interconnections linking eye-head circuits. Our model structure also simulates classical vestibulo-ocular reflex and pursuit nystagmus, and provides novel neural circuit and behavioral predictions, notably that both eye-head coordination and segmental limb coordination are possible without trajectory planning.


Subject(s)
Eye Movements/physiology , Head Movements/physiology , Models, Neurological , Action Potentials , Animals , Brain Stem/anatomy & histology , Brain Stem/physiology , Cats , Cerebellum/anatomy & histology , Cerebellum/physiology , Haplorhini , Humans , Neural Networks, Computer , Neural Pathways/anatomy & histology , Neural Pathways/physiology , Neurons/physiology , Nonlinear Dynamics
10.
Curr Biol ; 26(12): R491-R492, 2016 06 20.
Article in English | MEDLINE | ID: mdl-27326707

ABSTRACT

A fundamental concept in neuroscience is the receptive field, the area of space over which a neuron gathers information. Until about 25 years ago, visual receptive fields were thought to be determined entirely by the pattern of retinal inputs, so it was quite surprising to find neurons in primate cortex with receptive fields that changed position every time a saccade was executed [1]. Although this discovery has figured prominently into theories of visual perception, there is still much debate about the nature of the phenomenon: Some studies report forward remapping[1-3], in which receptive fields shift to their postsaccadic locations, and others report convergent remapping, in which receptive fields shift toward the saccade target [4]. These two possibilities can be difficult to distinguish, particularly when the two types of remapping lead to receptive field shifts in similar directions [5], as was the case in virtually all previous experiments. Here we report new data from neurons in primate cortical area V4, where both types of remapping have previously been reported [3,6]. Using an experimental configuration in which forward and convergent remapping would lead to receptive field shifts in opposite directions, we show that forward remapping is the dominant type of receptive field shift in V4.


Subject(s)
Visual Cortex/physiology , Visual Fields/physiology , Animals , Macaca fascicularis
11.
Nat Commun ; 7: 10402, 2016 Feb 01.
Article in English | MEDLINE | ID: mdl-26832423

ABSTRACT

Visual neurons typically receive information from a limited portion of the retina, and such receptive fields are a key organizing principle for much of visual cortex. At the same time, there is strong evidence that receptive fields transiently shift around the time of saccades. The nature of the shift is controversial: Previous studies have found shifts consistent with a role for perceptual constancy; other studies suggest a role in the allocation of spatial attention. Here we present evidence that both the previously documented functions exist in individual neurons in primate cortical area V4. Remapping associated with perceptual constancy occurs for saccades in all directions, while attentional shifts mainly occur for neurons with receptive fields in the same hemifield as the saccade end point. The latter are relatively sluggish and can be observed even during saccade planning. Overall these results suggest a complex interplay of visual and extraretinal influences during the execution of saccades.


Subject(s)
Macaca fascicularis , Saccades/physiology , Visual Cortex/physiology , Animals , Female , Male , Neurons/physiology
12.
Brain ; 138(Pt 12): 3760-75, 2015 Dec.
Article in English | MEDLINE | ID: mdl-26412850

ABSTRACT

This paper questions the prominent role that the parietal lobe is thought to play in the processing of corollary discharges for saccadic eye movements. A corollary discharge copies the motor neurons' signal and sends it to brain areas involved in monitoring eye trajectories. The classic double-step saccade task has been used extensively to study these mechanisms: two targets (T1 and T2) are quickly (40-150 ms) flashed sequentially in the periphery. After the extinction of the fixation point, subjects are to make two saccades (S1 and S2), in the dark, to the remembered locations of the targets in the order they appeared. The success of S2 requires a corollary discharge encoding S1's vector. Patients with a parietal lobe lesion, particularly on the right, are impaired at generating an accurate S2 when S1 is directed contralesionally, but not ipsilesionally, thought due to an impaired contralesional corollary discharge. In contrast, we hypothesize that failure on the classic double-step task is due to visual processing and attentional deficits that commonly result from lesions of the parietal lobe and imperfect data analysis methods. Here, we studied parietal patients who fail in the classic double-step task when tested and data analysed according to previously published methods. We then tested our patients on two modified versions of the double-step task, designed to mitigate deficits other than corollary discharge that may have confounded previous investigations. In our 'exogenous' task, T2 was presented prior to T1 and for longer (T2: 800-1200 ms, T1: 350 ms) than in the classic task. S1 went to T1 and S2 to T2, all in the dark. All patients who completed sufficient trials had a corollary discharge for contralesional and ipsilesional S1s (5/5). In our 'endogenous' task, a single target was presented peripherally for 800-1200 ms. After extinction of target and fixation point, patients made first an 'endogenous' S1, of self-determined amplitude either to the left or right, before making S2 to the remembered location of the previously flashed target. To be successful, a corollary discharge of endogenous S1-generated in the dark-was required in the calculation of S2's motor vector. Every parietal patient showed evidence of using corollary discharges for endogenous S1s in the ipsilesional and contralesional directions (6/6). Our results support the hypothesis, based on our previous studies of corollary discharge mechanisms in hemidecorticate patients, and electrophysiological studies by others in monkey, that corollary discharges for left and right saccades are available to each cortical hemisphere.


Subject(s)
Functional Laterality/physiology , Models, Biological , Parietal Lobe/pathology , Parietal Lobe/physiopathology , Saccades/physiology , Case-Control Studies , Female , Humans , Male , Parietal Lobe/physiology , Photic Stimulation , Reaction Time/physiology , Reproducibility of Results , Visual Perception/physiology
13.
Neuron ; 85(3): 615-27, 2015 Feb 04.
Article in English | MEDLINE | ID: mdl-25600124

ABSTRACT

Traveling waves of neural activity are frequently observed to occur in concert with the presentation of a sensory stimulus or the execution of a movement. Although such waves have been studied for decades, little is known about their function. Here we show that traveling waves in the primate extrastriate visual cortex provide a means of integrating sensory and motor signals. Specifically, we describe a traveling wave of local field potential (LFP) activity in cortical area V4 of macaque monkeys that is triggered by the execution of saccadic eye movements. These waves sweep across the V4 retinotopic map, following a consistent path from the foveal to the peripheral representations of space; their amplitudes correlate with the direction and size of each saccade. Moreover, these waves are associated with a reorganization of the postsaccadic neuronal firing patterns, which follow a similar retinotopic progression, potentially prioritizing the processing of behaviorally relevant stimuli.


Subject(s)
Psychomotor Performance/physiology , Reaction Time/physiology , Saccades/physiology , Visual Cortex/physiology , Visual Perception/physiology , Animals , Macaca mulatta , Photic Stimulation/methods , Random Allocation
14.
Cortex ; 63: 232-49, 2015 Feb.
Article in English | MEDLINE | ID: mdl-25299582

ABSTRACT

Patients who have had a cerebral hemisphere surgically removed as adults can generate accurate leftward and rightward saccadic eye movements, a task classically thought to require two hemispheres each controlling contralateral saccades. Here, we asked whether one hemisphere can generate sequences of saccades, the success of which requires the use of corollary discharges. Using a double-step saccade paradigm, we tested two hemidecorticate subjects who, by definition, are contralesionally hemianopic. In experiment 1, two targets, T1 and T2, were flashed in their seeing hemifield and subjects had to look in the dark to T1, then T2. In experiment 2, only one target was flashed; before looking at it, the subject had first to saccade voluntarily elsewhere. Both subjects were able to complete the tasks, independent of first and second saccade direction and whether the saccades were voluntarily or visually triggered. Both subjects displayed a strategy, typical in hemianopia, of making multiple-step saccades and placing, at overall movement-end, the recalled locations of T1 and T2 on off-foveal locations in their seeing hemifield, in a retinal area typically spanning a 5-15° window, depending on the subject, trial type and target eccentricity. In summary, a single hemisphere monitored the amplitude and direction of the first multiple-step saccade sequence bilaterally, and combined this information with the recalled initial retinotopic location of T2 (no longer visible) to generate a correct target-directed second saccade sequence in the dark. Unexpectedly, our hemidecorticate subjects performed better on the double-step task than subjects with isolated unilateral parietal lesions, reported in the literature to have marked deficiencies in monitoring contralesional saccadic eye movements. Thus, plasticity-dependent mechanisms that lead to recovery of function after hemidecortication are different than those deployed after smaller lesions. This implies a reconsideration of the classical links between behavioural deficits and discrete cortical lesions.


Subject(s)
Hemispherectomy , Saccades/physiology , Visual Perception/physiology , Adult , Female , Humans , Male , Photic Stimulation , Reaction Time/physiology
15.
Cortex ; 49(3): 861-76, 2013 Mar.
Article in English | MEDLINE | ID: mdl-22703968

ABSTRACT

Patients missing a cortical hemisphere, removed surgically at adulthood, cannot consciously see a visual probe stimulus (P) flashed in their blind contralesional, hemifield. Nevertheless, they have a low-level form of blindsight wherein P can affect the reaction time of a manual response to the appearance of a visual target in their seeing hemifield. This ability is thought to require the pathway from retina-to-ipsilesional superior colliculus (SC) to cortex of the remaining hemisphere (Leh et al., 2006a, 2006b, 2009). Apart from emitting ascending signals, the SC normally sends saccade commands to the brainstem, a function seemingly conserved after hemidecortication because such patients can generate voluntary and accurate saccades bilaterally (Herter and Guitton, 2004). However, they cannot generate goal-directed saccades to P in their blind hemifield. We hypothesized that, in hemidecorticate patients, P might influence anti-saccades directed to the blind hemifield, to the mirror location of a visual cue presented in the seeing hemifield. We used anti-saccades because our patients could scale their anti-saccade amplitudes approximately according to different cue locations, thereby permitting us to control the end point of their anti-saccades to the blind hemifield. We identified in these patients a new form of blindsight wherein unseen P, if properly timed at the anti-saccade goal location in the blind hemifield, reduced the reaction time and improved the accuracy of anti-saccades directed to that general location. We hypothesize that P in the blind hemifield produced low-level signals in the ipsilesional SC that, if appropriately located and timed relative to anti-saccade goal and onset, interacted with anti-saccade motor preparatory activity - produced by descending commands to SC from the remaining hemisphere - so as to modify both anti-saccade reaction time and end point. Our results support normally encoded and functionally useful, but subliminal, signals in the retina-to-ipsilesional SC-to-reticular pathway of hemidecorticate patients.


Subject(s)
Cerebral Cortex/surgery , Perceptual Disorders/physiopathology , Saccades/physiology , Visual Fields/physiology , Visual Perception/physiology , Adult , Cerebral Cortex/physiopathology , Female , Humans , Male , Photic Stimulation , Reaction Time/physiology
16.
J Neurophysiol ; 108(10): 2653-67, 2012 Nov.
Article in English | MEDLINE | ID: mdl-22933722

ABSTRACT

Saccades are useful for directing the high-acuity fovea to visual targets that are of behavioral relevance. The selection of visual targets for eye movements involves the superior colliculus (SC), where many neurons respond to visual stimuli. Many of these neurons are also activated before and during saccades of specific directions and amplitudes. Although the role of the SC in controlling eye movements has been thoroughly examined, far less is known about the nature of the visual responses in this area. We have, therefore, recorded from neurons in the intermediate layers of the macaque SC, while using a sparse-noise mapping procedure to obtain a detailed characterization of the spatiotemporal structure of visual receptive fields. We find that SC responses to flashed visual stimuli start roughly 50 ms after the onset of the stimulus and last for on average ~70 ms. About 50% of these neurons are strongly suppressed by visual stimuli flashed at certain locations flanking the excitatory center, and the spatiotemporal pattern of suppression exerts a predictable influence on the timing of saccades. This suppression may, therefore, contribute to the filtering of distractor stimuli during target selection. We also find that saccades affect the processing of visual stimuli by SC neurons in a manner that is quite similar to the saccadic suppression and postsaccadic enhancement that has been observed in the cortex and in perception. However, in contrast to what has been observed in the cortex, decreased visual sensitivity was generally associated with increased firing rates, while increased sensitivity was associated with decreased firing rates. Overall, these results suggest that the processing of visual stimuli by SC receptive fields can influence oculomotor behavior and that oculomotor signals originating in the SC can shape perisaccadic visual perception.


Subject(s)
Neurons/physiology , Superior Colliculi/physiology , Visual Fields/physiology , Animals , Fixation, Ocular , Macaca , Male , Neurons/classification , Photic Stimulation , Psychomotor Performance , Saccades/physiology , Superior Colliculi/cytology
17.
J Neurophysiol ; 108(1): 39-56, 2012 Jul.
Article in English | MEDLINE | ID: mdl-22457469

ABSTRACT

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.


Subject(s)
Attention/physiology , Fixation, Ocular/physiology , Functional Laterality/physiology , Head Movements/physiology , Torque , Adult , Electrooculography , Feedback , Female , Humans , Male , Orientation/physiology , Reaction Time , Time Factors
18.
PLoS One ; 7(12): e52195, 2012.
Article in English | MEDLINE | ID: mdl-23284931

ABSTRACT

Visual neurons have spatial receptive fields that encode the positions of objects relative to the fovea. Because foveate animals execute frequent saccadic eye movements, this position information is constantly changing, even though the visual world is generally stationary. Interestingly, visual receptive fields in many brain regions have been found to exhibit changes in strength, size, or position around the time of each saccade, and these changes have often been suggested to be involved in the maintenance of perceptual stability. Crucial to the circuitry underlying perisaccadic changes in visual receptive fields is the superior colliculus (SC), a brainstem structure responsible for integrating visual and oculomotor signals. In this work we have studied the time-course of receptive field changes in the SC. We find that the distribution of the latencies of SC responses to stimuli placed outside the fixation receptive field is bimodal: The first mode is comprised of early responses that are temporally locked to the onset of the visual probe stimulus and stronger for probes placed closer to the classical receptive field. We suggest that such responses are therefore consistent with a perisaccadic rescaling, or enhancement, of weak visual responses within a fixed spatial receptive field. The second mode is more similar to the remapping that has been reported in the cortex, as responses are time-locked to saccade onset and stronger for stimuli placed in the postsaccadic receptive field location. We suggest that these two temporal phases of spatial updating may represent different sources of input to the SC.


Subject(s)
Macaca/physiology , Superior Colliculi/physiology , Animals , Photic Stimulation , Visual Fields/physiology , Visual Perception/physiology
19.
J Vis ; 11(12)2011 Oct 06.
Article in English | MEDLINE | ID: mdl-21980187

ABSTRACT

In primates, inspection of a visual scene is typically interrupted by frequent gaze shifts, occurring at an average rate of three to five times per second. Perceptually, these gaze shifts are accompanied by a compression of visual space toward the saccade target, which may be attributed to an oculomotor signal that transiently influences visual processing. While previous studies of compression have focused exclusively on saccadic eye movements made with the head artificially immobilized, many brain structures involved in saccade generation also encode combined eye-head gaze shifts. Thus, in order to understand the interaction between gaze motor and visual signals, we studied perception during eye-head gaze shifts and found a powerful compression of visual space that was spatially directed toward the intended gaze (and not the eye movement) target location. This perceptual compression was nearly constant in duration across gaze shift amplitudes, suggesting that the signal that triggers compression is largely independent of the size and kinematics of the gaze shift. The spatial pattern of results could be captured by a model that involves interactions, on a logarithmic map of visual space, between two loci of neural activity that encode the gaze shift vector and visual stimulus position relative to the fovea.


Subject(s)
Models, Neurological , Saccades/physiology , Space Perception/physiology , Superior Colliculi/physiology , Vision, Binocular/physiology , Animals , Biomechanical Phenomena/physiology , Fixation, Ocular/physiology , Fovea Centralis/physiology , Head , Humans , Immobilization/methods , Male , Photic Stimulation/methods , Primates , Psychomotor Performance/physiology
20.
J Neurophysiol ; 106(4): 1862-74, 2011 Oct.
Article in English | MEDLINE | ID: mdl-21753030

ABSTRACT

Our perception of the positions of objects in our surroundings is surprisingly unaffected by movements of the eyes, head, and body. This suggests that the brain has a mechanism for maintaining perceptual stability, based either on the spatial relationships among visible objects or internal copies of its own motor commands. Strong evidence for the latter mechanism comes from the remapping of visual receptive fields that occurs around the time of a saccade. Remapping occurs when a single neuron responds to visual stimuli placed presaccadically in the spatial location that will be occupied by its receptive field after the completion of a saccade. Although evidence for remapping has been found in many brain areas, relatively little is known about how it interacts with sensory context. This interaction is important for understanding perceptual stability more generally, as the brain may rely on extraretinal signals or visual signals to different degrees in different contexts. Here, we have studied the interaction between visual stimulation and remapping by recording from single neurons in the superior colliculus of the macaque monkey, using several different visual stimulus conditions. We find that remapping responses are highly sensitive to low-level visual signals, with the overall luminance of the visual background exerting a particularly powerful influence. Specifically, although remapping was fairly common in complete darkness, such responses were usually decreased or abolished in the presence of modest background illumination. Thus the brain might make use of a strategy that emphasizes visual landmarks over extraretinal signals whenever the former are available.


Subject(s)
Saccades/physiology , Space Perception/physiology , Superior Colliculi/physiology , Animals , Darkness , Fixation, Ocular , Light , Macaca mulatta , Male , Photic Stimulation , Psychomotor Performance/physiology , Visual Fields
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