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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.

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., Competing Interests: The authors declare no competing interest.

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., Competing Interests: The authors declare no conflict of interest.

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., (Copyright © 2016 the authors 0270-6474/16/369227-13$15.00/0.)

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.

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., (© The Author (2015). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: journals.permissions@oup.com.)

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., (Copyright © 2015 Elsevier Inc. All rights reserved.)

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., (Copyright © 2014 Elsevier Ltd. All rights reserved.)

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., (Copyright © 2012 Elsevier Ltd. All rights reserved.)

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.

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.

Individuals who have undergone hemispherectomy for treatment of intractable epilepsy offer a rare and valuable opportunity to examine the ability of a single cortical hemisphere to control oculomotor performance. We used peripheral auditory events to trigger saccades, thereby circumventing dense postsurgical hemianopia. In an antisaccade task, patients generated numerous unintended short-latency saccades toward contralesional auditory events, indicating pronounced limitations in the ability of a single hemicortex to exert normal inhibitory control over ipsilateral (i.e., contralesional) reflexive saccade generation. Despite reflexive errors, patients retained an ability to generate correct antisaccades in both directions. The prosaccade task revealed numerous contralesional express saccades, a robust contralesional gap effect, but the absence of both effects for ipsilesional saccades. These results indicate limits to the saccadic control capabilities following hemispherectomy: A single hemicortex can mediate antisaccades in both directions, but plasticity does not extend fully to the bilateral inhibition of reflexive saccades. We posit that these effects are due to altered control dynamics that reduce the responsivity of the superior colliculus on the intact side and facilitate the release of an auditory-evoked ocular grasp reflex into the blind hemifield that the intact hemicortex has difficulty suppressing.

Our ability to explore our surroundings requires a combination of high-resolution vision and frequent rotations of the visual axis toward objects of interest. Such gaze shifts are themselves a source of powerful retinal stimulation, and so the visual system appears to have evolved mechanisms to maintain perceptual stability during movements of the eyes in space. The mechanisms underlying this perceptual stability can be probed in the laboratory by briefly presenting a stimulus around the time of a saccadic eye movement and asking subjects to report its position. Under such conditions, there is a systematic misperception of the probes toward the saccade end point. This perisaccadic compression of visual space has been the subject of much research, but few studies have attempted to relate it to specific brain mechanisms. Here, we show that the magnitude of perceptual compression for a wide variety of probe stimuli and saccade amplitudes is quantitatively predicted by a simple heuristic model based on the geometry of retinotopic representations in the primate brain. Specifically, we propose that perisaccadic compression is determined by the distance between the probe and saccade end point on a map that has a logarithmic representation of visual space, similar to those found in numerous cortical and subcortical visual structures. Under this assumption, the psychophysical data on perisaccadic compression can be appreciated intuitively by imagining that, around the time of a saccade, the brain confounds nearby oculomotor and sensory signals while attempting to localize the position of objects in visual space.

In three patients who had one cortical hemisphere removed surgically (hemidecortication), we studied visually-triggered saccades directed contralateral to the intact cortical hemisphere (i.e., ipsilesional saccades). Both saccade reaction times (SRTs) and accuracy of these saccades have been reported as abnormal in hemidecorticate patients, but not monkeys. One explanation for this difference is that deficits in hemidecorticate patients may not have been directly caused by removal of cortical oculomotor structures themselves, but may have been a manifestation of compensatory strategies used to cope with contralesional hemianopia. We hypothesized that deficits in saccade performance to the ipsilesional (seeing) visual hemifield would be directly linked to how easily patients could localize targets in their blind hemifield with searching saccades. To test this hypothesis, we examined how deficits in our patients varied when targets were: (1) randomly presented to either the seeing or blind hemifield for long durations thereby permitting searching saccades in the blind hemifield; (2) presented as in Experiment 1, but briefly flashed thereby removing visual feedback prior to saccade onset thereby rendering searching saccades useless; (3) briefly flashed as in Experiment 2, but at random locations in only the seeing hemifield (blind hemifield irrelevant). Mean SRTs to the seeing hemifield were 165 ms longer than normal in Experiment 2, but only about 40 ms longer in Experiments 1 and 3. Saccade accuracy was characterized by task-dependent hypometria in all three experiments with a mean undershoot of about twice the amplitude variance. The largest undershoots were in Experiments 2 and 3. Our data suggest that deficits resulted from the direct effects of the lesions themselves coupled with context-dependent strategies used to cope with contralesional hemianopia.

Anatomical, electrophysiological and lesion studies indicate that each cortical hemisphere normally generates saccades directed to the contralateral side. In contrast, in patients who had an entire cortical hemisphere removed surgically (hemidecortication), the remaining hemicortex can generate both contraversive and ipsiversive saccades. However, current evidence indicates that ipsiversive saccades are grossly inaccurate. The obvious reason for this is that hemidecorticate patients are blind in the hemifield ipsilateral to the remaining hemicortex, and therefore normal visual signals are not available to drive ipsiversive saccades. However, absent vision also implies that visual error signals are not available to calibrate ipsiversive movements. Furthermore, the innate anatomical substrate needed to support accurate ipsiversive saccade control, in addition to the normal contraversive control, appears sparse. We show here that, in spite of these obstacles, hemidecorticate patients could generate accurate ipsiversive saccades in a task that dissociated hemianopia from saccade direction. In this task, while the patients fixated a central fixation target (FT), saccade targets (STs) were briefly presented to the intact visual hemifield contralateral to the intact hemicortex. The FT was then moved towards and beyond the former location of the ST which evoked tracking eye movements that moved the eyes towards and then beyond the ST, thereby moving the goal, ST, into the blind visual hemifield ipsilateral to the intact hemicortex. When the FT was extinguished, the patients generated, in the dark, ipsiversive saccades that moved their eyes to the remembered location of the ST with the same accuracy as normal control subjects. This indicates that a single hemicortex can mediate accurate bidirectional saccade control via fully functional bilateral connections from cortex to brainstem oculomotor structures. The mechanisms whereby visual signals can calibrate ipsiversive saccades remain elusive.

Rapid coordinated eye-head movements, called saccadic gaze shifts, displace the line of sight from one location to another. A critical structure in the gaze control circuitry is the superior colliculus (SC) of the midbrain, which drives gaze saccades by relaying cortical commands to brainstem eye and head motor circuits. We proposed that the SC lies within a gaze feedback loop and generates an error signal specifying gaze position error (GPE), the distance between target and current gaze positions. We investigated this feedback hypothesis in cats by briefly stopping head motion during large ( approximately 50 degrees ) gaze saccades made in the dark. This maneuver interrupted intended gaze saccades and briefly immobilized gaze (a plateau). After brake release, a corrective gaze saccade brought the gaze on goal. In the caudal SC, the firing frequency of a cell gradually increased to a maximum that just preceded the optimal gaze saccade encoded by the position of the cell and then declined back to zero near gaze saccade end. In brake trials, the activity level just preceding a brake-induced plateau continued steadily during the plateau and waned to zero only near the end of the corrective saccade. The duration of neural activity was stretched to reflect the increased time to target acquisition, and firing frequency during a plateau was proportional to the GPE of the plateau. In comparison, in the rostral SC, the duration of saccade-related pauses in fixation cell activity increased as plateau duration increased. The data show that the cat's SC lies in a gaze feedback loop and that it encodes GPE.

The superior colliculus (SC) is important for generating coordinated eye-head gaze saccades. Its deeper layers contain a retinotopically organized motor map in which each site is thought to encode a specific gaze saccade vector. Here we show that this fundamental assumption in current models of collicular function does not hold true during horizontal multi-step gaze shifts in darkness that are directed to a goal and composed of a sequence of gaze saccades separated by periods of steady fixation. At the start of a multi-step gaze shift in cats, neural activity on the SC's map was located caudally to encode the overall amplitude of the gaze displacement, not the first saccade in the sequence. As the gaze shift progressed, the locus of activity moved to encode the error between the goal and the current gaze position. Contrary to common belief, the locus of activity never encoded gaze saccade amplitude, except for the last saccade in the sequence.

The superior colliculus (SC), via its projections to the pons, is a critical structure for driving rapid orienting movements of the visual axis, called gaze saccades, composed of coordinated eye-head movements. The SC contains a motor map that encodes small saccade vectors rostrally and large ones caudally. A zone in the rostral pole may have a different function. It contains superior colliculus fixation neurons (SCFNs) with probable projections to omnipause neurons (OPNs) of the pons. SCFNs and OPNs discharge tonically during visual fixation and pause during single-step gaze saccades. The OPN tonic discharge inhibits saccades and its cessation (pause) permits saccade generation. We have proposed that SCFNs control the OPN discharge. We compared the discharges of SCFNs and OPNs recorded while cats oriented horizontally, to the left and right, in the dark to a remembered target. Cats used multiple-step gaze shifts composed of a series of small gaze saccades, of variable amplitude and number, separated by periods of variable duration (plateaus) in which gaze was immobile or moving at low velocity (<25 degrees /s). Just after contralaterally (ipsilaterally) presented targets, the firing frequency of SCFNs decreased to almost zero (remained constant at background). As multiple-step gaze shifts progressed in either direction in the dark, these activity levels prevailed until the distance between gaze and target [gaze position error (GPE)] reached approximately 16 degrees. At this point, firing frequency gradually increased, without saccade-related pauses, until a maximum was reached when gaze arrived on target location (GPE = 0 degrees). SCFN firing frequency encoded GPE; activity was not correlated to characteristics or occurrence of gaze saccades. By comparison, after target presentation to left or right, OPN activity remained steady at pretarget background until first gaze saccade onset, during which activity paused. During the first plateau, activity resumed at a level lower than background and continued at this level during subsequent plateaus until GPE approximately 8 degrees was reached. As GPE decreased further, tonic activity during plateaus gradually increased until a maximum (greater than background) was reached when gaze was on goal (GPE = 0 degrees). OPNs, like SCFNs, encoded GPE, but they paused during every gaze saccade, thereby revealing, unlike for SCFNs, strong coupling to motor events. The firing frequency increase in SCFNs as GPE decreased, irrespective of trajectory characteristics, implies these cells get feedback on GPE, which they may communicate to OPNs. We hypothesize that at the end of a gaze-step sequence, impulses from SCFNs onto OPNs may suppress further movements away from the target.