Eye position effects on the remapped memory trace of visual motion in cortical area MST.
ABSTRACT: After a saccade, most MST neurons respond to moving visual stimuli that had existed in their post-saccadic receptive fields and turned off before the saccade ("trans-saccadic memory remapping"). Neuronal responses in higher visual processing areas are known to be modulated in relation to gaze angle to represent image location in spatiotopic coordinates. In the present study, we investigated the eye position effects after saccades and found that the gaze angle modulated the visual sensitivity of MST neurons after saccades both to the actually existing visual stimuli and to the visual memory traces remapped by the saccades. We suggest that two mechanisms, trans-saccadic memory remapping and gaze modulation, work cooperatively in individual MST neurons to represent a continuous visual world.
Project description:Perception of a stable visual world despite eye motion requires integration of visual information across saccadic eye movements. To investigate how the visual system deals with localization of moving visual stimuli across saccades, we observed spatiotemporal changes of receptive fields (RFs) of motion-sensitive neurons across periods of saccades in the middle temporal (MT) and medial superior temporal (MST) areas. We found that the location of the RFs moved with shifts of eye position due to saccades, indicating that motion-sensitive neurons in both areas have retinotopic RFs across saccades. Different characteristic responses emerged when the moving visual stimulus was turned off before the saccades. For MT neurons, virtually no response was observed after the saccade, suggesting that the responses of these neurons simply reflect the reafferent visual information. In contrast, most MST neurons increased their firing rates when a saccade brought the location of the visual stimulus into their RFs, where the visual stimulus itself no longer existed. These findings suggest that the responses of such MST neurons after saccades were evoked by a memory of the stimulus that had preexisted in the postsaccadic RFs ("memory remapping"). A delayed-saccade paradigm further revealed that memory remapping in MST was linked to the saccade itself, rather than to a shift in attention. Thus, the visual motion information across saccades was integrated in spatiotopic coordinates and represented in the activity of MST neurons. This is likely to contribute to the perception of a stable visual world in the presence of eye movements.
Project description:Eye movements create an ever-changing image of the world on the retina. In particular, frequent saccades call for a compensatory mechanism to transform the changing visual information into a stable percept. To this end, the brain presumably uses internal copies of motor commands. Electrophysiological recordings of visual neurons in the primate lateral intraparietal cortex, the frontal eye fields, and the superior colliculus suggest that the receptive fields (RFs) of special neurons shift towards their post-saccadic positions before the onset of a saccade. However, the perceptual consequences of these shifts remain controversial. We wanted to test in humans whether a remapping of motion adaptation occurs in visual perception.The motion aftereffect (MAE) occurs after viewing of a moving stimulus as an apparent movement to the opposite direction. We designed a saccade paradigm suitable for revealing pre-saccadic remapping of the MAE. Indeed, a transfer of motion adaptation from pre-saccadic to post-saccadic position could be observed when subjects prepared saccades. In the remapping condition, the strength of the MAE was comparable to the effect measured in a control condition (33±7% vs. 27±4%). Contrary, after a saccade or without saccade planning, the MAE was weak or absent when adaptation and test stimulus were located at different retinal locations, i.e. the effect was clearly retinotopic. Regarding visual cognition, our study reveals for the first time predictive remapping of the MAE but no spatiotopic transfer across saccades. Since the cortical sites involved in motion adaptation in primates are most likely the primary visual cortex and the middle temporal area (MT/V5) corresponding to human MT, our results suggest that pre-saccadic remapping extends to these areas, which have been associated with strict retinotopy and therefore with classical RF organization. The pre-saccadic transfer of visual features demonstrated here may be a crucial determinant for a stable percept despite saccades.
Project description:Saccades are rapid eye movements that change the direction of gaze, although the full-field image motion associated with these movements is rarely perceived. The attenuation of visual perception during saccades is referred to as saccadic suppression. The mechanisms that produce saccadic suppression are not well understood. We recorded from neurons in the dorsal medial superior temporal area (MSTd) of alert macaque monkeys and compared the neural responses produced by the retinal slip associated with saccades (active motion) to responses evoked by identical motion presented during fixation (passive motion). We provide evidence for a neural correlate of saccadic suppression and expand on two contentious results from previous studies. First, we confirm the finding that some neurons in MSTd reverse their preferred direction during saccades. We quantify this effect by calculating changes in direction tuning index for a large cell population. Second, it has been noted that neural activity associated with saccades can arrive in the parietal cortex <or=30 ms earlier than activity produced by similar visual stimulation during fixation. This led to the question of whether the saccade-related responses were visual in origin or were motor signals arising from saccade-planning areas of the brain. By comparing the responses to saccades made over textured backgrounds of different contrasts, we provide strong evidence that saccade-related responses were visual in origin. Refinements of the possible models of saccadic suppression are discussed.
Project description:When we explore a static visual scene, our eyes move in a sequence of fast eye movements called saccades, which are separated by fixation periods of relative eye stability. Based on uncertain sensory and cognitive inputs, the oculomotor system must decide, at every moment, whether to initiate a saccade or to remain in the fixation state. Even when we attempt to maintain our gaze on a small spot, small saccades, called microsaccades, intrude on fixation once or twice per second. Because microsaccades occur at the boundary of the decision to maintain fixation versus starting a saccade, they offer a unique opportunity to study the mechanisms that control saccadic triggering. Abnormal saccadic intrusions can occur during attempted fixation in patients with neurodegenerative disorders. We have implemented a model of the triggering mechanism of saccades, based on known anatomy and physiology, that successfully simulates the generation of saccades of any size-including microsaccades in healthy observers, and the saccadic intrusions that interrupt attempted fixation in parkinsonian patients. The model suggests that noisy neuronal activity in the superior colliculus controls the state of a mutually inhibitory network in the brain stem formed by burst neurons and omnipause neurons. When the neuronal activity is centered at the rostral pole, the system remains at a state of fixation. When activity is perturbed away from this center, a saccade is triggered. This perturbation can be produced either by the intent to move one's gaze or by random fluctuations in activity.
Project description:Spatial computations underlying the coordination of the hand and eye present formidable geometric challenges. One way for the nervous system to simplify these computations is to directly encode the relative position of the hand and the center of gaze. Neurons in the dorsal premotor cortex (PMd), which is critical for the guidance of arm-reaching movements, encode the relative position of the hand, gaze, and goal of reaching movements. This suggests that PMd can coordinate reaching movements with eye movements. Here, we examine saccade-related signals in PMd to determine whether they also point to a role for PMd in coordinating visual-motor behavior. We first compared the activity of a population of PMd neurons with a population of parietal reach region (PRR) neurons. During center-out reaching and saccade tasks, PMd neurons responded more strongly before saccades than PRR neurons, and PMd contained a larger proportion of exclusively saccade-tuned cells than PRR. During a saccade relative position-coding task, PMd neurons encoded saccade targets in a relative position code that depended on the relative position of gaze, the hand, and the goal of a saccadic eye movement. This relative position code for saccades is similar to the way that PMd neurons encode reach targets. We propose that eye movement and eye position signals in PMd do not drive eye movements, but rather provide spatial information that links the control of eye and arm movements to support coordinated visual-motor behavior.
Project description:Humans typically make several saccades per second. This provides a challenge for the visual system as locations are largely coded in retinotopic (eye-centered) coordinates. Spatial remapping, the updating of retinotopic location coordinates of items in visuospatial memory, is typically assumed to be limited to robust, capacity-limited and attention-demanding working memory (WM). Are pre-attentive, maskable, sensory memory representations (e.g. fragile memory, FM) also remapped? We directly compared trans-saccadic WM (tWM) and trans-saccadic FM (tFM) in a retro-cue change-detection paradigm. Participants memorized oriented rectangles, made a saccade and reported whether they saw a change in a subsequent display. On some trials a retro-cue indicated the to-be-tested item prior to probe onset. This allowed sensory memory items to be included in the memory capacity estimate. The observed retro-cue benefit demonstrates a tFM capacity considerably above tWM. This provides evidence that some, if not all sensory memory was remapped to spatiotopic (world-centered, task-relevant) coordinates. In a second experiment, we show backward masks to be effective in retinotopic as well as spatiotopic coordinates, demonstrating that FM was indeed remapped to world-centered coordinates. Together this provides conclusive evidence that trans-saccadic spatial remapping is not limited to higher-level WM processes but also occurs for sensory memory representations.
Project description:In the oculomotor system, spatial updating is the ability to aim a saccade toward a remembered visual target position despite intervening eye movements. Although this has been the subject of extensive experimental investigation, there is still no unifying theoretical framework to explain the neural mechanism for this phenomenon, and how it influences visual signals in the brain. Here, we propose a unified state-space model (SSM) to account for the dynamics of spatial updating during two types of eye movement; saccades and smooth pursuit. Our proposed model is a non-linear SSM and implemented through a recurrent radial-basis-function neural network in a dual Extended Kalman filter (EKF) structure. The model parameters and internal states (remembered target position) are estimated sequentially using the EKF method. The proposed model replicates two fundamental experimental observations: continuous gaze-centered updating of visual memory-related activity during smooth pursuit, and predictive remapping of visual memory activity before and during saccades. Moreover, our model makes the new prediction that, when uncertainty of input signals is incorporated in the model, neural population activity and receptive fields expand just before and during saccades. These results suggest that visual remapping and motor updating are part of a common visuomotor mechanism, and that subjective perceptual constancy arises in part from training the visual system on motor tasks.
Project description:Saccadic eye movements occur in sequences, gathering new information about the visual environment to support successful task completion. Here, we examine the control of these saccadic sequences and specifically the extent to which the spatial aspects of the saccadic responses are programmed in parallel. We asked participants to saccade to a series of visual targets and, while they shifted their gaze around the display, we displaced select targets. We found that saccade landing position was deviated toward the previous location of the target suggesting that partial parallel programming of target location information was occurring. The saccade landing position was also affected by the new target location, which demonstrates that the saccade landing position was also partially updated following the shift. This pattern was present even for targets that were the subject of the next fixation. Having a greater preview about the sequence path influenced saccade accuracy with saccades being less affected by relocations when there is less preview information. The results demonstrate that landing positions from a saccade sequence are programmed in parallel and combined with more immediate visual signals.
Project description:We experience a visually stable world despite frequent retinal image displacements induced by eye, head, and body movements. The neural mechanisms underlying this remain unclear. One mechanism that may contribute is transsaccadic remapping, in which the responses of some neurons in various attentional, oculomotor, and visual brain areas appear to anticipate the consequences of saccades. The functional role of transsaccadic remapping is actively debated, and many of its key properties remain unknown. Here, recording from two monkeys trained to make a saccade while directing attention to one of two spatial locations, we show that neurons in the middle temporal area (MT), a key locus in the motion-processing pathway of humans and macaques, show a form of transsaccadic remapping called a memory trace. The memory trace in MT neurons is enhanced by the allocation of top-down spatial attention. Our data provide the first demonstration, to our knowledge, of the influence of top-down attention on the memory trace anywhere in the brain. We find evidence only for a small and transient effect of motion direction on the memory trace (and in only one of two monkeys), arguing against a role for MT in the theoretically critical yet empirically contentious phenomenon of spatiotopic feature-comparison and adaptation transfer across saccades. Our data support the hypothesis that transsaccadic remapping represents the shift of attentional pointers in a retinotopic map, so that relevant locations can be tracked and rapidly processed across saccades. Our results resolve important issues concerning the perisaccadic representation of visual stimuli in the dorsal stream and demonstrate a significant role for top-down attention in modulating this representation.
Project description:Each saccade shifts the projections of the visual scene on the retina. It has been proposed that the receptive fields of neurons in oculomotor areas are predictively remapped to account for these shifts. While remapping of the whole visual scene seems prohibitively complex, selection by attention may limit these processes to a subset of attended locations. Because attentional selection consumes time, remapping of attended locations should evolve in time, too. In our study, we cued a spatial location by presenting an attention-capturing cue at different times before a saccade and constructed maps of attentional allocation across the visual field. We observed no remapping of attention when the cue appeared shortly before saccade. In contrast, when the cue appeared sufficiently early before saccade, attentional resources were reallocated precisely to the remapped location. Our results show that pre-saccadic remapping takes time to develop suggesting that it relies on the spatial and temporal dynamics of spatial attention.