Remapping for visual stability

Visual perception is based on both incoming sensory signals and information about ongoing actions. Recordings from single neurons have shown that corollary discharge signals can influence visual representations in parietal, frontal and extrastriate visual cortex, as well as the superior colliculus (SC). In each of these areas, visual representations are remapped in conjunction with eye movements. Remapping provides a mechanism for creating a stable, eye-centred map of salient locations. Temporal and spatial aspects of remapping are highly variable from cell to cell and area to area. Most neurons in the lateral intraparietal area remap stimulus traces, as do many neurons in closely allied areas such as the frontal eye fields the SC and extrastriate area V3A. Remapping is not purely a cortical phenomenon. Stimulus traces are remapped from one hemifield to the other even when direct cortico-cortical connections are removed. The neural circuitry that produces remapping is distinguished by significant plasticity, suggesting that updating of salient stimuli is fundamental for spatial stability and visuospatial behaviour. These findings provide new evidence that a unified and stable representation of visual space is constructed by redundant circuitry, comprising cortical and subcortical pathways, with a remarkable capacity for reorganization.     

Right-hemispheric dominance for visual remapping in humans

We review evidence showing a right-hemispheric dominance for visuo-spatial processing and representation in humans. Accordingly, visual disorganization symptoms (intuitively related to remapping impairments) are observed in both neglect and constructional apraxia. More specifically, we review findings from the intervening saccade paradigm in humans--and present additional original data--which suggest a specific role of the asymmetrical network at the temporo-parietal junction (TPJ) in the right hemisphere in visual remapping: following damage to the right dorsal posterior parietal cortex (PPC) as well as part of the corpus callosum connecting the PPC to the frontal lobes, patient OK in a double-step saccadic task exhibited an impairment when the second saccade had to be directed rightward. This singular and lateralized deficit cannot result solely from the patient's cortical lesion and, therefore, we propose that it is due to his callosal lesion that may specifically interrupt the interhemispheric transfer of information necessary to execute accurate rightward saccades towards a remapped target location. This suggests a specialized right-hemispheric network for visuo-spatial remapping that subsequently transfers target location information to downstream planning regions, which are symmetrically organized.     

Visual stability and the motion aftereffect: a psychophysical study revealing spatial updating

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.     

The Effects of Visual Control and Distance in Modulating Peripersonal Spatial Representation

In the presence of vision, finalized motor acts can trigger spatial remapping, i.e., reference frames transformations to allow for a better interaction with targets. However, it is yet unclear how the peripersonal space is encoded and remapped depending on the availability of visual feedback and on the target position within the individual’s reachable space, and which cerebral areas subserve such processes. Here, functional magnetic resonance imaging (fMRI) was used to examine neural activity while healthy young participants performed reach-to-grasp movements with and without visual feedback and at different distances of the target from the effector (near to the hand–about 15 cm from the starting position–vs. far from the hand–about 30 cm from the starting position). Brain response in the superior parietal lobule bilaterally, in the right dorsal premotor cortex, and in the anterior part of the right inferior parietal lobule was significantly greater during visually-guided grasping of targets located at the far distance compared to grasping of targets located near to the hand. In the absence of visual feedback, the inferior parietal lobule exhibited a greater activity during grasping of targets at the near compared to the far distance. Results suggest that in the presence of visual feedback, a visuo-motor circuit integrates visuo-motor information when targets are located farther away. Conversely in the absence of visual feedback, encoding of space may demand multisensory remapping processes, even in the case of more proximal targets.     

Sensory and behavioral properties of neurons in posterior parietal cortex of the awake, trained monkey.

Neurons in posterior parietal cortex of the awake, trained monkey respond to passive visual and/or somatosensory stimuli. In general, the receptive fields of these cells are large and nonspecific. When these neurons are studied during visually guided hand movements and eye movements, most of their activity can be accounted for by passive sensory stimulation. However, for some visual cells, the response to a stimulus is enhanced when it is to be the target for a saccadic eye movement. This enhancement is selective for eye movements into the visual receptive field since it does not occur with eye movements to other parts of the visual field. Cells that discharge in association with a visual fixation task have foveal receptive fields and respond to the spots of light used as fixation targets. Cells discharging selectively in association with different directions of tracking eye movements have directionally selective responses to moving visual stimuli. Every cell in our sample discharging in association with movement could be driven by passive sensory stimuli. We conclude that the activity of neurons in posterior parietal cortex is dependent on and indicative of external stimuli but not predictive of movement.     

Human parietal cortex in action

Experiments using functional neuroimaging and transcranial magnetic stimulation in humans have revealed regions of the parietal lobes that are specialized for particular visuomotor actions, such as reaching, grasping and eye movements. In addition, the human parietal cortex is recruited by processing and perception of action-related information, even when no overt action occurs. Such information can include object shape and orientation, knowledge about how tools are employed and the understanding of actions made by other individuals. We review the known subregions of the human posterior parietal cortex and the principles behind their organization.     

Reduced variability of ongoing and evoked cortical activity leads to improved behavioral performance

Sensory responses of the brain are known to be highly variable, but the origin and functional relevance of this variability have long remained enigmatic. Using the variable foreperiod of a visual discrimination task to assess variability in the primate cerebral cortex, we report that visual evoked response variability is not only tied to variability in ongoing cortical activity, but also predicts mean response time. We used cortical local field potentials, simultaneously recorded from widespread cortical areas, to gauge both ongoing and visually evoked activity. Trial-to-trial variability of sensory evoked responses was strongly modulated by foreperiod duration and correlated both with the cortical variability before stimulus onset as well as with response times. In a separate set of experiments we probed the relation between small saccadic eye movements, foreperiod duration and manual response times. The rate of eye movements was modulated by foreperiod duration and eye position variability was positively correlated with response times. Our results indicate that when the time of a sensory stimulus is predictable, reduction in cortical variability before the stimulus can improve normal behavioral function that depends on the stimulus.     

From visual affordances in monkey parietal cortex to hippocampo-parietal interactions underlying rat navigation.

This paper explores the hypothesis that various subregions (but by no means all) of the posterior parietal cortex are specialized to process visual information to extract a variety of affordances for behaviour. Two biologically based models of regions of the posterior parietal cortex of the monkey are introduced. The model of the lateral intraparietal area (LIP) emphasizes its roles in dynamic remapping of the representation of targets during a double saccade task, and in combining stored, updated input with current visual input. The model of the anterior intraparietal area (AIP) addresses parietal-premotor interactions involved in grasping, and analyses the interaction between the AIP and premotor area F5. The model represents the role of other intraparietal areas working in concert with the inferotemporal cortex as well as with corollary discharge from F5 to provide and augment the affordance information in the AIP, and suggests how various constraints may resolve the action opportunities provided by multiple affordances. Finally, a systems-level model of hippocampo parietal interactions underlying rat navigation is developed, motivated by the monkey data used in developing the above two models as well as by data on neurones in the posterior parietal cortex of the monkey that are sensitive to visual motion. The formal similarity between dynamic remapping (primate saccades) and path integration (rat navigation) is noted, and certain available data on rat posterior parietal cortex in terms of affordances for locomotion are explained. The utility of further modelling, linking the World Graph model of cognitive maps for motivated behaviour with hippocampal-parietal interactions involved in navigation, is also suggested. These models demonstrate that posterior parietal cortex is not only itself a network of interacting subsystems, but functions through cooperative computation with many other brain regions.     

A neural computation for visual acuity in the presence of eye movements

Humans can distinguish visual stimuli that differ by features the size of only a few photoreceptors. This is possible despite the incessant image motion due to fixational eye movements, which can be many times larger than the features to be distinguished. To perform well, the brain must identify the retinal firing patterns induced by the stimulus while discounting similar patterns caused by spontaneous retinal activity. This is a challenge since the trajectory of the eye movements, and consequently, the stimulus position, are unknown. We derive a decision rule for using retinal spike trains to discriminate between two stimuli, given that their retinal image moves with an unknown random walk trajectory. This algorithm dynamically estimates the probability of the stimulus at different retinal locations, and uses this to modulate the influence of retinal spikes acquired later. Applied to a simple orientation-discrimination task, the algorithm performance is consistent with human acuity, whereas naive strategies that neglect eye movements perform much worse. We then show how a simple, biologically plausible neural network could implement this algorithm using a local, activity-dependent gain and lateral interactions approximately matched to the statistics of eye movements. Finally, we discuss evidence that such a network could be operating in the primary visual cortex.     

Visual attention and stability

In the present review, we address the relationship between attention and visual stability. Even though with each eye, head and body movement the retinal image changes dramatically, we perceive the world as stable and are able to perform visually guided actions. However, visual stability is not as complete as introspection would lead us to believe. We attend to only a few items at a time and stability is maintained only for those items. There appear to be two distinct mechanisms underlying visual stability. The first is a passive mechanism: the visual system assumes the world to be stable, unless there is a clear discrepancy between the pre- and post-saccadic image of the region surrounding the saccade target. This is related to the pre-saccadic shift of attention, which allows for an accurate preview of the saccade target. The second is an active mechanism: information about attended objects is remapped within retinotopic maps to compensate for eye movements. The locus of attention itself, which is also characterized by localized retinotopic activity, is remapped as well. We conclude that visual attention is crucial in our perception of a stable world.     

Perisaccadic Remapping and Rescaling of Visual Responses in Macaque Superior Colliculus

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.     

Perisaccadic mislocalization orthogonal to saccade direction

Saccadic eye movements transiently distort perceptual space. Visual objects flashed shortly before or during a saccade are mislocalized along the saccade direction, resembling a compression of space around the saccade target. These mislocalizations reflect transient errors of processes that construct spatial stability across eye movements. They may arise from errors of reference signals associated with saccade direction and amplitude or from visual or visuomotor remapping processes focused on the saccade target's position. The second case would predict apparent position shifts toward the target also in directions orthogonal to the saccade. We report that such orthogonal mislocalization indeed occurs. Surprisingly, however, the orthogonal mislocalization is restricted to only part of the visual field. This part comprises distant positions in saccade direction but does not depend on the target's position. Our findings can be explained by a combination of directional and positional reference signals that varies in time course across the visual field.     

Evidence for the lateral intraparietal area as the parietal eye field.

It has long been appreciated that the posterior parietal cortex plays a role in the processing of saccadic eye movements. Only recently has it been discovered that a small cortical area, the lateral intraparietal area, within this much larger area appears to be specialized for saccadic eye movements. Unlike other cortical areas in the posterior parietal cortex, the lateral intraparietal area has strong anatomical connections to other saccade centers, and its cells have saccade-related responses that begin before the saccades. The lateral intraparietal area appears to be neither a strictly visual nor strictly motor structure; rather it performs visuomotor integration functions including determining the spatial location of saccade targets and forming plans to make eye movements.     

Proprioceptive alignment of visual and somatosensory maps in the posterior parietal cortex

A touch on one hand can enhance the response to a visual stimulus delivered at a nearby location [1, 2], improving our interactions with the external world. In order to keep such visual-tactile spatial interactions effective, the brain updates the continuous postural changes, like those typically accompanying hand actions, through proprioception, thus maintaining the somatosensory and visual maps in spatial register [2, 3]. The posterior parietal cortex (PPC) might be critical for such a spatial remapping [4]; nevertheless, a direct causal demonstration of its involvement is lacking. Here, we found that unattended touches to one hand enhanced visual sensitivity for phosphenes induced by occipital trancranial magnetic stimulation (TMS) [5] when the touched hand was spatially coincident to the reported location of the phosphenes in external space. Notably, this spatially specific crossmodal facilitation was maintained after hand crossing, suggesting an efficient visual-tactile remapping. Critically, after 1 Hz repetitive TMS interference [6] over the PPC, but not over the primary somatosensory cortex, phosphene detection was still enhanced by spatially coincident touches with uncrossed hands, but it was enhanced by spatially noncoincident touches after hand crossing. This is the first causal evidence in humans that the PPC constantly updates the representation of the body in space in order to facilitate crossmodal interactions.     

Effects of Attention to Auditory Motion on Cortical Activations during Smooth Pursuit Eye Tracking

Background

In contrast to traditional views that consider smooth pursuit as a relatively automatic process, evidence has been reported for the importance of attention for accurate pursuit performance. However, the exact role that attention might play in the maintenance of pursuit remains unclear.

Methodology/Principal Findings

We analysed the neuronal activity associated with healthy subjects executing smooth pursuit eye movements (SPEM) during concurrent attentive tracking of a moving sound source, which was either in-phase or in antiphase to the executed eye movements. Assuming that attentional resources must be allocated to the moving sound source, the simultaneous execution of SPEM and auditory tracking in diverging directions should result in increased load on common attentional resources. By using an auditory stimulus as a distractor rather then a visual stimulus we guaranteed that cortical activity cannot be caused by conflicts between two simultaneous visual motion stimuli. Our results revealed that the smooth pursuit task with divided attention led to significantly higher activations bilaterally in the posterior parietal cortex and lateral and medial frontal cortex, presumably containing the parietal, frontal and supplementary eye fields respectively.

Conclusions

The additional cortical activation in these areas is apparently due to the process of dividing attention between the execution of SPEM and the covert tracking of the auditory target. On the other hand, even though attention had to be divided the attentional resources did not seem to be exhausted, since the identification of the direction of the auditory target and the quality of SPEM were unaffected by the congruence between visual and auditory motion stimuli. Finally, we found that this form of task-related attention modulated not only the cortical pursuit network in general but also affected modality specific and supramodal attention regions.     

The effects of simulated microgravity on characteristics of slow presaccadic potentials

The parameters of saccades and presaccadic slow potentials were studied in seven right-handed male volunteers with a dominant right eye before and after exposure to 6-day dry immersion. Visual stimuli were presented using three light diodes, which were located in the center of the visual field (the central fixation stimulus) and 10° to the right and left of it (peripheral stimuli (PSs)). The subjects performed a test with simple saccades to a PS and a test with antisaccades to the point located symmetrically in the opposite visual field. The EEG (19 monopolar leads) and electrooculogram were recorded. To isolate slow potentials, backward EEG averaging was performed, with the moment of switching on the PS serving as a trigger for the averaging. It was found that the characteristics of saccadic eye movements did not substantially change after exposure to immersion. However, both tests revealed a change in topography and a decrease in the amplitude of presaccadic slow negative potentials (PSNPs) during immersion. Characteristically, the focus of presaccadic negativity shifted to the right hemisphere so that the PSNP amplitude sharply decreased in the left and increased in the right hemisphere. A significant decrease in the PSNP amplitude on day 6 of immersion was found in the midline and left-hemispheric frontal and parietal leads. It may be suggested that, because of support unloading and a decrease in proprioceptive input, exposure to microgravity causes a decrease in the activity of the left hemisphere and prefrontal and parietal cortices, initially involved in preparation and realization of motor responses. The activation of the right hemisphere could be of compensatory character.     

The Role of the Caudal Superior Parietal Lobule in Updating Hand Location in Peripheral Vision: Further Evidence from Optic Ataxia

Patients with optic ataxia (OA), who are missing the caudal portion of their superior parietal lobule (SPL), have difficulty performing visually-guided reaches towards extra-foveal targets. Such gaze and hand decoupling also occurs in commonly performed non-standard visuomotor transformations such as the use of a computer mouse. In this study, we test two unilateral OA patients in conditions of 1) a change in the physical location of the visual stimulus relative to the plane of the limb movement, 2) a cue that signals a required limb movement 180° opposite to the cued visual target location, or 3) both of these situations combined. In these non-standard visuomotor transformations, the OA deficit is not observed as the well-documented field-dependent misreach. Instead, OA patients make additional eye movements to update hand and goal location during motor execution in order to complete these slow movements. Overall, the OA patients struggled when having to guide centrifugal movements in peripheral vision, even when they were instructed from visual stimuli that could be foveated. We propose that an intact caudal SPL is crucial for any visuomotor control that involves updating ongoing hand location in space without foveating it, i.e. from peripheral vision, proprioceptive or predictive information.     

A new visual area on the inferior wall of the cat cruciate sulcus

Properties of 187 neurons in the inferior wall of the cruciate sulcus, in an area where electrical stimulation evoked unidirectional saccadic eye movements, were investigated in waking cats. Of the total number 172 responded to visual stimulation. Neurons in the surface layers of the cortex responded to simple visual stimuli: light or dark spots or bars, both stationary and moving at speeds of around 30 deg/sec. These neurons showed no selectivity as regards stimulus orientation but sometimes behaved selectively toward the direction of their movements. In the intermediate layers the maximal neuronal response was obtained to a model of a bird flaping its wings. Neuronal responses in the depth of the cortex were characterized by selectivity to movement of stimuli toward or away from the animal in a certain part of the visual field, irrespective of whether a light stimulus was presented against a dark background or a dark stimulus against the light background. Responses to visual stimulation were exhibited only if the animal was in a state of activation, when the EEG showed desynchronization, and they were absent in a state of quite wakefulness. No responses were obtained to auditory or somatic stimulation. Responses to visual stimulation were not found in neurons of the medial wall of the brain beneath the cruciate sulcus, but responses were recorded to eye movements of definite size or orientation. It is postulated that at least two contiguous retinotopically organized zones exist in this part of the brain. Activity of one of them is connected with visual function, that of the other with eye movements.Institute for Problems in Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 16, No. 6, pp. 766–773, November–December, 1984.     

The role of the posterior parietal cortex in coordinate transformations for visual-motor integration

Lesion to the posterior parietal cortex in monkeys and humans produces spatial deficits in movement and perception. In recording experiments from area 7a, a cortical subdivision in the posterior parietal cortex in monkeys, we have found neurons whose responses are a function of both the retinal location of visual stimuli and the position of the eyes in the orbits. By combining these signals area 7 a neurons code the location of visual stimuli with respect to the head. However, these cells respond over only limited ranges of eye positions (eye-position-dependent coding). To code location in craniotopic space at all eye positions (eye-position-independent coding) an additional step in neural processing is required that uses information distributed across populations of area 7a neurons. We describe here a neural network model, based on back-propagation learning, that both demonstrates how spatial location could be derived from the population response of area 7a neurons and accurately accounts for the observed response properties of these neurons.     

A deficit in covert attention after parietal cortex inactivation in the monkey

Although the parietal cortex has been repeatedly implicated in controlling attention, the nature and importance of this contribution remain unclear. Here we show that inactivating the lateral intraparietal area in monkeys delays the detection of a visual target located in the contralateral visual field. This effect was observed using different visual scene configurations, e.g., with distractors that differ in number or that differ from the target by a conjunction of shape and color or by a single feature. Since eye movements were not allowed during the searching tasks, these results argue for an unambiguous role of the parietal cortex in the top-down control of attentional deployment in space.