Carol L. Colby

Updating of the visual representation in monkey striate and extrastriate cortex during saccades.

Neurons in the lateral intraparietal area, frontal eye field, and superior colliculus exhibit a pattern of activity known as remapping. When a salient visual stimulus is presented shortly before a saccade, the representation of that stimulus is updated, or remapped, at the time of the eye movement. This updating is presumably based on a corollary discharge of the eye movement command. To investigate whether visual areas also exhibit remapping, we recorded from single neurons in extrastriate and striate cortex while monkeys performed a saccade task. Around the time of the saccade, a visual stimulus was flashed either at the location occupied by the neurons receptive field (RF) before the saccade (old RF) or at the location occupied by it after the saccade (new RF). More than half (52%) of V3A neurons responded to a stimulus flashed in the new RF even though the stimulus had already disappeared before the saccade. These neurons responded to a trace of the flashed stimulus brought into the RF by the saccade. In 16% of V3A neurons, remapped activity began even before saccade onset. Remapping also was observed at earlier stages of the visual hierarchy, including in areas V3 and V2. At these earlier stages, the proportion of neurons that exhibited remapping decreased, and the latency of remapped activity increased relative to saccade onset. Remapping was very rare in striate cortex. These results indicate that extrastriate visual areas are involved in the process of remapping.

Action-Oriented Spatial Reference Frames in Cortex

Preparation of this review was supported by the National Science Foundation (IBN-9753013) and the James S. McDonnell Foundation (97-20). I thank M. E. Goldberg and M. Behrmann for comments on the manuscript.

Spatial updating in human parietal cortex.

Single neurons in monkey parietal cortex update visual information in conjunction with eye movements. This remapping of stimulus representations is thought to contribute to spatial constancy. We hypothesized that a similar process occurs in human parietal cortex and that we could visualize it with functional MRI. We scanned subjects during a task that involved remapping of visual signals across hemifields. We observed an initial response in the hemisphere contralateral to the visual stimulus, followed by a remapped response in the hemisphere ipsilateral to the stimulus. We ruled out the possibility that this remapped response resulted from either eye movements or visual stimuli alone. Our results demonstrate that updating of visual information occurs in human parietal cortex.

Cortical networks subserving pursuit and saccadic eye movements in humans: an FMRI study.

High‐field (3 Tesla) functional magnetic resonance imaging (MRI) was used to investigate the cortical circuitry subserving pursuit tracking in humans and compare it to that for saccadic eye movements. Pursuit performance, relative to visual fixation, elicited activation in three areas known to contribute to eye movements in humans and in nonhuman primates: the frontal eye field, supplementary eye field, and intraparietal sulcus. It also activated three medial regions not previously identified in human neuroimaging studies of pursuit: the precuneus and the anterior and posterior cingulate cortices. All six areas were also activated during saccades. The spatial extent of activation was similar for saccades and pursuit in all but two regions: spatial extent was greater for saccades in the superior branch of the frontal eye field and greater for pursuit in posterior cingulate cortex. This set of activations for smooth pursuit parallels the network of oculomotor areas characterized in nonhuman primates and complements recent studies showing that common cortical networks subserve oculomotor functions and spatial attention in humans. Hum. Brain Mapping 8:209–225, 1999.

Turning On and Off with Excitation: The Role of Spike-Timing Asynchrony and Synchrony in Sustained Neural Activity

Delay-related sustained activity in the prefrontal cortex of primates, a neurological analogue of working memory, has been proposed to arise from synaptic interactions in local cortical circuits. The implication is that memories are coded by spatially localized foci of sustained activity. We investigate the mechanisms by which sustained foci are initiated, maintained, and extinguished by excitation in networks of Hodgkin-Huxley neurons coupled with biophysical spatially structured synaptic connections. For networks with a balance between excitation and inhibition, a localized transient stimulus robustly initiates a localized focus of activity. The activity is then maintained by recurrent excitatory AMPA-like synapses. We find that to maintain the focus, the firing must be asynchronous. Consequently, inducing transient synchrony through an excitatory stimulus extinguishes the sustained activity. Such a monosynaptic excitatory turn-off mechanism is compatible with the working memory being wiped clean by an efferent copy of the motor command. The activity that codes working memories may be structured so that the motor command is both the read-out and a direct clearing signal. We show examples of data that is compatible with our theory.

Auditory and visual attention modulate motion processing in area MT

Behavioral and physiological studies have established that visual attention to a given feature or location can modulate early visual processing. In the present experiment, we asked whether auditory attention can likewise influence visual processing. We used a visual illusion, the motion aftereffect (MAE), to assess the effects of visual and auditory attention on motion processing in human area MT+. We acquired psychophysical and functional magnetic resonance imaging (fMRI) data while subjects fixated and viewed moving and stationary stimuli in alternating blocks. For each of four motion conditions, we measured the duration of the subsequent MAE, the time for activity in MT+ to return to baseline after motion adaptation (decay time), and the magnitude of MT+ activity during motion adaptation. For each subject, we first obtained measures of motion processing in the absence of attentional demands, by comparing reversing and expanding motion conditions. Subjects perceived the MAE following adaptation to expanding but not reversing motion, as observed previously, and decay times in MT+ were selectively prolonged after expanding motion. We then assessed the effects of performing either a visual or an auditory attentional task during expanding motion adaptation. Performance of the attentional task, whether visual or auditory, produced a significant reduction of subsequent MAE perception and associated decay times in MT+, as compared to expanding motion with fixation only. Both attentional tasks also reduced the magnitude of activation during motion adaptation. These data show that auditory attention, like visual attention, can modify sensory processing at a remarkably early stage of the visual hierarchy.

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.

Active Vision in Parietal and Extrastriate Cortex

Vision is an active process. We do not see the world directly; rather, we construct a representation of it from sensory inputs in combination with internal, nonvisual signals. In the case of spatial perception, our representation of the visual scene must take into account our own movements. This allows us to perceive the world as stationary despite the constant eye movements that produce new images on the retina. How is this perceptual stability achieved? Our central hypothesis is that a corollary discharge of the eye movement command updates, or remaps, an internal representation when the eyes move. In support of this hypothesis, the authors review evidence that parietal cortex and extrastriate visual areas in both monkeys and humans participate in spatial updating. These findings shed new light on the neural circuitry involved in producing a stable and coherent perception of visual space.

Attention and active vision.

Visual perception results from the interaction of incoming sensory signals and top down cognitive and motor signals. Here we focus on the representation of attended locations in parietal cortex and in earlier visual cortical areas. We review evidence that these spatial representations are modulated not only by selective attention but also by the intention to move the eyes. We describe recent experiments in monkey and human that elucidate the mechanisms and circuitry involved in updating, or remapping, the representations of salient stimuli. Two central ideas emerge. First, selective attention and remapping are closely intertwined, and together contribute to the percept of spatial stability. Second, remapping is accomplished not by a single area but by the participation of parietal, frontal and extrastriate cortex as well as subcortical structures. This neural circuitry is distinguished by significant redundancy and plasticity, suggesting that the updating of salient stimuli is fundamental for spatial stability and visuospatial behavior. We conclude that multiple processes and pathways contribute to active vision in the primate brain.

Shape selectivity and remapping in dorsal stream visual area LIP

We explore the visual world by making rapid eye movements (saccades) to focus on objects and locations of interest. Despite abrupt retinal image shifts, we see the world as stable. Remapping contributes to visual stability by updating the internal image with every saccade. Neurons in macaque lateral intraparietal cortex (LIP) and other brain areas update information about salient locations around the time of a saccade. The depth of information transfer remains to be thoroughly investigated. Area LIP, as part of the dorsal visual stream, is regarded as a spatially selective area, yet there is evidence that LIP neurons also encode object features. We sought to determine whether LIP remaps shape information. This knowledge is important for understanding what information is retained from each glance. We identified 82 remapping neurons. First, we presented shapes within the receptive field and tested for shape selectivity in a fixation task. Among the remapping neurons, 28 neurons (34%) were selective for shape. Second, we presented the same shapes in the future location of the receptive field around the time of the saccade and tested for shape selectivity during remapping. Thirty-one (38%) neurons were selective for shape. Of 11 neurons that were shape selective in both tasks, 5 showed significant correlation between shape selectivity in the two tasks. Across the population, there was a weak but significant correlation between responses to shape in the two tasks. Our results provide neurophysiological evidence that remapped responses in area LIP can encode shape information as well as spatial information.