Eye movement preparation modulates neuronal responses in area V4 when dissociated from attentional demands.
ABSTRACT: We examined whether the preparation of saccadic eye movements, when behaviorally dissociated from covert attention, modulates activity within visual cortex. We measured single-neuron and local field potential (LFP) responses to visual stimuli in area V4 while monkeys covertly attended a stimulus at one location and prepared saccades to a potential target at another. In spite of the irrelevance of visual information at the saccade target, visual activity at that location was modulated at least as much as, and often more than, activity at the covertly attended location. Modulations of activity at the attended and saccade target locations were qualitatively similar and included increased response magnitude, stimulus selectivity, and spiking reliability, as well as increased gamma and decreased low-frequency power of LFPs. These results demonstrate that saccade preparation is sufficient to modulate visual cortical representations and suggest that the interrelationship of oculomotor and attention-related mechanisms extends to posterior visual cortex.
Project description:Neurons in sensory areas of the neocortex are known to represent information both about sensory stimuli and behavioral state, but how these 2 disparate signals are integrated across cortical layers is poorly understood. To study this issue, we measured the coding of visual stimulus orientation and of behavioral state by neurons within superficial and deep layers of area V4 in monkeys while they covertly attended or prepared eye movements to visual stimuli. We show that whereas single neurons and neuronal populations in the superficial layers conveyed more information about the orientation of visual stimuli than neurons in deep layers, the opposite was true of information about the behavioral relevance of those stimuli. In particular, deep layer neurons encoded greater information about the direction of planned eye movements than superficial neurons. These results suggest a division of labor between cortical layers in the coding of visual input and visually guided behavior.
Project description:With each eye movement, the image of the world received by the visual system changes dramatically. To maintain stable spatiotopic (world-centered) visual representations, the retinotopic (eye-centered) coordinates of visual stimuli are continually remapped, even before the eye movement is completed. Recent psychophysical work has suggested that updating of attended locations occurs as well, although on a slower timescale, such that sustained attention lingers in retinotopic coordinates for several hundred milliseconds after each saccade. To explore where and when this "retinotopic attentional trace" resides in the cortical visual processing hierarchy, we conducted complementary functional magnetic resonance imaging and event-related potential (ERP) experiments using a novel gaze-contingent task. Human subjects executed visually guided saccades while covertly monitoring a fixed spatiotopic target location. Although subjects responded only to stimuli appearing at the attended spatiotopic location, blood oxygen level-dependent responses to stimuli appearing after the eye movement at the previously, but no longer, attended retinotopic location were enhanced in visual cortical area V4 and throughout visual cortex. This retinotopic attentional trace was also detectable with higher temporal resolution in the anterior N1 component of the ERP data, a well established signature of attentional modulation. Together, these results demonstrate that, when top-down spatiotopic signals act to redirect visuospatial attention to new retinotopic locations after eye movements, facilitation transiently persists in the cortical regions representing the previously relevant retinotopic location.
Project description:During the preparation of saccadic eye movements, visual attention is confined to the target of intended fixation and there is a corresponding diminution of visual sensitivity at nontarget locations. Neurons within the macaque visual cortex exhibit correlates of these perceptual changes, such as in area V4, where neuronal responses are enhanced during the preparation of saccades to stimuli within the receptive field (RF), and responses are suppressed during the preparation of saccades to other locations. Both the perceptual and neurophysiological effects suggest that the sensitivity of visual cortical neurons to input is dynamic during saccade preparation. We probed the contrast sensitivity of area V4 neurons to nontarget stimuli at varying times during the preparation of saccades to locations outside of the neuron's receptive field. We found that the contrast sensitivity of many neurons is profoundly altered within 50 ms of saccade onset. The luminance or color contrast sensitivity of individual V4 neurons could increase, decrease, or remain unchanged before saccade onset. For luminance contrast sensitivity, decreases in sensitivity were more frequent and larger in magnitude, resulting in an overall decrement in sensitivity across the population. For color contrast, the effects were smaller and more heterogeneous, resulting in little or no overall change in sensitivity across the population. Our results demonstrate the dynamic influence that saccade preparation has on the sensitivity of visual cortical neurons and suggest a basis for the changes in perception known to occur during saccade preparation.
Project description:We have previously shown that when a stimulus consisting of two concentric rings moves, saccade latencies are much longer (by 150 ms) when attention is directed to the larger ring than to the smaller ring. Here, we investigated whether this effect can be explained by a deferral of the "cost" of making a saccade while the target remains inside the attentional field, or by purely visual factors (eccentricity or contrast). We found 1) latencies were shorter when attention was directed to small features irrespective of retinal eccentricity; 2) saccade latency distributions were systematically determined by the ratio between the amplitude of the stimulus step and the diameter of the attended ring: stimulus steps that were larger than the attended ring resulted in short latencies, whereas steps smaller than the attended ring resulted in proportionally longer and more variable latencies; 3) this effect was not seen in manual reaction times to the same target movement; and 4) suprathreshold changes in the contrast of targets, mimicking possible attentional effects on perceived contrast and saliency, had little effect on latency. We argue that the spatial scale of attention determines the urgency of saccade motor preparation processes by changing the rate and rate variability of the underlying decision signal, to defer the cost of saccades that result in little visual benefit.
Project description:A hallmark of visual cortical neurons is their selectivity for stimulus pattern features, such as color, orientation, or shape. In most cases this feature selectivity is hard-wired, with selectivity manifest from the beginning of the response. Here we show that when a task requires that a monkey distinguish between patterns, V4 develops a selectivity for the sought-after pattern, which it does not manifest in a task that does not require the monkey to distinguish between patterns. When a monkey looks for a target object among an array of distractors, V4 neurons become selective for the target ?50 ms after the visual latency independent of the impending saccade direction. However, when the monkey has to only make a saccade to the spatial location of the same objects without discriminating their pattern, V4 neurons do not distinguish the search target from the distractors. This selectivity for stimulus pattern develops roughly 40 ms after the same neurons' selectivity for basic pattern features like orientation or color. We suggest that this late-developing selectivity is related to the phenomenon of feature attention and may contribute to the mechanisms by which the brain finds the target in visual search.
Project description: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 neuron's 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.
Project description:Our eyes continually jump around the visual scene to bring the high-resolution, central part of our vision onto objects of interest. We are oblivious to these abrupt shifts, perceiving the visual world to appear reassuringly stable. A process called remapping has been proposed to mediate this perceptual stability for attended objects by shifting their retinotopic representation to compensate for the effects of the upcoming eye movement. In everyday vision, observers make goal-directed eye movements towards items of interest bringing them to the fovea and, for these items, the remapped activity should impinge on foveal regions of the retinotopic maps in visual cortex. Previous research has focused instead on remapping for targets that were not saccade goals, where activity is remapped to a new peripheral location rather than to the foveal representation. We used functional magnetic resonance imaging (fMRI) and a phase-encoding design to investigate remapping of spatial patterns of activity towards the fovea/parafovea for saccade targets that were removed prior to completion of the eye movement. We found strong evidence of foveal remapping in retinotopic visual areas, which failed to occur when observers merely attended to the same peripheral target without making eye movements towards it. Significantly, the spatial profile of the remapped response matched the orientation and size of the saccade target, and was appropriately scaled to reflect the retinal extent of the stimulus had it been foveated. We conclude that this remapping of spatially structured information to the fovea may serve as an important mechanism to support our world-centered sense of location across goal-directed eye movements under natural viewing conditions.
Project description:The signature of spatial attention effects has been demonstrated through saccade planning and working memory. Although saccade planning and working memory have been commonly linked to attention, the comparison of effects resulting from saccade planning and working memory is less explored. It has recently been shown that spatial attention interacts with local luminance at the attended location. When bright and dark patch stimuli are presented simultaneously in the periphery, thereby producing no change in global luminance, pupil size is nonetheless smaller when the locus of attention overlaps with the bright, compared to the dark patch stimulus (referred to as the local luminance modulation). Here, we used the local luminance modulation to directly compare the effects of saccade planning and spatial working memory. Participants were required to make a saccade towards a visual target location (visual-delay) or a remembered target location (memory-delay) after a variable delay, and the bright and dark patch stimuli were presented during the delay period between target onset and go signal. Greater pupil constriction was observed when the bright patch, compared to the dark patch, was spatially aligned with the target location in both tasks. However, the effects were diminished when there was no contingency implemented between the patch and target locations, particularly in the memory-delay task. Together, our results suggest the involvement of similar, but not identical, attentional mechanisms through saccade planning and working memory, and highlight a promising potential of local pupil luminance responses for probing visuospatial processing.
Project description:During natural behavior, saccades and attention act together to allocate limited neural resources. Attention is generally mediated by retinotopic visual neurons; therefore, specific neurons representing attended features change with each saccade. We investigated the neural mechanisms that allow attentional targeting in the face of saccades. Specifically, we looked for predictive changes in attentional modulation state or receptive field position that could stabilize attentional representations across saccades in area V4, known to be necessary for attention-dependent behavior. We recorded from neurons in monkeys performing a novel spatiotopic attention task, in which performance depended on accurate saccade compensation. Measurements of attentional modulation revealed a predictive attentional "hand-off" corresponding to a presaccadic transfer of attentional state from neurons inside the attentional focus before the saccade to those that will be inside the focus after the saccade. The predictive nature of the hand-off ensures that attentional brain maps are properly configured immediately after each saccade.
Project description:Traditional perceptual learning protocols rely almost exclusively on long periods of uninterrupted fixation. Taking a first step towards understanding perceptual learning in natural vision, we had observers report the orientation of a briefly flashed stimulus (clockwise or counterclockwise from a reference orientation) presented strictly during saccade preparation at a location offset from the saccade target. For each observer, the saccade direction, stimulus location, and orientation remained the same throughout training. Subsequently, we assessed performance during fixation in three transfer sessions, either at the trained or at an untrained location, and either using an untrained (Experiment 1) or the trained (Experiment 2) stimulus orientation. We modeled the evolution of contrast thresholds (i.e., the stimulus contrast necessary to discriminate its orientation correctly 75% of the time) as an exponential learning curve, and quantified departures from this curve in transfer sessions using two new, complementary measures of transfer costs (i.e., performance decrements after the transition into the Transfer phase). We observed robust perceptual learning and associated transfer costs for untrained locations and orientations. We also assessed if spatial transfer costs were reduced for the remapped location of the pre-saccadic stimulus-the location the stimulus would have had (but never had) after the saccade. Although the pattern of results at that location differed somewhat from that at the control location, we found no clear evidence for perceptual learning at remapped locations. Using novel, model-based ways to assess learning and transfer costs, our results show that location and feature specificity, hallmarks of perceptual learning, subsist if the target stimulus is presented strictly during saccade preparation throughout training.