The superior colliculus (SC) is part of a network of brain areas that directs saccadic eye movements, overtly shifting both gaze and attention from position to position, in space. Here, we seek direct evidence that the SC also contributes to the control of covert spatial attention, a process that focuses attention on a region of space different from the point of gaze. While requiring monkeys to keep their gaze fixed, we tested whether microstimulation of a specific location in the SC spatial map would enhance visual performance at the corresponding region of space, a diagnostic measure of covert attention. We find that microstimulation improves performance in a spatially selective manner: thresholds decrease at the location in visual space represented by the stimulated SC site, but not at a control location in the opposite hemifield. Our data provide direct evidence that the SC contributes to the control of covert spatial attention. discrimination ͉ psychophysics S everal lines of evidence suggest that eye movements and covert attention may be mediated by the same neural mechanisms (1-3). For example, a human subject can direct attention to a specific location in space, thereby gaining a measurable advantage in visual performance, even while maintaining fixation at an altogether different location (4). During a saccadic eye movement, however, the subject is unable to direct attention to any location other than the endpoint of that eye movement (5).In the monkey, electrophysiological experiments have increasingly implicated eye-movement planning structures in the control of covert spatial attention. Following the original observation by Goldberg and Wurtz (6) of attention-related neural activity in the superior colliculus (SC) (7, 8), single-unit recordings have detected attentional effects in other eye movementrelated areas of the brain, including the inferior parietal cortex (9-11) and the frontal eye fields (FEF) (12)(13)(14). Recent studies by Bisley and Goldberg (15) in the lateral intraparietal area and by Ignashchenkova et al. (16) in the SC were particularly incisive because the neural effects correlated parametrically with variations in the strength and timing of attentional effects in the behavioral data. Electrophysiological evidence, however, is necessarily correlative and cannot demonstrate that neural activity causes behavior (17).Remarkable studies published recently by Moore and Fallah (18,19) bridged this gap. Using visual threshold measurements as a behavioral metric of attention, they showed that electrical microstimulation of the FEF improved psychophysical performance by facilitating the deployment of attention to the location of the visual stimulus. The effect was spatially localized to the region of the visual field encoded at the stimulation site and thus could not be attributed to a general increase in arousal or vigilance. This was a landmark study first because of its implications concerning the neural substrate of visuo-spatial attention, but more importantly because it is the only d...
Complex cells in striate cortex of macaque showed a rapid pattern-specific adaptation. Adaptation made cells more sensitive to orientation change near the adapting orientation. It reduced correlations among the responses of populations of cells, thereby increasing the information transmitted by each action potential. These changes were brought about by brief exposures to stationary patterns, on the time scale of a single fixation. Thus, if successive fixations expose neurons' receptive fields to images with similar but not identical structure, adaptation will remove correlations and improve discriminability.
Normal eye movements ensure that the visual world is seen episodically, as a series of often stationary images. In this paper we characterize the responses of neurons in striate cortex to stationary grating patterns presented with abrupt onset. These responses are distinctive. In most neurons the onset of a grating gives rise to a transient discharge that decays with a time constant of 100 msec or less. The early stages of response have higher contrast gain and higher response gain than later stages. Moreover, the variability of discharge during the onset transient is disproportionately low. These factors together make the onset transient an information-rich component of response, such that the detectability and discriminability of stationary gratings grows rapidly to an early peak, within 150 msec of the onset of the response in most neurons. The orientation selectivity of neurons estimated from the first 150 msec of discharge to a stationary grating is indistinguishable from the orientation selectivity estimated from longer segments of discharge to moving gratings. Moving gratings are ultimately more detectable than stationary ones, because responses to the former are continuously renewed. The principal characteristics of the response of a neuron to a stationary grating-the initial high discharge rate, which decays rapidly, and the change of contrast gain with time-are well captured by a model in which each excitatory synaptic event leads to an immediate reduction in synaptic gain, from which recovery is slow.
Lennie. Local signals from beyond the receptive fields of striate cortical neurons. J Neurophysiol 90: 822-831, 2003. First published April 30, 2003 10.1152/jn.00005.2003. We examined in anesthetized macaque how the responses of a striate cortical neuron to patterns inside the receptive field were altered by surrounding patterns outside it. The changes in a neuron's response brought about by a surround are immediate and transient: they arise with the same latency as the response to a stimulus within the receptive field (this argues for a source locally in striate cortex) and become less effective as soon as 27 ms later. Surround signals appeared to exert their influence through divisive interaction (normalization) with those arising in the receptive field. Surrounding patterns presented at orientations slightly oblique to the preferred orientation consistently deformed orientation tuning curves of complex (but not simple) cells, repelling the preferred orientation but without decreasing the discriminability of the preferred grating and ones at slightly oblique orientations. By reducing responsivity and changing the tuning of complex cells locally in stimulus space, surrounding patterns reduce the correlations among responses of neurons to a particular stimulus, thus reducing the redundancy of image representation. I N T R O D U C T I O N"End-stopping" and "side-stopping" are well-known properties of receptive fields in striate cortex (V1) (Hubel and Wiesel 1965;Maffei and Fiorentini 1976). A pattern that extends beyond the receptive field often elicits a weaker response than a pattern that just fills it. This surrounding zone of inhibition is not generally considered part of the receptive field because stimuli falling on it cannot by themselves elicit a response. The most suppressive surrounding patterns usually have the same orientation and spatial frequency as those to which the receptive field is best tuned (Blakemore and Tobin 1972;Cavanaugh et al. 2002b;DeAngelis et al. 1994;Gilbert and Wiesel 1990;Levitt and Lund 1997;Nelson and Frost 1978;Sillito et al. 1995).It has been argued that the surround helps figure-ground segregation by suppressing signals within patches of uniform texture (Bradley and Andersen 1998;Lamme 1995;Sillito et al. 1995;Tanaka et al. 1986) and that it adjusts the responsivity of a neuron to the ambient contrast in the neighborhood of the receptive field (Cavanaugh et al. 2002a). We wondered if the surround might confer an additional benefit. In natural images, the correlation between the statistics of two regions declines with the separation of the regions (Simoncelli and Schwartz 1999). If a pattern falling on the surround consistently suppressed a neuron's response to a pattern of similar orientation falling on the receptive field, it might repel the neuron's orientation tuning curve, thereby reducing the correlation (redundancy) among visual signals that arise from adjacent image regions of similar structure. In this respect, the surround would act in the spatial domain in much the...
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