Rapid enhancement of visual cortical response discriminability by microstimulation of the frontal eye field

Abstract

Visual attention provides a means of selecting among the barrage of information reaching the retina and of enhancing the perceptual discriminability of relevant stimuli. Neurophysiological studies in monkeys and functional imaging studies in humans have demonstrated neural correlates of these perceptual improvements in visual cortex during attention. Importantly, voluntary attention improves the discriminability of visual cortical responses to relevant stimuli. Recent work aimed at identifying sources of attentional modulation has implicated the frontal eye field (FEF) in driving spatial attention. Subthreshold microstimulation of the FEF enhances the responses of area V4 neurons to spatially corresponding stimuli. However, it is not known whether these enhancements include improved visual-response discriminability, a hallmark of voluntary attention. We used receiver-operator characteristic analysis to quantify how well V4 responses discriminated visual stimuli and examined how discriminability was affected by FEF microstimulation. Discriminability of responses to stable visual stimuli decayed over time but was transiently restored after microstimulation of the FEF. As observed during voluntary attention, the enhancement resulted only from changes in the magnitude of V4 responses and not in the relationship between response magnitude and variance. Enhanced response discriminability was apparent immediately after microstimulation and was reliable within 40 ms of microstimulation onset, indicating a direct influence of FEF stimulation on visual representations. These results contribute to the mounting evidence that saccade-related signals are a source of spatial attentive selection.cognition ͉ gain control ͉ oculomotor ͉ prefrontal cortex ͉ visual perception C overt visual attention selectively enhances relevant signals from among the flood of information that enters the eye. Perception of attended stimuli is enhanced in a variety of ways (1-3), but in general discrimination of attended stimuli is improved (4). Neurophysiological studies in monkeys and functional imaging studies in humans have demonstrated neural correlates of these perceptual improvements in visual cortex during attention (5-7). Recent work has implicated saccaderelated circuits in driving modulations of visual processing during spatial attention. Specifically, subthreshold microstimulation of the frontal eye field (FEF), an area involved in the control of voluntary saccadic eye movements (8, 9), improves performance on an attention task (10, 11) and transiently enhances visual responses in extrastriate area V4 (12, 13). It is known that voluntary attention improves the discriminability of V4 neuronal responses (14,15) and that the enhanced discriminability results from selective changes in the magnitude of visual responses but not in their reliability (16). Although the effects of FEF microstimulation on V4 responses mirror those of voluntary attention in some respects (12, 13), how FEF microstimulation affects response discriminability and reli...

Dynamic sensitivity of area V4 neurons during saccade preparation

“…Withdrawing attention from RF stimuli, without a concomitant saccade, reduces the luminance contrast sensitivity of V4 neurons to Ϸ66% of the sensitivity measured during attention. Thus, although the change in sensitivity caused by varying covert attention appears to be smaller than the change with saccades (overt attention), the effects of both types of attention on V4 neurons are consistent with evidence that they are both driven by oculomotor mechanisms (11)(12)(13). The effects of overt and covert attention on luminance contrast also supports the view that neuronal sensitivity is related to the probability that a saccade will be made to a neuron's RF (18), reaching the lowest probability when targeting stimuli outside of the RF just before saccade onset.…”

“…Each animal was surgically implanted with a head post, a scleral eye coil, and a recording chamber. Craniotomies were performed on the prelunate gyrus for access to dorsal V4 (12). Eye position was monitored with a scleral search coil and digitized at 500 Hz (CNC Engineering).…”

“…The perceptual and neurophysiological effects of covert attention are thought to result at least in part from a direct influence of saccade-related signals on visual cortical representations (10). For example, the attentional modulation of visually driven responses of area V4 neurons can be recreated by electrical microstimulation within the frontal eye field (FEF) (11)(12)(13). Specifically, microstimulation of the FEF at sites that spatially overlap RFs of recorded V4 neurons transiently enhances the response to stable RF stimuli.…”

FEF inactivation with improved optogenetic methods

“…We found a rebound in firing rate at the end of the illumination period, which was more pronounced in one of the two monkeys. A recent study suggests that it may be possible to sculpt light pulses (i.e., to ramp down the intensity of illumination over hundreds of milliseconds) to lessen postinhibition rebound firing, if desired The rebound spikes appear to be far fewer than needed to induce a saccade in the FEF, and are even fewer than the briefest FEF microstimulation bias we could find in the literature (86,87), where 20 ms of 200-Hz microstimulation (four pulses) was required to enhance V4 firing statistically in response to visual stimuli and yet no change in behavior resulted. Thus, it seems unlikely that the rebound played a role in the behavioral effects.…”

The Premotor theory of attention: Time to move on?

“…There is evidence that activating monkey FEF using microstimulation is sufficient to bias attention (Armstrong et al, 2006;Armstrong & Moore, 2007;Moore & Fallah, 2001), but this bias is unlikely to originate from the specific activation of neurons involved in motor preparation as compelling neurophysiological evidence suggests that covert attention and saccade control are mediated by separate neuronal populations in FEF (Juan et al, 2008;Juan et al, 2004;Sato & Schall, 2003;Thompson et al, 1997;Thompson et al, 2005). Furthermore, it is probable that the perceptual enhancements observed at saccade goals prior to saccade execution are driven by the mechanisms which ensure the maintenance of perceptual stability which do not operate when no saccade is executed (Duhamel et 30 al., 1992;Khan et al, 2009).…”