Neural Control of Visual Search by Frontal Eye Field: Effects of Unexpected Target Displacement on Visual Selection and Saccade Preparation

Abstract

Murthy A, Ray S, Shorter SM, Schall JD, Thompson KG. Neural control of visual search by frontal eye field: effects of unexpected target displacement on visual selection and saccade preparation. J Neurophysiol 101: 2485-2506, 2009. First published March 4, 2009 doi:10.1152/jn.90824.2008. The dynamics of visual selection and saccade preparation by the frontal eye field was investigated in macaque monkeys performing a search-step task combining the classic double-step saccade task with visual search. Reward was earned for producing a saccade to a color singleton. On random trials the target and one distractor swapped locations before the saccade and monkeys were rewarded for shifting gaze to the new singleton location. A race model accounts for the probabilities and latencies of saccades to the initial and final singleton locations and provides a measure of the duration of a covert compensation process-targetstep reaction time. When the target stepped out of a movement field, noncompensated saccades to the original location were produced when movement-related activity grew rapidly to a threshold. Compensated saccades to the final location were produced when the growth of the original movement-related activity was interrupted within target-step reaction time and was replaced by activation of other neurons producing the compensated saccade. When the target stepped into a receptive field, visual neurons selected the new target location regardless of the monkeys' response. When the target stepped out of a receptive field most visual neurons maintained the representation of the original target location, but a minority of visual neurons showed reduced activity. Chronometric analyses of the neural responses to the target step revealed that the modulation of visually responsive neurons and movement-related neurons occurred early enough to shift attention and saccade preparation from the old to the new target location. These findings indicate that visual activity in the frontal eye field signals the location of targets for orienting, whereas movement-related activity instantiates saccade preparation. I N T R O D U C T I O NTo investigate the neural basis of the decision processes of saccade target selection, we have recorded neural activity in the frontal eye field (FEF) of macaque monkeys trained to perform visual search tasks (Bichot and Schall 1999; Bichot et al.

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“…Furthermore, spike rates in the lateral intraparietal area rise like a decision accumulator for a particular saccadic response 78,79 , and microstimulating this area biases responses in a way that is consistent with a shift in the accumulated decision variable 80 . Accumulating activity in frontal eye field motor neurones also predicts motor decisions, as shown recently using a visual search task 81 .…”

Separate Visual Signals for Saccade Initiation during Target Selection in the Primate Superior Colliculus

“…Both the FEF and LIP are strongly associated with target selection (Schall and Thompson, 1999;Schall, 2001;Ipata et al, 2006;Thomas and Paré, 2007). Previous studies have demonstrated a significant degree of independence between visual selection and saccade initiation in the FEF (Thompson et al, 1997;Woodman et al, 2008;Murthy et al, 2009). These authors conclude that variability in SRT is correlated with postvisual/postperceptual processes in the FEF, except when visual processes are taxed by increased targetdistractor similarity (Sato et al, 2001(Sato et al, , 2003.…”

Frontal-Subcortical Circuits Involved in Reactive Control and Monitoring of Gaze

“…These no-step-slow and no-step-fast trials were modeled separately. Compensated trials were compared with these latency-matched no-step-slow trials; such latency matching is common practice in neurophysiology (Hanes et al, 1998;Murthy et al, 2009), electrophysiology (Reinhart et al, 2012, and human fMRI (Aron and Poldrack, 2006) studies. Rest (fixation) trials were not explicitly modeled and therefore constituted an implicit baseline.…”

“…Using the oculomotor countermanding task, nonhuman primate studies have investigated the cellular basis of reactive inhibition . Computational modeling and neurophysiology studies have also explored rapid modification of saccade plans using the oculomotor search-step task (Camalier et al, 2007;Murthy et al, 2009;Ramakrishnan et al, 2012). Existing neurophysiology and computational modeling work provides an unprecedented basis from which to understand reactive action control in humans.…”