Separate evaluation of target facilitation and distractor suppression in the activity of macaque lateral intraparietal neurons during visual search

Abstract

Nishida S, Tanaka T, Ogawa T. Separate evaluation of target facilitation and distractor suppression in the activity of macaque lateral intraparietal neurons during visual search. J Neurophysiol 110: 2773-2791. First published September 25, 2013 doi:10.1152/jn.00360.2013.-During visual search, neurons in the lateral intraparietal area (LIP) discriminate the target from distractors by exhibiting stronger activation when the target appears within the receptive field than when it appears outside the receptive field. It is generally thought that such target-discriminative activity is produced by the combination of target-related facilitation and distractor-related suppression. However, little is known about how the target-discriminative activity is constituted by these two types of neural modulation. To address this issue, we recorded activity from LIP of monkeys performing a visual search task that consisted of target-present and target-absent trials. Monkeys had to make a saccade to a target in the target-present trials, whereas they had to maintain fixation in the target-absent trials, in which only distractors were presented. By introducing the activity from the latter trials as neutral activity, we were able to separate the target-discriminative activity into targetrelated elevation and distractor-related reduction components. We found that the target-discriminative activity of most LIP neurons consisted of the combination of target-related elevation and distractorrelated reduction or only target-related elevation. In contrast, targetdiscriminative activity composed of only distractor-related reduction was observed for very few neurons. We also found that, on average, target-related elevation was stronger and occurred earlier compared with distractor-related reduction. Finally, we consider possible underlying mechanisms, including lateral inhibitory interactions, responsible for target-discriminative activity in visual search. The present findings provide insight into how neuronal modulations shape targetdiscriminative activity during visual search. visual search; electrophysiology; lateral intraparietal area; nonhuman primate; saccade IN A VISUAL SEARCH, the target must be discriminated from distractors to direct covert attention and/or an overt saccade toward the target locus. Initial visual activity in the lateral intraparietal area (LIP), a crucial area involved in visual search (Liu et al. 2010;Wardak et al. 2002), does not discriminate the target. However, later activity involving stronger discharge rates when the target appears within the receptive field (targetrelated activity) than when it appears outside the receptive field (distractor-related activity) does discriminate the target (Balan et al. 2008;Buschman and Miller 2007;Ipata et al. 2006;Ogawa and Komatsu 2009;Thomas and Paré 2007). It is generally thought that such target-distractor discriminative activity is produced by the facilitation of target-related activity and the suppression of distractor-related activity. However, no systematic study h...

Transition of target-location signaling in activity of macaque lateral intraparietal neurons during delayed-response visual search

“…6A), which is consistent with previous reports (Balan et al 2008;Buschman and Miller 2007;Ipata et al 2006;Nishida et al 2013;Ogawa and Komatsu 2009;Thomas and Paré 2007). The reaction-time visual search task did not require a delay before the saccadic response, and as such, the acrossneuron MI pattern may have been different from that of the delayed-response task.…”

“…The distractor response of the decreasetype neurons decayed fast and decreased almost to the baseline level even before stimulus offset (Fig. 5F), although the target response exhibited the substantial activity even in the same stimulus period, suggesting that these neurons receive signals for strong distractor suppression that is beneficial to shaping activity for visual selection (Falkner et al 2010;Nishida et al 2013). Therefore, consistent with MI changes, the differential response profiles of these two types of neurons might be linked with the heterogeneous functional roles for memory maintenance and visual discrimination.…”

“…When the computer detected a saccadic eye movement, the visual stimuli and the fixation spot were immediately extinguished. The reaction-time visual search task contained trials with various stimulus configurations and target-absent (catch) trials in which all stimuli were identical distractors and the monkeys were required to hold the fixation throughout the trial (for details, see Nishida et al 2013). However, only data from trials in which the array stimuli were the same as those used in the delayed-response visual search task were included in the analysis of the present study.…”

“…visual search; working memory; saccade; lateral intraparietal area; nonhuman primate THE LATERAL INTRAPARIETAL AREA (LIP) plays a crucial role in signaling behaviorally relevant locations in the visual field to guide future actions during visuomotor transformation (Andersen and Cui 2009; Bisley and Goldberg 2010;Gold and Shadlen 2007;Gottlieb and Snyder 2010;Wardak et al 2011). LIP neurons encode the location of a target among distractors during visual search by exhibiting elevated activation when the target is presented inside the neuron's receptive field relative to when the distractor is presented inside the receptive field (Balan et al 2008;Buschman and Miller 2007;Ipata et al 2006;Nishida et al 2013; Thomas and Paré 2007). They also exhibit persistent activation (delay-period activity) to represent the location where an extinguished target had been presented in memory-guided saccade (Chafee and Goldman-Rakic 1998;Gnadt and Andersen 1988;Nishida et al 2014).…”

Visual attention spreads broadly but selects information locally

“…A previous report demonstrated attention modulation with broad spatial tuning in early visual cortices 36 . Selection of attended location and/or inhibition of adjacent areas have also been shown at relatively later stages controlled by higher visual centers such as the frontal eye field 37 and lateral intraparietal cortex 38 39 40 . These results are consistent with a multistage attention mechanism.…”