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

White, Brian J.; Munoz, Douglas P.

doi:10.1523/jneurosci.5349-10.2011

Cited by 36 publications

(49 citation statements)

References 47 publications

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“…Here, we have seen that such stimuli, visible only to short wave cones (S-cones) and presented on a background of luminance noise, were perfectly able to produce dips of similar amplitude than those elicited by luminance stimuli matched in salience. However, such S-cone dips were delayed, consistent with previous reports that signals from isoluminant chromatic stimuli arrive in SC 15-30 ms later than luminance signals but are comparable in amplitude (White et al, 2009;White and Munoz, 2011).…”

Section: Anatomysupporting

confidence: 90%

“…Saccades to stimuli visible only to the chromatic S-cone channel are 20 -40 ms slower than to luminance stimuli matched in salience or detectability , and it has been reported recently that signals from isoluminant chromatic stimuli arrive in SC 15-30 ms later than luminance signals, although these signals do not appear to differ in size (White et al, 2009;White and Munoz, 2011). Thus, the model predicts that chromatic signals would produce delayed dips but of an equivalent amplitude to those of luminance distractors (Fig.…”

Section: Linking the Exogenous Signal To Stimulus Propertiesmentioning

confidence: 67%

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Saccadic Inhibition Reveals the Timing of Automatic and Voluntary Signals in the Human Brain

Bompas¹,

Sumner²

2011

J. Neurosci.

189

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Neurophysiological and phenomenological data on sensorimotor decision making are growing so rapidly that it is now necessary and achievable to capture it in biologically inspired models, for advancing our understanding in both research and clinical settings. However, the main impediment in moving from elegant models with few free parameters to more complex biological models in humans lies in constraining the more numerous parameters with behavioral data (without human single-cell recording). Here we show that a behavioral effect called "saccadic inhibition" (1) is predicted by existing complex (neuronal field) models, (2) constrains crucial temporal parameters of the model, precisely enough to address individual differences, and (3) is not accounted for by current simple decision models, even after significant additions. Visual onsets appearing while an observer plans a saccade knock out a subpopulation of saccadic latencies that would otherwise occur, producing a clear dip in the latency distribution. This overlooked phenomenon is remarkably well time locked across conditions and observers, revealing and characterizing a fast automatic component of visual input to oculomotor competition. The neural field model not only captures this but predicts additional features that are borne out: the dips show spatial specificity, are lawfully modulated in contrast, and occur with S-cone stimuli invisible to the retinotectal route. Overall, we provide a way forward for applying precise neurophysiological models of saccade planning in humans at the individual level.

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Section: Anatomysupporting

confidence: 90%

Section: Linking the Exogenous Signal To Stimulus Propertiesmentioning

confidence: 67%

Saccadic Inhibition Reveals the Timing of Automatic and Voluntary Signals in the Human Brain

Bompas¹,

Sumner²

2011

J. Neurosci.

189

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“…Additionally, the proportion of correct responses was significantly greater under the Easy condition relative to the Hard condition for monkey Y (Light-Easy vs. Light-Hard: t 70 ϭ 18.8, P Ͻ 0.0001; Dim-Easy vs. Dim-Hard: t 70 ϭ 13.6, P Ͻ 0.0001) and for monkey S (Light-Easy vs. Light-Hard: t 50 ϭ 11.8, P Ͻ 0.0001; Dim-Easy vs. Dim-Hard: t 50 ϭ 7.8, P Ͻ 0.0001). Thus saccadic reaction time was prolonged and the proportion of correct responses was reduced when stimulus luminance decreased and/or target-distractor similarity increased, reflecting changes in search difficulty (Bichot et al 1999;Sato et al 2001Sato et al , 2003Thompson et al 2005;White and Munoz 2011).…”

Section: Discussionmentioning

confidence: 99%

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

Nishida

Tanaka

Ogawa

2013

Journal of Neurophysiology

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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...

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“…1B) is multilayered but is often described as having two dominant functional layers, a superior colliculus superficial layer (SCs) associated exclusively with visual processing and a superior colliculus multisensory-cognitive-motor intermediate layer (SCi) linked to the control of attention and gaze (19)(20)(21)(22). Because SCs is interconnected with multiple visual areas (23-25), it is in an ideal location to pool diverse visual inputs to form a feature-agnostic saliency representation.…”

mentioning

confidence: 99%

Superior colliculus encodes visual saliency before the primary visual cortex

White

Kan

Lévy

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

121

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Models of visual attention postulate the existence of a bottom-up saliency map that is formed early in the visual processing stream. Although studies have reported evidence of a saliency map in various cortical brain areas, determining the contribution of phylogenetically older pathways is crucial to understanding its origin. Here, we compared saliency coding from neurons in two early gateways into the visual system: the primary visual cortex (V1) and the evolutionarily older superior colliculus (SC). We found that, while the response latency to visual stimulus onset was earlier for V1 neurons than superior colliculus superficial visual-layer neurons (SCs), the saliency representation emerged earlier in SCs than in V1. Because the dominant input to the SCs arises from V1, these relative timings are consistent with the hypothesis that SCs neurons pool the inputs from multiple V1 neurons to form a feature-agnostic saliency map, which may then be relayed to other brain areas.M ost theories and computational models of saliency postulate that visual input is transformed into a topographic representation of visual conspicuity (Fig. 1A, red), whereby certain stimuli stand out from others based on low-level features of the input image (Fig. 1A, blue) (1-3). The concept of a priority map describes a combined representation of visual saliency and behavioral relevancy (Fig. 1A, yellow), which is thought to be the core determinant of attention and gaze (4, 5). To date, most studies have reported evidence of saliency and/or priority maps in a distributed network of cortical brain areas [e.g., primary visual cortex (V1) (6-9), visual area 4 (V4) (10), lateral intraparietal area (LIP) (11-13), and frontal eye fields (14, 15)]. However, there is mounting evidence for a subcortical saliency mechanism in the premammalian optic tectum (16-18) or superior colliculus (SC) in primates (Fig. 1B). The primate SC, which has received a lot of attention for its role as an oculomotor hub, might be considered an unlikely candidate for a visual salience map, but there is a rich history of research on visual attention in the SC (a recent review is in ref. 19), which has broadened our perspective of its role in processes previously thought to be the domain of neocortex.The SC (Fig. 1B) is multilayered but is often described as having two dominant functional layers, a superior colliculus superficial layer (SCs) associated exclusively with visual processing and a superior colliculus multisensory-cognitive-motor intermediate layer (SCi) linked to the control of attention and gaze (19)(20)(21)(22). Because SCs is interconnected with multiple visual areas (23-25), it is in an ideal location to pool diverse visual inputs to form a feature-agnostic saliency representation. Recently (26), it has been shown that the activity of SCs neurons, with dominant inputs that arise from the retina and V1 (Fig. 1B) (24, 25), is well-predicted by a computational saliency model that has been validated on the free viewing behavior of humans (27) and nonhuman prima...

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

Cited by 36 publications

References 47 publications

Saccadic Inhibition Reveals the Timing of Automatic and Voluntary Signals in the Human Brain

Saccadic Inhibition Reveals the Timing of Automatic and Voluntary Signals in the Human Brain

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

Superior colliculus encodes visual saliency before the primary visual cortex

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