Neuron-specific contribution of the superior colliculus to overt and covert shifts of attention

Ignashchenkova, Alla; Dicke, Peter W.; Haarmeier, Thomas; Thier, Peter

doi:10.1038/nn1169

Cited by 354 publications

(304 citation statements)

References 33 publications

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“…By contrast, responses of neurons with purely movementrelated activity were suppressed, suggesting that some neurons participate selectively in saccade production and others participate in covert visual selection. Similarly, another study that recorded neuronal activity in the SC while monkeys performed a visual discrimination task found that visuomovement neurons were active during covert shifts of attention (31). Thus, both the FEF and SC contain neurons that signal the locus of attention.…”

Section: Discussionmentioning

confidence: 89%

“…Therefore, unless our observations were due primarily to antidromic activation of neurons outside the FEF, e.g., in the lateral intraparietal area (LIP), our results imply that FEF neurons, perhaps by way of other structures activated orthodromically, enhance representations in visual cortex during spatial attention. Indeed, the FEF projects to the superior colliculus (SC) and area LIP, two areas known to be involved in both saccade control and visual attention (23,27,28,31,32). Thus, there are several pathways by which FEF stimulation could act on visual responses.…”

Section: Discussionmentioning

confidence: 99%

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

Armstrong

Moore²

2007

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

173

122

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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...

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Section: Discussionmentioning

confidence: 89%

Section: Discussionmentioning

confidence: 99%

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

Armstrong

Moore²

2007

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

173

122

View full text Add to dashboard Cite

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“…Such selection-related activity occurs at the same time that neuronal activity in visual areas of the cortex is enhanced during attentional tasks (Reynolds and Desimone, 1999;Ghose and Maunsell, 2002). This SC selection-related activity is modulated when the monkey attends to a region of the visual field (Kustov and Robinson, 1996), and this modulation occurs only with a spatial cue for that region (Ignashchenkova et al, 2004). The logic then is that the delay activity of these SC neurons might be directed not only to preparing for a saccade to one part of the visual field but also to providing a spatial attention signal to cortex that modulates the activity of visual cortical neurons related to the same part of the visual field.…”

Section: Sc and Visual Spatial Attentionmentioning

confidence: 97%

Drivers from the deep: the contribution of collicular input to thalamocortical processing

Wurtz

Sommer

Cavanaugh

2005

Progress in Brain Research

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A traditional view of the thalamus is that it is a relay station which receives sensory input and conveys this information to cortex. This sensory input determines most of the properties of first order thalamic neurons, and so is said to drive, rather than modulate, these neurons. This holds as a rule for first order thalamic nuclei, but in contrast, higher order thalamic nuclei receive much of their driver input back from cerebral cortex. In addition, higher order thalamic neurons receive inputs from subcortical movement-related centers. In the terminology popularized from studies of the sensory system, can we consider these ascending motor inputs to thalamus from subcortical structures to be modulators, subtly influencing the activity of their target neurons, or drivers, dictating the activity of their target neurons? This chapter summarizes relevant evidence from neuronal recording, inactivation, and stimulation of pathways projecting from the superior colliculus through thalamus to cerebral cortex. The study concludes that many inputs to the higher order nuclei of the thalamus from subcortical oculomotor areas -from the superior colliculus and probably other midbrain and pontine regions -should be regarded as motor drivers analogous to the sensory drivers at the first order thalamic nuclei. These motor drivers at the thalamus are viewed as being at the top of a series of feedback loops that provide information on impending actions, just as sensory drivers provide information about the external environment.

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“…1B) and project directly to the brainstem saccade generator (23)(24)(25). Functionally, these neurons have multisensory and oculomotor responses and have been shown to play a central role in spatial attention (19,20). This has led to the hypothesis that SCi is best described as a priority map for the control of attention and gaze (4) (Fig.…”

Section: Surround Modulation Emerges Earlier and Stronger In Scs Thanmentioning

confidence: 99%

“…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.

115

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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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Neuron-specific contribution of the superior colliculus to overt and covert shifts of attention

Cited by 354 publications

References 33 publications

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

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

Drivers from the deep: the contribution of collicular input to thalamocortical processing

Superior colliculus encodes visual saliency before the primary visual cortex

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