Does the Superior Colliculus Control Perceptual Sensitivity or Choice Bias during Attention? Evidence from a Multialternative Decision Framework

Sridharan, Devarajan; Steinmetz, Nicholas A.; Moore, Tirin; Knudsen, Eric I.

doi:10.1523/jneurosci.4505-14.2017

Cited by 54 publications

(103 citation statements)

References 52 publications

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“…A modeling study of behavioral data from monkeys engaged in attention demanding tasks indicated that the effects of SC inactivations are accounted for best by a disruption in the routing of visual information in the forebrain [20]. The results presented in this study are consistent with OT lesions having the same effect in birds.…”

Section: Resultssupporting

confidence: 81%

“…A second possibility is that the OT lesions interfered with the routing of orientation information from the Wulst to decision networks that guide behavioral choice. A recent modeling study indicates that, in monkeys, the signal that ascends from the SC to the thalamus exerts such a routing effect on visual information in the forebrain [20]. …”

Section: Introductionmentioning

confidence: 99%

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Space-Specific Deficits in Visual Orientation Discrimination Caused by Lesions in the Midbrain Stimulus Selection Network

et al. 2017

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Summary Perceptual decisions require both analysis of sensory information and selective routing of relevant information to decision networks. This study explores the contribution of a midbrain network to visual perception in chickens. Analysis of visual orientation information in birds takes place in the forebrain sensory area called the Wulst, as it does in the primary visual cortex (V1) of mammals. In contrast, the midbrain, which receives parallel retinal input, encodes orientation poorly, if at all. We discovered, however, that small electrolytic lesions in the midbrain severely impair a chicken’s ability to discriminate orientations. Focal lesions were placed in the optic tectum (OT) and in the nucleus isthmi pars parvocellularis (Ipc) – key nodes in the midbrain stimulus selection network – in chickens trained to perform an orientation discrimination task. A lesion in the OT caused a severe impairment in orientation discrimination specifically for targets at the location in space represented by the lesioned location. Distracting stimuli increased the deficit. A lesion in the Ipc produced similar but more transient effects. We discuss the possibilities that performance deficits were caused by interference with orientation information processing (sensory deficit) versus with the routing of information in the forebrain (agnosia). The data support the proposal that the OT transmits a space specific signal that is required to gate orientation information from the Wulst into networks that mediate behavioral decisions, analogous to the role of ascending signals from the SC in monkeys. Furthermore, our results indicate a critical role for the cholinergic Ipc in this gating process.

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Section: Resultssupporting

confidence: 81%

Section: Introductionmentioning

confidence: 99%

Space-Specific Deficits in Visual Orientation Discrimination Caused by Lesions in the Midbrain Stimulus Selection Network

et al. 2017

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“…For example, activity in sensory cortices correlates not only with sensory stimuli but also with motor planning 6,7 , movement 8 , upcoming behavioral reports [9][10][11][12][13][14] , spatial attention 15,16 and reward 17 . Similarly, in motor regions such as the deep layers of the superior colliculus 18 , activity correlates with aspects of decision making and other cognitive functions 5,[19][20][21][22][23] . The brain regions implicated to date in sensory-guided behavior include neocortex, basal ganglia, thalamus, and midbrain.…”

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confidence: 99%

Distributed correlates of visually-guided behavior across the mouse brain

Steinmetz

Zatka-Haas

Carandini

et al. 2018

Preprint

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Behavior arises from neuronal activity, but it is not known how the active neurons are distributed across brain regions and how their activity unfolds in time. Here, we used high-density Neuropixels probes to record from ~30,000 neurons in mice performing a visual contrast discrimination task. The task activated 60% of the neurons, involving nearly all 42 recorded brain regions, well beyond the regions activated by passive visual stimulation. However, neurons selective for choice (left vs. right) were rare, and found mostly in midbrain, striatum, and frontal cortex. Those in midbrain were typically activated prior to contralateral choices and suppressed prior to ipsilateral choices, consistent with a competitive midbrain circuit for adjudicating the subject's choice. A brain-wide state shift distinguished trials in which visual stimuli led to movement. These results reveal concurrent representations of movement and choice in neurons widely distributed across the brain.neurons in multiple brain areas during each recording session, for multiple days per mouse (n=92 probe insertions over 39 sessions in 10 mice, Fig 1h-j). We identified the firing times of individual neurons using Kilosort 33 and determined their anatomical locations by combining electrophysiological features with histological reconstruction of fluorescentlylabeled probe tracks (Fig 1g, see Methods). Across all sessions we recorded from 29,134 neurons (n=747 ± 38 neurons per session, mean±s.e.), of which 22,458 were localizable to one of 42 brain regions. Of these, 60.0% Figure 1 | Recordings in 42 brain regions during a two-alternative unforced choice task. a, Mice earned water rewards by turning a wheel to indicate which of two visual gratings had higher contrast, or not turning if no stimulus was presented. When stimuli had equal contrast, a Left or Right choice was rewarded with 50% probability. Grey rectangles with dashed dividers indicate the three computer screens surrounding the mouse. Arrows (not visible to the mouse) indicate the coupled movement of the visual stimulus with the wheel, and the colored dashed circle (not visible to the mouse) indicates the stimulus location at which a reward was delivered. b, Timeline of the task. Subjects were free to move as soon as the stimulus appeared, but the stimulus was fixed in place and rewards were unavailable until after an auditory go cue. If no movement was made for 1.5 s after the go cue, a NoGo was registered. The grey region is the analysis window, from 0 to 0.4 s after stimulus onset. c, Average task performance across subjects, n=10 subjects, 39 sessions, 9,538 trials. Colormaps depict the probability of each choice given the combination of contrasts presented. d, Reaction time as a function of stimulus contrast and presence of competing stimuli. e, Mice were head-fixed with forepaws on the wheel while multiple Neuropixels probes were inserted for each recording. f, Frontal view of subject performing the behavioral task during Neuropixels recording, with forepaws on wheel and lick spout for...

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“…These are, in order: (i) the cued location (Cu), (ii) the location in an adjacent quadrant, ipsilateral (Ip) or (iii) contralateral (Co) to the cue, and (iv) the location in the quadrant diagonally opposite to the cue (Op). The behavioral responses in the 5x5 contingency table were analyzed with a multidimensional signal detection model, the m-ADC model (36)(37)(38), to quantify psychophysical parameters (sensitivity and bias) at each location. In Figure 1C we show a schematic of a twodimensional (2-ADC) model, for illustrative purposes, although these data were analyzed with a fourdimensional (4-ADC) model (see Methods).…”

Section: A Change Detection Task Protocol: After An Initial Fixationmentioning

confidence: 99%

“…Because a salient exogenous cue also suppresses visual processing of stimulus information, we designed two post-cue control conditions which permitted isolating pre-cueing attentional effects from visual interference effects of the cue. Subjects' behavior was analyzed with a recently developed multidimensional signal detection model (36)(37)(38) that permitted quantifying exogenous cueing effects on sensitivity and bias at each location. The results reveal key dissociations between sensitivity and bias changes induced by exogenous cueing, and provide mechanistic insights into how exogenous cueing systematically facilitates behavioral accuracies and reaction times by modulating sensitivity and bias.…”

Section: Introductionmentioning

confidence: 99%

Exogenous attention facilitates performance through dissociable sensitivity and bias mechanisms

Sagar

Sengupta

Sridharan

2018

Preprint

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Selective attention enables prioritizing the most important information for differential sensory processing and decision-making. Here, we address an active debate regarding whether attention reflects a unitary phenomenon or involves the operation of dissociable sensory enhancement (perceptual sensitivity) and decisional gating (choice bias) processes. We developed a multialternative task in which participants detected and localized orientation changes in gratings at one of four spatial locations. Exogenous attention cues (high contrast flashes) preceded or followed the change events in close temporal proximity. Analysis of participants' behavior with a multidimensional signal detection model revealed markedly distinct effects of exogenous cueing on perceptual sensitivity and choice bias. Whereas sensitivity enhancement was localized to the stimulus proximal to the exogenous cue, bias enhancement occurred even for distal stimuli in the cued hemifield. Modulations of sensitivity and bias were uncorrelated at both cued and uncued locations. Finally, exogenous cueing produced reaction time benefits only at the cued location and costs only at locations contralateral to the cue. These disparate effects of exogenous cueing on sensitivity, bias and reaction times could be parsimoniously explained within the framework of a diffusion-decision model, in which the drift rate was determined by a linear combination of sensitivity and bias at each location. Exogenous cueing effects on sensitivity and bias differed systematically from previously reported effects of endogenous cueing. We propose that the search for shared neural substrates of exogenous and endogenous attention would benefit from investigating neural correlates of their component sensory and decisional mechanisms.When we voluntarily direct attention "endogenously", we are able to better perceive stimuli at the attended location (sensitivity), and to prioritize information from that location for guiding behavioral decisions (bias). But when a salient stimulus, such as a flash of lightning, captures our attention "exogenously", does it also produce these same effects? To answer this question, we designed a multiple alternative task in which task events occurred in close conjunction with salient exogenous cues (high contrast flashes). We discovered that exogenous attention enhanced both sensitivity and bias for cued stimuli, but each of these changes followed distinct spatial patterns across locations. Our results provide novel insights into component processes of exogenous attention and motivate the search for their neural correlates.

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Does the Superior Colliculus Control Perceptual Sensitivity or Choice Bias during Attention? Evidence from a Multialternative Decision Framework

Cited by 54 publications

References 52 publications

Space-Specific Deficits in Visual Orientation Discrimination Caused by Lesions in the Midbrain Stimulus Selection Network

Space-Specific Deficits in Visual Orientation Discrimination Caused by Lesions in the Midbrain Stimulus Selection Network

Distributed correlates of visually-guided behavior across the mouse brain

Exogenous attention facilitates performance through dissociable sensitivity and bias mechanisms

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