scholarly journals A causal role for mouse superior colliculus in visual perceptual decision-making

2019 ◽  
Author(s):  
Lupeng Wang ◽  
Kerry McAlonan ◽  
Sheridan Goldstein ◽  
Charles R. Gerfen ◽  
Richard J. Krauzlis

AbstractThe superior colliculus (SC) is arguably the most important visual structure in the mouse brain and is well-known for its involvement in innate responses to visual threats and prey items. In other species, the SC plays a central role in voluntary as well as innate visual functions, including crucial contributions to selective attention and perceptual decision-making. In the mouse, the possible role of the SC in voluntary visual choice behaviors has not been established. Here, we demonstrate that the mouse SC plays a causal role in visual perceptual decision-making by transiently inhibiting SC activity during an orientation-change detection task. First, unilateral SC inhibition induced spatially specific deficits in detection. Hit rates were reduced and reaction times increased for orientation changes in the contralateral but not ipsilateral visual field. Second, the deficits caused by SC inhibition were specific to a temporal epoch coincident with early visual burst responses in the SC. Inhibiting SC during this 100-ms period caused a contralateral detection deficit, whereas inhibition immediately before or after did not. Third, SC inhibition reduced visual detection sensitivity. Psychometric analysis revealed that inhibiting SC visual activity significantly increased detection thresholds for contralateral orientation changes. In addition, effects on detection thresholds and lapse rates caused by SC inhibition were larger in the presence of a competing visual stimulus, indicating a role for the mouse SC in visual target selection. Together, our results demonstrate that the mouse SC plays a crucial role in voluntary visual choice behaviors.Significance statementThe mouse superior colliculus has become a popular model for studying the circuit organization and development of the visual system. Although the SC is a fundamental component of the visual pathways in mice, its role in visual perceptual decision-making is not clear. By investigating how temporally precise SC inhibition influenced behavioral performance during a visually guided orientation change detection task, we identified a 100-ms temporal epoch of SC visual activity that is crucial for the ability of mice to detect behaviorally relevant visual changes. In addition, we found that SC inhibition also caused deficits in visual target selection. Thus, our findings highlight the importance of the SC for visual perceptual choice behavior in the mouse.

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Hironori Maruyama ◽  
Natsuki Ueno ◽  
Isamu Motoyoshi

AbstractIn many situations, humans make decisions based on serially sampled information through the observation of visual stimuli. To quantify the critical information used by the observer in such dynamic decision making, we here applied a classification image (CI) analysis locked to the observer's reaction time (RT) in a simple detection task for a luminance target that gradually appeared in dynamic noise. We found that the response-locked CI shows a spatiotemporally biphasic weighting profile that peaked about 300 ms before the response, but this profile substantially varied depending on RT; positive weights dominated at short RTs and negative weights at long RTs. We show that these diverse results are explained by a simple perceptual decision mechanism that accumulates the output of the perceptual process as modelled by a spatiotemporal contrast detector. We discuss possible applications and the limitations of the response-locked CI analysis.


2018 ◽  
Author(s):  
Mohsen Rakhshan ◽  
Vivian Lee ◽  
Emily Chu ◽  
Lauren Harris ◽  
Lillian Laiks ◽  
...  

AbstractPerceptual decision making is influenced by reward expected from alternative options or actions, but the underlying neural mechanisms are currently unknown. More specifically, it is debated whether reward effects are mediated through changes in sensory processing and/or later stages of decision making. To address this question, we conducted two experiments in which human subjects made saccades to what they perceived to be the first or second of two visually identical but asynchronously presented targets, while we manipulated expected reward from correct and incorrect responses on each trial. We found that unequal reward caused similar shifts in target selection (reward bias) between the two experiments. Moreover, observed reward biases were independent of the individual’s sensitivity to sensory signals. These findings suggest that the observed reward effects were determined heuristically via modulation of decision-making processes instead of sensory processing and thus, are more compatible with response bias rather than perceptual bias. To further explain our findings and uncover plausible neural mechanisms, we simulated our experiments with a cortical network model and tested alternative mechanisms for how reward could exert its influence. We found that our observations are more compatible with reward-dependent input to the output layer of the decision circuit. Together, our results suggest that during a temporal judgment task, the influence of reward information on perceptual choice is more compatible with changing later stages of decision making rather than early sensory processing.


2018 ◽  
Author(s):  
Noor Seijdel ◽  
Sara Jahfari ◽  
Iris I.A. Groen ◽  
H. Steven Scholte

A fundamental component of interacting with our environment is gathering and interpretation of sensory information. When investigating how perceptual information shapes the mechanisms of decision-making, most researchers have relied on the use of manipulated or unnatural information as perceptual input, resulting in findings that may not generalize to real-world scenes. Unlike simplified, artificial stimuli, real-world scenes contain low-level regularities (natural scene statistics) that are informative about the structural complexity of a scene, which the brain could exploit during perceptual decision-making. In this study, participants performed an animal detection task on low, medium or high complexity scenes as determined by two biologically plausible natural scene statistics, contrast energy (CE) or spatial coherence (SC). In experiment 1, stimuli were sampled such that CE and SC both influenced scene complexity. Diffusion modeling showed that both the speed of information processing and the required evidence were affected by the low-level scene complexity. Experiment 2a/b refined these observations by showing how the isolated manipulation of SC alone resulted in weaker but comparable effects on decision-making, whereas the manipulation of only CE had no effect. Overall, performance was best for scenes with intermediate complexity. Our systematic definition of natural scene statistics quantifies how complexity of natural scenes interacts with decision-making in an animal detection task. We speculate that the computation of CE and SC could serve as an indication to adjust perceptual decision-making based on the complexity of the input.


2021 ◽  
Author(s):  
Hironori Maruyama ◽  
Natsuki Ueno ◽  
Isamu Motoyoshi

In many situations, humans make decisions based on serially sampled information through the observation of visual stimuli. To quantify the critical information used by the observer in such dynamic decision making, we here applied a classification image (CI) analysis locked to the observer's reaction time (RT) in a simple detection task for a luminance target that gradually appeared in dynamic noise. We found that the response-locked CI shows a spatiotemporally biphasic weighting profile that peaked about 300 ms before the response, but this profile substantially varied depending on RT; positive weights dominated at short RTs and negative weights at long RTs. We show that these diverse results are explained by a simple perceptual decision mechanism that accumulates the output of the perceptual process as modelled by a spatiotemporal contrast detector. We discuss possible applications and the limitations of the response-locked CI analysis.


2018 ◽  
Author(s):  
Jochem van Kempen ◽  
Gerard M. Loughnane ◽  
Daniel P. Newman ◽  
Simon P. Kelly ◽  
Alexander Thiele ◽  
...  

AbstractThe timing and accuracy of perceptual decision making is exquisitely sensitive to fluctuations in arousal. Although extensive research has highlighted the role of neural evidence accumulation in forming decisions, our understanding of how arousal impacts these processes remains limited. Here we isolated electrophysiological signatures of evidence accumulation alongside signals reflecting target selection, attentional engagement and motor output and examined their modulation as a function of both tonic and phasic arousal, indexed by baseline and task-evoked pupil diameter, respectively. For both pupillometric measures, the relationship with reaction time was best described by a second-order, U-shaped, polynomial. Additionally, the two pupil measures were predictive of a unique set of EEG signatures that together represent multiple information processing steps of perceptual decision-making, including evidence accumulation. Finally, we found that behavioural variability associated with fluctuations in both tonic and phasic arousal was largely mediated by variability in evidence accumulation.


2020 ◽  
Vol 40 (19) ◽  
pp. 3768-3782 ◽  
Author(s):  
Lupeng Wang ◽  
Kerry McAlonan ◽  
Sheridan Goldstein ◽  
Charles R. Gerfen ◽  
Richard J. Krauzlis

2018 ◽  
Vol 115 (7) ◽  
pp. E1588-E1597 ◽  
Author(s):  
Brian Odegaard ◽  
Piercesare Grimaldi ◽  
Seong Hah Cho ◽  
Megan A. K. Peters ◽  
Hakwan Lau ◽  
...  

Recent studies suggest that neurons in sensorimotor circuits involved in perceptual decision-making also play a role in decision confidence. In these studies, confidence is often considered to be an optimal readout of the probability that a decision is correct. However, the information leading to decision accuracy and the report of confidence often covaried, leaving open the possibility that there are actually two dissociable signal types in the brain: signals that correlate with decision accuracy (optimal confidence) and signals that correlate with subjects’ behavioral reports of confidence (subjective confidence). We recorded neuronal activity from a sensorimotor decision area, the superior colliculus (SC) of monkeys, while they performed two different tasks. In our first task, decision accuracy and confidence covaried, as in previous studies. In our second task, we implemented a motion discrimination task with stimuli that were matched for decision accuracy but produced different levels of confidence, as reflected by behavioral reports. We used a multivariate decoder to predict monkeys’ choices from neuronal population activity. As in previous studies on perceptual decision-making mechanisms, we found that neuronal decoding performance increased as decision accuracy increased. However, when decision accuracy was matched, performance of the decoder was similar between high and low subjective confidence conditions. These results show that the SC likely signals optimal decision confidence similar to previously reported cortical mechanisms, but is unlikely to play a critical role in subjective confidence. The results also motivate future investigations to determine where in the brain signals related to subjective confidence reside.


eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
Jochem van Kempen ◽  
Gerard M Loughnane ◽  
Daniel P Newman ◽  
Simon P Kelly ◽  
Alexander Thiele ◽  
...  

The timing and accuracy of perceptual decision-making is exquisitely sensitive to fluctuations in arousal. Although extensive research has highlighted the role of various neural processing stages in forming decisions, our understanding of how arousal impacts these processes remains limited. Here we isolated electrophysiological signatures of decision-making alongside signals reflecting target selection, attentional engagement and motor output and examined their modulation as a function of tonic and phasic arousal, indexed by baseline and task-evoked pupil diameter, respectively. Reaction times were shorter on trials with lower tonic, and higher phasic arousal. Additionally, these two pupil measures were predictive of a unique set of EEG signatures that together represent multiple information processing steps of decision-making. Finally, behavioural variability associated with fluctuations in tonic and phasic arousal, indicative of neuromodulators acting on multiple timescales, was mediated by its effects on the EEG markers of attentional engagement, sensory processing and the variability in decision processing.


2020 ◽  
Author(s):  
E.J. Jun ◽  
A. Bautista ◽  
M.D. Nunez ◽  
T. Tak ◽  
E. Alvarez ◽  
...  

A popular model of decision-making suggests that in primates, including humans, decisions evolve within forebrain structures responsible for preparing voluntary actions; a concert referred to as embodied cognition. Embodied cognition posits that in decision tasks, neuronal activity generally associated with preparing an action, actually reflects the accumulation of evidence for a particular decision. Testing the embodied cognition model causally is challenging because dissociating the evolution of a decision from preparing a motor act is difficult, if the same neuronal activity instantiates both processes. Ideally, one would show that manipulation of neuronal activity thought to be involved in movement preparation actually alters decisions, and not movement preparation. Here, trained monkeys performed a two-choice perceptual decision-making task in which they judged the orientation of a dynamic Glass pattern before and after unilateral, reversible inactivation of a brainstem area involved in preparing eye movements, the superior colliculus (SC). Surprisingly, we found that unilateral SC inactivation produced significant decision biases and changes in reaction times consistent with a role for the SC in evidence accumulation. Fitting signal detection theory and sequential sampling models (drift-diffusion and urgency-gating) to the data revealed that SC inactivation produced a decrease in the relative evidence for contralateral decisions. Control experiments showed that SC inactivation did not result in eye movement biases ruling out interpretations based on motor preparation or spatial attentional impairment. The results provide causal evidence for an embodied cognition model of perceptual decision-making and provide compelling evidence that the SC of primates plays a causal role in how evidence is accumulated for perceptual decisions, a process that is usually attributed to the cerebral cortex.


2021 ◽  
pp. 1-10
Author(s):  
Shou-Han Zhou ◽  
Gerard Loughnane ◽  
Redmond O'Connell ◽  
Mark A. Bellgrove ◽  
Trevor T.-J. Chong

Abstract Current models of perceptual decision-making assume that choices are made after evidence in favor of an alternative accumulates to a given threshold. This process has recently been revealed in human electrophysiological (EEG) recordings, but an unresolved issue is how these neural mechanisms are modulated by competing, yet task-irrelevant, stimuli. In this study, we tested 20 healthy participants on a motion direction discrimination task. Participants monitored two patches of random dot motion simultaneously presented on either side of fixation for periodic changes in an upward or downward motion, which could occur equiprobably in either patch. On a random 50% of trials, these periods of coherent vertical motion were accompanied by simultaneous task-irrelevant, horizontal motion in the contralateral patch. Our data showed that these distractors selectively increased the amplitude of early target selection responses over scalp sites contralateral to the distractor stimulus, without impacting on responses ipsilateral to the distractor. Importantly, this modulation mediated a decrement in the subsequent buildup rate of a neural signature of evidence accumulation and accounted for a slowing of RTs. These data offer new insights into the functional interactions between target selection and evidence accumulation signals, and their susceptibility to task-irrelevant distractors. More broadly, these data neurally inform future models of perceptual decision-making by highlighting the influence of early processing of competing stimuli on the accumulation of perceptual evidence.


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