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

Abstract

<jats:title>Abstract</jats:title><jats:p>The 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.</jats:p><jats:sec><jats:title>Significance statement</jats:title><jats:p>The 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.</jats:p></jats:sec>

Probabilistic discrimination of relative stimulus features in mice

“…Our model helped estimate orientation discrimination acuity, which reached 6 degrees of angle difference. The orientation discrimination acuity of mice has been previously measured in detectiontype tasks, such as 2AFC with a distractor (Reuter, 1987), and in change detection tasks (Glickfeld et al, 2013;Wang et al, 2020). Acuity measures have been reported as thresholds or just-noticeable differences (JND) and commonly rely on model-derived values, such as the model-based inverse of a certain success rate (Glickfeld et al, 2013), mean of the fitted Gaussian (Wang et al, 2020), or √2…”

State-dependent changes in perception and coding in the mouse somatosensory cortex

“…Nevertheless, if vS1 is not required for sensory decision making, one alternative explanation for the observed results is that neuronal activity in the somatosensory cortex and behavioral outcomes may both be modulated by state independently. State may affect behavioral outcomes via subcortical processing circuits such as brainstem (Tsunematsu et al, 2020) and thalamic nuclei (Sieveritz et al, 2019) and superior colliculus (Crapse et al, 2018;Wang et al, 2020) . The state-modulations in subcortical circuits may then be transmitted to sensory cortex producing choice-related activity in vS1 (Yang et al, 2016).…”

Inhibitory midbrain neurons mediate decision making

“…5a). We reasoned that if GABAergic activity makes contralateral choices more likely, then contralateral choices would be more likely to occur on trials with more light-elicited spikes-particularly on "difficult" trials in which the sensory evidence indicating reward side was weak 9,16,20,43 . Figure 5b shows, for an example GABAergic neuron, that contralateral choices are more likely on trials in which photoactivation induced more spikes, as demonstrated by a positive exponential fit to trial-by-trial data (Methods).…”

“…Spatial choiceselecting where to attend or to moveis ideal for this purpose: it is an adaptive form of decision making that is critical for survival, and several lines of evidence, across primates, cats and rodents, implicate the intermediate and deep layers of the midbrain superior colliculus (SC) in this function [7][8][9] . Targets in contralateral space are represented in the SC earlier than in other choice-related brain regions [10][11][12][13][14][15] , and manipulating SC activity during choice produces predictable choice biases [15][16][17][18][19][20] . These and other data showing that SC activity reflects target value and other decision-related variables 12,21,22 demonstrate that the SC, traditionally appreciated for initiating orienting motor commands, is required for choosing where to move 7 .…”