A Causal Role for Mouse Superior Colliculus in Visual Perceptual Decision-Making

J Neurosci. 2020 May 6;40(19):3768-3782. doi: 10.1523/JNEUROSCI.2642-19.2020. Epub 2020 Apr 6.

Abstract

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 of both sexes 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 is necessary for the normal performance of voluntary visual choice behaviors.SIGNIFICANCE STATEMENT The mouse superior colliculus (SC) 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.

Keywords: decision-making; mouse; perception; superior colliculus; vision; visual attention.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Animals
  • Attention / physiology
  • Choice Behavior / physiology*
  • Female
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neurons / physiology
  • Superior Colliculi / physiology*
  • Visual Perception / physiology*