MCA: Arbitration between cortical and subcortical control of behavior

Science has made major strides in understanding how animals including humans use sensory information to guide actions. Higher brain areas, including cerebral cortex, are involved in accumulating evidence and triggering decisions. But much of our every-day behavior is controlled by unconscious, automatic, or instinctive responses to sensory stimuli. Those responses can be accomplished by sub-cortical sensory brain areas alone. This study will address the crucial question of how these two types of sensory-driven behavior interact. In particular, when these two mechanisms conflict, what processes in the brain determine whether the more deliberate, cortical, or the more automatic, sub-cortical, response will prevail? This study will leverage the fact that some visual behaviors of mice require cortical processing, while others do not. By creating a novel task in which these two behaviors come into conflict, the researchers will observe how mice resolve the conflict, and determine what brain mechanisms underlie the arbitration for control. This simple case relates to broader questions about how conscious, intentional choices shape or override implicit or innate behavioral drives, and how factors like stress or fatigue affect the balance of power between cortex and subcortex. As a Mid-Career Advancement award, the project has the important additional objective of providing advanced technical training to an established research investigator through an interdisciplinary collaboration, thus contributing to strategic workforce development, broadening participation in STEM, and enabling convergence research. The project will also further the investigator’s work on promoting rigor, robustness and reproducibility of science through educational and research initiatives. In rodents, some visual behaviors depend on the intact function of primary visual cortex (V1), including discriminating the orientation of stripes in a grating patch. Other visual behaviors are cortex-independent, including reporting the location of a grating patch. This study will train freely behaving mice to report which of two simultaneously presented grating stimuli has a target orientation, and separately train them to report which of two simultaneously presented grating stimuli has higher contrast. They will use optogenetic silencing to confirm that V1 is required for the orientation discrimination task, but not the contrast discrimination task. Then they will challenge the mice to perform the orientation discrimination task while the contrast cue either supports the same choice, is neutral, or is in conflict. The researchers expect that mice will be able to learn to override subcortically driven salience responses, and choose correct orientation targets even when they are less salient. But they expect that this conflict will induce a significant increase in errors. They will use machine-learning-based pose estimation to analyze in detail the orienting behavioral responses and model the underlying decision-making. Finally, they will record bilaterally in all layers of the superior colliculus to observe the dynamics with which the competing visual targets vie for determination of motor control, in trials in which cortex wins versus loses the contest for control of behavior. This work will establish a new model system for dissecting the neural circuitry and computational algorithms through which cortical processing exerts influence over cortex-independent sensory-guided behaviors. This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.