A FRONTAL-COLLICULAR CIRCUIT FOR ROUTING VISUAL DISTRACTIONS INTO GOAL-DEPENDENT BEHAVIOR

Can we predict when visual distractors capture attention? Visual distractors can trigger overt responses or remain unattended, yet the underlying circuitry remains poorly understood due to the predominant use of paradigms restricted to head-restrained animals or fear responses. Here, we demonstrate a novel paradigm using self-initiated visual search to trigger animal navigation, enabling the randomized mid-flight presentation of salient visual stimuli to assess distractibility within goal-dependent behavior. Computer vision methods were applied on imaging data to capture behavioral state transitions, which ranged from attentive distractor engagement to stimulus neglect. To quantitatively characterize these behavioral states, we derived multiple kinematic metrics from the animals' movement patterns. This analytical framework enabled implementation of linear discriminant models to classify visual distraction intensity based on motion signatures and to predict distraction levels from preceding search-related behavioral patterns. During this paradigm, we manipulated and recorded from glutamatergic and GABAergic neurons in the intermediate layer of the lateral superior colliculus (l.SCi) to study whether this conserved circuitry tunes visual distractors. In vivo cell-type-specific calcium recordings via fiber photometry revealed their involvement, while optogenetic and chemogenetic manipulations enhanced or reduced their visual distraction routing. We also characterized involvement and/or modulation from upstream circuits, such as motor cortex and retina to SC projections, using the above methods. Motor cortex electrophysiological recording and movement signatures indicated lower task-engaged states before distracted responses. We propose that l.SCi glutamatergic and GABAergic neurons route visual distraction in an excitatory or inhibitory manner, subject to upstream-derived modulation during task-dependent behavior.