Ancient midbrain inhibitory neurons control selective spatial attention

Kavli Affiliate: Shreesh P. Mysore

| Authors: Ninad B Kothari, Wen-Kai You, Arunima Banerjee, Qingcheng Zhang and Shreesh P Mysore

| Summary:

Animal behavior at any instant is guided by information from only a subset of the plethora of stimuli in their sensory environments. The neural circuit mechanisms that select a behaviorally relevant ‘target’ from one location while ignoring distracting stimuli from all others remain unclear. Here, we report the discovery of an explicit neural mechanism for distracter suppression across space. In freely behaving mice engaged in a human-like task of selective spatial attention, we show that bilateral silencing of a group of parvalbumin-positive inhibitory neurons in the brainstem, PLTi, disrupts attentional target selection. This disruption occurred only when a distractor contained conflicting information, revealing that, contrary to the prevailing cortico-centric view, the brainstem PLTi is necessary for combining both top-down and bottom-up information to drive attentional target selection. Notably, unlike cortical and subcortical structures previously implicated in spatial attention, silencing of PLTi did not impair single-target visual perception, motor-plan selection or task-specific orienting movements, unveiling PLTi as a specialized brain module for competitive distracter suppression. Strikingly, PLTi also powerfully controls the accurate positioning as well as categorical precision of each animal’s cognitive threshold separating the attentional target from distracters. Mechanistically, PLTi’s role in attentional behavior is mediated by its sculpting of neural computations in the superior colliculus. The evolutionarily conserved PLTi may, therefore, be a dedicated brainstem engine for driving selective spatial attention in vertebrates. One-Sentence Summary Evolutionarily conserved inhibitory neurons in the mouse midbrain are required for ignoring distracters and selecting the next target of spatial attention.

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