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Authors & Affiliations
Mahsa Altafi, Changwan Chen, Mihaela-Anca Corbu, Aleksandra Trenk, Hanna van den Munkhof, Kristin Weineck, Franziska Bender, Marta Carus-Cadavieco, Alisa Bakhareva, Tatiana Korotkova, Alexey Ponomarenko
Abstract
Innate behaviours such as food intake, social interaction, and novel objects exploration meet multiple needs adaptively and sequentially, suggesting the existence of a hitherto elusive brain dynamics, encoding possible upcoming behaviours. Using electrophysiological neuronal recordings in freely-behaving mice, support vector machine classification and multicolor optogenetics, we show that during behavioural transitions, possible upcoming behaviours are encoded by behaviour-related phase signatures of neuronal populations in lateral hypothalamus (LH) that are active near beta oscillation (15-30 Hz) peaks. Optogenetic inhibition from the lateral preoptic area (LPO) at this phase eliminated behavioural transitions. Out-of-phase LH-LPO stimulation disrupted the coordination of phase signatures of the three behaviours, lacking the typical for transitions increase of their magnitude near oscillation peaks. In-phase LH-LPO stimulation, initiated upon social contact, reduced the latency to feeding onset but not to novel object exploration or new social contact episodes, maintaining transition phase signatures for feeding. Upon behaviour onset, phase signatures became nearly anti-phase with the activity during transitions. In contrast to behavioural transitions, current behaviours were predicted with accuracies near the chance level. We show that transitions are elicited by beta-rhythmic inputs from the medial prefrontal cortex, synchronizing with LH ‘transition cells’ encoding multiple behaviours. Downstream of the LH, dopamine neurons in the ventral tegmental area increase firing during beta oscillations and also encode behavioural transitions. Thus, a hypothalamic transition state encodes alternative future behaviours and enables rapid coordination with cognitive and reward-processing circuitries, commanding adaptive social and eating behaviours.C.C., M.A., T.K. and A.P. contributed equally to this work.