Abstract

Annual changes in the environment threaten survival, and numerous biological processes in mammals adjust to this challenge via seasonal encoding by the suprachiasmatic nucleus (SCN). To tune behavior according to day length, SCN neurons display unified rhythms with synchronous phasing when days are short, but will divide into two sub-clusters when days are long. The transition between SCN states is critical for maintaining behavioral responses to seasonal change, but the mechanisms regulating this form of neuroplasticity remain unclear. Here we identify that a switch in chloride transport and GABAA signaling is critical for maintaining state plasticity in the SCN network. Further, we reveal that blocking excitatory GABAA signaling locks the SCN into its long day state. Collectively, these data demonstrate that plasticity in GABAA signaling dictates how clock neurons interact to maintain environmental encoding. Further, this work highlights factors that may influence susceptibility to seasonal disorders in humans.

Highlights

  • Rhythms generated by the circadian system serve to anticipate changes in the environment caused by the Earth’s rotation (Hut and Beersma, 2011; Pittendrigh, 1960)

  • Previous work has predicted that the seasonal switch to excitatory GABAA signaling will alter how the suprachiasmatic nucleus (SCN) clock is reset by tonic GABA stimulation (DeWoskin et al, 2015)

  • We provide novel insight into seasonal encoding by revealing that the photoperiodic switch in GABAA signaling is necessary for restoring SCN function after it is disrupted by light

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Summary

Introduction

Rhythms generated by the circadian system serve to anticipate changes in the environment caused by the Earth’s rotation (Hut and Beersma, 2011; Pittendrigh, 1960). The SCN itself is a network of clock cells that interact with one another to regulate emergent circuit properties, process photic cues, and provide daily signals to downstream tissues (Evans, 2016; Hastings et al, 2018). The circadian molecular clock drives cellular rhythms, intercellular interactions among SCN neurons synchronize, amplify, and stabilize rhythms of cells within the network (Evans, 2016; Hastings et al, 2018). The SCN network serves as both daily clock and annual calendar, and defining the circuit-level mechanisms by which SCN neurons interact is paramount for understanding the temporal regulation of behavior and physiology

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