Abstract
SummaryClassical and modern ethological studies suggest that animal behavior is organized hierarchically across timescales, such that longer-timescale behaviors are composed of specific shorter-timescale actions. Despite progress relating neuronal dynamics to single-timescale behavior, it remains unclear how different timescale dynamics interact to give rise to such higher-order behavioral organization. Here, we show, in the nematode Caenorhabditis elegans, that a behavioral hierarchy spanning three timescales is implemented by nested neuronal dynamics. At the uppermost hierarchical level, slow neuronal population dynamics spanning brain and motor periphery control two faster motor neuron oscillations, toggling them between different activity states and functional roles. At lower hierarchical levels, these faster oscillations are further nested in a manner that enables flexible behavioral control in an otherwise rigid hierarchical framework. Our findings establish nested neuronal activity patterns as a repeated dynamical motif of the C. elegans nervous system, which together implement a controllable hierarchical organization of behavior.
Highlights
Animal behavior unfolds over a wide range of timescales, from sub-second muscle contractions to circadian rhythms
We rely on a precise definition based on propagation and, use ‘‘head-casts’’ instead of ‘‘foraging.’’ Forward locomotion consisted primarily of propagated-bends (Figure 1C) intermittently superimposed with episodes of head-cast oscillations (Figures S1A and S1E); when they did occur, head-cast oscillation cycles were typically faster than propagated-bend ones (Figure 1D)
Other B-class motor neurons (B-MNs) exhibited rhythmic activity (Figure 3A), but we found no significant coordination among them (Figure S2E)
Summary
Animal behavior unfolds over a wide range of timescales, from sub-second muscle contractions to circadian rhythms. Nervous systems act on each of these timescales but must coordinate across them to implement long-term behavioral strategies and avoid interfering actions. Classical (Dawkins, 1976; Tinbergen, 1951) and modern (Berman et al, 2016; Glaze and Troyer, 2006; Gomez-Marin et al, 2016; Marques et al, 2018; Wiltschko et al, 2015; Duistermars et al, 2018) ethological studies posit that such inter-timescale coordination is hierarchical, with longer timescales at higher hierarchical levels. Specific shorter-timescale actions are constrained to occur only in the context of a hierarch, a particular longer-timescale motor program or behavioral state (Dawkins, 1976). Modern quantitative analyses suggest that behaviors as diverse as birdsong and Drosophila locomotion are organized hierarchically (Berman et al, 2016; Glaze and Troyer, 2006)
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