Summary Locomotion is a fundamental motor function common to the animal kingdom. It is executed episodically and adapted to behavioural needs including exploration, requiring slow locomotion, and escaping behaviour, necessitating faster speeds. The control of these functions originates in brainstem structures although the neuronal substrate(s) supporting them are debated. Here, we show in mice that speed/gait selection are controlled by glutamatergic excitatory neurons (GlutNs) segregated in two distinct midbrain nuclei: the Cuneiform Nucleus (CnF) and the Pedunculopontine Nucleus (PPN). GlutNs in each of those two regions are sufficient for controlling slower alternating locomotor behavior but only GlutNs in the CnF are necessary for high-speed synchronous locomotion. Additionally, PPN- and CnF-GlutNs activation dynamics and their input and output connectivity matrices support explorative and escape locomotion, respectively. Our results identify dual regions in the midbrain that act in common to select context dependent locomotor behaviours.

Arrest of ongoing movements is an integral part of executing motor programs. Behavioral arrest may happen upon termination of a variety of goal-directed movements or as a global motor arrest either in the context of fear or in response to salient environmental cues. The neuronal circuits that bridge with the executive motor circuits to implement a global motor arrest are poorly understood. We report the discovery that the activation of glutamatergic Chx10-derived neurons in the pedunculopontine nucleus (PPN) in mice arrests all ongoing movements while simultaneously causing apnea and bradycardia. This global motor arrest has a pause-and-play pattern with an instantaneous interruption of movement followed by a short-latency continuation from where it was paused. Mice naturally perform arrest bouts with the same combination of motor and autonomic features. The Chx10-PPN-evoked arrest is different to ventrolateral periaqueductal gray-induced freezing. Our study defines a motor command that induces a global motor arrest, which may be recruited in response to salient environmental cues to allow for a preparatory or arousal state, and identifies a locomotor-opposing role for rostrally biased glutamatergic neurons in the PPN.

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