Role of spontaneous and sensory orexin network dynamics in rapid locomotion initiation. (April 2020)

• Record Type: Journal Article
• Authors: Karnani, Mahesh M.; Schöne, Cornelia; Bracey, Edward F.; González, J. Antonio; Viskaitis, Paulius; Li, Han-Tao; Adamantidis, Antoine; Burdakov, Denis
• Is Part Of: Progress in neurobiology. Volume 187(2020)
• Publication Date: 2020-04
• Subjects: Hypothalamus -- orexin/hypocretin neurons -- Locomotion -- Sensorimotor processing -- Ensemble imaging; Neurobiology -- Periodicals; Neurology -- Periodicals; Neurology -- Periodicals; Neurobiologie -- Périodiques; 612.8
• DOI: 10.1016/j.pneurobio.2020.101771
• Languages: English
• ISSNs: 0301-0082

Abstract

Graphical abstract: Highlights: Hypocretin/orexin neuron (HON) activation correlates with and is causally linked to locomotion initiation. HONs constitute 5 subtypes based on their dynamics before and during locomotion. About 2/3 HONs display excitatory sensory responses. HON sensory responses mediate a rapid sensory-locomotor transformation. Abstract: Appropriate motor control is critical for normal life, and requires hypothalamic hypocretin/orexin neurons (HONs). HONs are slowly regulated by nutrients, but also display rapid (subsecond) activity fluctuations in vivo . The necessity of these activity bursts for sensorimotor control and their roles in specific phases of movement are unknown. Here we show that temporally-restricted optosilencing of spontaneous or sensory-evoked HON bursts disrupts locomotion initiation, but does not affect ongoing locomotion. Conversely, HON optostimulation initiates locomotion with subsecond delays in a frequency-dependent manner. Using 2-photon volumetric imaging of activity of >300 HONs during sensory stimulation and self-initiated locomotion, we identify several locomotion-related HON subtypes, which distinctly predict the probability of imminent locomotion initiation, display distinct sensory responses, and are differentially modulated by food deprivation. By causally linking HON bursts to locomotion initiation, these findings reveal the sensorimotor importance of rapid spontaneous and evoked fluctuations in HON ensemble activity.