title: Enhanced sensory sampling precedes self-initiated locomotion in an electric fish.
abstract: Cortical activity precedes self-initiated movements by several seconds in mammals; this observation has led into inquiries on the nature of volition. Preparatory neural activity is known to be associated with decision making and movement planning. Self-initiated locomotion has been linked to increased active sensory sampling; however, the precise temporal relationship between sensory acquisition and voluntary movement initiation has not been established. Based on long-term monitoring of sensory sampling activity that is readily observable in freely behaving pulse-type electric fish, we show that heightened sensory acquisition precedes spontaneous initiation of swimming. Gymnotus sp. revealed a bimodal distribution of electric organ discharge rate (EODR) demonstrating down- and up-states of sensory sampling and neural activity; movements only occurred during up-states and up-states were initiated before movement onset. EODR during voluntary swimming initiation exhibited greater trial-to-trial variability than the sound-evoked increases in EODR. The sampling variability declined after voluntary movement onset as previously observed for the neural variability associated with decision making in primates. Spontaneous movements occurred randomly without a characteristic timescale, and no significant temporal correlation was found between successive movement intervals. Using statistical analyses of spontaneous exploratory behaviours and associated preparatory sensory sampling increase, we conclude that electric fish exhibit key attributes of volitional movements, and that voluntary behaviours in vertebrates may generally be preceded by increased sensory sampling. Our results suggest that comparative studies of the neural basis of volition may therefore be possible in pulse-type electric fish, given the substantial homologies between the telencephali of teleost fish and mammals.
authors.affiliation: Department of Physics, University of Ottawa, Ottawa, ON, Canada, K1N 6N5 Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, ON, Canada, K1H 8M5 Centre for Neural Dynamics, University of Ottawa, Ottawa, ON, Canada, K1N 6N5 jamesjun@gmail.com.
authors.forename: James J
authors.initials: JJ
authors.lastname: Jun
authors.affiliation: Department of Physics, University of Ottawa, Ottawa, ON, Canada, K1N 6N5 Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, ON, Canada, K1H 8M5 Centre for Neural Dynamics, University of Ottawa, Ottawa, ON, Canada, K1N 6N5.
authors.forename: André
authors.initials: A
authors.lastname: Longtin
authors.affiliation: Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, ON, Canada, K1H 8M5 Centre for Neural Dynamics, University of Ottawa, Ottawa, ON, Canada, K1N 6N5.
authors.forename: Leonard
authors.initials: L
authors.lastname: Maler
mesh_terms: D000161:Acoustic Stimulation; D000818:Animals; D001522:Behavior, Animal / Q000502:physiology; D004557:Electric Organ / Q000502:physiology*; D023702:Gymnotiformes / Q000502:physiology*; D013550:Swimming / Q000502:physiology*; D013997:Time Factors; D014741:Video Recording
keywords: Active sensing; Decision making; Readiness potential; Volition; Voluntary movement; Weakly electric fish