title: Sensory processing within cockroach antenna enables rapid implementation of feedback control for high-speed running maneuvers.
abstract: Animals are remarkably stable during high-speed maneuvers. As the speed of locomotion increases, neural bandwidth and processing delays can limit the ability to achieve and maintain stable control. Processing the information of sensory stimuli into a control signal within the sensor itself could enable rapid implementation of whole-body feedback control during high-speed locomotion. Here, we show that processing in antennal afferents is sufficient to act as the control signal for a fast sensorimotor loop. American cockroaches Periplaneta americana use their antennae to mediate escape running by tracking vertical surfaces such as walls. A control theoretic model of wall following predicts that stable control is possible if the animal can compute wall position (P) and velocity, its derivative (D). Previous whole-nerve recordings from the antenna during simulated turning experiments demonstrated a population response consistent with P and D encoding, and suggested that the response was synchronized with the timing of a turn executed while wall following. Here, we record extracellularly from individual mechanoreceptors distributed along the antenna and show that these receptors encode D and have distinct latencies and filtering properties. The summed output of these receptors can be used as a control signal for rapid steering maneuvers. The D encoding within the antenna in addition to the temporal filtering properties and P dependence of the population of afferents support a sensory-encoding notion from control theory. Our findings support the notion that peripheral sensory processing can enable rapid implementation of whole-body feedback control during rapid running maneuvers.
authors.affiliation: Biophysics Graduate Group, University of California - Berkeley, Berkeley, CA 94720-3220, USA jmmongeau@ucla.edu.
authors.forename: Jean-Michel
authors.initials: JM
authors.lastname: Mongeau
authors.affiliation: Department of Integrative Biology, University of California - Berkeley, Berkeley, CA 94720-3140, USA Department of Biology, University of Washington, Seattle, WA 98195-1800, USA.
authors.forename: Simon N
authors.initials: SN
authors.lastname: Sponberg
authors.affiliation: Center for Computational Biology, Montana State University, Bozeman, MT 59717-3148, USA.
authors.forename: John P
authors.initials: JP
authors.lastname: Miller
authors.affiliation: Department of Integrative Biology, University of California - Berkeley, Berkeley, CA 94720-3140, USA.
authors.forename: Robert J
authors.initials: RJ
authors.lastname: Full
mesh_terms: D000818:Animals; D057506:Arthropod Antennae / Q000166:cytology / Q000502:physiology*; D001522:Behavior, Animal / Q000502:physiology; D008465:Mechanoreceptors / Q000502:physiology; D008954:Models, Biological; D010526:Periplaneta / Q000502:physiology*; D012420:Running
keywords: Control theory; Mechanoreceptor; Periplaneta americana; Sensorimotor control; Sensory encoding; Tactile sensing