Sensory processing within cockroach antenna enables rapid implementation of feedback control for high-speed running maneuvers

Jean Michel Mongeau, Simon N. Sponberg, John P. Miller, Robert J. Full

Research output: Contribution to journalArticlepeer-review

8 Scopus citations

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.

Original languageEnglish (US)
Pages (from-to)2344-2354
Number of pages11
JournalJournal of Experimental Biology
Volume218
Issue number15
DOIs
StatePublished - Aug 1 2015

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Physiology
  • Aquatic Science
  • Animal Science and Zoology
  • Molecular Biology
  • Insect Science

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