Animals can expend energy to acquire sensory information by emitting signals and/or moving sensory structures. We propose that the energy from locomotion itself could permit control of a sensor, whereby animals use the energy from movement to reconfigure a passive sensor. We investigated high-speed, antenna-mediated tactile navigation in the cockroach Periplaneta americana. We discovered that the passive antennal flagellum can assume two principal mechanical states, such that the tip is either projecting backward or forward. Using a combination of behavioral and robotic experiments, we demonstrate that a switch in the antenna's state is mediated via the passive interactions between the sensor and its environment, and this switch strongly influences wall-tracking control. When the tip of the antenna is projected backward, the animals maintain greater body-to-wall distance with fewer body collisions and less leg–wall contact than when the tip is projecting forward. We hypothesized that distally pointing mechanosensory hairs at the tip of the antenna mediate the switch in state by interlocking with asperities in the wall surface. To test this hypothesis, we performed laser ablation of chemo-mechanosensory hairs and added artificial hairs to a robotic antenna. In both the natural and artificial systems, the presence of hairs categorically increased an antenna's probability of switching state. Antennal hairs, once thought to only play a role in sensing, are sufficient for mechanically reconfiguring the state of the entire antenna when coupled with forward motion. We show that the synergy between antennal mechanics, locomotion and the environment simplifies tactile sensing.
J.-M.M., A.D., J.L., N.J.C. and R.J.F. designed the experiments. J.-M.M., A.D. and J.L. conducted experiments and analysed the data. J.-M.M., A.D., N.J.C. and R.J.F. wrote the manuscript.
No competing interests declared.
This material is based upon work supported by the National Science Foundation (NSF) [Graduate Research Fellowship to J.-M.M.; Integrative Graduate Education and Research Traineeship Program 0903711 to R.J.F. and J.-M.M., CISE-0845749 to N.J.C. and A.D.]; and the United States Army Research Laboratory [Micro Autonomous Systems and Technology Collaborative Technology Alliance W911NF-08-2-0004 to R.J.F.].
- © 2013. Published by The Company of Biologists Ltd