The role of distributed viscoelastic coupling in sensory adaptation in an insect mechanoreceptor

Abstract

1. Time-dependent mechanical coupling in proprioceptive campaniform sensilla of the cockroach leg was investigated by measuring the compliance of the sensillar cap with punctate, sinusoidal mechanical stimuli at forcing frequencies ranging 3 mHz (0.003 Hz) to 100 Hz. Coupling was described in terms of linear transfer functions for cap compliance and for sensory discharge sensitivity to both cap indentation and applied force. 2. Most sensilla stiffened viscoelastically as a power of frequency, with median power coefficient −0.058 for compliance, and with indentation lagging force by a constant phase angle, median −8.4°. This behavior indicates broadly distributed viscoelastic rate constants in individual sensilla. The extent of viscoelasticity also varied among sensilla; about a third were purely elastic, with constant compliance and zero phase angle. 3. Discharge sensitivity increased with forcing frequency, usually as a power function, and the sinusoidally modulated discharge peaked sooner than both indentation and force by essentially constant phase angles. Median power coefficients were 0.51 for indentation sensitivity and 0.38 for force sensitivity; corresponding phase angles were somewhat smaller than for a power law, respective medians 39° and 30°. Purely elastic caps gave identical values for indentation and force. 4. This means all sensilla adapted, and all were rate sensitive; but in viscoelastic ones these effects were greater for indentation than for force. 5. Discharge sensitivity for a few sensilla deviated systematically from a power law in that power coefficients and phase angles increased somewhat with forcing frequency. 6. Computed responses for viscoelastic caps showed creep under constant force, and stress relaxation under constant indentation, with faster and greater sensory adaptation for indentation than for force. 7. We conclude cap compliance exerts a mild filtering action throughout the entire time course of adaptation in viscoelastic sensilla, but has no role in the adaptation of purely elastic ones.