Pulse-rate recognition in an insect: evidence of a role for oscillatory neurons

Abstract

Various mechanisms have been proposed as the neural basis for pulse-rate recognition in insects and anurans, including models employing high- and low-pass filters, autocorrelation, and neural resonance. We used the katydid Tettigonia cantans to test these models by measuring female responsiveness on a walking compensator to stimuli varying in temporal pattern. Each model predicts secondary responses to certain stimuli other than the standard conspecific pulse rate. Females responded strongly to stimuli with a pulse-rate equal to half the standard rate, but not to stimuli with double the standard rate. When every second pulse or interval was varied in length, females responded only when the resulting stimuli were rhythmic with respect to the period of the standard signal. These results provide evidence rejecting the use of either high-/low-pass filter networks or autocorrelation mechanisms. We suggest that rate recognition in this species relies on the resonant properties of neurons involved in signal recognition. According to this model, signals with a pulse rate equal to the resonant frequency of the neurons stimulate the female to respond. The results are discussed with regard to both neural and evolutionary implications of resonance as a mechanism for signal recognition.

Resonant neurons and bushcricket behaviour

“…1 and 2 we show that this simple model reproduces all the ''resonant'' properties of the bush cricket behaviour described in Bush and Schul (2006). Pulses of a constant duration (18 ms) played at frequencies from 8 to 67 Hz, produce the expected peak at 25 Hz, a second peak of half the size at 12.5 Hz, and a smaller increase at 8 Hz.…”

“…However, the mechanism by which this recognition occurs is still a matter of debate (Hennig et al 2004). Behavioural experiments on the bushcricket Tettigonia cantans (Bush and Schul 2006) compared three alternative explanations for the female's band-pass preference for the pulse rate in male song: a circuit involving separate high-pass and low-pass filters; autocorrelation; and resonance. A stronger response to songs at integer fractions of the preferred frequency, and to other nonnatural songs that reinforce that rhythm, suggested that resonance is the best explanation.…”

Calling Song Recognition in Female Crickets: Temporal Tuning of Identified Brain Neurons Matches Behavior

“…Our recordings did not provide evidence for resonance in the auditory network as stimulation with calling song patterns did not lead to ongoing oscillations of the membrane potential of any of the neurons recorded. Furthermore, neither our behavioral data nor the response functions of our neurons revealed a secondary peak at one-half of the optimal pulse period as suggested by Bush and Schul (2006). Only the membrane potential of B-LC3 in some preparations transiently oscillated at ϳ34 Hz when stimulated with a constant tone of 160 ms (Fig.…”

“…Evidence from Bush and Schul (2006) indicated that pattern selectivity may result from intrinsic membrane potential oscillations of auditory neurons resonating with the frequency of the species-specific pulse pattern. Our recordings did not provide evidence for resonance in the auditory network as stimulation with calling song patterns did not lead to ongoing oscillations of the membrane potential of any of the neurons recorded.…”

“…Hoy (1978) speculated that such an internal template could be derived from the same neural network that drives the central pattern generator for singing in males. Data from Bush and Schul (2006) indicate that temporal pattern recognition may be achieved by oscillatory responses of individual neurons. Based on intracellular recordings of auditory brain neurons, Schildberger (1984) suggested that temporal filtering is established by sequential processing in low-pass and high-pass filter neurons that finally shape the bandpass response properties of brain neurons that match the temporal tuning of female phonotaxis.…”