Processing of auditory information in insects

Abstract

Insects exhibit an astonishing diversity in the design of their ears and the subsequent processing of information within their auditory pathways. The aim of this review is to summarize and compare the present concepts of auditory processing by relating behavioral performance to known neuronal mechanisms. We focus on three general aspects, that is frequency, directional, and temporal processing. The first part compares the capacity (in some insects high) for frequency analysis in the ear with the rather low specificity of tuning in interneurons by looking at Q10dB values and frequency dependent inhibition of interneurons. Since sharpening of frequency does not seem to be the prime task of a set of differently tuned receptors, alternative hypotheses are discussed. Moreover, the physiological correspondence between tonotopic projections of receptors and dendritic organization of interneurons is not in all cases strong. The second part is concerned with directional hearing and thus with the ability for angular resolution of insects. The present concepts, as derived from behavioral performances, for angular resolution versus lateralization and serial versus parallel processing of directional and pattern information can be traced to the thoracic level of neuronal processing. Contralateral inhibition, a mechanism for enhancing directional tuning, appears to be most effective in parallel pathways, whereas in serial processing it may have detrimental effects on pattern processing. The third part, after some considerations of signal analysis in the temporal domain, demonstrates that closely related species often use different combinations of temporal parameters in their recognition systems. On the thoracic level, analysis of temporal modulation functions and effects of inhibition on spiking patterns reveals relatively simple processing, whereas brain neurons may exhibit more complex properties.

Auditory processing at two time scales by the cricketGryllus bimaculatus

“…By separation of time scales, cricket songs emit short-scale cues, such as the pulse periodicity, and large-scale features, such as the duration or period of chirps (Pollack, 2000). For the perception of both time scales, filter functions are known (Schildberger, 1984;Doherty, 1985a;Hedwig and Poulet, 2004;Hennig et al, 2004;Hennig, 2009). Activation of both filters and thus both time scales is important in crickets, although activation of a single filter may in some cases suffice to elicit positive responses by females (Tschuch, 1977;Hennig, 2009).…”

Timescale-Invariant Representation of Acoustic Communication Signals by a Bursting Neuron

“…Temporal parameters of songs are speciesspecific and decisive for song recognition in most insects that use acoustic signals (Hennig et al, 2004). For ectothermic species, such as grasshoppers, this poses a severe problem because their calling songs are faster or slower depending on the ambient temperature.…”

Resonant neurons and bushcricket behaviour

“…At the same time, detailed modelling of membrane currents is not necessary to reproduce the effects: a basic model of damped resonance is sufficient in this case. It is possible that the resonance could be a property of a neural circuit rather than an individual neuron, although there is some evidence that an identified neuron in the auditory system of the cricket Teleogryllus oceanicus does show a resonant response (Hennig et al 2004). It is interesting to note that the same model system could be driven by a constant tonic input to produce spikes at the pulse rate of the song, and thus could also serve as a pace-maker for the production of the song pattern by the male cricket.…”

“…Female response depends on recognition of the temporal pattern of song pulses. 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.…”