The physiology of ascending auditory interneurons in the tettigoniidCaedicia simplex (Orthoptera: Ensifera): response properties and a model of integration in the afferent auditory pathway

Abstract

1. Single unit recording from the oesophageal connectives was used to characterise the physiological responses to monaural stimulation of ascending auditory interneurons in the tettigoniidCaedicia simplex. 2. In terms of characteristic patterns of spike discharge, ascending auditory interneurons have been classified as tonic, phasic-tonic or phasic (Fig. 1). 3. According to suprathreshold, isoresponse criteria, tonic interneurons either are broadlytuned between 10–16 kHz or are more narrowlytuned to a single sound frequency below 10 kHz (Fig. 2A). All tonic interneurons recorded have a roll-off in sensitivity of 20–40 dB/octave above and below their frequencies of maximum sensitivity. This corresponds with the roll-offs applicable to primary afferent fibres. 4. Most phasic-tonic interneurons display uniform sensitivity to one of three different frequency bands (about 3 kHz in width) in the range 10-18 kHz (Fig. 2B). These three classes of phasictonic interneuron have roll-off in sensitivity of more than 50 dB/octave for sound frequencies below their range of maximum sensitivity. 5. In contrast, a distinct class of phasic-tonic interneuron is sharply-tuned to 16 kHz, the species' call frequency (Fig. 3 A). The roll-off in sensitivity of this class of interneuron 40–50 dB/octave for frequencies above and greater than 50 dB/octave for frequencies below 16 kHz. For frequencies below 16 kHz, this roll-off in sensitivity exceeds that of primary afferent fibres by a factor of two (Fig. 3B). 6. Phasic interneurons each are tuned to a single sound frequency in the range 10–16 kHz and have roll-off's in sensitivity of 40–50 dB/octave above and 20–30 dB/octave below their frequency of maximum sensitivity (Fig. 2C). 7. For tonic interneurons, a positive, approximately linear relationship exists between sound intensity and spike response that is similar for different sound frequencies (Fig. 4 A). 8. Phasic-tonic interneurons have a complex intensity-response characteristic that is dependent on sound frequency (Fig. 4B). For frequencies within or above the range of maximum sensitivity, the response increases at a rate of 6 spikes/20 dB, saturates at 10–12 spikes/stimulus and may then decline to as little as 2–3 spikes/stimulus at the higher sound intensities. For frequencies below the band of highest sensitivity the gradient, maximum response and dynamic range of the intensity characteristic progressively decrease. 9. Phasic interneurons produce a maximum of 2–4 spikes/stimulus and, as with tonic interneurons, the intensity characteristic is independent of sound frequency (Fig. 4C). 10. Two-tone experiments demonstrate that phasic-tonic interneurons are inhibited by a sensory response to sound frequencies below their band of highest sensitivity (Fig. 5) and that the onset of this inhibition is delayed by 20 ms, relative to that of excitation (Fig. 6). Similar two-tone experiments conducted on primary afferent fibres demonstrate that no such inhibition occurs at the periphery (Fig. 7). 11. Based on idealized frequency and intensity characteristics of primary afferent fibres (Fig. 8) derived from empirical data (Oldfield 1982, 1983) and on the characteristics of monaurally-stimulated ascending interneurons, a simple model of integration is developed, in which the response of each class of ascending interneuron is attributed to the sum of the inferred excitatory and inhibitory inputs provided by an array of separately-tuned primary afferent fibres. The model accurately predicts the responses of ascending auditory interneurons inC. simplex for the monaural case (Fig. 9).