Information processing at a central synapse suggests a noise filter in the auditory pathway of the noctuid moth

Summary

• 1. The central projections of the A1 afferent were confirmed via intracellular recording and staining with Lucifer Yellow in the pterothoracic ganglion of the noctuid moths,Agrotis infusa andApamea amputatrix (Fig. 1). Simultaneous recordings of the A1 afferent in the tympanal nerve (extracellularly) and in the pterothoracic ganglion (intracellularly) confirm the identity of the stained receptor as being the A1 cell.

• 2. The major postsynaptic arborizations of interneurone 501 in the pterothoracic ganglion were also demonstrated via intracellular recording and staining (Fig. 2). Simultaneous recordings of the A1 afferent (extracellularly) and neurone 501 (intracellularly) revealed that each A1 spike evokes a constant short latency EPSP in the interneurone (Fig. 2 Bi). Neurone 501 receives only monaural input from the A1 afferent on its soma side as demonstrated by electrical stimulation of each afferent nerve (Fig. 2Bii). EPSPs evoked in neurone 501 by high frequency (100 Hz) electrical stimulation of the afferent nerve did not decrement (Fig. 2Biii). These data are consistent with a monosynaptic input to neurone 501 from the A1 afferent.

• 3. The response of neurone 501 to a sound stimulus presented at an intensity near the upper limit of its linear response range (30 ms, 16 kHz, 80 dB SPL) was a plateau-like depolarization, with tonic spiking activity which continued beyond the end of the tone. The instantaneous spike frequency of the response was as high as 800 Hz, and was maintained at above 600 Hz for the duration of the tone (Fig. 3).

• 4. The relationship between the instantaneous spike frequency in the A1 afferent and that recorded simultaneously in neurone 501 is linear over the entire range of A1 spike frequencies evoked by white noise sound stimuli (Fig. 4). Similarly, the relationship between instantaneous spike frequency in the A1 afferent and the mean depolarization evoked in neurone 501 is also linear for all A1 spike frequencies tested (Fig. 5). No summation of EPSPs occurred for A1 spike frequencies below 100 Hz.

• 5. There is no evidence of either facilitation or depression of EPSPs in neurone 501 as both the overall level of depolarization and the amplitudes of individual EPSPs remained constant at high spike frequencies in the A1 afferent (Fig. 5). When coupled with the lack of inhibition in responses of neurone 501 to A1 afferent input, the data suggest that summation of synaptic events is also linear.

• 6. Individual EPSPs evoked in neurone 501 by the A1 afferent were recorded and their shapes analysed. The results (Fig. 6, Table 1) show the EPSPs to be of uniform amplitude, with fast rise times and time to peak, short half-widths and total duration, and a small decay time. The existence of such fast EPSPs accounts for the dynamics of information transfer at this first synapse of the auditory pathway.

• 7. The threshold and integration characteristics of neurone 501 suggest that its function in the defensive behaviour of the moth may be as a noise filter allowing the moth to distinguish sources of natural, high frequency sound (e.g., singing insects) from the echolocation calls of hunting bats.