Auditory DUM neurons in a bush‐cricket: A filter bank for carrier frequency

Abstract

In bush-crickets the first stage of central auditory processing occurs in the prothoracic ganglion. About 15 to 50 different auditory dorsal unpaired median neurons (DUM neurons) exist but they have not been studied in any detail. These DUM neurons may be classified into seven different morphological types, although, there is only limited correlation between morphology and physiological responses. Ninety seven percent of the stained neurons were local, 3% were intersegmental. About 90% project nearly exclusively into the auditory neuropile, and 45% into restricted areas therein. Lateral extensions overlap with the axons of primary auditory sensory neurons close to their branching point. DUM neurons are typically tuned to frequencies covering the range between 2 and 50 kHz and thereby may establish a filter bank for carrier frequency. Less than 10% of DUM neurons have their branches in adjacent and more posterior regions of the auditory neuropile and are mostly tuned to low frequencies, less sensitive than the other types and respond to vibration. Thirty five percent of DUM show indications of inhibition, either through reduced responses at higher intensities, or by hyperpolarizing responses to sound. Most DUM neurons produce phasic spike responses preferably at higher intensities. Spikes may be elicited by intracellular current injection. Preliminary data suggest that auditory DUM neurons have GABA as transmitter and therefore may inhibit other auditory interneurons. From all known local auditory neurons, only DUM neurons have frequency specific responses which appear suited for local processing relevant for acoustic communication in bush crickets.

Auditory DUM neurons in a bush-cricket: inhibited inhibitors

“…Picrotoxin eliminated or strongly reduced inhibition in auditory neurons of various bush-crickets (Stumpner 1998(Stumpner , 2002 and did so in DUM neurons as well. Obvious hyperpolarizing response of DUM neurons, which is typical for certain DUM neurons at specific frequencies and intensities (see Lefebvre et al 2018; Fig. 4) was lost or even replaced by excitation, similar as reported also for the AN1-neuron of A. nigrovittata (Stumpner 1998).…”

“…These neurites divided into the two typical U-shaped secondary and tertiary neurites projecting anteriorly to the edges of the auditory neuropile. This represents fully the described DUM neuron types "narrow" and "loops", which constitute the majority of auditory DUM neurons (Lefebvre et al 2018). The stainings of neuropilar structures often were more or less spotty and did not allow precise counting of such neurites, but clearly whole groups of such neurites were visible in the majority of ganglia-in general one could estimate about 5 to at least 10 of such secondary neurites in a prothoracic ganglion section.…”

“…At 50 dB SPL, the average tuning broadened following PTX application by 1.99 ± 4.76 kHz (N = 40) and following ringer application by only 0. Negative deflections occurring in the rising flank, interpreted as IPSPs before (Lefebvre et al 2018;Stumpner et al 2019), were abolished by PTX -application (Fig. 5a).…”

“…As a conclusion, few small GABA-negative somata may exist in A. nigrovittata, and they might belong to auditory DUM neurons. Therefore, it seems safe to conclude that the vast majority of auditory DUM-neurons contain GABA as a transmitter, which fits to their presumed inhibitory nature (Lefebvre et al 2018). One DUM neuron ("AV4") in the brain of D. melanogaster, which has been described as a member of a set of auditory temporal filters is GABAergic as well (Clemens et al 2015).…”

“…In sections that included the correct layer and were sufficiently thick, both levels of anteriorly directed secondary and tertiary neurites were visible (see Fig. 3a: orange and green neurites; see also online resource movie ESM3/M2 and Lefebvre et al 2018). Counting the number showing a well separated cluster of at least 32 medial somata, primary neurites originating from that cluster and at least nine secondary neurites of typical auditory DUM neuron shape projecting towards the auditory neuropile.…”