Auditory change detection by a single neuron in an insect

Abstract

The detection of novel signals in the auditory scene is an elementary task of any hearing system. In Neoconocephalus katydids, a primary auditory interneuron (TN-1) with broad spectral sensitivity, responded preferentially to rare deviant pulses (7 pulses/s repetition rate) embedded among common standard pulses (140 pulses/s repetition rate). Eliminating inhibitory input did not affect the detection of the deviant pulses. Detection thresholds for deviant pulses increased significantly with increasing amplitude of standard pulses. Responses to deviant pulses occurred when the carrier frequencies of deviant and standard were sufficiently different, both when the deviant had a higher or lower carrier frequency than the standard. Recordings from receptor neurons revealed that TN-1 responses to the deviant pulses did not depend on the population response strength of the receptors, but on the distribution of the receptor cell activity. TN-1 responses to the deviant pulse occurred only when the standard and deviant pulses were transmitted by different groups of receptor cells. TN-1 responses parallel stimulus specific adaptation (SSA) described in mammalian auditory system. The results support the hypothesis that the mechanisms underlying SSA and change-detection are located in the TN-1 dendrite, rather than the receptor cells.

Neural Mechanisms for Acoustic Signal Detection under Strong Masking in an Insect

“…The second mechanism for signal detection under noise is based on novelty detection as described previously (Schul and Sheridan, 2006;Schul et al, 2012;Siegert et al, 2013). The mechanism has two characteristics: broadband interneurons are excited with bursts of APs at the onset of the trill, but show subsequent strong adaptation.…”

“…However, these interneurons exploit the entire frequency range for responses to unmasked chirps. Schul and Sheridan (2006) described a similar mechanism for the detection of a bat echolocation signal in the presence of a continuous call of a conspecific with reliable responses to the bat call at SNRs of Ϫ18 dB at the masked threshold. Triblehorn and Schul (2013) suggested a model that stimulus-specific adaptation may occur in the dendrites for one signal without preventing a response to the other signal.…”

“…We identified three interneurons where the response to the continuous trill exhibits strong adaptation. In contrast, the response to the chirp is unaffected by the adaptation because of the 2 kHz component of the chirp not present in the trill (novelty detection; as suggested by Schul andSheridan, 2006 andSchul et al, 2012).…”

“…These mechanisms are shaped by exploiting the activity of receptors that are tuned to the 2 kHz component of the chirp: (1) selective tuning where some interneurons are selectively tuned to this low-frequency component and respond only to conspecific chirps and (2) novelty detection where broadly tuned interneurons use a mechanism called "novelty detection" (Schul et al, 2012) in which strong adaptation in response to the continuous trill ensures a selective response to the frequency "novelty" in the chirp. The responses of these specific interneurons sufficiently explain the reliable signal detection observed in behavior, even at very low SNRs.…”

Dynamic dendritic compartmentalization underlies stimulus-specific adaptation in an insect neuron

“…The Neoconocephalus (Orthoptera: Tettigoniidae) TN-1 neuron reliably responded to deviant pulses after responses to common standard pulses ceased, provided the standard and deviant pulses differed sufficiently in their carrier frequency (pitch) (Schul and Sheridan 2006;Schul et al 2012). Extensive physiological testing (Schul et al 2012) revealed that TN-1 adaptation to fast pulse rates did not result from 1) adaptation of its afferents, 2) synaptic depression of the afferent TN-1 excitatory synapses, or 3) known inhibitory inputs to TN-1. However, injection of a calcium chelator into TN-1 significantly delayed the adaptation to repeated stimulation; application of low-sodium saline significantly reduced adaptation to standard pulses (Triblehorn and Schul 2013).…”