Encoding of Sound Localization Cues by an Identified Auditory Interneuron: Effects of Stimulus Temporal Pattern

Abstract

An important cue for sound localization is binaural comparison of stimulus intensity. Two features of neuronal responses, response strength, i.e., spike count and/or rate, and response latency, vary with stimulus intensity, and binaural comparison of either or both might underlie localization. Previous studies at the receptor-neuron level showed that these response features are affected by the stimulus temporal pattern. When sounds are repeated rapidly, as occurs in many natural sounds, response strength decreases and latency increases, resulting in altered coding of localization cues. In this study we analyze binaural cues for sound localization at the level of an identified pair of interneurons (the left and right AN2) in the cricket auditory system, with emphasis on the effects of stimulus temporal pattern on binaural response differences. AN2 spike count decreases with rapidly repeated stimulation and latency increases. Both effects depend on stimulus intensity. Because of the difference in intensity at the two ears, binaural differences in spike count and latency change as stimulation continues. The binaural difference in spike count decreases, whereas the difference in latency increases. The proportional changes in response strength and in latency are greater at the interneuron level than at the receptor level, suggesting that factors in addition to decrement of receptor responses are involved. Intracellular recordings reveal that a slowly building, long-lasting hyperpolarization is established in AN2. At the same time, the level of depolarization reached during the excitatory postsynaptic potential (EPSP) resulting from each sound stimulus decreases. Neither these effects on membrane potential nor the changes in spiking response are accounted for by contralateral inhibition. Based on comparison of our results with earlier behavioral experiments, it is unlikely that crickets use the binaural difference in latency of AN2 responses as the main cue for determining sound direction, leaving the difference in response strength, i.e., spike count and/or rate, as the most likely candidate.

A Behavioral Role for Feature Detection by Sensory Bursts

“…Responses to long-lasting stimuli with Gaussian amplitude envelopes consist, after a rapid adaptation phase (Samson and Pollack, 2002), of both isolated spikes, separated by relatively long and variable ISIs, and of bursts, consisting of groups of spikes separated by short ISIs (typically 3-4 ms) (Fig. 1a).…”

“…Figure 3c shows the temporal distribution of spikes or bursts in the AN2 contralateral to the sound source relative to those in its ipsilateral counterpart. We focus on bilateral differences within the range of Ϯ10 ms, which encompasses the range of previously measured binaural latency differences of AN2 for trains of discrete sound pulses (Samson and Pollack, 2002). For 23% of ipsilateral bursts, a contralateral burst occurs within Ϯ10 ms (the area under the curve).…”

Effect of the Temporal Pattern of Contralateral Inhibition on Sound Localization Cues

“…For monaural stimulation with a 30 kHz RAM stimulus, short ISIs (Ͻ5 ms) are frequent during both time periods. In the sustained portion of the response, after adaptation is established (Samson and Pollack, 2002), AN2 spikes occur in bursts of highfrequency firing separated by more sparsely spaced spikes, as indicated by the bimodal distribution of ISIs typical of bursting neurons (Fig. 7B).…”

“…The probability of responding to ultrasound stimuli does not depend on stimulus temporal pattern, although temporal pattern may affect sustained responses (Pollack and ElFeghaly, 1993). Stimulus direction is determined from bilateral comparison of activity in AN2 (Nolen and Hoy, 1984;Samson and Pollack, 2002).…”

Central projections of auditory receptor neurons of crickets

“…Crickets use acoustic signals to recognize and localize both conspecifics and predators (echolocating bats). A number of recent studies have used electrophysiological, behavioral, and computational approaches to investigate the neural mechanisms underlying signal detection, frequency analysis, temporal processing, sound localization, and signal recognition (Imaizumi andPollack, 1999, 2001;Samson and Pollack, 2002;Hennig, 2003;Pollack, 2003;Nabatiyan et al, 2003;Reeve and Webb, 2003;Hedwig and Poulet, 2004;Pollack, 2004, 2005;Tunstall and Pollack, 2005). Relatively little is known, however, about the anatomical substrates of neural processing.…”