Temporal Masking Reveals Properties of Sound-Evoked Inhibition in Duration-Tuned Neurons of the Inferior Colliculus

Abstract

The inferior colliculus (IC) is the first place in the central auditory pathway where duration-selective neurons are found. Previous neuropharmacological and electrophysiological studies have shown that they are created there and have led to a conceptual model in which excitatory and inhibitory inputs are offset in time so that the cell fires only when sound duration is such that onset-and offsetevoked excitation coincide; the response is suppressed by inhibition at other durations. We tested predictions from the model using paired tone stimulation and extracellular recording in the IC of the big brown bat, Eptesicus fuscus. Responses to a best duration (BD) tone were used as a probe to examine the strength and time course of inhibition activated by a nonexcitatory (NE) tone of the same frequency but differing in duration. As the relative time between the BD and NE tones was varied, the activity evoked by the BD tone was affected in ways comparable with backward, simultaneous, and forward masking. Responses to the BD tone were completely suppressed at short interstimulus intervals when the BD tone preceded the NE tone. Suppression was also seen when the stimuli temporally overlapped and summed and at intervals when the BD tone followed the NE tone. The results show that duration-selective neurons receive an onsetevoked, inhibitory input that precedes their excitatory input. The period of leading inhibition was correlated with BD and first spike latency. The results suggest how inhibition in the CNS could explain temporal masking phenomena, including backward masking.

Encoding the Timing of Inhibitory Inputs

“…One potential role for delayed excitation of the sort that could be provided by the DCN is the identification of sound duration. Neurons in the IC of both bats and mice can show tuning to the duration of the stimulus (Brand et al 2000;Ehrlich et al 1997), and this depends on an interaction between early inhibition and a delayed excitation in the IC (Faure et al 2003). The delays in excitation that can be provided by the long latencies of DCN pyramidal cells could also contribute to this circuit.…”

Decoding stimulus duration from neural responses in the auditory midbrain

“…Detailed procedures for single unit recording from the ICc of the bat and identifying DTN responses are reported elsewhere (Faure et al 2003;Fremouw et al 2005;Aubie et al 2012). Briefly, a stainless steel post was affixed to the dorsal surface of the skull with cyanoacrylate adhesive 24 -48 h before the first recording session.…”

“…Long-pass DTNs respond only when the stimulus exceeds some minimum duration. Unlike typical sensory neurons that integrate stimulus energy, the minimum duration for evoking a response in a long-pass DTN does not decrease with increasing stimulus amplitude/energy (Faure et al 2003;Sayegh et al 2011;Aubie et al 2012). Because long-pass DTNs do not have a BD, they were not included in this study.…”

“…Spiking responses of short-pass and band-pass DTNs were typically transient and offset-evoked, meaning their first-spike latency (FSL; re stimulus onset) increased with increasing stimulus duration (Faure et al 2003); however, a minority of DTNs with onset-evoked responses and relatively constant FSLs with increasing stimulus duration were also observed and included in our analyses. Tuning profiles of the DTNs included in this study all showed a clear duration-selective response at ϩ20 dB (re threshold).…”

“…We measured spike counts and latencies from auditory DTNs in the mammalian IC to characterize the information content of duration-selective neural responses. Previous studies, including those by the authors, have characterized the spiking profile of DTNs by the shape of the duration tuning curve (i.e., short-pass, band-pass, or long-pass) and defined the neuronal best duration (BD) to be the stimulus duration that evoked the peak spike count (Casseday et al 1994(Casseday et al , 2000Ehrlich et al 1997;Faure et al 2003;Aubie et al 2009Aubie et al , 2012Sayegh et al 2011). To test this hypothesis, we measured information content of DTN spiking responses by calculating the stimulus-specific information (SSI) and estimated observed Fisher information (FI).…”