The dominant role of inhibition in creating response selectivities for communication calls in the brainstem auditory system

This review is concerned with how communication calls are processed and represented by populations of neurons in both the inferior colliculus (IC), the auditory midbrain nucleus, and the dorsal nucleus of the lateral lemniscus (DNLL), the nucleus just caudal to the IC. The review has five sections where focus in each section is on inhibition and its role in shaping response selectivity for communication calls. In the first section, the lack of response selectivity for calls in DNLL neurons is presented and discusses why inhibition plays virtually no role in shaping selectivity. In the second section, the lack of selectivity in the DNLL is contrasted with the high degree of response selectivity in the IC. The third section then reviews how inhibition in the IC shapes response selectivities for calls, and how those selectivities can create a population response with a distinctive response profile to a particular call, which differs from the population profile evoked by any other call. The fourth section is concerned with the specifics of inhibition in the IC, and how the interaction of excitation and inhibition creates directional selectivities for frequency modulations, one of the principal acoustic features of communication signals. The two major hypotheses for directional selectivity are presented. One is the timing hypothesis, which holds that the precise timing of excitation relative to inhibition is the feature that shapes directionality. The other hypothesis is that the relative magnitudes of excitation and inhibition are the dominant features that shape directionality, where timing is relatively unimportant. The final section then turns to the role of serotonin, a neuromodulator that can markedly change responses to calls in the IC. Serotonin provides a linkage between behavioral states and processing. This linkage is discussed in the final section together with the hypothesis that serotonin acts to enhances the contrast in the population responses to various calls over and above the distinctive population responses that were created by inhibition. This article is part of a Special Issue entitled "Communication Sounds and the Brain: New Directions and Perspectives".