Mechanisms of spectral and temporal integration in the mustached bat inferior colliculus

Abstract

This review describes mechanisms and circuitry underlying combination-sensitive response properties in the auditory brainstem and midbrain. Combination-sensitive neurons, performing a type of auditory spectro-temporal integration, respond to specific, properly timed combinations of spectral elements in vocal signals and other acoustic stimuli. While these neurons are known to occur in the auditory forebrain of many vertebrate species, the work described here establishes their origin in the auditory brainstem and midbrain. Focusing on the mustached bat, we review several major findings: (1) Combination-sensitive responses involve facilitatory interactions, inhibitory interactions, or both when activated by distinct spectral elements in complex sounds. (2) Combination-sensitive responses are created in distinct stages: inhibition arises mainly in lateral lemniscal nuclei of the auditory brainstem, while facilitation arises in the inferior colliculus (IC) of the midbrain. (3) Spectral integration underlying combination-sensitive responses requires a low-frequency input tuned well below a neuron's characteristic frequency (ChF). Low-ChF neurons in the auditory brainstem project to high-ChF regions in brainstem or IC to create combination sensitivity. (4) At their sites of origin, both facilitatory and inhibitory combination-sensitive interactions depend on glycinergic inputs and are eliminated by glycine receptor blockade. Surprisingly, facilitatory interactions in IC depend almost exclusively on glycinergic inputs and are largely independent of glutamatergic and GABAergic inputs. (5) The medial nucleus of the trapezoid body (MNTB), the lateral lemniscal nuclei, and the IC play critical roles in creating combination-sensitive responses. We propose that these mechanisms, based on work in the mustached bat, apply to a broad range of mammals and other vertebrates that depend on temporally sensitive integration of information across the audible spectrum.

Blurry topography for precise target-distance computations in the auditory cortex of echolocating bats

“…7). This timing result is in accordance with previous studies showing that pulse-evoked inhibition controls the latency of delay-tuned responses 25 . In all three species, the neuronal latency measured at the CD-MT point of the DRF was weakly correlated with the CD (that is, R ¼ 0.4 (P. quadridens and P. parnellii) and R ¼ 0.5 (C. perspicillata); see Supplementary Fig.…”

BOLD fMRI study of ultrahigh frequency encoding in the inferior colliculus

“…Such neurons exhibit either excitatory or inhibitory responses when two tones with distinctly different frequencies are presented simultaneously. It has been shown that facilitatory and inhibitory combination sensitivity originate in the IC and LL, respectively , with inhibition mechanisms and glycinergic inputs playing critical roles in creating such responses Wenstrup, 2005, 2006;Wenstrup et al, 2012). Previous electrophysiological studies also reported similar percentage of facilitatory and inhibitory combination-sensitive neurons.…”

“…Based on electrophysiological studies, they should also operate for combinations of an UHF and a lower frequency (Portfors and Felix, 2005;Portfors and Roberts, 2014;Portfors et al, 2009;Wenstrup et al, 2012). Such combinations were not examined in the present study, because a lower frequency itself would be expected to evoke BOLD responses, which would confound the combination-or distortion-evoked responses.…”

“…Combination sensitive neurons have been examined extensively in the IC of bats (Leroy and Wenstrup, 2000;Mittmann and Wenstrup, 1995;Wenstrup, 2005, 2006;Peterson et al, 2008;Portfors, 2004;Portfors and Wenstrup, 2002;Wenstrup et al, 2012) and mice (Felix and Portfors, 2007;Portfors and Felix, 2005). Such neurons exhibit either excitatory or inhibitory responses when two tones with distinctly different frequencies are presented simultaneously.…”

Cortical neurons of bats respond best to echoes from nearest targets when listening to natural biosonar multi-echo streams

“…The smaller the echo-delay the shorter the distance to an object. Within the ascending auditory pathway, neurons whose response is facilitated when presented with specific echo-delays can be found as early as in the auditory midbrain11 and these neurons are defined as target-distance or delay-tuned neurons.…”