The superior paraolivary nucleus shapes temporal response properties of neurons in the inferior colliculus

Abstract

The mammalian superior paraolivary nucleus (SPON) is a major source of GABAergic inhibition to neurons in the inferior colliculus (IC), a well-studied midbrain nucleus that is the site of convergence and integration for the majority ascending auditory pathways en route to the cortex. Neurons in the SPON and IC exhibit highly precise responses to temporal sound features, which are important perceptual cues for naturally occurring sounds. To determine how inhibitory input from the SPON contributes to the encoding of temporal information in the IC, a reversible inactivation procedure was conducted to silence SPON neurons while recording responses to amplitude-modulated tones and silent gaps between tones in the IC. The results show that SPON-derived inhibition shapes responses of onset and sustained units in the IC via different mechanisms. Onset neurons appear to be driven primarily by excitatory inputs and their responses are shaped indirectly by SPON-derived inhibition, whereas sustained neurons are heavily influenced directly by transient offset inhibition from the SPON. The findings also demonstrate that a more complete dissection of temporal processing pathways is critical for understanding how biologically important sounds are encoded by the brain.

Auditory deficits of Kcna1 deletion are similar to those of a monaural hearing impairment

“…The broad frequency tuning in wild type SPN neurons (Dehmel et al, 2002) enables across frequency integration to the benefit of better temporal resolution. The correct integration of convergent information of both SPNs within the inferior colliculus (Felix et al, 2014) might be the reason for the better performance of Kcna1 +/+ in the binaural gap detection task.…”

Cellular Computations Underlying Detection of Gaps in Sounds and Lateralizing Sound Sources

“…2, 3) [18, 66]. Third, their targets in the SPON could contribute to gap detection by signaling the offsets of sounds [70, 102–105]. Fourth, the finding that the reduction in g h is compounded by a reduction in g KL in octopus cells of Hcn1 −/− mice whereas the deficit in g KL is compensated in Kcna −/− mice could account for why there is a deficit in gap detection in Hcn1 −/− mice while there is no detectable deficit in Kcna −/− mice (Fig.…”

Forward masking in the superior paraolivary nucleus of the rat

“…In the awake marmoset preparation, Nelson et al (2009) proposed that SPON-derived offset inhibition may play a critical role in mediating forward masking in the IC. A recent study in our laboratory (Felix et al 2014) explored how the SPON contributes to gap detection and the processing of sinusoidally amplitude modulated (SAM) stimuli in the IC, and found that inactivation of the SPON significantly increased gap detection thresholds and decreased synchronization to SAM stimuli in IC units producing sustained responses. Thus, the main function of SPON-derived inhibition in the IC appears to be inducing a temporal segmentation of IC responses.…”

“…Thus, the MNTB and the SPON form a neural circuit that transforms an excitatory input from globular bushy cells into a transient GABAergic signal that occurs in response to stimulus offsets and discontinuities (Kadner and Berrebi 2008; Felix et al 2011). By reversibly inactivating the SPON, we recently demonstrated that SPON-derived inhibition serves to induce temporal segmentation in responses of IC neurons (Felix et al 2014). Taken together, these findings suggest that the SPON offset response may play a critical role in mediating forward masking in the IC.…”