The auditory corticocollicular system: Molecular and circuit-level considerations

Abstract

We live in a world imbued with a rich mixture of complex sounds. Successful acoustic communication requires the ability to extract meaning from those sounds, even when degraded. One strategy used by the auditory system is to harness high-level contextual cues to modulate the perception of incoming sounds. An ideal substrate for this process is the massive set of top-down projections emanating from virtually every level of the auditory system. In this review, we provide a molecular and circuit-level description of one of the largest of these pathways: the auditory corticocollicular pathway. While its functional role remains to be fully elucidated, activation of this projection system can rapidly and profoundly change the tuning of neurons in the inferior colliculus. Several specific issues are reviewed. First, we describe the complex heterogeneous anatomical organization of the corticocollicular pathway, with particular emphasis on the topography of the pathway. We also review the laminar origin of the corticocollicular projection and discuss known physiological and morphological differences between subsets of corticocollicular cells. Finally, we discuss recent findings about the molecular micro-organization of the inferior colliculus and how it interfaces with corticocollicular termination patterns. Given the assortment of molecular tools now available to the investigator, it is hoped that his review will help guide future research on the role of this pathway in normal hearing.

Connectional Modularity of Top-Down and Bottom-Up Multimodal Inputs to the Lateral Cortex of the Mouse Inferior Colliculus

“…Chernock et al (2004) reported previously that modules positive for GAD-67, PV, AChE, CO, and NADPH-d are present in the rat, but are absent in mouse, squirrel, cat, bat, macaque monkey, and barn owl. However, images of mouse tissue from other sources depict modular staining patterns in the LC for GAD-67, AChE, NADPH-d, and CO (Gonzalez-Lima and Cada, 1994;Paxinos and Franklin, 2004;Ono et al, 2005;Stebbings et al, 2014;Choy Buentello et al, 2015). In addition, images of stained tissue from other species reveal modules in the LC of the gerbil and the rhesus macaque (Paxinos et al, 1999;Cant and Benson, 2005).…”

“…The LC also receives top-down information from the superior colliculus (SC) and the somatosensory, auditory, and visual cortices (Cooper and Young, 1976;Robards, 1979;Adams, 1980;Faye-Lund, 1985;Winer et al, 1998). Previous studies that have mapped the terminal distributions of these pathways show that many of them form discontinuous patches within the LC in a number of species, including the mouse, guinea pig, cat, and monkey (Wise and Jones, 1977;Wiberg and Blomqvist, 1984;Faye-Lund and Osen, 1985;Wiberg et al, 1987;Saldaña and Merchań , 1992;Saldaña et al, 1996;Zhou and Shore, 2006;Stebbings et al, 2014).…”

“…Though Chernock et al (2004) have suggested that these modules are unique to the rat IC, they are clearly visible in mouse tissue stained for GAD-67, NADPH-d, AChE, and CO (Gonzalez-Lima and Cada, 1994;Paxinos and Franklin, 2004;Ono et al, 2005;Stebbings et al, 2014;Choy Buentello et al, 2015). In the present study, we sought to confirm the presence of these neurochemical modules in the mouse IC and to determine whether each marker stains the same set of modules or whether multiple modular networks exist within the LC.…”

Subcortical processing in auditory communication

“…The inferior colliculus (IC) forms a major convergence region within the auditory system, as it receives feed-forward projections from the auditory brainstem (Oliver, 1984(Oliver, , 1987Glendenning et al, 1992;Saint Marie et al, 1997), feedback projections from the auditory cortex (Winer et al, 1998;Winer, 2006;Stebbings et al, 2014 for a comprehensive review), and commissural connections from contralateral structures (Aitkin and Phillips, 1984). In turn, the IC sends descending fibres to a variety of brainstem nuclei (Huffman and Henson, 1990), and ascending projections to the auditory thalamus (Andersen et al, 1980).…”

Detailed Analysis of High Frequency Auditory Brainstem Response in Patients with Tinnitus: A Preliminary Study

“…These structures generate multiple feedback loops that extract meaning from afferent stimulation through modulation 14,15 . Cortical stimulation affects the tuning curves of subcortical structures causing specific regions in the subcortical system to become robustly tuned to higher levels of activity [16][17][18] .…”