Cholinergic top-down influences on the auditory brainstem

Abstract

Abstract:Descending connections are present in many sensory systems and support adaptive information processing. This allows the sensory brain to code a wider range of inputs. A well characterized descending system is the olivo-cochlear cholinergic innervation of the inner ear, which mediates a reduction of the sensitivity of the inner ear upon perception of intense sounds. Because this inhibits the response to background noise, the olivo-cochlear system supports detection of transient sound events. Olivo-cochlear neurons also innervate the cochlear nucleus through axon collaterals. Here, acetylcholine increases the excitability of central neurons without reducing their temporal precision. Thus their target neurons in the superior olivary complex can more effectively process binaural temporal cues. We argue that the central effect of the olivo-cochlear system augments the peripheral effect. In addition, olivo-cochlear cholinergic neurons are under top-down control of cortical inputs, providing further adaptability of information processing on the level of the auditory brainstem.Keywords: auditory brainstem; sound localization; cochlear nucleus; modulation; acetylcholine Imagine you return to a cocktail party after a quiet walk outside. Suddenly you are in a room filled with loud music and many talking people and are engulfed in intense noisiness coming from many directions. The sound level is much higher now and relevant information can be overpowered ("masked") by the various noise sources in the room. Identification and localization of individual speakers is still possible, although more difficult than in a quiet room. What are the mechanisms in the brain that allow you to do this? Sensory pathways are often mistakenly seen as purely ascending streams of information, where a given neuron feeds information only "upwards" to stations of increasing complexity in a higher hierarchical level. In a wellknown example, time-coding neurons in the cochlear nucleus are contacted by giant synaptic terminals of the auditory nerve (Felmy and Künzel, 2014) and pass information about the timing of the perceived sound up along the auditory pathway into binaural nuclei with more complex functions. These neurons are clearly dominated by information flow from hierarchically lower to higher stations, as the ascending synaptic connection from the auditory nerve onto the time-coding neuron is very powerful. Although it is well established that the auditory periphery and the first stages of the auditory pathway indeed show activity dependent dynamics, these adaptive phenomena can only rely on the limited information that is available at the given neuron. In this scheme, however, the background noise from the cocktail party could easily drown the important information, since one can expect it to activate the ascending stream of auditory information as intense as the relevant auditory event. However, recurrent connections within hierarchical levels and descending connections towards neurons in lower hierarchical orders that provide dyn...

Cholinergic innervation of principal neurons in the cochlear nucleus of the Mongolian gerbil

“…Several studies showed that the cholinergic system modulates the processing of auditory information in the auditory brainstem, including in the CN (Mulders et al, ; see Künzel & Wagner, for a recent review). Notably neurons in AVCN become more excitable under cholinergic influence (Fujino & Oertel, ; Goyer et al, ).…”

“…Cholinergic inputs affect neurons in the dorsal CN (DCN) (Caspary, Havey, & Faingold, ; Irie, Fukui, & Ohmori, ; Manzoor, Chen, & Kaltenbach, ; He, Wang, Petralia, & Brenowitz, ; Stefanescu & Shore, ) and VCN (Caspary et al, ; Fujino & Oertel, ; Goyer et al, ) via nicotinic and muscarinic acetylcholine receptors. However, even for the well‐studied stellate and bushy neurons in the anteroventral cochlear nucleus (AVCN) the role of the cholinergic modulation in hearing has only been vaguely defined (Künzel & Wagner, ). This is complicated by the fact that cholinergic axons projecting into the CN arise from more than one source: a large portion of cholinergic inputs to the CN are formed by collaterals of the descending olivocochlear bundle (OCB; Ryan, Keithley, Wang, & Schwartz, ; Horváth, Kraus, & Illing, ; Mulders, Winter, & Robertson, ; Guinan, ; Kishan, Lee, & Winer, ; Baashar, Robertson, & Mulders, ).…”

“…However, even for the well-studied stellate and bushy neurons in the anteroventral cochlear nucleus (AVCN) the role of the cholinergic modulation in hearing has only been vaguely defined (K€ unzel & Wagner, 2017). This is complicated by the fact that cholinergic axons projecting into the CN arise from more than one source: a large portion of cholinergic inputs to the CN are formed by collaterals of the descending olivocochlear bundle (OCB; Ryan, Keithley, Wang, & Schwartz, 1990;Horv ath, Kraus, & Illing, 2000;Mulders, Winter, & Robertson, 2002;Guinan, 2006;Kishan, Lee, & Winer, 2011;Baashar, Robertson, & Mulders, 2015).…”

Cholinergic modulation in the vertebrate auditory pathway

“…Cholinergic olivo-cochlear neurons include medial olivo-cochlear (MOC) and lateral olivo-cochlear (LOC) neurons. The anatomy and physiology of these efferent circuits has been reviewed in detail ( Ciuman, 2010 ; Künzel and Wagner, 2017 ; Fuchs and Lauer, 2019 ; Romero and Trussell, 2022 ). The efferent synaptic inhibition at cochlear hair cells has been shown to involve α9α10-containing nicotinic receptors ( Elgoyhen et al, 1994 , 2001 ; Taranda et al, 2009 ).…”

“…The effect of the olivo-cochlear reflex on the input–output encoding function of auditory fibers is well-known and has been thoroughly reviewed ( Guinan, 1996 ; Künzel and Wagner, 2017 ). It has also been suggested that activation of the olivo-cochlear reflex could improve signal detection from noisy backgrounds by transiently enhancing acoustic gain in auditory fibers ( Winslow and Sachs, 1988 ; Kawase et al, 1993 ).…”