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Cholinergic Top-Down Influences on the Auditory Brainstem

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Cholinergic Top-Down Influences on the Auditory Brainstem Neuroforum 2017; 23(1): A35–A44 Thomas Künzel* and Hermann Wagner Cholinergic top-down influences on the auditory brainstem DOI 10.1515/nf-2016-A107 Sensory pathways are often mistakenly seen as purely ascending streams of information, where a given neuron Abstract: Descending connections are present in many feeds information only “upwards” to stations of increas- sensory systems and support adaptive information pro- ing complexity in a higher hierarchical level. In a well- cessing. This allows the sensory brain to code a wider known example, time-coding neurons in the cochlear range of inputs. A well characterized descending system nucleus are contacted by giant synaptic terminals of the is the olivo-cochlear cholinergic innervation of the inner auditory nerve (Felmy and Künzel, 2014) and pass infor- ear, which mediates a reduction of the sensitivity of the mation about the timing of the perceived sound up along inner ear upon perception of intense sounds. Because this the auditory pathway into binaural nuclei with more com- inhibits the response to background noise, the olivo-coch- plex functions. These neurons are clearly dominated by lear system supports detection of transient sound events. information flow from hierarchically lower to higher sta- Olivo-cochlear neurons also innervate the cochlear nucle- tions, as the ascending synaptic connection from the au- us through axon collaterals. Here, acetylcholine increases ditory nerve onto the time-coding neuron is very powerful. the excitability of central neurons without reducing their Although it is well established that the auditory periphery temporal precision. Thus their target neurons in the supe- and the first stages of the auditory pathway indeed show rior olivary complex can more effectively process binau- activity dependent dynamics, these adaptive phenomena ral temporal cues. We argue that the central effect of the can only rely on the limited information that is available olivo-cochlear system augments the peripheral effect. In at the given neuron. In this scheme, however, the back- addition, olivo-cochlear cholinergic neurons are under ground noise from the cocktail party could easily drown top-down control of cortical inputs, providing further the important information, since one can expect it to ac- adaptability of information processing on the level of the tivate the ascending stream of auditory information as in- auditory brainstem. tense as the relevant auditory event. However, recurrent Keywords: auditory brainstem; sound localization; coch- connections within hierarchical levels and descending lear nucleus; modulation; acetylcholine connections towards neurons in lower hierarchical orders that provide dynamic and adaptive changes to the senso- ry systems are common in all sensory modalities (Engel et al., 2001; Briggs and Usrey, 2011; Gilbert and Li, 2013; Imagine you return to a cocktail party after a quiet walk D’Souza and Vijayaraghavan, 2014; Llorca-Torralba et al., outside. Suddenly you are in a room filled with loud mu- 2016), including the auditory brainstem. One especial- sic and many talking people and are engulfed in intense ly well characterized top-down connection in a sensory noisiness coming from many directions. The sound level pathway is the olivo-cochlear projection in the lower audi- is much higher now and relevant information can be over- tory brainstem, which mediates the so-called olivo-coch- powered (“masked”) by the various noise sources in the lear reflex (Guinan, 2006). This neuronal system is driven room. Identification and localization of individual speak- by auditory inputs and provides cholinergic innervation ers is still possible, although more difficult than in a quiet back to the inner ear and also to central neurons in the room. What are the mechanisms in the brain that allow lower auditory pathway, like the time-coding neurons in you to do this? the cochlear nucleus that we mentioned earlier. So while bottom-up computations definitely play a large role in time-coding neurons, descending projections become more important for optimal encoding of information as it *Corresponding author: Thomas Künzel, Institute for Biology 2, exists, for example, in adaptive processing. In this article, RWTH Aachen University, Worringerweg 3, 52074 Aachen, Germany, we shall first briefly review the anatomy and physiology E-Mail: [email protected] of the peripheral olivo-cochlear pathway, discuss its func- Hermann Wagner, Institute for Biology 2, RWTH Aachen University, tion in hearing and then move on to discuss recent find- Worringerweg 3, 52074 Aachen, Germany A36 T. Künzel and H. Wagner: Cholinerge Rückkopplungen auf den auditorischen Hirnstamm ings about the central effects of the olivo-cochlear inner- tivity inhibits auditory nerve activity (Groff and Liberman, vation on neurons in the cochlear nucleus. We shall use 2003; Darrow et al., 2006). this circuit as a study case for the general problem of the In contrast to the LOC system, more is known about interaction of feedforward and feedback connections. We MOC anatomy and physiology (Brown et al., 2003). Indi- will also work out that the function of centrally connected vidual MOC neurons respond to narrow-band sound. They collaterals of the olivo-cochlear innervation complement are innervated by neurons in the contralateral PVCN. Most the effects it has on the inner ear. This may in fact provide MOC axons cross the midline below the floor of the fourth additional avenues for complex top-down influences on ventricle and enter the inner ear through the vestibular adaptive information processing in the auditory pathway. part of the eighth nerve (Brown, 1993). These axons form the double-crossed pathway for the ipsilateral olivo-coch- lear reflex, where sound in the right cochlear nucleus ex- cites MOC neurons in the left brain hemisphere which, in Anatomy and physiology of the turn, innervate the right inner ear again. However, a cer- olivo-cochlear system tain proportion of MOC axons do not cross the midline. Instead, these axons join the ipsilateral OCB, forming a Auditory information reaches the brain via the auditory second pathway, where sound in the right ear excites MOC nerve that innervates the three subdivisions of the coch- neurons in the left hemisphere, which then innervate the lear nucleus. From there, auditory information is con- left inner ear. This contralateral reflex pathway is of spe- veyed to the superior olivary complex and other brain cial interest, because through the olivo-cochlear innerva- nuclei (Fig. 1A). The olivo-cochlear innervation (Fig. 1B) of tion sound in one ear may influence the way sounds in the inner ear, the so called olivo-cochlear bundle (OCB), the opposing ear are processed. From a mechanistic point is formed by the projecting axons of two major bilateral of view, it would be interesting to separate ipsi- and con- neuron groups, the medial (MOC) and the lateral (LOC) oli- tralateral contributions to the olivo-cochlear reflex. This vo-cochlear neurons (Brown, 2011). Both neuron groups are is possible experimentally by decoupling the input to the situated in close vicinity to the superior olivary complex. two ears: When playing broadband noise to one ear, the The MOC neurons are found close to the medial superior sensitivity of the other ear is reduced. This is called con- olive, mostly in the ventral nucleus of the trapezoid body, tralateral suppression and presumably mediated by the while the LOC neurons are found inside of and surround- olivo-cochlear system (Knudson et al., 2014). The exact ing the lateral superior olive (Radtke-Schuller et al., 2015). proportion of ipsi- vs. contralateral olivo-cochlear inner- Axons from both the contralateral and the ipsilateral MOC vation is variable and depends on the species and tono- and LOC innervate the inner ear (Brown, 1993). Axons from topic position on the cochlea. In general it is assumed, MOC neurons are thick and heavily myelinated, indicating that the ipsilateral component is 2–3 times stronger than rapid action potential conduction. In contrast, axons of the contralateral component (Guinan, 2006). However, LOC neurons are thin and non-myelinated, which indicates in humans the proportion of crossed vs. uncrossed MOC a slow function that is not time-critical. MOC axons form axons seems to be roughly equal. This also holds true for cholinergic contacts with the basal parts of outer hair cells the low frequency parts of the auditory system of animals (Wersinger and Fuchs, 2011; Elgoyhen and Katz, 2012). In (Guinan, 2006; Brown, 2011). Both contra- and ipsilateral contrast, LOC axons contact auditory nerve endings close MOC axons provide feedback to outer hair cells (OHC) with to inner hair cells and together with acetylcholine as a neu- cholinergic synapses. This synaptic contact is well stud- rotransmitter they use a variety of co-transmitters (Guinan, ied (Elgoyhen and Katz, 2012). Acetylcholine, upon release 2006). from the MOC axon, binds to pharmacologically unique The innervation of the LOC neurons is not well un- cholinergic receptors on the postsynaptic site. These re- derstood. It is assumed that LOC neurons are driven by ceptors contain alpha-9 and alpha-10 nicotinic acetyl- sound and receive inputs from the ipsilateral posteroven- choline-receptor subunits, which show a high calcium tral cochlear nucleus (PVCN). Axons of LOC neurons then conductivity (Elgoyhen et al., 2001). The fast effect of the almost exclusively innervate the ipsilateral cochlea. Thus acetylcholine-induced calcium influx is hyperpolarization the majority of LOC fibers are uncrossed. However, it re- of the OHC membrane potential mediated by calcium-acti- mains unclear what the exact effect of the innervation of vated potassium channels (Elgoyhen and Katz, 2012). This auditory nerve endings by the LOC axons is. Generally, hyperpolarization yields effective inhibition of the OHC LOC activity seems to modulate the excitability of auditory function by directly influencing the membrane-potential nerve fibers mostly in such a way that increased LOC ac- dependent motility of the OHC. Furthermore, on longer T.
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