Characterization of three cholinergic inputs to the cochlear nucleus

Beebe, Nichole L.; Herrera, Yoani; Noftz, William A; Roberts, Michael; Schofield, Brett R.

doi:10.1016/j.jchemneu.2023.102284

Cited by 3 publications

(3 citation statements)

References 112 publications

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“…Sources of ACh that project to AC have been identified primarily in the basal forebrain, while several regions between the cochlear nucleus and thalamus receive major cholinergic projections from the midbrain pontomesencephalic tegmentum (PMT) ( Shute and Lewis, 1967 ; Hallanger et al, 1987 ; Schofield et al, 2011 ; Figure 1B ). Furthermore, cholinergic cells have been identified in the SOC of rats ( Sherriff and Henderson, 1994 ), guinea pigs ( Motts et al, 2008 ), gerbils ( Beebe et al, 2021 ; Zhang et al, 2021 ), mouse ( Beebe et al, 2023 ) and human ( Mizukawa et al, 1986 ; Heckers et al, 1992 ). Among the periolivary nuclei, the ventral nucleus of trapezoid body (VNTB) has been identified as a major cholinergic source to CN in rats ( Gomez-Nieto et al, 2008 ), guinea pigs ( Mellott et al, 2011 ), gerbils ( Beebe et al, 2021 ), and mice ( Beebe et al, 2023 ).…”

Section: A Pervasive Cholinergic Network Influences the Ascending Aud...mentioning

confidence: 99%

“…Furthermore, cholinergic cells have been identified in the SOC of rats ( Sherriff and Henderson, 1994 ), guinea pigs ( Motts et al, 2008 ), gerbils ( Beebe et al, 2021 ; Zhang et al, 2021 ), mouse ( Beebe et al, 2023 ) and human ( Mizukawa et al, 1986 ; Heckers et al, 1992 ). Among the periolivary nuclei, the ventral nucleus of trapezoid body (VNTB) has been identified as a major cholinergic source to CN in rats ( Gomez-Nieto et al, 2008 ), guinea pigs ( Mellott et al, 2011 ), gerbils ( Beebe et al, 2021 ), and mice ( Beebe et al, 2023 ). Moreover, the lateral paragigantocellular nucleus (LPGi) has been recently identified as a novel cholinergic source that projects bilaterally to CN ( Beebe et al, 2023 ) and SOC ( Beebe et al, 2021 ).…”

Section: A Pervasive Cholinergic Network Influences the Ascending Aud...mentioning

confidence: 99%

“…Among the periolivary nuclei, the ventral nucleus of trapezoid body (VNTB) has been identified as a major cholinergic source to CN in rats ( Gomez-Nieto et al, 2008 ), guinea pigs ( Mellott et al, 2011 ), gerbils ( Beebe et al, 2021 ), and mice ( Beebe et al, 2023 ). Moreover, the lateral paragigantocellular nucleus (LPGi) has been recently identified as a novel cholinergic source that projects bilaterally to CN ( Beebe et al, 2023 ) and SOC ( Beebe et al, 2021 ). The LPGi has previously been associated with autonomic functions and sensory gating ( Stornetta et al, 2013 ; Schofield and Hurley, 2018 ), and it has numerous connections with auditory structures ( Andrezik et al, 1981 ; Kamiya et al, 1988 ).…”

Section: A Pervasive Cholinergic Network Influences the Ascending Aud...mentioning

confidence: 99%

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Cholinergic modulation in the vertebrate auditory pathway

Zhang,

Burger

2024

Front. Cell. Neurosci.

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Acetylcholine (ACh) is a prevalent neurotransmitter throughout the nervous system. In the brain, ACh is widely regarded as a potent neuromodulator. In neurons, ACh signals are conferred through a variety of receptors that influence a broad range of neurophysiological phenomena such as transmitter release or membrane excitability. In sensory circuitry, ACh modifies neural responses to stimuli and coordinates the activity of neurons across multiple levels of processing. These factors enable individual neurons or entire circuits to rapidly adapt to the dynamics of complex sensory stimuli, underscoring an essential role for ACh in sensory processing. In the auditory system, histological evidence shows that acetylcholine receptors (AChRs) are expressed at virtually every level of the ascending auditory pathway. Despite its apparent ubiquity in auditory circuitry, investigation of the roles of this cholinergic network has been mainly focused on the inner ear or forebrain structures, while less attention has been directed at regions between the cochlear nuclei and midbrain. In this review, we highlight what is known about cholinergic function throughout the auditory system from the ear to the cortex, but with a particular emphasis on brainstem and midbrain auditory centers. We will focus on receptor expression, mechanisms of modulation, and the functional implications of ACh for sound processing, with the broad goal of providing an overview of a newly emerging view of impactful cholinergic modulation throughout the auditory pathway.

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Section: A Pervasive Cholinergic Network Influences the Ascending Aud...mentioning

confidence: 99%

Section: A Pervasive Cholinergic Network Influences the Ascending Aud...mentioning

confidence: 99%

Section: A Pervasive Cholinergic Network Influences the Ascending Aud...mentioning

confidence: 99%

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Cholinergic modulation in the vertebrate auditory pathway

Zhang,

Burger

2024

Front. Cell. Neurosci.

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Differential cholinergic innervation of lemniscal versus non-lemniscal regions of the inferior colliculus

Noftz,

Echols,

Beebe

et al. 2024

Journal of Chemical Neuroanatomy

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GABAergic synapses between auditory efferent neurons and type II spiral ganglion afferent neurons in the mouse cochlea

Bachman,

Kitcher,

Vattino

et al. 2024

Preprint

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Cochlear outer hair cells (OHCs) are electromotile and are implicated in mechanisms of amplification of responses to sound that enhance sound sensitivity and frequency tuning. They send information to the brain through glutamatergic synapses onto a small subpopulation of neurons of the ascending auditory nerve, the type II spiral ganglion neurons (SGNs). The OHC synapses onto type II SGNs are sparse and weak, suggesting that type II SGNs respond primarily to loud and possibly damaging levels of sound. OHCs also receive innervation from the brain through the medial olivocochlear (MOC) efferent neurons. MOC neurons are cholinergic yet exert an inhibitory effect on auditory function as they are coupled to alpha9/alpha10 nicotinic acetylcholine receptors (nAChRs) on OHCs, which leads to calcium influx that gates SK potassium channels. The net hyperpolarization exerted by this efferent synapse reduces OHC activity-evoked electromotility and is implicated in cochlear gain control, protection against acoustic trauma, and attention. MOC neurons also label for markers of gamma-aminobutyric acid (GABA) and GABA synthesis. GABAB autoreceptor (GABABR) activation by GABA released from MOC terminals has been demonstrated to reduce ACh release, confirming important negative feedback roles for GABA. However, the full complement of GABAergic activity in the cochlea is not currently understood, including the mechanisms that regulate GABA release from MOC axon terminals, whether GABA diffuses from MOC axon terminals to other postsynaptic cells, and the location and function of GABAA receptors (GABAARs). Previous electron microscopy studies suggest that MOC neurons form contacts onto several other cell types in the cochlea, but whether these contacts form functional synapses, and what neurotransmitters are employed, are unknown. Here we use immunohistochemistry, optical neurotransmitter imaging and patch-clamp electrophysiology from hair cells, afferent dendrites, and efferent axons to demonstrate that in addition to presynaptic GABABR autoreceptor activation, MOC efferent axon terminals release GABA onto type II SGN afferent dendrites with postsynaptic activity mediated by GABAARs. This synapse may have multiple roles including developmental regulation of cochlear innervation, fine tuning of OHC activity, or providing feedback to the brain about MOC and OHC activity.

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Characterization of three cholinergic inputs to the cochlear nucleus

Cited by 3 publications

References 112 publications

Cholinergic modulation in the vertebrate auditory pathway

Cholinergic modulation in the vertebrate auditory pathway

Differential cholinergic innervation of lemniscal versus non-lemniscal regions of the inferior colliculus

GABAergic synapses between auditory efferent neurons and type II spiral ganglion afferent neurons in the mouse cochlea

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