Cholinergic cells of the pontomesencephalic tegmentum: Connections with auditory structures from cochlear nucleus to cortex

Abstract

Acetylcholine (ACh) is a neuromodulator that is likely to play a role in plasticity as well as other phenomena at many sites in the auditory system. The auditory cortex receives cholinergic innervation from the basal forebrain, whereas the cochlea receives cholinergic innervation from the superior olivary complex. Much of the remainder of the auditory pathways receives innervation from the pedunculopontine and laterodorsal tegmental nuclei, two nuclei referred to collectively as the pontomesencephalic tegmentum (PMT). The PMT provides the major source of ACh to the auditory thalamus and the midbrain, and is a substantial source (in addition to the superior olivary complex) of ACh in the cochlear nucleus. Individual cholinergic cells in the PMT often have axon branches that innervate multiple auditory nuclei, including nuclei on both sides of the brain as well as nuclei at multiple levels of the auditory system. The auditory cortex has direct axonal projections to the PMT cells, including cholinergic cells that project to the inferior colliculus or cochlear nucleus. The divergent projections of PMT cholinergic cells suggest widespread effects on the auditory pathways. These effects are likely to include plasticity as well as novelty detection, sensory gating, reward behavior, arousal and attention. Descending projections from the forebrain, including the auditory cortex, are likely to provide a high level of cognitive input to these cholinergic effects. Dysfunction associated with the cholinergic system may play a role in disorders such as tinnitus and schizophrenia.

Increased contralateral suppression of otoacoustic emissions indicates a hyperresponsive medial olivocochlear system in humans with tinnitus and hyperacusis

“…In humans, auditory discrimination, signal detection in noise, and stimulus-counting tasks, for instance, have been reported to result in increased activation of the MOC system (e.g., Mishra and Lutman 2014;Smith et al 2012). The increase may be mediated by known descending projections: directly from inferior colliculus or auditory cortex to MOC neurons, or indirectly from auditory cortex to cochlear nucleus (Brown et al 2013b;Mellott et al 2011;Mulders et al 2000aMulders et al , 2000bSchofield et al 2011). These same pathways and mechanisms may be responsible for increasing MOC activity in tinnitus and low SLT.…”

Presynaptic Neuronal Nicotinic Receptors Differentially Shape Select Inputs to Auditory Thalamus and Are Negatively Impacted by Aging

“…The pedunculopontine nucleus (PPTg) and the laterodorsal tegmental nucleus are brainstem nuclei that collectively comprise the pontomesencephalic tegmentum (PMT), which provides cholinergic input to the MGB (Morley and Kemp, 1981;Woolf, 1991;Schofield et al, 2011). The PMT has been implicated in many systems responsible for wakefulness, sleep, and attention (Jones, 1991;Kozak et al, 2005;Boucetta et al, 2014).…”

“…The PMT has been implicated in many systems responsible for wakefulness, sleep, and attention (Jones, 1991;Kozak et al, 2005;Boucetta et al, 2014). In the context of the auditory system, PMT neurons are critical in sensory gating and detecting novel/difficult-to-identify signals through a number of direct and indirect descending circuits (Schofield et al, 2011). The AC is known to have direct axonal projections to the PMT cells themselves (Schofield et al, 2011).…”

“…In the context of the auditory system, PMT neurons are critical in sensory gating and detecting novel/difficult-to-identify signals through a number of direct and indirect descending circuits (Schofield et al, 2011). The AC is known to have direct axonal projections to the PMT cells themselves (Schofield et al, 2011). Collectively, these top-down pathways provide the basis for augmenting the output of the PMT cholinergic system.…”

Cholinergic top-down influences on the auditory brainstem

“…It was shown that descending projections from the inferior colliculus (Brown et al, 2013), the auditory cortex and even non-auditory brain areas (Brown et al, 2013) reach all the way down to the olivo-cochlear neurons in the superior olivary complex. Furthermore, there is a whole class of cholinergic neurons in a midbrain area called the ponto-mesencephalic tegmentum that is under cortical control and projects widely into every station of the auditory pathway, including the cochlear nucleus (Behrens et al, 2002;Schofield et al, 2011;Mellott et al, 2011). The latter comprise about 25 % of all cholinergic axons in the cochlear nucleus of rodents.…”