Dopaminergic innervation of the mouse inner ear: Evidence for a separate cytochemical group of cochlear efferent fibers

Abstract

Immunostaining mouse cochleas for tyrosine hydroxylase (TH) and dopamine beta-hydroxylase suggests that there is a rich adrenergic innervation throughout the auditory nerve trunk and a small dopaminergic innervation of the sensory cell areas. Surgical cuts in the brainstem confirm these dopaminergic fibers as part of the olivocochlear efferent bundle. Within the sensory epithelium, TH-positive terminals are seen only in the inner hair cell area, where they intermingle with other olivocochlear terminals expressing cholinergic markers (vesicular acetylcholine transporter; VAT). Double immunostaining suggests little colocalization of TH and VAT; quantification of terminal volumes suggests that TH-positive fibers constitute only 10-20% of the efferent innervation of the inner hair cell area. Immunostaining of mouse brainstem revealed a small population of TH-positive cells in and around the lateral superior olive. Consistent with cochlear projections, double staining for the cholinergic marker acetylcholinesterase suggested that TH-positive somata are not cholinergic and vice versa. All observations are consistent with the view that a small dopaminergic subgroup of lateral olivocochlear neurons 1) projects to the inner hair cell area, 2) is distinct from the larger cholinergic group projecting there, and 3) may correspond to lateral olivocochlear "shell" neurons described by others (Warr et al. [1997] Hear. Res 108:89-111).

Catecholaminergic connectivity to the inner ear, central auditory, and vocal motor circuitry in the plainfin midshipman fish porichthys notatus

“…In mammals, the medial olivocochlear (MOC) efferent system is comprised of cholinergic neurons that function to inhibit outer hair cells (cochlear amplifier), while the lateral olivocochlear (LOC) efferent system is a heterogeneous mix of cholinergic, dopaminergic, γ-aminobutyric acid (GABA)-ergic and other peptidergic neurons (Darrow et al, 2006b;Gaborjan et al, 1999;Lendvai et al, 2011), whose function is less well known but has been demonstrated to either elicit slow excitation or slow suppression of the nerve output from inner hair cells of the cochlea (Groff and Liberman, 2003). In the LOC, GABA colocalizes with cholinergic efferent terminals, while dopamine comprises a small but separate population (5-35%) of efferents (Darrow et al, 2006b). The majority of DA terminals lack clear synaptic specializations (Lendvai et al, 2011).…”

The Actions of Dopamine Receptors in the Guinea Pig Cochlea

“…Lateral efferents contain a wide range of neurotransmitters including dopamine [Altschuler et al, , 1985Eybalin et al, 1993;Fex and Altschuler, 1984;Fex et al, 1986;Gil-Loyzaga et al, 1997;Jones et al, 1987;Maison et al, 2003;Safieddine et al, 1997;Sliwinska-Kowalska et al, 1989]. Excitatory [Le Prell et al, 2003 and inhibitory actions [Darrow et al, 2006] attributed to the lateral innervation have been inferred from lesion studies in guinea pigs and mice. Although species differences may be involved [Le Prell, 2007], divergent effects have also been found within one species following putative lateral efferent stimulation [Groff and Liberman, 2003].…”

A catechol- O -methyltransferase that is essential for auditory function in mice and humans

“…The lateral olivocochlear complex (LOC) sends efferents into the cochlea that synapse with the dendrites of afferent neurons that innervate IHCs (9,10). Though the full complement of neurotransmitters expressed by efferent neurons projecting to OHCs and IHCs is not known, a small number of the LOC-derived efferent fibers have been shown to be dopaminergic (11). Dopamine can also modulate the activity of afferent neurons that synapse on IHCs (9, 10).…”