Medial olivocochlear reflex interneurons are located in the posteroventral cochlear nucleus: A kainic acid lesion study in guinea pigs

Abstract

The medial olivocochlear (MOC) reflex arc is probably a three-neuron pathway consisting of type I spiral ganglion neurons, reflex interneurons in the cochlear nucleus, and MOC neurons that project to the outer hair cells of the cochlea. We investigated the identity of MOC reflex interneurons in the cochlear nucleus by assaying their regional distribution using focal injections of kainic acid. Our reflex metric was the amount of change in the distortion product otoacoustic emission (at 2f 1 -f 2 ) just after onset of the primary tones. This metric for MOC reflex strength has been shown to depend on an intact reflex pathway. Lesions involving the posteroventral cochlear nucleus (PVCN), but not the other subdivisions, produced long-term decreases in MOC reflex strength. The degree of cell loss within the dorsal part of the PVCN was a predictor of whether the lesion affected MOC reflex strength. We suggest that multipolar cells within the PVCN have the distribution and response characteristics appropriate to be the MOC reflex interneurons. Keywordshearing; outer hair cell; otoacoustic emission; superior oliveThe auditory system contains several descending pathways (Spangler and Warr, 1991), of which the best-studied is the olivocochlear (OC) efferents. OC neurons reside in the superior olivary complex and project to the cochlea (Fig. 1). The OC system is divided into two subsystems (reviewed by Warr, 1992;. Medial olivocochlear (MOC) neurons have cell bodies in the medial part of the superior olivary complex and project to outer hair cells. Lateral olivocochlear (LOC) neurons have cell bodies in or around the lateral superior olive and project to afferent fibers near inner hair cells (Warr and Guinan, 1979;Liberman, 1980;Liberman and Brown, 1986;Brown, 1987;Vetter and Mugnaini, 1992;Maison et al., 2003). Cholinergic MOC endings in the cochlea exert their effects by means of a nicotinic receptor (Vetter et al., 1999;Elgoyhen et al., 2001Elgoyhen et al., , 2003 that influences outer hair cell function and alters cochlear responses (Wiederhold and Kiang, 1970;Mountain, 1980;Siegel and Kim, 1982;Brown and Nuttall, 1984). For instance, activation of MOC neurons alters distortion product otoacoustic emissions (DPOAEs), causing rapid amplitude changes in the first several hundred milliseconds after primary-tone onset (Liberman et al., 1996;Kujawa and Liberman, 2001). The functional role of this sound-evoked feedback system may include adjusting *Correspondence to: M. Christian Brown, Eaton-Peabody Laboratory, Massachusetts Eye and Ear Infirmary, 243 Charles Street, Boston, MA 02114. E-mail: mcb@epl.meei.harvard.edu. Grant sponsor: National Institute on Deafness and Other Communication Disorders; Grant number: RO1 DC 01089; Grant number: RO1 DC 00188; Grant number: P30 DC05209; Grant number: T32 DC00020-11; Grant sponsor: Triological Society. NIH Public Access NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript cochlear gain, reducing effects of masking noise, and protecting the ear from acous...

Increased activation of the human cerebellum during pitch discrimination: A positron emission tomography (PET) study

“…Animal studies have in fact shown that the cerebellum receives direct afferents from both the cochlea (Brozoski et al, 2007;Morest et al, 1997) and the cochlear nucleus (Huang et al, 1982). The cerebellum in turn sends direct efferent projections to the superior olive (Earle and Matzke, 1974;Rossi et al, 1967; but see Gacek, 1973), as well as to those divisions of the cochlear nucleus (Gacek, 1973;Rossi et al, 1967) and of the inferior colliculus (Huffman and Henson, 1990) that are directly connected to the superior olive (Cant and Benson, 2003;Schofield and Cant, 1999;Thompson, 1991, 1993) and involved in olivocochlear function (De Venecia et al, 2005;Groff and Liberman, 2003;Huffman and Henson, 1990). Interpreted in the context of the hypothesis being tested here, this pathway provides the cerebellum an opportunity to evaluate the incoming auditory data and influence the way in which those data are subsequently acquired by auditory structures (Bower, 1997a).…”

Ultrastructure of synaptic input to medial olivocochlear neurons

“…Anatomical studies have shown direct projections from neurons in the cochlear nucleus that cross the midline to reach MOC neurons (Warr, 1969;Robertson and Winter, 1988;Thompson and Thompson, 1991a;Ye et al, 2000). Physiological studies of the MOC reflex suggest that the most important site in the cochlear nucleus is the posteroventral subdivision (PVCN) (Brown et al, 2003;de Venecia et al, 2005). Finally, MOC neurons, the thirdorder neurons of the reflex, project back to form branches to the cochlear nucleus (Rasmussen, 1960;Benson and Brown, 1990) and large endings on the outer hair cells of the cochlea (Kimura and Wersä ll, 1962;Liberman and Brown, 1986).…”

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

“…In the MOC system, auditory-nerve fibers project to a subpopulation of multipolar neurons in the posteroventral cochlear nucleus (PVCN), which in turn project to MOC neurons of the superior olivary complex (Brown et al 2013a;de Venecia et al 2005;Horváth et al 2003;Mulders et al 2007; Thompson and Thompson 1991).…”