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Descending Auditory Pathways

Our lab investigates the descending neural systems in the auditory pathway. Although their functions are poorly understood, these systems allow higher centers in the brain to control the activity of lower centers. We concentrate our studies on the olivocochlear system, which consists of several groups of brainstem neurons (Fig. 1) that control activity in the cochlea and the cochlear nucleus. These neurons respond to sound as part of a sound-evoked reflex, and we are working on the “wiring diagram” of the reflex pathways (Fig. 2). Parallel studies investigate similar issues for motoneurons that innervate the middle-ear muscles whose action regulates sound transmission through the middle ear. The types of synaptic inputs on these motoneurons are surprisingly diverse; (Fig. 3); some of these inputs enable the response to sound and other inputs modulate this response or perform other functions. A variety of approaches are taken in our research, including neural pathway tracing using the light microscope and investigation of synapses using the electron microscope. We also study evoked potentials and responses of single units from the brainstem and from the inner ear.

Olivocochlear Neurons in the Brainstem

Figure 1. Photomicrograph of a transverse section through the left side of the mouse brainstem,showing AChE staining (black) in presumed olivocochlear neurons in the superior olivary complex. Darkly-stained medial olivocochlear (MOC) neurons are present in the ventral nucleus of the trapezoid body (VNTB). Dendrites extend medially from these somata toward the trapezoid body (TB). A few stained neurons are located in the dorsal periolivary nucleus (DPO). Their distribution extends from just dorso-medial to the lateral superior olive (LSO) medially to come close to the edge of the medial nucleus of the trapezoid body (MNTB). Dendrites from DPO neurons project medially into the most dorsal part of the TB, which is dorsal to the MNTB. Stained MOC axons are visible projecting dorsally, which eventually form the olivocochlear bundle. More lightly-stained lateral olivocochlear (LOC) neurons are seen within (intrinsic neurons) and on the margins of (shell neurons) the LSO. LOC dendrites and axons are not well stained. Neutral red counterstain. Scale bar: 100 µm. from Brown MC and Levine JL (2008) Dendrites of Medial Olivocochlear (MOC) Neurons in Mouse. Neurosci. 154: 147-159.

Our Research Seeks to Identify the MOC Reflex Interneurons. Figure 2. Overview schematic indicating the pathways of the sound-evoked medial olivocochlear (MOC) reflexes to one cochlea, the ipsilateral cochlea on the right of the figure. The reflex pathway in response to ipsilateral sound begins in the ipsilateral cochlea with the response of outer and inner hair cells (OHC, IHC) and the type I afferent fibers of the auditory nerve (green color). These fibers project centrally into the cochlear nucleus and synapse there. A population of cochlear nucleus neurons form the MOC reflex interneurons (purple color); our work suggests that these reflex interneurons are multipolar neurons of the posteroventral subdivision of the cochlear nucleus. The interneurons send axons across the midline to innervate MOC neurons having a response to ipsilateral sound. These Ipsi neurons (blue color) send axons back across the midline to innervate outer hair cells (OHC) in the ipsilateral cochlea. The reflex pathway in response to contralateral sound begins in the contralateral cochlea and continues with type I nerve fibers. From the contralateral cochlear nucleus, reflex interneurons send axons that cross the midline to innervate Contra neurons (red color). In addition to these main inputs, both types of MOC neurons receive inputs that are not strong enough to produce a response on their own but do facilitate the response to the dominant ear (small arrows, “Facilitatory Inputs”). Modified from Brown, MC, de Venecia, RK, Guinan, JJ, Jr. (2003) Responses of MOC neurons: Specifying the interneurons of the reflex pathway. Exp. Brain Res. 153:491-498.

Research is also focused on Motoneurons Innervating the Middle Ear Muscles. Figure 3. Left: Examples of synaptic terminals found on labeled stapedius motoneurons (SMN, blue). A. Extensive terminal with large, round vesicles (orange) having the appearance of “beads-on-a-string” forming a synapse (arrowheads). Scale bar = 1.0 µm. B. Another large, round vesicle terminal (orange) with large, round vesicles that abuts the SMN for over 9 µm. One of four synapses formed by this terminal is visible in this section (arrowheads). Scale bar = 1 µm. C. Another terminal of the same type (orange) plus other types of terminals that contain pleomorphic vesicles (red), dense-core vesicles (DCV, magenta), and small round vesicles plus a small dense core vesicle (asterisk). Scale bar = 0.5 µm. D. Pleomorphic vesicle terminal (red) forming a complex relationship with a spine-like protrusion of an SMN. Scale bar = 0.5 µm Right: View of a reconstruction of the terminal (orange color) formed onto a SMN (blue color). The reconstruction was generated with 21 serial sections, one of which is shown in panel A. The terminal formed seven synapses (light color, one delineated by arrowheads). The origin of the swelling is the myelinated stalk visible at the lower right (dark orange color). Scale bar = 1 µm. from Lee DJ, Benson TE and Brown MC (2008) Diverse synaptic terminals on rat stapedius motoneurons. J. Assoc. Res. Otolaryngol. 9:321-333.