Auditory Brainstem Circuits That Mediate the Middle Ear Muscle Reflex (2024)

Stapedius Motoneurons

SMNs are located in close proximity to the facial motor nuclei bilaterally (Figure 4; Joseph et al., 1985; Rasmussen, 1946; Rouiller et al., 1989; Strominger et al., 1981; Windsor et al., 2007) and are distributed across the perifacial and periolivary regions in the cat (Lyon, 1978), and ventromedially and dorsomedially to the facial nuclei in guinea pigs (Strutz et al., 1988). SMNs have been reported to respond exclusively to either ipsilateral, contralateral, or bilateral acoustic stimulation (; Vacher et al., 1989) and are spatially organized around the facial motor nuclei according to their physiological responses to sound (Joseph et al., 1985; Lyon, 1978; ). A similar spatial arrangement of neural innervation to the muscle fibers of the stapedius has not yet been described ().

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Figure 4.

Horseradish peroxidase (HRP) labeled stapedius motoneuron (SMN) in a rat model

Note: Center image: low magnification electron micrograph of HRP-labeled SMN with black reaction product granules (scale bar = 10 mm). Lower left inset: drawing of the left half of a coronal section of rat brainstem demonstrating the location of the labeled SMN ventro-medial to the facial nerve motor nucleus (VII). PVCN-posteroventral cochlear nucleus. Upper right inset image: bright-field photomicrograph of the same epoxy-embedded labeled SMN.

Source: D. J. Lee et al. (2008). Reprinted with permission from the Association for Research in Otolaryngology.

In cat, the stapedius has a higher innervation ratio than the tensor tympani (Blevins, 1964; Joseph et al., 1985). For instance, close to 1,100 SMNs in cat are found in the perifacial and peri-olivary regions of the brainstem (Joseph et al., 1985), and these SMNs supply approximately 1,730 stapedius muscle fibers. The stapedius therefore has an innervation ratio of 1:1.6 (Blevins, 1964; Wiener-Vacher et al., 1999).

In guinea pig and rat, SMNs are located both ventromedially and dorsomedially, relative to the motor facial nucleus (Rouiller et al., 1989). They are spatially organized according to their physiologic responses to sound presented to the ipsilateral or contralateral ear (; Vacher et al., 1989). SMNs are felt to receive nonauditory inputs as well. The MEMs contract in response to self-generated vocalization () to minimize self-stimulation. Serotoninergic terminals on SMNs may modulate activity of the stapedius reflex (). Finally, higher brain centers may provide cortical control over contraction of the stapedius muscle (Borg et al., 1984; Gelfand, 1984; Gelfand, 1998; Moller, 1984; ; Stach et al., 1984). The sources of these descending inputs to SMNs are not known.

We hypothesized that the diversity of inputs on SMNs would be reflected in a variety of terminal types on these motoneurons. The ultrastructural features of synaptic terminals on retrogradely labeled SMNs in rat were studied using electron microscopy (D. J. Lee et al., 2008). In SMNs, both the proximal dendrites and SMN cell bodies were seen to be densely and evenly populated with synaptic terminals (D. J. Lee et al., 2008). A variety of inputs on SMNs with both excitatory and inhibitory properties were described. These terminals were classified into five major types according to the size and shape of their synaptic vesicles (Figure 5; D. J. Lee et al., 2008). The most common synaptic terminal type contained small, round vesicles (Figures 5B and ​and5D;5D; D. J. Lee et al., 2008), and these were felt to be excitatory (Uchizona, 1965). Similar terminals containing small round vesicles were observed on MOC neurons (), and the source of these terminals were multipolar neurons residing in the CN. It is uncertain whether SMNs receive inputs from multipolar neurons or other neurons found in the CN ().

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Figure 5.

Electron micrographs of the major terminal types seen on the stapedial motoneuron (SMN) from Figure 4.

Note: Five types of synaptic terminals (see key) found on SMNs (cyan). Panel A: Synaptic terminals with pleomorphic vesicles (Pleo, red) and large, round vesicles (Lg Rnd, orange). Panel B: Synaptic terminal with small, round vesicles (Sm Rnd, yellow) and dense core vesicles (DCV). Panel C: Synaptic terminal with round vesicles of different sizes (Het Rnd, lavender). Panel D: Low magnification electron micrograph demonstrating the distribution of synaptic terminals on the SMN cell body and proximal dendrites. Synaptic terminals are color coded according to vesicle shape and size. The proportion of membrane in contact with synaptic terminals was approximately 50%. Scale bar = 0.5 μm (A-C), scale bar = 10 μm (D). Source: D. J. Lee et al. (2008). Reprinted with permission from the Association for Research in Otolaryngology.

The second most common synaptic terminal type on SMNs contained large, round vesicles (Figure 5A; D. J. Lee et al., 2008). These large round terminals ranged in size and one putative source of these inputs on SMNs is the globular bushy cell in the CN. Smith, Joris, Carney, and Yin (1991) described projections of globular bushy cells to the caudal brainstem near the facial motor nucleus where SMNs are located (Smith et al., 1991). In their study, large round vesicles were also seen in terminals of globular bushy cells. Our study revealed additional terminal types on SMNs (Figure 5A). The complex integration of inputs by SMNs reflected by the diversity of synaptic terminals seen in our ultrastructural study of SMN terminals may account for the multifunctionality of the MEM reflex (D. J. Lee et al., 2008).

Tensor Tympani Motoneurons

In cat, it has been demonstrated that only 700 TTMNs supply approximately 4,000 tensor tympani muscle fibers (Blevins, 1964; ) to give the tensor tympani an innervation ratio of 1:5.7. TTMNs are found immediately ventrolateral to the trigeminal motor nuclei (Billig et al., 2007; Itoh et al., 1986; Lyon, 1978; Mizuno et al., 1982; Mukerji et al., 2009; Rouiller et al., 1986; Spangler et al., 1982; Strominger et al., 1981; Windsor et al., 2007; Figure 6). The location of TTMNs are thought to correlate to “Cell Group K,” a specific area in the brainstem containing motoneurons that supply the masseter, digastric, and Eustachian tube muscles (; ; ). Within this region, TTMNs are arranged as a crescent-shaped column (Mukerji et al., 2009; Rouiller et al., 1986) extending rostrally to the medial aspect of the lateral lemniscus (Billig et al., 2007; Spangler et al., 1982). This pattern of distribution is described as being distinct from the trigeminal motor nucleus in terms of location, cell body size, and dendritic spread (). For this reason, an area exclusively consisting of TTMNs is considered to be a separate “tensor tympani motor nucleus of V” rather than an accessory of the trigeminal motor nucleus (; ). Unlike SMNs, TTMNs have not been shown to be spatially located around the trigeminal motor nuclei according to their individual physiological responses to stimuli.

Recently, our group studied the morphology and dendritic characteristics of mouse TTMNs using a retrograde neuronal tracer called Fluoro-Gold (Mukerji et al., 2009). Each TTMN was categorized into one of three subtypes, based on the number and orientation of the primary dendrites that projected from its cell body (Figure 7). “Octopus-like” TTMNs (most commonly found) had two dendrites projecting from one side of the cell body. “Stellate” TTMNs (least commonly found) had three or more dendrites projecting from the cell body and “fusiform” TTMNs had two dendrites projecting from opposing poles of the cell body (Mukerji et al., 2009). The different TTMN subtypes may reflect the variety of auditory and nonauditory inputs that trigger TT contraction and are similar to the range of neuron cell body morphology in the CN (Adams, 1986; Kiang et al., 1973; Rhode et al., 1983; ).

The orientation and distribution of dendrites contribute to the ability of a neuron to receive and respond to stimuli (; ; ; Sotnikov, 2005; ). In our mouse study, TTMNs formed sparsely branched dendrites that radiated in all directions (Mukerji et al., 2009; Figure 8). TTMN dendrites directed dorsomedially were more frequent and were the longest, some extending for distances longer than 600 μm (Figure 9). A similar orientation and length bias exists for medially projecting dendrites of MOC neurons that receive inputs from the contralateral side of the brainstem in mice ().

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Figure 9.

Polar plot of tensor tympani motoneuron (TTMN) dendritic length and orientation

Note: Polar plot shows the lengths (μm) and dendritic angles (°) of reconstructed fluoro-gold labeled dendrites across each TTMN subtype; octopus-like (circles), stellate (stars), and fusiform (squares). Dendrites directed dorsomedially were more numerous and were the longest in length. Inset shows measurement of dendritic angle by drawing a line from soma to dendrite tip and measuring the angle of this line with respect to the dorsal direction.

Source: Mukerji et al. (2009). Reprinted with permission from Brain Research.

Since TTMNs dendrites appear to project well beyond the immediate region of labeled motoneurons (; Mukerji et al., 2009), they present a large surface area on which to receive synaptic inputs. For example, Friauf and Baker (1985) observed a mean of five heavily branched primary dendrites emanating from each labeled TTMN in cat. These dendrites traveled for long distances and radiated into areas near the superior olivary complex (SOC; ). In both cat and mouse, TTMN dendrites avoid crossing the trigeminal motor nucleus (; Mukerji et al., 2009). The separate and distinct organization of TTMN dendrites further supports the presence of physiological differences between TTMNs and the motoneurons of the trigeminal motor nucleus ().

The proximal dendrites of TTMNs are known to receive the majority of synaptic input compared with the cell body, which is relatively sparsely innervated (D. J. Lee et al., 2008). These TTMN terminals receive inputs from the CN (Billig et al., 2007), serotoninergic sources (Thompson et al., 1998), and higher cortical areas (Gelfand, 1984, 1998), all of which mediate the MEM reflex during auditory and nonauditory behaviors.

The synaptic terminals on retrogradely labeled rat TTMNs were recently investigated using electron microscopy in our laboratory (D. J. Lee et al., 2008; Figure 10). The frequency and morphology of terminal types observed on TTMNs were similar to that seen on SMNs (Benson et al., 2008; D. J. Lee et al., 2008). Synaptic terminals on TTMNs were classified into the four terminal types according to the size and shape of the synaptic vesicles. They were named (a) large round, (b) small round, (c) pleomorphic, and (d) heterogeneous. Compared with SMNs, there were slightly fewer small round terminal types found on TTMNs (D. J. Lee et al., 2008). SMNs also received a rare Cistern-type terminal that was not seen on TTMNs (D. J. Lee et al., 2008). In TTMNs, terminal types with round vesicles (large round and small round) were most common (Figure 10) accounting for approximately 80% of the terminal types (D. J. Lee et al., 2008). This is a much higher percentage than that found on spinal motoneurons (40% to 45%; ). The relatively high proportion of terminal types containing round vesicles signifies that the TTMNs receive mainly excitatory input (Uchizona, 1965). The presence of some pleomorphic terminal types (Figure 10C) suggests that TTMNs also receive some inhibitory input. As in the case of SMNs, the assignment of TTMN terminal types to the cell bodies of origin has not been established. The CN, SOC, serotoninergic sources, and higher cortex are all possible sources (Billig et al., 2007; Gelfand, 1984; Stach et al., 1984; Thompson et al., 1998).

Direct Projections of CN Interneuron to Motoneurons

Work by Billig et al. (2007) has used PRV to determine the location and identity of the tensor tympani reflex interneurons in the CN. Following injection of the tensor tympani with PRV, bilateral transynaptically labeled neurons (mean neuronal counts: eight ipsilateral, five contralateral) in the dorsal and dorsomedial regions of the AVCN were seen (Billig et al., 2007; Figures 11 and 12A). Labeled neurons were also found in the dorsal PVCN, although to a lesser extent (Figure 12B). Based on both morphological appearance (large somas and orientation of dendrites that radiate across the CN; ) and location in the AVCN, the majority of labeled neurons were classified as “radiate multipolar cells” (Billig et al., 2007). Radiate multipolar neurons have been previously shown to project to the dorsal cochlear nucleus (DCN) on the same side (; ) and are similar in appearance to the large commissural neurons that traveled to the contralateral CN (Cant, 1982; ; ; Wenthold, 1987). Billig et al. (2007) observed that the number of labeled neurons increased bilaterally in the AVCN at longer survival times (69 to 71 hours; means of 21 ipsilateral vs. 30 contralateral neurons). A few neurons were also detected in the PVCN and DCN, centered mostly along the border between the two regions (Billig et al., 2007). These findings represent the first description of putative MEM reflex interneurons in the CN.

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Figure 11.

Camera Lucida drawings of ventral cochlear nucleus (VCN) labeling

Note: Brainstem atlas shows the locations of pseudo-rabies virus (PRV)–labeled neurons in the ventral cochlear nucleus (VCN) following injection into the right tensor tympani muscle. Survival times ranged from 48 to 62 hours. Each symbol represents a labeled neuron. Neurons on right side of each diagram are located ipsilateral to the PRV injection. The number between diagrams indicates the relative rostrocaudal distance in mm of the section from the obex. Arrows with A-C letters indicate the locations of infected neurons shown in Figure 13. 8n, vestibulocochlear nerve; AVCN, anterolateral cochlear nucleus; DCN, dorsal cochlear nucleus; GrC, granular layer of cochlear nuclei; PVCN, posteroventral cochlear nucleus.

Source: Billig et al. (2007). Reprinted with permission from Brain Research.

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Figure 12.

Pseudo-rabies virus (PRV)–labeled ventral cochlear nucleus (VCN) neurons following injection into the tensor tympani muscle

Note: Panels A and B: Radiate multipolar cells in the anteroventral cochlear nucleus (AVCN). Panel C: Large cell at junction of the posteroventral cochlear nucleus (PVCN) and the Schwann-cell border of the cochlear nerve. Scale bars represent 50 μm.

Source: Billig et al. (2007). Reprinted with permission from Brain Research.

Preliminary results from a similar series of time-graded survival experiments by Windsor et al. (2007) demonstrated labeled CN interneurons 48 to 53, 62 to 72, and 96 to 120 hours following injection of PRV into rat stapedius and tensor tympani muscles. For stapedius injections, the majority of labeled neurons were seen bilaterally in the rostral half of the PVCN but also within regions clustered around the PVCN and DCN, with a mean neuronal count of four ipsilateral and five contralateral (Figure 13A). Minimal labeling was seen bilaterally in the AVCN and auditory nerve root (Windsor et al., 2007). Tensor tympani injections, however, exhibited a different labeling pattern in which CN neurons were seen bilaterally in the rostral half of the dorsal AVCN (Figure 13B; Windsor et al., 2007) similar to the work of Billig et al. (2007). No labeling was seen in the PVCN, DCN, or auditory nerve root following tensor tympani injections.

The difference in locations of CN interneurons between the stapedius and tensor tympani alludes to the possible existence of two separate groups of reflex interneurons in the CN involved in the MEM reflexes, namely, those in the PVCN controlling the stapedial reflex and those in the AVCN controlling the tensor tympani reflex. Observations by Billig et al. (2007) also strongly support the presence of direct fibers from the VCN bilaterally to the TTMNs based on the temporal course of viral replication (Billig et al., 2007). Consistent labeling was noted in the VCN (without SOC labeling) at survival times ranging between 48 and 62 hours, suggesting that the tensor tympani reflex may also consist of three neurons: cochlea → VCN → motoneurons (Billig et al., 2007). Direct connections between the CN and the motoneurons, without involvement of an additional synapse have been demonstrated, though the physiological relevance of a direct connection is still unclear (Billig et al., 2007; Borg, 1973; Itoh et al., 1987; ; Van Noort, 1969). For instance, Itoh et al. (1987) provided evidence of direct afferent fibers projecting from the VCN to the TTMNs in cats after injecting a retrograde tracer into the pontine tegmentum, a region in the brainstem containing TTMNs. Labeled neurons were observed bilaterally in the DCN and VCN (Itoh et al., 1987). Similar direct projections have been observed for other descending auditory pathways, such as the MOC reflex (; Ye et al., 2000). It is not clear whether there is a similar direct projection of CN interneurons to stapedial motoneurons.

Based on the tonotopical organization of the VCN () and the cochleotopical organization of the auditory nerve fibers in the VCN (; ), the spatial arrangement of radiate multipolar CN interneurons controlling the tensor tympani could occupy the high frequency regions of the VCN (Fekete et al., 1984; Liberman, 1991). The minimal labeling of neurons found in the auditory nerve supports the involvement of the tensor tympani in the acoustic startle reflex (). Projections of CN interneurons directly onto the MEM reflex motoneurons have been described as being similar to those seen in the MOC pathway (; Ye et al., 2000).

Indirect Projections of CN Interneuron to Motoneurons

Previous studies using transneuronal tracers (Rouiller et al., 1986, 1989) have revealed an additional synapse in the SOC that might be involved in the central pathways of the MEM reflex. Specifically, after injecting herpes virus suis into the rat stapedius muscle, Rouiller et al. (1989) described labeled neurons at the level of the SOC in the mediotrapezoid region. In a similar experiment, transneuronally infected neurons appeared close to the SOC bilaterally after injection of herpes virus suis into rat tensor tympani (Rouiller et al., 1986). These findings suggest that some CN interneurons traveled indirectly to MEM motoneurons by way of the SOC. However, labeled neurons in these early viral studies did not represent the entire network of neurons involved in the MEM reflex pathways as CN interneurons were not labeled in these experiments.

Billig et al. (2007) detected a small number of labeled cells bilaterally in the MNTB of the SOC as early as 62 hours following the injection of PRV into the rat tensor tympani (Table 1). There was a clear ipsilateral dominance, with some labeling also seen in the periolivary (PO) cell groups. More obvious labeling in both the MNTB and the dorsal, medioventral, and lateral aspects of the PO cell groups was observed following inoculation times between 69 and 71 hours. After 69 hours, Billig et al. (2007) reported a mean of 38 ipsilateral labeled neurons compared with 18 contralateral labeled neurons in the SOC. After a survival time of 78 to 80 hours, the number of labeled neurons in the SOC increased to a mean of 462 ipsilateral versus 246 contralateral neurons (Billig et al., 2007). On the basis of their morphology, the labeled neurons were characterized as “marginal cells,” “microneurons” and other cell types that could not be classified (Billig et al., 2007). The presence of these cell types in the SOC was deemed significant because prior studies have shown that marginal cells in the VCN project to the PO cell groups and the contralateral MNTB of the SOC (). Additionally, neurons originating in the PO and MNTB have also been shown to project to the TTMNs on both sides in rabbit (Borg, 1973) and rat (Rouiller et al., 1986).

Preliminary results from PRV injections into rat stapedius and tensor tympani muscle (Windsor et al., 2007) also showed transneuronally labeled neurons in the bilateral PO cell groups dorsal and medial to the lateral superior olive (LSO) 48, 62, and 96 hours following an injection but not to the extent and increasing pattern as described by Billig et al. (2007; Figure 14).

Involvement of the SOC suggests that one possible MEM reflex circuit diagram would include four neurons: cochlea (spiral ganglion cell) → VCN (reflex interneuron) → SOC (superior olivary complex) → motoneuron. The SOC is a relay station for ascending and descending auditory information traveling to and from both ears. Some of the fiber tracts leaving the CN send collaterals to the SOC before forming the lateral lemniscus, a specialized tract of axons that carries acoustic information from the CN to various brainstem nuclei and the midbrain (; ). It is located medial to the CN in the caudal portion of the pons and consists of three main nuclei, namely the medial superior olive (MSO), the LSO, and the MNTB. The MSO receives inputs from bushy cells of both CN and is sensitive to interaural time differences. The LSO receives excitatory inputs from the bushy cells of the ipsilateral CN, inhibitory inputs from the contralateral CN, and responds exclusively to interaural amplitude differences (; ; ; ). Through the information processed by both nuclei, the SOC collectively assists in sound localization by analyzing time and amplitude differences between acoustic signals. There are also between six and nine PO cell groups interspersed around the three main nuclei.

The SOC plays an as yet undefined role in the MEM reflex pathway. Early mechanical degenerative studies have demonstrated that CN interneurons synapsed onto third-order neurons in the SOC on the same and opposite side of the stimulated ear (Borg, 1972, 1973). This was based on surgical lesions made in the medial part of the SOC that affected both the contralateral and the ipsilateral sound evoked MEM reflex in rabbit (Borg, 1972, 1973; Moller, 1984).

There are possibly coexisting indirect pathways (Moller, 1984; ; ; ) that are multisynaptic and travel in parallel to the main MEM reflex arc. These pathways are largely unidentified and are likely to involve the extra-pyramidal system (Courville, 1966). For example, anatomical degenerative studies have demonstrated that when lesions of the reticular formation are made rostral to the SOC, there is degeneration in the facial motor nuclei (Borg, 1973). Compared with the direct pathways, the indirect pathways are slower and more sensitive to medications such as barbiturates and dependent on the arousal state of the organism (; ; Salomon, 1963). The presence of several pathways involved in the MEM reflex may explain the multi-functionality of the tensor tympani and stapedius muscles in response to a wide array of auditory and nonauditory behaviors.

The authors declared no potential conflicts of interest with respect to the authorship and/or publication of this article.

The authors disclosed receipt of the following financial support for the research and/or authorship of this article:

This work is supported by NIH-NIDCD K08DC006285 and the Norwegian State Funding Lending Agency.

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