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date: 17 September 2019

Axon Trajectories in the Auditory Brainstem

Abstract and Keywords

This chapter summarizes what is known about the organization of the axons that make up the white matter of the auditory brainstem. The sources of the axons in each of the major fiber bundles (the dorsal and intermediate acoustic striae, the ventral acoustic stria or trapezoid body, and the lateral lemniscus) are reviewed, and, where information is available, the organization of specific groups of axons within the fiber bundles is described. The chapter collects the extensive but scattered information about axon trajectories into one place, both to provide a summary of what is known and also to indicate important gaps in our knowledge. The emphasis is almost entirely on the routes followed by groups of axons over the relatively long distances between structures and on the organization of specific types of axons within the fiber bundles; information about the termination patterns of the axons can be obtained from the references cited and throughout the chapter. Because knowledge about axon trajectories has considerable practical value (as, for example, in designing and interpreting both anatomical and physiological studies), the most useful information is species specific. Fortunately, at least at our current level of understanding, the components and relative positions of the major fiber bundles are remarkably similar across species (undoubtedly reflecting a common mammalian developmental plan).

Keywords: dorsal acoustic stria, intermediate acoustic stria, ventral acoustic stria, trapezoid body, lateral lemniscus, white matter, auditory brainstem

The auditory brainstem is made up of many types of neurons grouped into a number of complex structures. Understanding the interconnections among these structures has been a major focus of neuroanatomical studies for over a century. An important goal of the studies has been the construction of detailed maps of the connections with respect to the origins and termination patterns of the numerous neuronal populations that constitute the basic units of the system. Such maps form a logical foundation for interpretation (p. 474) of physiological and functional studies, often lead to the development of new hypotheses, and can provide inspiration for computational models.

The auditory system is one of the more complicated sensory systems in terms of the number of brainstem structures that form its parts, and many reviews of the connections among these structures are available (e.g., Rouiller, 1997; Thompson & Schofield, 2000; Oertel & Wickesberg, 2002; Smith & Spirou, 2002; Malmierca, 2003; Cant, 2005; Schofield, 2005; Malmierca & Hackett, 2010; Schofield, 2011; Cant & Oliver, 2018). In broad outline, inputs from the cochlea are distributed to the dorsal and ventral cochlear nuclei in the caudal brainstem. Specific neuronal populations in the cochlear nuclei project to nuclei in the superior olivary complex, the nuclei of the lateral lemniscus, and/or the inferior colliculus. The inferior colliculus additionally receives inputs from neurons in the superior olive and nuclei of the lateral lemniscus, which are also interconnected with each other. The inferior colliculus, in turn, provides most (although not quite all) ascending auditory input to the forebrain. Some auditory structures are interconnected by commissural projections, and descending projections arise and terminate at all levels from the forebrain to the lower brainstem.

Summary information about the interconnections among auditory nuclei and the constituent neuronal populations is generally presented in the form of schematic representations known as “wiring diagrams.” Although such diagrams are often quite detailed, they almost never provide realistic information about the routes followed by the axons as they pass between structures. In this sense, the wiring diagrams might be compared to the commonly used maps of underground train systems in large cities, in which spatial information is ignored in order to emphasize links between origins and terminations.1 Just as the subway maps do not accurately depict geographical relationships, neuronal wiring diagrams are almost always distorted topologically with respect to the complex three-dimensional arrangements of the axons that provide the links. Obviously, the rationale for both types of maps is that the nodes or connection points are the sites of functional significance and the routes travelled are of lesser interest. Nevertheless, information about the trajectories followed by particular axon bundles is important, and sometimes essential, for the implementation and interpretation of experiments designed to investigate both structure and function.

Although detailed information about the three-dimensional organization of the white matter is generally omitted from reviews of auditory neuroanatomy, a considerable amount is known about the trajectories taken by specific groups of axons through the brainstem. The period from the late 1800s through the 1960s was a time of intense neuroanatomical study of the brains of many species, both mammalian and non-mammalian. The major fiber bundles that carry auditory information were described by investigators who used degeneration and myelin staining techniques to study auditory connectivity (history reviewed by Papez, 1930; Rasmussen, 1946). Since these methods were better suited to establishing fiber trajectories and general patterns of connectivity than to establishing details of synaptic organization, the early papers often went into great detail about the organization of the white matter. By the 1970s, the main structures (p. 475) in both the gray and white matter were known, and as better methods became available for the study of nuclear and synaptic organization, less emphasis was devoted to the details of fiber trajectories. However, a number of assiduous authors have taken care to describe the routes followed by projection neurons, and new information about the organization of the tracts is still being gathered.

In this review, I have attempted to collect the extensive but scattered information about axon trajectories into one place, both to provide a summary of what is known and also to indicate important gaps in our knowledge. The emphasis is almost entirely on the routes followed by groups of axons over the relatively long distances between structures and on the organization of specific types of axons within the fiber bundles; information about the termination patterns of the axons can be obtained from the references cited throughout the chapter. Because knowledge about axon trajectories has considerable practical value (as, for example, in designing and interpreting both anatomical and physiological studies), the most useful information is species specific. Fortunately, at least at our current level of understanding, the components and relative positions of the major fiber bundles are remarkably similar across species (undoubtedly reflecting a common mammalian developmental plan; cf. Cant, 1998). The most detailed descriptions are available for the cat, but information is also available for species as diverse as commonly used laboratory rodents, opossum, various species of bats, various species of monkeys, baboon, chimpanzee, and human (cited where appropriate).

Routes Followed by Ascending Auditory Axons

The principal cell axons that connect the cochlear nuclei with other parts of the brainstem travel in one of three major fiber tracts, named according to their relative location along the dorsal to ventral dimension of the neuraxis: the dorsal acoustic stria (DAS; stria of Monakow), the intermediate acoustic stria (IAS; stria of Held), and the ventral acoustic stria (commonly referred to as the trapezoid body [TB]). The striae may contain axons from sources other than the cochlear nuclei as well. A fourth major brainstem auditory fiber bundle, the lateral lemniscus (LL), includes the rostral extension of axons in the three acoustic striae and also contains ascending axons that arise in the superior olivary complex and the nuclei of the lateral lemniscus. All of the major tracts may further contain descending projections, as well as commissural fibers. The components (and/or the organization) of a tract usually vary along its extent as axons join and leave it. (For this reason, a tract should not generally be equated with one particular set of axons.) Some of the components of the major auditory tracts that are described in this chapter are illustrated in Figures 17.1–3, and information about known components of the tracts is summarized in Figure 17.4.

(p. 476) Dorsal Acoustic Stria

The DAS extends from the medial border of the dorsal cochlear nucleus, forming a cap of axons on the dorsal aspect of the inferior cerebellar peduncle,2 to the ventral pole of the lateral lemniscus, which many of its axons join. The axons of both types of principal cells in the dorsal cochlear nucleus, the fusiform and giant cells, form the main components of the DAS as they leave the cochlear nucleus (cat: Fernandez & Karapas, 1967; van Noort, 1969; Osen, 1972; Adams & Warr, 1976; Smith et al., 2005; opossum: Willard & Martin, 1983; horseshoe bat: Vater & Feng, 1990; Rhesus monkey: Barnes et al., 1943; Strominger, 1973; human: Moore & Osen, 1979). These axons form major components of the DAS throughout its course and so define the trajectory of the entire tract. The stria travels rostrally and medially away from the dorsal cochlear nucleus while also dipping ventrally as it spreads out through the middle of the pontine tegmentum, where it crosses the midline (Figure 17.2, panels 4 and 5). The tract then dips further ventrally toward the rostral and dorsal aspect of the superior olivary complex, where many of its axons turn to join the lateral lemniscus. Fernandez and Karapas (1967, their Figure 4) illustrate the course of the DAS in the cat at eight transverse levels through the brainstem, providing a good appreciation of its three-dimensional extent (see also Adams & Warr, 1976, their figure 1; Smith et al., 2005).3 As they enter the tegmentum, the axons from the dorsal cochlear nucleus appear to split into two or more separate bundles (cat: Papez, 1930; Adams & Warr, 1976); the significance of the split is not clear.

In the pontine tegmentum, the axons from the dorsal cochlear nucleus are joined in the DAS by axons from the principal cells of the lateral superior olivary nucleus that innervate the contralateral inferior colliculus. These axons leave the olivary complex dorsally and then turn medially to join the DAS (cat: van Noort, 1969; Elverland, 1978; Glendenning & Masterton, 1983; ferret: Henkel et al., 2007, see their figure 1C for an illustration of the convergence of the axons from the dorsal cochlear nucleus and the lateral superior olivary nucleus in the pontine tegmentum; mustache bat: Vater et al., 1995). After crossing the midline, the axons from the dorsal cochlear nucleus and those from the lateral superior olivary nucleus turn ventrally before then turning rostrally and dorsally to enter the lateral lemniscus.

Intermediate Acoustic Stria

The IAS is the smallest of the three acoustic striae (cat: Fernandez & Karapas, 1967; Adams & Warr, 1976; Smith et al., 1993a, 2005; Adams, 1997; rat: Harrison & Feldman, 1970; horseshoe bat: Vater & Feng, 1990; Rhesus monkey: Barnes et al., 1943; Strominger, 1973; chimpanzee: Strominger et al., 1977; human: Moore & Osen, 1979). Earlier literature contains some confusion about the cells of origin but it seems now generally agreed that most, if not all, of the ascending fibers in the IAS are the axons of octopus cells, which travel dorsally from the posteroventral cochlear nucleus, forming a bundle (p. 477) caudal to the DAS (cat: Warr, 1969, 1982; Osen, 1972; Adams, 1997; Smith et al., 2005; rat: Harrison & Feldman, 1970; Friauf & Ostwald, 1988; mouse: Felix et al., 2017). Like those of the DAS, the axons of the IAS loop over the inferior cerebellar peduncle as they leave the cochlear nucleus, but they then make a sharp turn ventrally to course along the medial border of the spinal trigeminal nucleus. As they reach the level of the caudal superior olivary complex, they turn medially and course parallel to the dorsal surface of that complex to cross the midline. On the contralateral side, the bundle of axons splits into several fascicles, some of which pass through olivary regions before rejoining the others to enter the lateral lemniscus (cat: Warr, 1982; rat: Friauf & Ostwald, 1988). The octopus cell axons in the IAS terminate in elaborate calyx-like terminations in the ventral portion of the contralateral ventral nucleus of the lateral lemniscus (cat: Stotler, 1953; Adams, 1997; Smith et al., 2005; rat: Friauf & Oswald, 1988; mouse: Felix et al., 2017; guinea pig: Schofield & Cant, 1997; human: Adams, 1997).

Ventral Acoustic Stria

The largest and most complex of the three acoustic striae, the ventral acoustic stria, is more commonly referred to as the trapezoid body (TB) in reference to the shape of the fiber bundle at the midline. The tract spans the width of the ventral brainstem at the level of the superior olivary complex; axons in the tract pass through and around the olivary nuclei. At the midline, it lies dorsal to the medullary pyramids. The TB contains almost all of the ascending axons of principle cells in the ventral cochlear nucleus (cat: Warr, 1966, 1969, 1972, 1982; van Noort, 1969; rat: Harrison & Warr, 1962; Harrison & Irving, 1966a, b; Harrison & Feldman, 1970; gerbil: Russell & Moore, 1995; guinea pig: Thompson & Thompson, 1991; dog (beagle): Goldberg & Brown, 1968; several species of bats: Zook & Casseday, 1985; Vater & Feng, 1990; Rhesus monkey: Strominger & Strominger, 1971; chimpanzee: Strominger et al., 1977; human: Moore & Osen, 1979). The tract is highly organized across its three dimensions (cat: van Noort, 1969; Brownell, 1975; Warr, 1982; rat: Harrison & Feldman, 1970). As axons leave the ventral cochlear nucleus, those from rostral regions are located rostrally and those from caudal parts are located caudally. The fibers travel in parallel as they course to the midline so the same rostral-to-caudal organization is evident there. The axons are further organized with respect to axon diameter and at least some of them are organized topographically with respect to frequency (cat: Brownell, 1975; Warr, 1982; Spirou et al., 1990). The differences in axon diameter give the TB a layered appearance. The dorsal-most layer contains medium-sized axons; the middle layer, which does not extend all the way to the rostral pole of the TB, contains large axons. The ventral, superficial layer, which is enlarged at the rostral pole of the TB, contains mainly thin axons. Some mixing of axon diameters occurs between the dorsal and middle axon layers (cat: Brownell, 1975). The axons of most of the cell populations in the cochlear nuclei and other neurons that send axons into the TB have been associated with one of these layers.

(p. 478) The medium-diameter axons of the spherical bushy cells in the anteroventral cochlear nucleus project through the dorsal half of the TB (cat: Warr, 1966, 1982; Brownell, 1975; Smith et al., 1993b; gerbil: N. B. Cant, unpublished observations; Figure 17.1) and occupy approximately the rostral two-thirds at the midline, where they are organized according to frequency (cat: Brownell, 1975; Spirou et al., 1990). The spherical bushy cell axons pass through or around the lateral and medial superior olivary nuclei on the ipsilateral side (forming terminations), traverse the medial nucleus of the trapezoid body (without terminating), cross the midline (forming terminations in the contralateral medial superior olivary nucleus), and turn rostrally to join the lateral lemniscus, where they terminate in the ventral nucleus (cat: Warr, 1966; Smith et al., 1993b; Beckius et al., 1999; rat: Harrison & Irving, 1966a). (The path followed by these axons is “dorsal” relative to the position of other axons in the TB; as they pass through the superior olivary complex itself, many of the axons may run ventral to the main nuclei [Warr, 1966; Smith et al., 1993b; Harrison & Irving, 1966a]).

The large-diameter axons of the globular bushy cells in the ventral cochlear nucleus project into the middle layer of the TB. These axons are among the largest in the auditory system and are the source of calyces in the contralateral medial nucleus of the trapezoid body (cat: Warr, 1969, 1972, 1982; Tolbert et al., 1982; Spirou et al., 1990; Smith et al., 1991; rat: Harrison & Warr, 1962; Harrison & Irving, 1966a, b; Friauf & Ostwald, 1988; mouse, gerbil, and several species of bat: Kuwabara et al., 1991). The very large, heavily myelinated axons course ventral to the nuclei of the superior olivary complex along most of its caudal-to-rostral dimension, although they are not present at the rostral pole (Brownell, 1975; Warr, 1982). They give off collateral branches to several periolivary nuclei on the ipsilateral side, cross the midline in the ventral half of the TB, send thick branches into the contralateral medial nucleus of the trapezoid body, and continue laterally and rostrally to join the lateral lemniscus. The axons terminate in the ventral nucleus of the lateral lemniscus. Unlike the fibers in the dorsal half of the TB at the midline, the ventral fibers do not appear to be organized topographically with respect to frequency (Brownell, 1975; Spirou et al., 1990). In the rat, a small number of equally thick axons arise from cells of the cochlear nerve root but travel in the most ventral part of the TB (rat: Lee et al., 1996; López et al., 1999).

Many of the multipolar neurons in the ventral cochlear nucleus project directly to the inferior colliculus. These neurons are referred to by a number of different names (cf. Oertel et al., 2011), but it is generally agreed that those that project to the IC have thin axons and leave the cochlear nucleus via the TB (cat: Warr, 1969, 1972, 1982; van Noort, 1969; Brownell, 1975; Smith & Rhode, 1989; Spirou et al., 1990; Smith et al., 1993a; Thompson, 1998; guinea pig: Thompson & Thompson, 1991; gerbil and chinchilla: Ostapoff et al., 1994; mouse: Oertel et al., 1990). Many of the multipolar cell axons enter the most ventral fiber layer in the TB, but axons of multipolar cells may be found throughout the dorsal-to-ventral dimension of the tract (cat: Warr, 1969; Smith et al., 1993a; rat: Doucet & Ryugo, 2003; mouse: Darrow et al., 2012; guinea pig: Thompson & Thompson, 1991). The trajectory pattern of the multipolar cell axons from the rostral (p. 479) (p. 480) pole of the ventral cochlear nucleus differs in detail from that of those that arise more caudally. The most rostral axons take an “obliquely anterior [rostral]” course and cross the midline at the rostral extreme of the TB (rostral to the nuclei themselves, sometimes straying into the area of the pontine nuclei; cat: Warr, 1966; gerbil: N. B. Cant, unpublished observations; Figure 17.2, panels 1–3). These axons do not appear to innervate the olivary nuclei; on the contralateral side they enter the LL at its ventral pole (Figure 17.2, panel 3).

Axon Trajectories in the Auditory BrainstemClick to view larger

Figure 17.1. Drawings to illustrate the path followed by spherical bushy cell (SBC) axons through the dorsal and rostral part of the trapezoid body. Panels 1a and 2a: Horizontal sections through the superior olivary complex of a gerbil in which biotinylated dextran amine (BDA) was injected into the medial superior olivary nucleus (MSO; injection site indicated by the black spot), filling SBC axons from the anteroventral cochlear nuclei on both sides of the brain. (These sections are from Case 644, described in Cant, 2013.) Panels 1b and 2b: Cytochrome oxidase-reacted sections adjacent to the BDA-reacted sections in panels 1a and 2a, respectively. Rostral is to the right for all horizontal sections. Inset: For purposes of orientation, the approximate levels of the horizontal sections are cross-referenced to the levels of three transverse sections from another gerbil. Dorsal is to the top for the transverse sections. Abbreviations for all figures: AVCN, anteroventral cochlear nucleus; BDA, biotinylated dextran amine (a tracer that is transported both anterogradely and retrogradely through axons); CST, corticospinal tract; DAS, dorsal acoustic stria; DCN, dorsal cochlear nucleus; DNLL, dorsal nucleus of the lateral lemniscus; IC, inferior colliculus; IPF, interpeduncular fossa; LL, lateral lemniscus; LNTB, lateral nucleus of the trapezoid body; LSO, lateral superior olivary nucleus; MCP, middle cerebellar peduncle; MG, medial geniculate nucleus; MNTB, medial nucleus of the trapezoid body; MSO, medial superior olivary nucleus; PVCN, posteroventral cochlear nucleus; pyr, medullary pyramid; SBC, spherical bushy cell; SOC, superior olivary complex; SPN, superior paraolivary nucleus; TB, trapezoid body; VCN, ventral cochlear nucleus; VII, motor nucleus of the seventh nerve; VNLL, ventral nucleus of the lateral lemniscus; VNTB, ventral nucleus of the trapezoid body; Vnr, trigeminal nerve root.

In contrast, the axons that arise from the multipolar cells in the “multipolar cell area” of the ventral cochlear nucleus (Osen, 1969) travel in the caudal half of the TB and cross the midline in parallel with the other groups of TB axons (cat: Warr, 1972). Just after they pass ventral to the contralateral medial nucleus of the trapezoid body, these axons make an almost right-angle turn and course rostrally so that they are now oriented perpendicular to the crossing TB axons (cat: Warr, 1972, 1982; Smith et al., 1993b; gerbil: N. B. Cant, unpublished observations, Figure 17.2, panels 1 and 2). Therefore, whereas the TB contains axons arranged in parallel order at the midline, in the region of the superior olivary complex, it also contains axons that course longitudinally with respect to the long axis of the brainstem. Along their caudal-to-rostral course, the multipolar cell axons give rise to terminals in the ventral nucleus of the trapezoid body (cat: Warr, 1972; Smith et al., 1993a).

A small contingent of axons that project from the caudal cochlear nucleus to the midbrain do not enter the TB directly but rather course rostrally along the medial margin of the anteroventral cochlear nucleus to enter the TB at its rostral extreme (cat: Warr, 1972, 1982; Thompson, 1998). This small bundle of axons was called the “lateral trapezoid body tract” by Warr (1972), who traced it as far as the ventral part of the LL. It may arise from small cells in the region of the granule cell layer (Thompson, 1998).

Lateral Lemniscus and Paralemniscal Fibers

The LL (Figure 17.3) contains ascending inputs to the IC from the cochlear nuclei, superior olivary complex, and nuclei of the lateral lemniscus, and it is also the route of (p. 481) (p. 482) some descending systems. It is the most complex of the major auditory fiber tracts and is also the least well-understood in terms of the organization of its components. Detailed studies, such as those described for the TB (e.g., Warr, 1966, 1982; van Noort, 1969; Brownell, 1975; Spirou et al., 1990), have not been reported. The LL lies near the lateral surface of the brainstem and spans the distance between the ventral pons (immediately rostral to the superior olivary complex) and the dorsal midbrain, where its ascending fibers enter the inferior colliculus. The LL surrounds the dorsal and ventral (p. 483) nuclei of the lateral lemniscus, and the nuclei themselves are penetrated by bundles of fasciculated axons.

Axon Trajectories in the Auditory BrainstemClick to view larger

Figure 17.2. Drawings to illustrate the paths followed by axons that project into and out of the inferior colliculus (IC). Panels 1–5: Horizontal sections through the brainstem of a gerbil in which BDA was injected into the right IC. The rostral direction is to the right of the figure. (These sections are from Case 419, described in Cant and Benson, 2006.) The approximate levels of the horizontal sections are indicated at three transverse levels in the inset (the same transverse sections shown in Figure 17.1). In this case, many axons are labeled in the ventral TB (both ascending and descending axons) but almost no axons are labeled in the dorsal TB (asterisk on panel 3; the spherical bushy cells do not project to the IC and so are not labeled in this case). Multipolar cells of the AVCN travel in the extreme rostral part of the TB (panels 1–3). Multipolar cells of the PVCN cross the midline more caudally and then turn rostrally to run parallel to the VNTB. The red arrows on panels 1 and 2 indicate the area in which the axons make the turn. Descending fibers from the inferior colliculus also run parallel to the VNTB and may be intermingled with those from the cochlear nucleus. Gray fill on the drawings indicates places where terminal branching of the axons was so dense that it was impossible to mark individual axons. Abbreviations as in legend for Figure 17.1.

Axon Trajectories in the Auditory BrainstemClick to view larger

Figure 17.3. Panels A–F: Drawings to illustrate axons in the LL in the same case shown in Figure 17.2. Panel G: Transverse section from a gerbil in which BDA was injected into the inferior colliculus (Case 430, described in Cant & Benson, 2006). The approximate levels for the top six panels are indicated by the blue lines on the transverse section. (The sections lie near those shown in Figure 17.2 but are at slightly different dorsal-to-ventral levels. The top edge of each box indicates the same distance from the midline for each section, and the right edge indicates the same distance from the front of the brain.) Abbreviations as in Figure 17.1.

The rostral, caudal, and lateral boundaries of the LL are fairly well defined, but the medial boundary is less distinct, fading into the adjacent lateral tegmentum in an area known as the paralemniscal region (also referred to as Monakow’s area in the older literature; see Varga et al., 2008, for a detailed discussion of this complex tegmental region). Rasmussen (1946) called the fibers surrounding the rostral, lateral, and caudal aspects of the nuclei the LL proper and the region medial to the nuclei the paralemniscal zone. In contrast to the more restricted sources of axons in the LL proper, the paralemniscal zone is traversed by a large variety of fibers from both auditory and non-auditory areas (e.g., Herbert et al., 1997). Axons in this region from nuclei in the lower brainstem that project directly to the medial geniculate nucleus, bypassing the inferior colliculus (e.g., Henkel, 1983), have been referred to as the central acoustic tract (discussed in, e.g., Casseday et al., 1989).

The LL, like the TB, is organized such that axons of some cell types are segregated from one another while others appear to be intermingled. The topography is complex. Axons of different cell types occupy specific zones within the medial-to-lateral and rostral-to-caudal dimensions. Further, because some axons join the tract along its ventral-to-dorsal axis, others terminate in the nuclei of the lateral lemniscus, and a few appear to change position as they course through the tract, there is also a dorsal-to-ventral organization. As noted in the following sections, many authors have noted whether axons from specific sources run in lateral or medial “bands” of the LL (i.e., lateral or medial with respect to the nuclear groups), but only a few comment on the rostral-to-caudal organization of the component axons. This an important omission because the white matter surrounding the nuclei of the lateral lemniscus appears thicker in the rostral-to-caudal dimension than in the lateral-to-medial dimension (Figure 17.3), and it is highly likely that axons that are described as having a lateral or medial location are distributed differentially in the rostral-to-caudal dimension as well.

Axons from the Cochlear Nuclei that Enter the Lateral Lemniscus

Most, if not all of the axons that arise in the cochlear nuclei and travel in one of the three acoustic striae described previously continue into the LL. Axons in the TB, IAS, and DAS join the LL near the rostral boundary of the superior olivary complex or along its ventral-to-dorsal extent. Some of these axons terminate in the nuclei of the lateral lemniscus, while others continue to the midbrain to terminate in the inferior colliculus. Axons from different parts of the cochlear nuclear complex travel in different parts of the LL.

(p. 484) After the fibers of the DAS that originate from the contralateral dorsal cochlear nucleus cross the midline, they dip ventrally toward the superior olivary complex and then turn dorsally and rostrally to ascend to the midbrain in the paralemniscal tegmentum (cat: Rasmussen, 1946; Warr, 1966; Fernandez & Karapas, 1967; van Noort, 1969; Osen, 1972; Glendenning et al., 1981; Smith et al., 2005; rabbit: Borg, 1973; horseshoe bat: Vater & Feng, 1990; Rhesus monkey: Barnes et al., 1943). As they course dorsally, they also move laterally so that they appear to enter the inferior colliculus with the other fibers of the LL proper (the white matter). Observations by Osen (1972) in kittens suggested that the axons of the giant cells and fusiform cells may be separate as they enter the inferior colliculus; lesions of the rostral part of the LL, near its entrance to the inferior colliculus, led to degeneration of fusiform cells but not of giant cells in the dorsal cochlear nucleus. In contrast to the route followed by the contralateral axons from the dorsal cochlear nucleus, the axons that arise in the ipsilateral dorsal cochlear nucleus (a relatively small number) travel in the lateral band of the LL (Warr, 1966).

The multipolar cell axons that project from both the contralateral and ipsilateral ventral cochlear nuclei to the inferior colliculus travel in the lateral band of the LL (cat: Warr, 1966, Osen, 1972; Glendenning et al., 1981; Oliver, 1987; rat: Harrison & Warr, 1962; gerbil: Benson & Cant, 2008; opossum: Willard & Martin, 1983; horseshoe bat: Vater & Feng, 1990). Some of them may also be located in the white matter rostral to the nuclei (cat: Osen, 1972; Warr, 1972, 1982; gerbil: Benson & Cant, 2008), a point that is better appreciated in horizontal and sagittal planes of section than in the more commonly used transverse plane. Some authors also report that axons from the ventral cochlear nucleus may travel through the nuclei rather than in the white matter surrounding them (cat: Osen, 1972; rat: Saldaña et al., 2009; horseshoe bat: Vater & Feng, 1990); these may be the axons of cells other than the multipolar cells.

The axons of globular and spherical bushy cells and octopus cells also send branches into the LL (cat: Warr, 1982; Smith et al., 1991, 1993b, 2005; rat: Friauf & Ostwald, 1988; guinea pig: Schofield & Cant, 1997). These axons terminate in the nuclei of the lateral lemniscus and do not reach the inferior colliculus. The octopus cell axons terminate in the ventral part of the ventral nucleus, but the bushy cell axons probably terminate throughout the ventral nuclei (reviewed by Oertel & Wickesberg, 2002). Whether the projection from the ventral cochlear nucleus to the dorsal nucleus of the lateral lemniscus (Glendenning et al., 1981; Shneiderman et al., 1988) is solely from multipolar cells on their way to the inferior colliculus or whether the axons of other cell types project so far dorsally is not known. Some or all of these axons may travel in fascicles interspersed among the cells of the nuclei of the lateral lemniscus rather than in the surrounding tract itself (cat: Glendenning & Masterton 1983; horseshoe bat: Vater & Feng, 1990). In the rat, the large axons that arise from cochlear root neurons ascend for some distance in the rostral band of the LL before leaving the tract to innervate multiple tegmental areas (rat: López et al., 1999; Nodal & Lopéz, 2003).

(p. 485) Axons from the Nuclei of the Superior Olivary Complex that Enter the LL

Most projections from the superior olivary complex to the inferior colliculus arise from principal cells in the medial and lateral superior olivary nuclei (MSO and LSO, respectively), but there are also projections from other olivary nuclei (reviewed by Schofield, 2005). Axons that arise from the ipsilateral MSO course dorsally through that nucleus (guinea pig: Smith, 1995; gerbil: Kuwabara & Zook, 1999) and then turn rostrally and laterally to join the LL, where most, if not all of them, travel in the medial band close to the nuclei of the lateral lemniscus (cat: Rasmussen, 1946; van Noort, 1969; Elverland, 1978; Henkel & Spangler, 1983, their Figure 5; Henkel, 1997; mustache bat: Zook & Casseday, 1987; Vater et al. 1995). Some of the MSO axons may course in the LL rostral to the nuclei (Henkel & Spangler 1983). Axons from principal cells in the LSO that project to the ipsilateral inferior colliculus (mainly glycinergic, Saint Marie et al., 1989 [cat]) also exit the nucleus dorsally and join those from the MSO to travel to the inferior colliculus in the medial band or paralemniscal region (cat: Rasmussen, 1946; van Noort, 1969; Elverland, 1978; Glendenning et al., 1981; mustache bat: Vater et al., 1995). Like those from the MSO, some of the axons from the LSO may also run in the rostral LL (Glendenning et al., 1981, their Figure 10). Some authors report that a few axons from the MSO and LSO run in the lateral band of the LL, but Henkel & Spangler (1983) argue that the axons in question probably arise from other olivary sources.

Axons from the LSO that project to the contralateral inferior colliculus cross the midline in the DAS (see previous discussion) and appear to remain together with the axons from the dorsal cochlear nucleus as they travel to the inferior colliculus in the medial (paralemniscal) band of the LL (suggested by figures in Elverland, 1978 [cat]; Glendenning et al., 1981 [cat]; Casseday et al., 1988 [horseshoe bat]). The organization of these fibers in the medial band with respect to those from the ipsilateral LSO and MSO is not known. If the axons from the two sides do remain segregated in the LL, the organization prefigures that in the central nucleus of the inferior colliculus, where the terminations from the ipsilateral and contralateral LSOs are non-overlapping, terminations from the contralateral dorsal cochlear nucleus overlap those from the contralateral LSO, and those from the ipsilateral MSO overlap those from the ipsilateral LSO (cat: Shneiderman & Henkel, 1987; Oliver et al., 1997; Loftus et al., 2004).

Axons from several additional populations of olivary cells appear to be located in specific parts of the LL. Thick axons of GABAergic cells in the superior paraolivary nucleus travel to the inferior colliculus in the paralemniscal zone, passing through the paralemniscal nucleus (rat: Saldaña et al., 2009). Axons from the medial and ventral nuclei of the trapezoid body, on the other hand, ascend through the nuclei or are located in the lateral and/or rostral bands of the LL (cat: Glendenning & Masterton, 1983; Henkel & Spangler, 1983; Spangler et al., 1985; Smith et al., 1998; rat: Sommer et al., 1993; Warr & Beck, 1996; horseshoe bat: Casseday et al., 1988). Many of these projections, like the (p. 486) ipsilateral projections from the lateral superior olivary nucleus, are glycinergic (chinchilla and guinea pig: Saint Marie & Baker, 1990).

Projections to the inferior colliculus from the nuclei of the lateral lemniscus themselves appear to course dorsally through the nuclei rather than in the surrounding fiber tract (cat: Kudo, 1981; Whitley & Henkel, 1984; rat: Merchán et al., 1994).

Routes Followed by Descending Auditory Axons

Almost all auditory structures contain populations of neurons that send axons to nuclei at lower levels of the neuraxis. Collectively, these projections make up the descending auditory pathways (reviewed by Saldaña, 1993; Thompson, 2005; Schofield, 2011). Routes taken by the descending axons have not been documented as completely as those of the ascending systems, but some authors have taken care to illustrate and discuss the routes taken by specific systems. Like the fibers of the ascending pathways, those of the descending pathways appear to follow defined, stereotypic routes (e.g., Feliciano et al., 1995).

Descending Pathways from the Auditory Cortex

Axons arising from pyramidal cells in most, if not all, fields of auditory cortex travel with other corticobulbar and corticospinal fibers through the internal capsule and cerebral peduncles, where they occupy its most lateral part (cat: Rasmussen, 1964; rat: Feliciano et al. 1995; Saldaña et al., 1996; reviewed by Saldaña, 2015). Descending axons follow at least three routes into the ipsilateral inferior colliculus (rat: Feliciano et al., 1995). Two bundles of thick axons leave the peduncle at the level of the midbrain. One of these runs directly into the inferior colliculus through its rostral pole. The second runs more laterally to enter via the brachium of the inferior colliculus. A third group of axons leaves the descending cortical tract at the pontine level and then courses dorsally in the paralemniscal region and rostral band of the LL. Some of these fibers reach the inferior colliculus but others appear to terminate in tegmental areas (rat: Feliciano et al., 1995; Saldaña et al., 1996). Within the inferior colliculus, terminations from the three groups appear to intermingle. Whether the three groups of fibers arise from separate sources and/or have different targets within the inferior colliculus is not known. A few of the cortical fibers cross to the contralateral inferior colliculus via the collicular commissure.

For the most part, the cortical projections to the superior olivary complex and cochlear nuclei arise from different populations of neurons (rat: Doucet et al., 2002) and follow different routes through the brainstem (rat: Feliciano et al. 1995; guinea pig: Coomes and Schofield 2004). The cortical fibers that innervate the superior olivary (p. 487) complex travel with the corticospinal tract as far as the medullary pyramids, where they turn to enter the superior olivary complex and split into two bundles, a small bundle that spreads over the dorsal aspect of the complex and a larger bundle that courses caudally, giving rise to terminals along the rostral-to-caudal extent of the ventral nucleus of the trapezoid body (perpendicular to the crossing fibers of the TB).

On the other hand, most of the cortical fibers that innervate the cochlear nuclei follow a route unrelated to the major auditory fiber bundles (rat: Feliciano et al., 1995). These axons leave the cerebral peduncles in the midbrain and run in a dorsal and caudal direction to reach the level of the middle cerebellar peduncle. They course next to the peduncle until they reach the dorsal aspect of the anteroventral cochlear nucleus, which they enter through the dorsal region known as the subpeduncular area (cat, rat and mouse: Mugnaini et al., 1980; Osen et al., 1984; Weedman et al., 1996). The few cortical fibers that innervate the contralateral superior olivary complex and/or cochlear nucleus cross the midline in the TB and those that innervate the cochlear nucleus may then follow a circuitous route into the subpeduncular corner that mimics that of the ipsilateral projection (rat: Feliciano et al., 1995; guinea pig: Coomes & Schofield, 2004).

Descending Pathways from the Inferior Colliculus to the Superior Olivary Complex and the Cochlear Nuclei

Projections to the superior olivary complex and cochlear nuclei appear to arise from largely separate populations of neurons in the inferior colliculus (rat: Okoyama et al., 2006; guinea pig: Coomes & Schofield, 2004). Both projections reach their targets via the LL, but whether they travel in the same or separate parts of the tract is not clear. Most authors report that descending collicular fibers travel through the nuclei or in the lateral band of the LL (cat: van Noort, 1969; rat: Faye-Lund, 1986; Caicedo & Herbert, 1993; Saldaña, 1993; Malmierca et al., 1996; rabbit: Borg, 1973; Rhesus monkey: Moore & Goldberg, 1966). However, Rasmussen (1960) states that the axons destined for the cochlear nucleus travel in “Monakow’s bundle” (i.e., the medial band of the LL).

At the rostral pole of the superior olive, collicular fibers that innervate olivary nuclei leave the LL to run along the rostral-to-caudal axis of the ventral nucleus of the trapezoid body, forming terminations along its length (rat: Vetter et al., 1993; guinea pig: Thompson & Thompson, 1993). Thus, these axons course perpendicular to the crossing fibers of the trapezoid body and parallel to the cortical axons that also innervate the ventral nucleus.

The collicular axons that innervate the cochlear nucleus also travel from rostral to caudal through the TB. In the caudal part of the tract, they turn laterally or medially to travel to the ipsilateral or contralateral cochlear nuclei, respectively (cat: Conlee & Kane, 1982). At the border of the cochlear nucleus, they turn dorsally to pass between the medial border of the posteroventral cochlear nucleus and the lateral boundary of the inferior cerebellar peduncle as the “centrifugal bundle of Lorente de Nó” (cat: Rasmussen, (p. 488) 1960; van Noort, 1969; Adams & Warr, 1976; rat: Caicedo & Herbert, 1993; Malmierca et al., 1996; mouse: Lorente de Nó, 1981, his figure 6-4). The major target of the recurrent bundle is the granule cell layer associated with the dorsal cochlear nucleus (Malmierca et al., 1996). As already noted, this is also the major target of projections from the auditory cortex. Thus, the terminations of the cortical and collicular projections ultimately appear to overlap, although the axons reach the nucleus via quite different routes.

Descending Pathways from the Superior Olivary Complex to the Cochlear Nucleus and Cochlea

Nuclei of the superior olivary complex send bilateral projections to the cochlear nuclei via all three acoustic striae (cat: van Noort, 1969; Elverland, 1977; Adams & Warr, 1976; Spangler et al. 1987; rat: Warr & Beck, 1996; rabbit: Borg, 1973). These projections include the only descending inputs to the cochlear nucleus that have been identified as inhibitory (guinea pig: Benson & Potashner, 1990; Ostapoff et al., 1997). Most of the contralateral projections are GABAergic, whereas the ipsilateral projections are mainly glycinergic.

At the midline, crossing axons from the ventral nucleus of the trapezoid body (the main source of contralateral projections to the cochlear nucleus) travel in rostral and dorsal portions of the trapezoid body (cat: Spangler et al., 1987; rat: Warr & Beck, 1996; Gómez-Nieto et al., 2008). Whether they are segregated from the axons of the spherical bushy cells or interspersed among them is not known, but as descending axons approach the medial boundary of the cochlear nucleus, both glycinergic (large) axons and GABAergic (small) axons are gathered into distinct fascicles, separated from the ascending fibers of the TB (guinea pig: Kolston et al., 1992; but not present in baboon: Moore et al., 1996).

Cholinergic axons of the olivocochlear bundle (to be discussed further) send branches into the cochlear nucleus as they pass by it in the vestibular nerve root; the branches enter the ventral cochlear nucleus all along its medial border (cat: Osen & Roth, 1969; Brown et al., 1988; rat: White & Warr, 1983; Osen et al., 1984; mouse: Brown et al., 1988, 1991; Brown, 1993; guinea pig: Winter et al., 1989; gerbil: Ryan et al., 1990; Brown et al., 1988; but apparently not present in human: Moore & Osen, 1979). In rodents, another group of cholinergic axons that arise in the ventral nucleus of the trapezoid body travel to the ventral cochlear nucleus in the TB and innervate the large neurons in the cochlear nerve root (rat: Sherriff & Henderson, 1994; Gómez-Nieto et al., 2008).

The best-characterized descending auditory projections are those from neurons in the superior olivary complex that travel in the olivocochlear bundle to the cochlea (reviewed by Warr, 1992). The discovery of this projection was a consequence of keen interest in the so-called olivary peduncle, a bundle of axons present in a variety of species that extends almost vertically between the superior olivary complex and the floor of the fourth ventricle (Papez, 1930; Rasmussen, 1946; see Rasmussen for a concise history (p. 489) of the long interest in this bundle of axons). Rasmussen (1946) discovered the source of these fibers in the superior olivary complex and demonstrated that they crossed the midline in the floor of the fourth ventricle and travelled with the vestibular nerve root out of the brain. He gave the bundle the name used today, the olivocochlear bundle (OCB; see White & Warr, 1983, their figures 2 and 3, for detailed illustrations of the course of the OCB fibers in the brainstem [rat]). At the level of the cochlea, the OCB fibers form the vestibular anastomosis of Oort, leaving the vestibular nerve root and entering the cochlear modiolus (e.g., cat: Arnesen & Osen, 1984).

Not all OCB fibers cross the midline (see e.g., Warr, 1992); those that do not cross course parallel and lateral to the crossing fibers in the olivary peduncle (Rasmussen, 1960). Brown (1993) followed individually labeled axons of these lateral OCB fibers and demonstrated that many of them turn medially (with the crossing fibers) before looping back to project out of the brain on the same side (see his figure 17.1 for illustrations of the course taken by both medial and lateral OCB fibers [mouse]). The anatomical detail is significant for interpretation of lesion studies because it suggests that large lesions, even if placed near the midline, could damage both crossed and uncrossed axons (Brown, 1993). Although it is sometimes suggested that axons that project out of the medial and lateral superior olivary nuclei join the olivary peduncle before entering the LL, this was explicitly denied by Papez (1930) and Rasmussen (1946). Rather, for a short distance, these axons run lateral and parallel to the fibers of the olivary peduncle.

Brainstem Commissures

In addition to the decussating axons that connect auditory nuclei with those at different levels of the brainstem, commissural projections interconnect the right and left cochlear nuclei and inferior colliculi. In both cases, these projections are made up of both excitatory and inhibitory axons.

Connections between the Cochlear Nuclei on the Two Sides of the Brain

Commissural connections between the cochlear nuclei (cat: Adams & Warr, 1976; Cant & Gaston, 1982; guinea pig: Shore et al., 1992; Schofield & Cant, 1996) consist of both excitatory and inhibitory components (guinea pig: Wenthold, 1987; rat: Alibardi, 1998, 2006). Large inhibitory (glycinergic) axons arise from multipolar neurons in the ventral cochlear nucleus and leave via the “commissural stria,” a loose bundle of glycine-positive axons adjacent and rostral to the DAS (cat: Smith et al., 2005; guinea pig: Kolston et al., 1992; mouse: Brown et al., 2013; baboon: Moore et al., 1996). The commissural fibers cross the midline in the DAS (mouse: Brown et al., 2013), where they spread out in the (p. 490) dorsal-to-ventral dimension and so appear to be intermingled with the crossing axons from the dorsal cochlear nucleus and the lateral superior olivary nucleus. Near the point where the DAS joins the LL, some of the commissural axons peel off ventrally to enter the TB. Others course dorsally to enter the dorsal cochlear nucleus via the DAS (or perhaps the adjacent commissural stria). Some of the commissural axons do not turn but rather course straight toward the cochlear nucleus (passing through the trigeminal nucleus and tract) to enter the ventral cochlear nucleus along its medial border (cat: Cant & Gaston, 1982; Smith et al., 2005; guinea pig: Schofield & Cant, 1996; mouse: Brown, et al., 2013, their figures 2 and 3; baboon: Moore et al., 1996). Whether the excitatory component of the commissure follows the same or different routes is not known.

Midbrain Commissures

Thick axons arising from the GABAergic cells of one dorsal nucleus of the lateral lemniscus project across the midline to the nucleus on the opposite side via the prominent commissure of Probst (cat: Adams & Mugnaini, 1984; Henkel & Shneiderman, 1988; Hutson et al., 1991; squirrel monkey: Goldberg & Moore, 1967; gerbil: N. B. Cant, unpublished observations; Figure 17.1, panel 5). The commissure takes an almost straight path across the midline ventral to the periaqueductal gray nuclei, and the large axons enter the opposite dorsal nucleus from its rostral aspect (cat: Kudo, 1981; Figure 17.3, panel F). The only other known components of this commissure are axons that project from the dorsal nucleus of the lateral lemniscus to the contralateral inferior colliculus and axons that project from the nucleus sagulum on one side to that on the other (cat: Henkel & Shneiderman, 1988; Hutson et al., 1991).

Projections from one inferior colliculus to that on the opposite side travel via the prominent collicular commissure that lies dorsal to the cerebral aqueduct (reviewed by Saldaña and Merchán, 2005). Other axons that travel in this commissure include projections from the inferior colliculus to the contralateral medial geniculate nucleus and axons from lower brainstem nuclei that first enter the ipsilateral colliculus and then cross to the opposite side (cat: Hutson et al., 1991; rat: Viñuela et al., 2011).

Routes Followed by Non-auditory Inputs to Auditory Nuclei

Several somatosensory nuclei, including the dorsal column nuclei and spinal nuclei of the trigeminal nerve provide input to the auditory system (e.g., tree shrew: Schroeder & Jane, 1971; rat: Massopust et al., 1985). Like other axons leaving the dorsal column (p. 491) nuclei, the axons that innervate auditory structures course ventrally and medially as internal arcuate fibers, cross the midline, and join the contralateral medial lemniscus to run rostrally. At the level of the pontine nuclei, axons destined for the inferior colliculus move into the nearby LL and travel in its most lateral part to reach the dorsal midbrain (Schroeder & Jane, 1971). Presumably, axons destined for the cochlear nuclei (e.g., rat: Weinburg & Rustioni, 1987) leave the medial lemniscus at the level of the superior olivary complex to join the trapezoid body, but this has not been explicitly demonstrated.

Axons from the spinal nucleus of the trigeminal nerve that project to the inferior colliculus cross to the contralateral side and course ventrally to join the trigeminothalamic tract adjacent to the medial lemniscus. At the pontine level, the axons peel away from this tract to enter the LL and ascend to the inferior colliculus (Zhou & Shore, 2006). The location of the axons within the lateral lemniscus was not specified. Axons that project from the spinal nucleus of the trigeminal nerve to the cochlear nuclei course along the spinal trigeminal tract and enter the cochlear nucleus via either the IAS or the DAS (Zhou & Shore, 2004). Routes taken by other non-auditory inputs to the brainstem auditory structures (reviewed by Cant & Oliver, 2018; Schofield & Hurley, 2018) have not been described in detail.

Some axons that initially travel in the medial lemniscus and the trigeminothalamic tract enter the LL before again peeling off to innervate portions of the midbrain reticular formation and the deep layers of the superior colliculus (rat: Massopust et al., 1985; Macaque monkey: Wiberg et al., 1987). Thus, a few axons that travel in the ventral LL may not be part of the auditory system.

Conclusion

Information about the trajectories followed by specific groups of axons (summarized in Figure 17.4) has been used by experimental psychologists, neurophysiologists, molecular and cellular biologists, developmental neurobiologists, and neuroanatomists to design and interpret experiments that have furthered our knowledge of auditory function. However, there are important gaps in our knowledge concerning the organization of the white matter of the auditory system, and it is logical to suggest that filling the gaps could lead to improved experimental protocols and more informed interpretation of a wide variety of studies. Descriptions of the organization of axons in the lateral lemniscus and the associated nuclei of the lateral lemniscus are especially incomplete. It is possible that axons from specific sources are bundled together in that tract and segregated from axons from other sources (as is the case to a large extent in the trapezoid body), but the descriptions of the trajectories are insufficient to allow even tentative conclusions about many of the axons that travel in this tract. Even relatively simple analyses of axons in cross section at several dorsal-to-ventral levels of the lateral lemniscus (as was done for (p. 492) the trapezoid body at the midline) could lead to new insights into the organization of that tract. Studies in which glycinergic and/or GABAergic axons are specifically labeled could add further information about the organization of axons of specific cell types. As noted at the beginning of this chapter, some of the earliest studies of the auditory pathways emphasized descriptions of the major tracts. With the continuing improvement of non-invasive methods of imaging fiber tracts in the brain, methods that can be used in both humans and experimental animals, there is reason for renewed interest in the specific details of the organization of those tracts (e.g., Schmahmann et al., 2007; Calabrese et al., 2015; Tarabichi et al., 2018). These new methods are becoming available at a time when there is also increasing recognition that abnormalities in the brainstem may contribute significantly to hearing disorders (e.g., Felix et al., 2018; Palmer & Berger, 2018). Neuroanatomical studies of the tracts will continue to be important for validating and interpreting new methods that have potential for improved understanding of human disease.

Axon Trajectories in the Auditory BrainstemClick to view larger

Figure 17.4. Summary of the components of the three acoustic striae (A) and of the lateral lemniscus (B), as described in the text. The red box indicates the relative locations (from dorsal to ventral) of auditory fiber bundles in the pons at the midline. (i, ipsilateral; c, contralateral; other abbreviations as in Figure 17.1.)

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Notes:

(1.) The fascinating history of the development of topological subway maps begins in the 1930s with Harry Beck, who developed the first such map for users of the London Underground (e.g., Toor, 2013). Similar maps are now used in most major cities of the world, with the interesting exception of New York City (Rawsthorn, 2012). Nowadays, we take such maps for granted, but we know better than to rely on them when navigating above ground.

(2.) In marsupials, the dorsal cochlear nucleus is located medial to the peduncle so that the DAS does not pass over it (e.g., Aitkin, 1996).

(3.) Although Fernandez and Karapas (1967) appear to equate the DAS with the axons from the dorsal cochlear nucleus, here it is considered (in conformity with most authors) that the DAS extends only as far as the rostral aspect of the superior olivary complex, where many of its axons enter the lateral lemniscus.