Auditory and lateral line inputs to the midbrain of an aquatic anuran: neuroanatomic studies in Xenopus laevis.

The torus semicircularis of anurans, which is homologous to the inferior colliculus in mammals, is an important area for processing auditory information. In particular, the torus is implicated in the ability to discriminate between different frog calls, which typically vary in beat or click rate (Rose and Capranica, 1983, 1984, 1985; Alder and Rose, 1998). Because neural processing of the temporal features of sounds is poorly understood, the torus provides an attractive target system from both computational and behavioral standpoints. The neuroanatomy of the torus has been extensively studied in terrestrial anurans (Wilczynski, 1981; Wilczynski and Neary, 1983; Feng and Lin, 1991), but in the aquatic anuran Xenopus laevis, data are sparse and conflicting (Paton et al., 1982; Nikundiwe and Nieuwenhuys, 1983; Will et al., 1985b; Lowe, 1986). Unlike adult terrestrial frogs, aquatic anurans maintain an intact lateral line system and this modality is also processed in the torus (Elepfandt, 1996); how lateral line and acoustic information interact is not known. By what pathway does auditory information arrive at the torus? Xenopus has a modified tympanum, located just under the skin on the side of the head, into which the middle ear bones insert (Wever, 1985). Anuran acoustic end organs include the amphibian and basilar papillae, the saccule, and the lagena (Feng et al., 1975; Caston et al., 1977; Baird and Lewis, 1986). Auditory information derived from movement of the sensing membranes and hair cells within the auditory end organs is conveyed to the medulla by means of axons of the 8th nerve, which projects to the dorsal medullary nucleus, or DMN (Matesz, 1979; Wever, 1985; Will et al., 1985a; Will and Fritzch, 1988). The DMN projects to the superior olive and the nucleus of the lateral lemniscus; these together with the DMN, in turn, project to the midbrain auditory region, the torus semicircularis (Wilczynski, 1981; Wilczynski and Capranica, 1984). The anuran torus itself includes three subnuclei: the principal, laminar, and magnocellular (Potter, 1965). The organization of the torus semicircularis in X. laevis superficially resembles that of terrestrial frogs. Neuroanatomic and electrophysiological studies suggested that auditory information goes primarily to the principal nucleus (Will et al., 1985b; Lowe, 1986). However, a 2-deoxyglucose study using deafened and hemideafened male X. laevis suggested instead that auditory information is restricted to the laminar nucleus (Paton et al., 1982). This subnucleus is further distinguished by the presence of cells that concentrate gonadal steroid hormones (Morrell et al., 1975; Kelley, 1980). The torus semicircularis also processes a second sensory modality, the detection of near field changes in water pressure sensed by the lateral line system (Elepfandt, 1996). This input enters the central nervous system by means of the lateral line nerves, which innervate the lateral line nucleus (n.LL) located medial to the DMN (Will et al., 1985a). Cells of the n.LL project to the torus directly (Plassmann, 1980; Altman and Dawes, 1981; Lowe, 1986). In Xenopus, the lateral line system remains intact into adulthood, whereas in terrestrial frogs, the lateral line system degenerates during metamorphosis and is absent in the adult. Which subnuclei of the torus receive lateral line input has not been studied extensively; Lowe’s results (1986) suggest input to the magnocellular nucleus (as per Will et al., 1985b). In any case, the maintenance of a functional lateral line system in adults complicates the organization of the torus in Xenopus relative to terrestrial Anura. Whether the laminar nucleus receives any direct input from either sensory system is also unclear. To determine which subnuclei of the torus receive auditory input and lateral line input, respectively, in Xenopus laevis, we carried out a detailed neuroanatomic study of the torus. We injected tracers into each subnucleus of the torus specifically and mapped their respective afferents and efferents. In addition, we used the method of Golgi to characterize the dendritic arborization patterns of neurons in each subnucleus. The information thus obtained will be helpful in understanding temporal processing of auditory and lateral line information in Xenopus laevis.