John M. Zook

Intracellular labeling of afferents to the lateral superior olive in the bat, Eptesicus fuscus

An in vitro tissue slice preparation of the bat brain stem was used to label intracellularly individual axons projecting to the lateral superior olive from two different sources: the medial nucleus of the trapezoid body (MNTB) and the anteroventral cochlear nucleus (AVCN). The tracing of individually labeled MNTB axons into the lateral superior olive reaffirms the long accepted indirect route by which information from the contralateral ear reaches the lateral superior olive. While the MNTB appears to relay input from the contralateral AVCN, information from the ipsilateral ear reaches the lateral superior olive via a direct projection from the ipsilateral AVCN. Axons from the contralateral and ipsilateral pathways have different distribution patterns upon the fusiform cells of the lateral superior olive. Axon terminals of MNTB principal cells have a perisomatic and proximal dendritic distribution pattern. Axon terminal varicosities from the ipsilateral anteroventral cochlear nucleus are distributed primarily to more distal dendrites.

Geniculo-collicular descending projections in the gerbil.

Axonal projections were labeled using a combination of tract-tracing and intracellular staining to examine the connection between the auditory thalamus and tectum. We report descending projections from the medial and dorsal divisions of the medial geniculate body to the external nucleus of the ipsilateral inferior colliculus and lower brainstem of the gerbil. These were studied in quasi-parasagittal brain slice preparations containing auditory thalamus, tectum and brainstem. Slices were cut in a curved, roughly parasagittal plane from the level of the thalamus to the brainstem. When properly cut, a single thick slice included most of the ipsilateral auditory cell groups and pathways at these levels. The geniculo-collicular projections were revealed after extracellular injections of Biocytin and rhodamine-conjugated biotinylated dextran amine in the medial geniculate body were applied to these slices. Furthermore, cells in the medial geniculate body that had been retrogradely prelabeled with a fluorescent tracer, Fluoro-Gold, injected in the inferior colliculus were intracellularly labeled to confirm the presence of the descending axons. In these preparations, single cells with descending axons were traced through their entire extent to their terminals in the inferior colliculus. Our results clearly demonstrate the geniculo-collicular descending projection and suggest a thalamo-tectal feedback loop.

Local collateral projections from the medial superior olive to the superior paraolivary nucleus in the gerbil.

Local collateral projections from the medial superior olivary nucleus in the gerbil auditory brainstem were examined to study the possible communication of this nucleus with periolivary cell groups. The projections were investigated using intracellular and extracellular labeling with Biocytin in the medial superior olive (MSO) in brainstem tissue slices. Collateral axons were found to branch from the main axons of the central cells of the MSO as the latter passed through a dorsally neighboring periolivary nucleus, the superior paraolivary nucleus (SPN), toward the ipsilateral inferior colliculus (IC), their traditionally accepted target. Bouton-like endings and en passant varicosities of these collaterals appeared to contact the somata and proximal dendrites of cells within the SPN. Furthermore, close observation revealed that these collaterals terminate on at least two types of SPN cells. Intracellular labeling of the collateral axons of the MSO neurons combined with retrograde prelabeling of their target cells, however, revealed that the collaterals selectively contact the cells of the SPN that project to the ipsilateral IC. A link between the MSO and SPN has not been reported previously. This connection is of interest since SPN cells themselves project either to the cochlear nuclei (CN) or the IC. The MSO-SPN projection identified here raises the possibility that the latter may serve as an ancillary channel to convey MSO information to the IC.

Some Comparative Aspects of Auditory Brainstem Cytoarchitecture in Echolocating Mammals: Speculations on the Morphological Basis of Time-Domain Signal Processing

A number of studies have described the gross morphology and general hypertrophy of the auditory brainstem nuclei in Cetacea and Chiroptera (See Henson, 1970 for review; Zvorykin, 1959, 1963). However, there have been only a few attempts to describe the cytoarchitecture of the auditory brainstem in detail (Osen & Jansen, 1965; Schweizer, 1981; Zook & Casseday, 1982) or to make comparisons of brainstem auditory cytoarchitecture between echolocating species of bats and marine mammals. We will begin here to take a closer look at the auditory brainstem of a number of microchiropteran and odontocete cetacean species, initially focusing upon a few distinctive cytoarchitectonic patterns found in three cell groups: the anteroventral cochlear nucleus (AVCN), the medial nucleus of the trapezoid body (MNTB) and the ventral nucleus of the lateral lemniscus (VNLL). In some species of bat and dolphin, cells in these nuclei form orderly rows or columns that are more uniformly aligned than is found in most nonecholocating mammals. In the two dolphin species examined, rows of cells perpendicular or at an angle to the fibers of the trapezoid body are present in the caudal part of the AVCN and in the MNTB. Within the VNLL in some bat species there is a distinctive alignment of cell soma, in columns rather than rows, parallel to fiber bundles.

A Potential System of Delay-Lines in the Dolphin Auditory Brainstem

This is the second of an ongoing series of reports on the comparative cytoarchitecture of the dolphin auditory brainstem. The previous report (Zook et al., 1988) focused on unusually ordered cell arrangements within three auditory brainstem cell groups: the ventral cochlear nucleus (VCN), the medial nucleus of the trapezoid body (MNTB) and the ventral nucleus of the lateral lemniscus. Part of each cell group is distinguished by an orderly alignment of cells into straight rows or columns.

Projections of Cochlear Nucleus to Superior Olivary Complex in an Echolocating Bat: Relation to Function

Studies of comparative neuroanatomy provide information about structural variations that in turn can be clues to function. It is in this spirit that we use the mustached bat Pteronotus parnellii as our example in this paper on the inputs from the cochlear nucleus to the superior olivary complex. We will show that the projections from the cochlear nucleus to the lateral superior olive (LSO) are virtually identical to those of other mammals, but the projections to the medial superior olive (MSO) are different in that the ipsilateral input is extremely sparse. We shall propose that this difference is in the proportion of the ipsilateral to contralateral inputs, not that there is a unique input to the MSO of the mustached bat. We will focus on the functional consequences of the unusual pattern of inputs to MSO. We will argue that one of the consequences of the bat’s adaptations for echolocation is the evolution of the MSO into a structure in which a difference in projections from one cochlear nucleus produces great functional differences.

Superior Olivary Cells with Descending Projections to the Cochlear Nucleus

The cochlear nucleus is the target of a greater concentration of descending projections than any other auditory structure, including the cochlea (Rasmussen,’ 64; Cant and Morest,’ 78; Spangler and Warr,’ 91). In contrast to the rest of the central auditory system, parts of the cochlear nucleus may receive more descending afferents than ascending afferents (Kane and Conlee,’ 79; Conlee and Kane,’ 82; Spangler et al.,’ 87). Despite their unusual numbers and potential importance, the descending inputs to the cochlear nucleus have received limited attention. Consequently, we have an equally limited understanding of the contribution of descending projections to the functional integrity of the cochlear nucleus. General stimulation of the descending fibers has broad inhibitory effects upon unit activity, although some facilitory effects have also been reported (Pfalz,’ 62; Comis and Whitfield,’ 68; Starr and Wernick,’ 68; Comis and Davies,’ 69; Comis,’ 70; Mast,’ 70; Bourk,’ 76; Brown and Buchwald,’ 76; Caspary,’ 86). Pickles and Comis (’73) and Pickles (’76) have argued that descending input may enhance signal detection in noise by influencing critical bandwidth, but this concept has not been developed. Others have suggested an influence of descending input on the effective encoding of complex signals (Frisina et al.,’ 90; Shore et al.,’ 91). Still other proposed roles of the descending auditory pathways, such as loudness protection, might be expected to function at the level of the cochlea rather than at the level of the cochlear nucleus (Cody and Johnstone,’ 82; Liberman,’ 88).