The fine structure of nerve endings in the nucleus of the trapezoid body and the ventral cochlear nucleus

Abstract

Large, calyciform axonal endings, as well as typical terminal boutons, have been previously described in the ventral cochlear nucleus and the nucleus of the trapezoid body by light microscopists. In the present study, these endings were examined with the electron microscope in chinchillas, rats, and a cat after perfusion fixation with osmium tetroxide. The calyces were found to consist of elongated processes arising from myelinated axons and making multiple synaptic contacts with perikarya and dendrites. This finding suggests that an important property of calyces is the large amount of synaptic activity that they can bring to bear on a single postsynaptic structure. Adjacent to the calyciform endings were variable numbers of boutons that made synaptic contacts with the same perikarya and dendrites. The majority of boutons contained smaller synaptic vesicles than those present in the calyces, implying both anatomical and functional differences between these two types of ending. It is suggested that many of these boutons in the ventral cochlear nucleus are endings of centrifugal, inhibitory fibers described by previous workers.Held (1893) and others (e.g., Ram6n y Cajal, '34; Harrison and Irving, '65) have described calyciform terminations of axons in mammalian auditory nuclei. When impregnated with the Golgi method, these calyces of Held appear at the terminations of axons as expansions of variable size from which arise processes of variable shape. These elongated processes provide for large areas of apposition between a single axonal ending and a perikaryon or dendrite. It has been shown that similar calyciform axonal endings in chick ciliary ganglia are electrically coupled with ganglion cells (Martin and Pilar, '63a, b, '64), and thorough cytological studies of these calyces are available (e.g., Takahashi and Hama, '65). It therefore seemed of interest to examine the auditory calyces with the electron microscope, and to compare their structure to that of the chick ciliary ganglion calyces.Among the calyciform endings in mammalian auditory nuclei are other axonal endings which appear as typical terminal boutons in Golgi preparations (Ram6n y Cajal, '09). They are distinguished from calyces by their smaller size and simple shape. In the cochlear nucleus, many of these appear to be endings of axons from AM. J. ANAT., 1 1 8 : 375-390.higher auditory centers (Rasmussen, '60), which are probably inhibitory (Pfalz, '62). A second objective of this study was to identify these endings and to determine their synaptic relationships with the calyces and adjacent neurons. MATERIALS AND METHODSThe material for the present report consisted of four adult rats, three adult chinchillas, and one adult cat. The regions studied most intensively were the nucleus of the trapezoid body in rat, and the ventral cochlear nucleus in chinchilla.Animals were first anesthetized with chloral hydrate, and the body temperature lowered to 26°C (Wolfe, '65). The brains were fixed by perfusion through the aorta with balanced salt solution...

Primary innervation of the avian and mammalian cochlear nucleus

“…Because the calycine endings are among the largest in the brain, they engender considerable interest. They are typified by multiple, punctate individual synaptic contacts, associated large, round synaptic vesicles (50-60 nm in diameter), coverings by astrocytic processes, and extracellular spaces between the ending and postsynaptic cell body [51,63,72,95,205]. Intra-axonal labeling and degeneration studies reveal that both large and small endings share these cytologic features, emphasizing the idea that synapses of primary auditory fibers are identical [28,51,203].…”

Multiple Large Inputs to Principal Cells in the Mouse Medial Nucleus of the Trapezoid Body

“…Each input had all the electrophysiological characteristics ascribed to the calyceal inputs to these cells, suggesting that some cells may receive multiple calyces as described anatomically in the ventral cochlear nucleus (Lenn and Reese 1966). In the 101 cells we examined for the occurrence of this phenomenon (after the cell in which we first noticed it serendipitously), we identified it in six more cells; as discussed in the following text, this may represent an underestimate of the true frequency.…”

“…Axons from the globular bushy cells in the ventral cochlear nucleus (VCN) cross the midline in the trapezoid body and give rise to one or two calyces (Smith et al 1991). Anatomical studies in the young and mature rat (Casey and Feldman 1985;Kandler and Friauf 1993;Sätzler et al 2002;Taschenberger et al 2002), cat (Morest 1968a;Smith et al 1991), and other animals (e.g., Lenn and Reese 1966) have reported that each postsynaptic principal cell receives input from only one calyx. In addition to the calyceal synapse, other, smaller, bouton contacts onto the principal cell and its dendrites have been observed (e.g., Lenn and Reese 1966).…”

“…Anatomical studies in the young and mature rat (Casey and Feldman 1985;Kandler and Friauf 1993;Sätzler et al 2002;Taschenberger et al 2002), cat (Morest 1968a;Smith et al 1991), and other animals (e.g., Lenn and Reese 1966) have reported that each postsynaptic principal cell receives input from only one calyx. In addition to the calyceal synapse, other, smaller, bouton contacts onto the principal cell and its dendrites have been observed (e.g., Lenn and Reese 1966). One study in the cat indicated that the small contacts may cover as much of the principal cell as the calyx (Smith et al 1991) although most studies have reported a lower fraction.…”

Slack and Slick KNaChannels Regulate the Accuracy of Timing of Auditory Neurons

“…In mammals, globular bushy neurons of the anterior ventral cochlear nucleus (aVCN) and principal neurons in the medial nucleus of the trapezoid body (MNTB) are capable of firing action potentials that are faithfully locked to the phase of incoming stimuli at frequencies up to ϳ600 Hz (Brownell, 1975;Banks and Smith, 1992;Wu and Kelly, 1993;Taschenberger and von Gersdorff, 2000). MNTB neurons are important relay elements that receive a secure synaptic input from the contralateral aVCN via the calyx of Held (Lenn and Reese, 1966;Morest, 1968Morest, , 1973Forsythe and Barnes-Davies, 1993) and send an inhibitory projection to the ipsilateral medial superior olive (MSO) and lateral superior olive (LSO). Both the MSO and LSO also receive direct excitatory projections from the aVCN.…”