Development of glycinergic cells and puncta in nuclei of the superior olivary complex of the postnatal ferret
Corresponding Author
Craig K. Henkel
Department of Neurobiology and Anatomy, Program in Neuroscience, Bowman Gray School of Medicine, Winston-Salem, North Carolina 27157-1010
Department of Neurobiology and Anatomy, Bowman Gray School of Medicine, Medical Center Boulevard, Winston-Salem, NC 27157Search for more papers by this authorJudy K. Brunso-Bechtold
Department of Neurobiology and Anatomy, Program in Neuroscience, Bowman Gray School of Medicine, Winston-Salem, North Carolina 27157-1010
Search for more papers by this authorCorresponding Author
Craig K. Henkel
Department of Neurobiology and Anatomy, Program in Neuroscience, Bowman Gray School of Medicine, Winston-Salem, North Carolina 27157-1010
Department of Neurobiology and Anatomy, Bowman Gray School of Medicine, Medical Center Boulevard, Winston-Salem, NC 27157Search for more papers by this authorJudy K. Brunso-Bechtold
Department of Neurobiology and Anatomy, Program in Neuroscience, Bowman Gray School of Medicine, Winston-Salem, North Carolina 27157-1010
Search for more papers by this authorAbstract
The distribution of glycine-immunopositive cells and axonal endings was studied in the adult and early postnatal ferret superior olive. As in other species, the most prominent glycine-immunopositive cell group in the adult ferret superior olive was the medial nucleus of the trapezoid body. Other darkly immunostained cells were present, although more scattered, in most periolivary regions, including the lateral and ventral trapezoid body nuclei. In the lateral superior olivary nuclei, glycine-immunopositive cells were intermingled with immunonegative cells. A comparable population of cells in the ipsilateral lateral superior olivary nucleus was retrogradely labeled in cases with unilateral injections of tritiated glycine in the inferior colliculus. Glycine-immunopositive puncta were widely distributed in the neuropil in most periolivary regions, including dense accumulations in the dorsomedial periolivary region and ventral and lateral nuclei of the trapezoid body. In the lateral and medial superior olivary nuclei, immunopositive puncta were distributed around the principal cells in characteristic perisomatic halos.
In postnatal ferrets, immunopositive cell bodies were first observed by postnatal day 7 and were distributed in regions comparable to regions in the adult, with the exception that immunopositive cells in the lateral superior olivary nucleus did not appear until about postnatal day 28. There was diffuse staining in the neuropil in principal and periolivary nuclei by postnatal day 7. During the third postnatal week, the immunostaining in the neuropil began to take on a more granular appearance and immunopositive puncta could be seen by postnatal day 35. In the lateral and medial superior olivary nuclei, the earliest distribution of immunostaining in the neuropil was nonuniform, being greater in the high-frequency, medial, and ventral regions, respectively. The density gradient in these areas was gradually eliminated over the next 2 postnatal weeks as immunostained processes and endings appeared over greater portions of the nuclei. © 1995 Wiley-Liss, Inc.
Literature Cited
- Adams, J. C. (1981) Heavy metal intensification of DAB-based HRP reaction product. J. Histochem. Cytochem. 29: 775.
- Adams, J. C. (1983) Cytology of periolivary cells and the organization of their projections in cat. J. Comp. Neurol. 215: 275–289.
- Adams, J. C., and E. Mugnaini (1990) Immunocytochemieal evidence for inhibitory and disinhibitory circuits in the superior olive. Hearing Res. 49: 281–298.
- Aoki, E., R., Semba, H. Keino, K. Kato, and S. Kashiwamata (1988) Glycine-like immunoreactivity in the rat auditory pathway. Brain Res. 442: 63–71.
- Brunso-Bechtold, J. K., C. X., Henkel, and C. Linville (1990a) Synaptic organization in the adult ferret medial superior olive. J. Comp. Neurol. 294: 389–398.
- Brunso-Bechtold, J. K., C. K., Henkel, and S. L. Vinsant (1990b) Embryonic development of the mammalian hindbrain auditory decussation. Soc. Neurosci. Abstr. 16: 668.
- Brunso-Bechtold, J. K., C. K., Henkel, and C. Linville (1992) Ultrastructural development of the medial superior olive (MSO) in the ferret. J. Comp. Neurol. 324: 539–556.
- Cant, N. B., and J. H. Casseday (1986) Projections from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei. J. Comp. Neurol. 247: 457–476.
- Cant, N. B., and R. L. Hyson (1992) Projections from the lateral nucleus of the trapezoid body to the medial superior olivary nucleus in the gerbil. Hearing Res. 58: 26–34.
- Carr, C. E., I., Fujita, and M. Konishi (1989) Distribution of GABAergic neurons and terminals in the auditory system of the barn owl. J. Comp. Neurol. 286: 190–207.
- Caspary, D. M., L. P., Rybak, and C. L. Faingold (1985) The effects of inhibitory and excitatory amino-acid neurotransmitters on the response properties of brainstem auditory neurons. In D. G. Drescher (ed): Auditory Biochemistry. Springfield, IL: Charles C. Thomas, pp. 198–226.
- Code, R. A., G. D., Burd, and E. W. Rubel (1989) Development of GABA immunoreactivity in brainstem auditory nuclei of the chick: Ontogeny of gradients in terminal staining. J. Comp. Neurol. 284: 504–518.
- Edwards, S. B. (1972) The ascending and descending projections of the red nucleus in the cat: An experimental study using an autoradiographic tracing method. Brain Res. 48: 45–63.
- Finlayson, P. G., and D. M. Caspary (1989) Synaptic potentials of chinchilla lateral superior olivary neurons. Hearing Res. 40: 221–228.
- Glendenning, K. K., and B. N. Baker (1988) Neuroanatomical distribution of receptors for three potential inhibitory neurotransmitters in the brainstem auditory nuclei of the cat. J. Comp. Neurol. 275: 288–308.
- Glendenning, K. K., K. A., Hutson, and R. B. Masterton (1985) Acoustic chiasm II: Anatomical basis of binaurality in lateral superior olive of cat. J. Comp. Neurol. 232: 261–285.
- Goldberg, J. M., and P. B. Brown (1969) Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: Some physiological mechanisms of sound localization. J. Neurophysiol. 32: 613–636.
- Grothe, B., and D. H. Sanes (1992) In vitro analysis of synaptic integration in the medial superior olive. Soc. Neurosci. Abstr. 18: 151.
- Guinan, J. J., S. S., Guinan, and B. E. Norris (1972a) Single auditory units in the superior olivary complex. L Responses to sounds and classification based on physiological properties. Int. J. Neurosci. 4: 101–120.
- Guinan, J. J., B. E., Norris, and S. S. Guinan (1972b) Single auditory units in the superior olivary complex. II. Locations of unit categories and tonotopic organization. Int. J. Neurosci. 4: 147–166.
- Helfert, R. H., J. M. Juiz, S. C. Bledsoe Jr., J. M. Bonneau, R. J. Wenthold, and R. A. Altschuler (1992) Patterns of glutamate, glycine, and GABA immunolabeling in four synaptic terminal classes in the lateral superior olive of the guinea pig. J. Comp. Neurol. 323: 305–325.
- Henkel, C. K., and J. K. Brunso-Bechtold (1990) Dendritic morphology and development in the ferret medial superior olivary nucleus. J. Comp. Neurol. 294: 377–388.
- Henkel, C. K., and J. K. Brunso-Bechtold (1991) Dendritic morphology and development in the ferret lateral superior olivary nucleus. J. Comp. Neurol. 313: 259–272.
- Hsu, S. M., L., Raine, and H. Fanger (1981) The use of avidin-biotin peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. J. Histochem. Cytochem. 29: 577–580.
- Irvine, D. R. F. (1986) The auditory brainstem. In D. Ottoson (ed): Progress in Sensory Physiology, Vol. 7. New York: Springer-Verlag, pp. 79–121.
- Kuwabara, N., and J. M. Zook (1992) Projections to the medial superior olive from the medial and lateral nucleus of the trapezoid body in rodents and bats. J. Comp. Neurol. 324: 522–538.
- Moore, D. R. (1982) Late onset of hearing in the ferret. Brain Res. 253: 309–311.
- Moore, D. R. (1988) Development and plasticity of the central auditory system. In C. T. Jones (ed): Fetal and Neonatal Development. Perinatology Press, Ithaca, NY: pp. 203–212.
- Moore, M. J., and D. M. Caspary (1983) Strychnine blocks binaural inhibition in lateral superior olivary neurons. J. Neurosci. 3: 237–242.
- Morest, D. K. (1968) The collateral system of the medial nucleus of the trapezoid body of the cat. Its neuronal architecture and relation to the olivo-cochlear bundle. Brain Res. 9: 288–311.
- Morey, A. L., and S. Carlile (1990) Auditory brainstem of the ferret: Maturation of the brainstem auditory evoked response. Dev. Brain Res. 52: 279–288.
- Moushegian, G., A., Rupert, and M. A. Whitcomb (1967) Stimulus coding by medial superior olivary neurons. J. Neurophysiol. 30: 1239–1261.
- Perkins, R. E. (1973) An electron microscopic study of synaptic organization in the medial superior olive of normal and experimental chinchillas. J. Comp. Neurol. 148: 387–416.
- Rubel, E. W. (1978) Ontogeny of structure and function in the vertebrate auditory system. In M. Jacobson (ed): Handbook of Sensory Physiology. New York: Springer-Verlag, pp. 135–237.
- Saint Marie, R. L., and R. A. Baker (1990) Neurotransmitter-specific uptake and retrograde transport of (3H)glycine from the inferior colliculus by ipsilateral projections of the superior olivary complex and nuclei of the lateral lemniscus. Brain Res. 524: 244–253.
- Saint Marie, R. L., E. M. Ostapoff, D. K. Morest, and R. J. Wenthold (1989) Glycine-immunopositive projection of the cat lateral superior olive: Possible role in midbrain ear dominance. J. Comp. Neurol. 279: 382–396.
- Sanes, D. H. (1990) An in vitro analysis of sound localization mechanisms in the gerbil lateral superior olive. J. Neurosci. 10: 3494–3506.
- Sanes, D. H., and V. Siverls (1991) Development and specificity of inhibitory terminal arborizations in the central nervous system. J. Neurobiol. 22: 837–854.
- Sanes, D. H., and G. F. Wooten (1987) Development of glycine receptor distribution in the lateral superior olive of the gerbil. J. Neurosci. 7: 3803–3811.
- Sanes, D. H., M., Merickel, and E. W. Rubel (1989) Evidence for an alteration of the tonotopic map in the gerbil cochlea during development. J. Comp. Neurol. 279: 436–444.
- Schofield, B. R. (1994) Projections to the cochlear nuclei from principal cells in the medial nucleus of the trapezoid body in guinea pigs. J. Comp. Neurol. 344: 83–100.
- Spangler, K. M., W. B., Warr, and C. K. Henkel (1985) The projections of principal cells of the medial nucleus of the trapezoid body in the cat. J. Comp. Neurol. 238: 249–262.
- Spangler, K. M., N. B., Cant, C. K. Henkel, G. R. Farley, and W. B. Warr (1987) Descending projections from the superior olivary complex to the cochlear nucleus of the cat. J. Comp. Neurol. 259: 452–465.
- Stotler, W. A. (1953) An experimental study of the cells and connections of the superior olivary complex of the cat. J. Comp. Neurol. 98: 401–433.
- Tsuchitani, C., and J. C. Boudreau (1967) Encoding of stimulus frequency and intensity by cat superior olivary S-segment cells. J. Acoust. Soc. Am. 42: 794–805.
- Vetter, D. E., J. C., Adams, and E. Mugnaini (1991) Chemically distinct rat olivocochlear neurons. Synapse 7: 21–43.
- Von Bartheld, C. S., R. A. Code, and E. W. Rubel (1989) GABAergic neurons in brainstem auditory nuclei of the chick: Distribution, morphology, and connectivity. J. Comp. Neurol. 287: 470–483.
- Warr, W. B. (1975) Olivocochlear and vestibular efferent neurons of the feline brainstem: Their location, morphology, and number determined by retrograde axonal transport and acetylcholinesterase histochemistry. J. Comp. Neurol. 161: 159–182.
- Wenthold, R. J., D., Huie, R. A. Altschuler, and K. A. Reeks (1987) Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex. Neuroscience 22: 897–912.
- Wenthold, R. J., R. A., Altschuler, and D. R. Hampson (1990) Immunocytochemistry of neurotransmitter receptors. J. Elec. Microsc. Techn. 15: 81–96.
- Yin, T. C. T., and J. C. K. Chan (1990) Interaural time sensitivity in medial superior olive of cat. J. Neurophysiol. 64: 465–488.
- Zook, J. M., and R. A. DiCaprio (1988) Intracellular labeling of afferents to the lateral superior olive in the bat, Eptesicus fuscus. Hearing Res. 34: 141–148.