Calcium-binding proteins and GABA reveal spatial segregation of cell types within the developing lateral superior olivary nucleus of the ferret

Microscopy Research and Technique

Volumn 41, Issue 3, 1998, Pages 234-245

  Henkel, Craig K ^a   Brunso Bechtold, Judy K ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Calbindin; Calretinin; Development; GABA; Gradient; Lateral superior olivary nucleus; Parvalbumin

Indexed keywords

AMINO ACIDS; BUTYRIC ACID; CALCIUM; CYTOLOGY; NEURONS; PROTEINS; SHELLS (STRUCTURES);

CALBINDIN; CALCIUM BINDING PROTEINS; CALRETININ; CELL-BE; CELL/B.E; DEVELOPMENT; GAMMA AMINO BUTYRIC ACID; GRADIENT; LATERAL SUPERIOR OLIVARY NUCLEUS; PARVALBUMIN;

CELLS;

4 AMINOBUTYRIC ACID; CALBINDIN; CALCIUM BINDING PROTEIN; CALRETININ; GLYCINE; PARVALBUMIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; FERRET; IMMUNOHISTOCHEMISTRY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SUPERIOR OLIVARY NUCLEUS;

ANIMALIA; MUSTELA PUTORIUS FURO;

EID: 0032080927     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0029(19980501)41:3<234::AID-JEMT7>3.0.CO;2-T     Document Type: Article

References (66)

1. Adams, J.C., and Mugnaini, E. (1990) Immunocytochemical evidence for inhibitory and disinhibitory circuits in the superior olive. Hear. Res., 49:281-298.
2. Adolphs, R. (1993) Acetylcholinesterase staining differentiates functionally distinct auditory pathways in the barn owl. J. Comp. Neurol., 329:365-377.
3. Antal, M., Polgár, E., Chalmers, J., Minson, J.B., Llewellyn-Smith, I., Heizmann, C.W., and Somogyi, P. (1991) Different populations of parvalbumin- and calbindin-D28k-immunoreactive neurons contain GABA and accumulate 3H-D-aspartate in the dorsal horn of the rat spinal cord. J. Comp. Neurol. 314:114-124.
4. Aoki, E., Semba, R., Seto-Ohshima, A., Heizmann, C.W., and Kashiwa-mata, S. (1990) Coexistence of parvalbumin and glycine in the rat brainstem. Brain Res., 525:140-143.
5. Bennett-Clarke, C.A., Chiaia, N.L., Jacquin, M.F., and Rhoades, R.W. (1992) Parvalbumin and calbindin immunocytochemistry reveal functionally distinct cell groups and vibrissa-related patterns in the trigeminal brainstem complex of the adult rat. J. Comp. Neurol., 320:323-338.
6. Braun, K., Scheich, H., Heizmann, C.W., and Hunziker, W. (1991) Parvalbumin and calbindin-D28K immunoreactivity as developmental markers of auditory and vocal motor nuclei of the zebra finch. Neuroscience, 40:853-869.
7. Brauth, S.E. (1990) Investigation of central auditory nuclei in the budgerigar with cytochrome oxidase histochemistry. Brain Res., 508:142-146.
8. Brunso-Bechtold, J.K., Henkel, C.K., and Linville, C. (1992) Ultrastructural development of the medial superior olive (MSO) in the ferret. J. Comp. Neurol., 324:539-556.
9. Caicedo, A., D'Aldin, C., Puel, J.L., and Eybalin, M. (1996) Distribution of calcium-binding protein immunoreactivities in the guinea pig auditory brainstem. Anat. Embryol. (Berl.), 194:465-487.
10. Cant, N.B. (1984) The fine structure of the lateral superior olivary nucleus of the cat. J. Comp. Neurol., 227:63-77.
11. Carr, C.E. (1993) Processing of temporal information in the brain. Annu. Rev. Neurosci., 16:223-243.
12. Carr, P.A., and Nagy, J.I. (1993) Emerging relationships between cytochemical properties and sensory modality transmission in primary sensory neurons. Brain Res. Bull., 30:209-219.
13. Celio, M.R. (1986) Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. Science, 231:995-997.
14. El-Kashlan, H.K., Niparko, J.K., Altschuler, R.A., and Miller, J.M. (1991) Direct electrical stimulation of the cochlear nucleus: Surface vs. penetrating stimulation. Otolaryngol. Head Neck Surg., 105:533-543.
15. Friauf, E. (1993) Transient appearance of calbindin-D28k-positive neurons in the superior olivary complex of developing rats. J. Comp. Neurol., 334:59-74.
16. Friauf, E. (1994) Distribution of calcium-binding protein calbindin-D28k in the auditory system of adult and developing rats. J. Comp. Neurol., 349:193-211.
17. Frisina, R.D., Zettel, M.L., Kelley, P.E., and Walton, J.P. (1995) Distribution of calbindin D-28k immunoreactivity in the cochlear nucleus of the young adult chinchilla. Hear. Res., 85:53-68.
18. Glendenning, K.K., and Masterton, R.B. (1983) Acoustic chiasm: Efferent projections of the lateral superior olive. J. Neurosci., 3:1521-1537.
19. Glendenning, K.K., Baker, B.N., Hutson, K.A., and Masterton, R.B. (1992) Acoustic chiasm V: Inhibition and excitation in the ipsilateral and contralateral projections of LSO. J. Comp. Neurol., 319:100-122.
20. Hashikawa, T., Rausell, E., Molinari, M., and Jones, E.G. (1991) Parvalbumin- and calbindin-containing neurons in the monkey medial geniculate complex: Differential distribution and cortical layer specific projections. Brain Res., 544:335-341.
21. Helfert, R.H., and Schwartz, I.R. (1986) Morphological evidence for the existence of multiple neuronal classes in the cat lateral superior olivary nucleus. J. Comp. Neurol., 244:533-549.
22. Henkel, C.K., and Brunso-Bechtold, J.K. (1993) Laterality of superior olive projections to the inferior colliculus in adult and developing ferret. J. Comp. Neurol., 331:458-468.
23. Henkel, C.K., and Brunso-Bechtold, J.K. (1995) Development of glycinergic cells and puncta in nuclei of the superior olivary complex of the postnatal ferret. J. Comp. Neurol., 354:470-480.
24. Henkel, C.K., and Brunso-Bechtold, J.K. (1996) Development of GABAergic circuits in the auditory brainstem of the ferret. Soc. Neurosci. Abstr., 22:124.
25. Hogan, D., and Berman, N.E.J. (1993) Transient expression of calbindin-D28k immunoreactivity in layer V pyramidal neurons during postnatal development of kitten cortical areas. Dev. Brain Res., 74:177-192.
26. Hsu, S.M., Raine, L., and Fanger, H. (1981) 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.
27. Johnson, J.K., and Casagrande, V.A. (1995) Distribution of calcium-binding proteins within the parallel visual pathways of a primate (Galago crassicaudatus). J. Comp. Neurol., 356:238-260.
28. Kelley, P.E., Frisina, R.D., Zettel, M.L., and Walton, J.P. (1992) Differential calbindin-like immunoreactivity in the brain stem auditory system of the chinchilla. J. Comp. Neurol., 320:196-212.
29. Kosaki, H., Hashikawa, T., He, J., and Jones, E.G. (1997) Tonotopic organization of auditory cortical fields delineated by parvalbumin immunoreactivity in macaque monkeys. J. Comp. Neurol., 386:304-316.
30. Kotak, V.C., and Sanes, D.H. (1997) A shift from GABAergic to glycinergic transmission in the developing LSO. Soc. Neurosci. Abstr., 23:1549.
31. Kudo, M., Kitao, Y., Okoyama, S., Moriya, M., and Kawano, J. (1996) Crossed projection neurons are generated prior to uncrossed projection neurons in the lateral superior olive of the rat. Dev. Brain Res., 95:72-78.
32. Liberman, M.C. (1991) Central projections of auditory-nerve fibers of differing spontaneous rate. I. Anteroventral cochlear nucleus. J. Comp. Neurol., 313:240-258.
33. Liu, F.-C., and Graybiel, A.M. (1992) Heterogeneous development of calbindin-D28K expression in the striatal matrix. J. Comp. Neurol., 320:304-322.
34. Lohmann, C., and Friauf, E. (1996) Distribution of the calcium-binding proteins parvalbumin and calretinin in the auditory brainstem of adult and developing rats. J. Comp. Neurol., 367:90-109.
35. Maler, L., Jande, S., and Lawson, E.M. (1984) Localization of vitamin D-dependent calcium binding protein in the electrosensory and electromotor system of high frequency gymnotid fish. Brain Res., 301:166-170.
36. Matsubara, J.A. (1990) Calbindin D-28K immunoreactivity in the cat's superior olivary complex. Brain Res., 508:353-357.
37. McMullen, N.T., De Venecia, R.K., Smelser, C.B., and Lossmann, S.D. (1994) Calcium-binding protein expression delineates subdivisions of rabbit medial geniculate complex. Soc. Neurosci. Abstr., 20:977.
38. Mize, R.R., Jeon, C.-J., Butler, G.D., Luo, Q., and Emson, P.C. (1991) The calcium binding protein calbindin-D 28K reveals subpopulations of projection and interneurons in the cat superior colliculus. J. Comp. Neurol., 307:417-436.
39. Moore, D.R., Russell, F.A., and Cathcart, N.C. (1995) Lateral superior olive projections to the inferior colliculus in normal and unilaterally deafened ferrets. J. Comp. Neurol., 357:204-216.
40. Morino-Wannier, P., Fujita, S.C., and Jones, E.G. (1992) GABAergic neuronal populations in monkey primary auditory cortex defined by co-localized calcium binding proteins and surface antigens. Exp. Brain Res., 88:422-432.
41. 14C)2-deoxyglucose labeling of synaptic activity in the central auditory system. J. Comp. Neurol., 245:553-565.
42. Okoyama, S., Nakayama, K., and Kudo, M. (1996) A possible role of transient AChE expression in the medial geniculate of developing rats. Neuroreport, 7:1067-1071.
43. Oliver, D., and Shneiderman, A. (1991) The anatomy of the inferior colliculus: A cellular basis for integration of monaural and binaural information. In: Neurobiology of Hearing. Vol. II. The Central Auditory System. R.A. Altschuler, R.P. Bobbin, B.M. Clopton, and D.W. Hoffman, eds. Raven Press, New York, pp. 195-222.
44. Ramon y Cajal, S. (1909) Histologie du Systeme Nerveux de L'Homme et des Vertebres. Vol. 1. Instituto Ramon y Cajal, Madrid (1972 reprint).
45. Romand, R. (1987) Tonotopic evolution during development. Hear. Res., 28:117-123.
46. Rubel, E.W. (1978) Ontogeny of structure and function in the vertebrate auditory system. In: Handbook of Sensory Physiology. M. Jacobson, ed. Springer-Verlag, New York, pp. 135-237.
47. Rübsamen, R. (1992) Postnatal development of central auditory frequency maps. J. Comp. Physiol. [A], 170:129-143.
48. Saint Marie, R.L., Ostapoff, E.M., Morest, D.K., and Wenthold, R.J. (1989) Glycine-immunoreactive projection of the cat lateral superior olive: possible role in midbrain ear dominance. J. Comp. Neurol., 279:382-396.
49. Sanes, D.H. (1993) The development of synaptic function and integration in the central auditory system. J. Neurosci., 13:2627-2637.
50. Sanes, D.H., and Siverls, V. (1991) Development and specificity of inhibitory terminal arborizations in the central nervous system. J. Neurobiol., 22:837-854.
51. Sanes, D.H., and Wooten, G.F. (1987) Development of glycine receptor distribution in the lateral superior olive of the gerbil. J. Neurosci., 7:3803-3811.
52. Sanes, D.H., Geary, W.A., Wooten, G.F., and Rubel, E.W. (1987) Quantitative distribution of the glycine receptor in the auditory brain stem of the gerbil. J. Neurosci., 7:3793.
53. Sanes, D.H., Song, J., and Tyson, J. (1992) Refinement of dendritic arbors along the tonotopic axis of the gerbil lateral superior olive. Dev. Brain Res., 67:47-55.
54. Schofield, B.R., and Cant, N.B. (1991) Organization of the superior olivary complex in the guinea pig. I. Cytoarchitecture, cytochrome oxidase histochemistry, and dendritic morphology. J. Comp. Neurol., 314:645-670.
55. Seto-Ohshima, A., Aoki, E., Semba, R., Emson, P.C., and Heizmann, C.W. (1990) Parvalbumin immunoreactivity in the central auditory system of the gerbil: A developmental study. Neurosci. Lett., 119:60-63.
56. Shneiderman, A., Oliver, D.L., and Henkel, C.K. (1988) Connections of the dorsal nucleus of the lateral lemniscus: An inhibitory parallel pathway in the ascending auditory system. J. Comp. Neurol., 276:188-208.
57. Solbach, S., and Celio, M.R. (1991) Ontogeny of the calcium binding protein parvalbumin in the rat nervous system. Anat. Embryol. (Berl.), 184:103-124.
58. Spitzer, N.C. (1991) A developmental handshake: Neuronal control of ionic currents and their control of neuronal differentiation. J. Neurobiol., 22:659-673.
59. Takahashi, T.T., Carr, C.E., Brecha, N.C., and Konishi, M. (1987) Calcium binding protein-like immunoreactivity labels the terminal field of nucleus laminaris of the barn owl. J. Neurosci., 7:1843-1856.
60. Vater, M., and Braun, K. (1994) Parvalbumin, calbindin D-28k, and calretinin immunoreactivity in the ascending auditory pathway of horseshoe bats. J. Comp. Neurol., 341:534-558.
61. Webster, W.R., Batini, C., Buisseret-Delmas, C., Compoint, C., Guegan, M., and Thomasset, M. (1990) Colocalization of calbindin and GABA in medial nucleus of the trapezoid body of the rat. Neurosci. Lett., 111:252-257.
62. Wenstrup, J.J., Ross, L.S., and Pollak, G.D. (1986) Binaural response organization within a frequency-band representation of the inferior colliculus: Implications for sound localization. J. Neurosci., 6:962-973.
63. Wenthold, R.J. (1991) Neurotransmitters of brainstem auditory nuclei. In: Neurobiology of Hearing. Vol. II. The Central Auditory System. R.A. Altschuler, R.P. Bobbin, B.M. Clopton, and D.W. Hoffman, eds. Raven Press, New York, pp. 121-139.
64. Winsky, L., and Jacobowitz, D.M. (1995) Effects of unilateral cochlea ablation on the distribution of calretinin mRNA and immunoreactivity in the guinea pig ventral cochlear nucleus. J. Comp. Neurol., 354:564-582.
65. Zettel, M.L., Carr, C.E., and O'Neill, W.E. (1991) Calbindin-like immunoreactivity in the central auditory system of the mustached bat, Pteronotus parnelli. J. Comp. Neurol., 313:1-16.
66. Zirpel, L., and Rubel, E.W. (1996) Eighth nerve activity regulates intracellular calcium concentration of avian cochlear nucleus neurons via a metabotropic glutamate receptor. J. Neurophysiol., 76:4127-4139.