Organization of ventrolateral periolivary cells of the cat superior olive as revealed by PEP-19 immunocytochemistry and Nissl stain
1996; Wiley; Volume: 368; Issue: 1 Linguagem: Inglês
10.1002/(sici)1096-9861(19960422)368
ISSN1096-9861
AutoresGeorge A. Spirou, Albert S. Berrebi,
Tópico(s)Biochemical Analysis and Sensing Techniques
ResumoJournal of Comparative NeurologyVolume 368, Issue 1 p. 100-120 Organization of ventrolateral periolivary cells of the cat superior olive as revealed by PEP-19 immunocytochemistry and Nissl stain George A. Spirou, Corresponding Author George A. Spirou [email protected] Departments of Otolaryngology—HNS, Physiology, and Anatomy, West Virginia University School of Medicine, Morgantown, West Virginia 26506-9200Department of Otolaryngology, West Virginia University School of Medicine, P.O. Box 9200, Morgantown, WV 26506-9200.Search for more papers by this authorAlbert S. Berrebi, Albert S. Berrebi Departments of Otolaryngology—HNS, Physiology, and Anatomy, West Virginia University School of Medicine, Morgantown, West Virginia 26506-9200Search for more papers by this author George A. Spirou, Corresponding Author George A. Spirou [email protected] Departments of Otolaryngology—HNS, Physiology, and Anatomy, West Virginia University School of Medicine, Morgantown, West Virginia 26506-9200Department of Otolaryngology, West Virginia University School of Medicine, P.O. Box 9200, Morgantown, WV 26506-9200.Search for more papers by this authorAlbert S. Berrebi, Albert S. Berrebi Departments of Otolaryngology—HNS, Physiology, and Anatomy, West Virginia University School of Medicine, Morgantown, West Virginia 26506-9200Search for more papers by this author First published: 22 April 1996 https://doi.org/10.1002/(SICI)1096-9861(19960422)368:1 3.0.CO;2-7Citations: 26AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Abstract Ventrolateral periolivary cell groups, through their descending projections to the cochlear nucleus (CN) and local projections to principal nuclei of the superior olive, may participate in brainstem mechanisms mediating such tasks as signal detection in noisy environments and sound localization. Understanding the function of these cell groups can be improved by increased knowledge of the organization of their synaptic inputs in relation to their cellular characteristics. Immunocytochemistry for PEP-19 (a putative calcium binding protein) reveals four patterns of immunolabeling within the ventrolateral periolivary region. Three of the patterns, which have distinct fiber and punctate labeling characteristics, help to define three subdivisions of the lateral nucleus of the trapezoid body (LNTB). The fourth pattern defines two other nuclei, the anterolateral periolivary nucleus (rostral) and the posterior periolivary nucleus (caudal), which display many immunoreactive cell bodies but little fiber and punctate labeling. One of the subdivisions of the LNTB contains large PEP-19 immunolabeled puncta arranged in pericellular nests. Analysis of Nissl-stained sections reveals a neuronal population that resembles globular cells of the ventral cochlear nucleus (VCN) and which colocalizes with pericellular nests of large immunolabeled puncta. Cell counts reveal that roughly 10,000 neurons constitute the cat ventrolateral periolivary region, 9,000 of which are found in the LNTB. Three-dimensional reconstructions of auditory brainstem nuclei clarify the complex spatial relationships among these structures. © 1996 Wiley-Liss, Inc. Literature Cited Abercrombie, M. (1946) Estimation of nuclear population from microtome sections. Anat. Rec. 94: 239–247. Adams, J. C. (1983) Cytology of periolivary cells and the organization of their projections in the cat. J. Comp. Neurol. 215: 275–289. Adams, J. C., and W. B. Warr (1976) Origins of axons in the cat's acoustic striae determined by injection of horseradish peroxidase into severed tracts. J. Comp. Neurol. 170: 107–121. Andersen, R. A., G. L. Roth, L. M. Aitkin, and M. M. Merzenich (1980) The efferent projections of the central nucleus and the pericentral nucleus of the inferior colliculus in the cat. J. Comp. Neurol. 194: 649–662. Banks, M., and P. H. Smith (1992) Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body. J. Neurosci. 12: 2819–2837. Berrebi, A. S., and E. Mugnaini (1991) Distribution and targets of the cartwheel cell axon in the dorsal cochlear nucleus of the guinea pig. Anat. Embryol. 183: 427–454. Berrebi, A. S., and G. A. Spirou (1994) PEP-19 immunolabeling of VCN bushy cells and their terminals in the superior olivary complex of the cat. Soc. Neurosci. Abstr. 20: 975. Boudreau, J. C., and C. Tsuchitani (1970) Cat superior olive S-segment cell discharge to tonal stimulation. Contr. Sens. Physiol. 4: 143–213. Bourk, T. R., J. M. Mielcarz, and B. E. Norris (1981) Tonotopic organization of the anteroventral cochlear nucleus of the cat. Hear. Res. 4: 215–241. Brawer, J. R., D. K. Morest, and E. C. Kane (1974) The neuronal architecture of the cochlear nucleus of the cat. J. Comp. Neurol. 155: 251–300. y Cajal, S. R. (1911) Histologie du Système Nerveux de l'Homme et des Vertébrés. Paris, Maloine. Cant, N. B. (1991) Projections to the lateral and medial superior olivary nuclei from the spherical and globular bushy cells of the anteroventral cochlear nucleus. In R. A. Altschuler, R. P. Bobbin, B. M. Clopton, and D. W. Hoffman (ads): Neurobiology of Hearing: The Central Auditory System. New York: Raven Press, pp. 99–120. Cant, N. B. (1992) The cochlear nucleus: Neuronal types and their synaptic organization. In D. B. Webster, A. N. Popper, and R. R. Fay (ads): The Mammalian Auditory Pathway: Neuroanatomy. New York: Springer-Verlag, pp. 66–116. 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. Hear. Res. 58: 26–34. Conlee, J. W., and E. S. Kane (1982) Descending projections from the inferior colliculus to the dorsal cochlear nucleus in the rat: an autoradiographic study. Neuroscience 7: 161–178. Elverland, H. H. (1977) Descending connections between the superior olivary and cochlear nuclear complexes in the cat studied by autoradiographic and horseradish peroxidase methods. Exp. Brain Res. 27: 397–412. Fernandez, C., and F. Karapas (1967) The course and termination of the striae of Monakow and Held in the cat. J. Comp. Neurol. 131: 371–386. Guinan, J. J., S. S. Guinan, and B. E. Norris (1972a) Single auditory units in the superior olivary complex I: Responses to sounds and classifications 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 -if unit categories and tonotopic organization. Int. J. Neurosci, 4: 147–166. Harrison, J. M., and W. B. Warr (1962) A study of the cochlear nuclei and ascending auditory pathways of the medulla. J. Comp. Neurol. 119: 341–380. Kuwabara, N., and J. M. Zook (1992) Projections to the medial superior olive from the medial and lateral nuclei of the trapezoid body in rodents and bats. J. Comp. Neurol. 324: 522–538. Lorente de Nó, R. (1981) The Primary Acoustic Nuclei. New York: Raven Press. Manis, P. B., and S. O. Marx (1991) Outward currents in isolated ventral cochlear nucleus neurons. J. Neurosci. 11: 2865–2880. 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. Mugnaini, E., A. S. Berrebi, J. I. Morgan, and A.-L. Dahl (1987) The polypeptide PEP-19 is a marker for Purkinje neurons in cerebellar cortex and cartwheel neurons in the dorsal cochlear nucleus. Arch. Ital. Biol. 126: 41–67. van Noort, J. (1969) The Structure and Connections of the Inferior Colliculus. The Netherlands: Van Gorcum & Co., Assen. Oertel, D. (1983) Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus. J. Neurosci. 3: 2043–2053. Osen, K. K. (1969) Cytoarchitecture of the cochlear nuclei in the cat. J. Comp. Neurol. 136: 453–484. Osen, K. K., E. Mugnaini, A.-L. Dahl, and A. H. Christiansen (1984) Histochemical localization of acetylcholinesterase in the cochlear and superior olivary nuclei A reappraisal with emphasis on the cochlear granule cell system. Arch. Ital. Biol. 122: 169–212. Papez, J. W. (1930) The superior olivary nucleus: Its fiber connections. Arch. Neurol. Psychiat. 24: 1–20. Rasmussen, G. L. (1946) The olivary peduncle and other fiber projections of the superior olivary complex. J. Comp. Neurol. 84: 141–219. Rose, J. E., R. Galambos, and J. R. Hughes (1959) Microelectrode studies of the cochlear nuclei of the cat. Bull. Johns Hopkins Hosp. 104: 211–251. Rouiller, E. M., and D. K. Ryugo (1984) Intracellular marking of physiologically characterized cells in the ventral cochlear nucleus of the cat. J. Comp. Neurol. 225: 167–186. Ryugo, D. K., and E. M. Rouiller (1988) The central projections of intracellularly labeled auditory nerve fibers in cats: Morphometric correlations with physiological properties. J. Comp. Neurol. 271: 130–142. Schofield, B. R., and N. B. Cant (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. Schofield, B. R., and N. B. Cant (1992) Organization of the superior olivary complex in the guinea pig: II. Patterns of projection from the periolivary nuclei to the inferior colliculus. J. Comp. Neurol. 317: 438–455. Schwartz, I. R. (1992) The superior olivary complex and lateral lemniscal nuclei. In D. B. Webster, A. N. Popper, and R. R. Fay (ads): The Mammalian Auditory Pathway: Neuroanatomy. New York: Springer Verlag, pp. 117–167. Smith, P. H., P. X. Joris, L. H. Carney, and T. C. T. Yin (1991) Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat. J. Comp. Neurol. 304: 387–407. Spangler, K. M., and W. B. Warr (1991) The descending auditory system. In R. A. Altschuler, R. P. Bobbin, B. M. Clopton, and D. W. Hoffman (ads): Neurobiology of Hearing: The Central Auditory System. New York: Raven Press, pp. 27–46. 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: 249–261. 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. Spirou, G. A., and A. S. Berrebi (1994) Large synaptic terminals in the lateral nucleus of the trapezoid body of the cat are PEP-19 immunoreactive. Soc. Neurosci. Abstr. 20: 975. Spirou, G. A., and A. S. Berrebi (1995) Anatomical basis for fast feedback from the lateral nucleus of the trapezoid body to the cochlear nucleus. In G. Manley, G. Klump, C. Kuppl, H. Fastl, and H. Oeckinghaus (ads): Advances in Hearing Research. London: World Scientific, pp. 275–287. Spirou, G. A., W. E. Brownell, and M. Zidanic (1990) Single fiber recordings from cat trapezoid body and HRP labeling of globular bushy cell axons. J. Neurophysiol. 63: 1169–1190. Spirou, G. A., B. J. May, D. D. Wright, and D. K. Ryugo (1993) Frequency organization of the dorsal cochlear nucleus in cats. J. Comp. Neurol. 329: 36–52. Spirou, G. A., M. P. Walker, and A. S. Berrebi (1995) Connectivity of the lateral nucleus of the trapezoid body it cats. ARO Abstr. 18: 39. Sternberger, L. A. (1979) Immunocytochemistry, 2nd ed. New York: Wiley. Stotler, W. A. (1953) An experimental study of the cells and connections of the superior olivary complex of the cat. J. Comp. Neurol. 98: 401–432. Taber, E. (1961) The cytoarchitecture of the brain stem of the cat. I. Brain stem nuclei of cat. J. Comp. Neurol. 116: 27–70. Tolbert, L. P., D. K. Morest, and D. A. Yurgelun-Todd (1982) The neuronal architecture of the anteroventral cochlear nucleus of the cat in the region of the cochlear nerve root: Horseradish peroxidase labeling of identified cell types. Neuroscience 7: 3031–3052. Tsuchitani, C. (1977) Functional organization of lateral cell groups of cat superior olivary complex. J. Neurophysiol. 40: 296–318. Uchizono, K. (1965) Characteristics of excitatory and inhibitory synapses in the central nervous system of cat. Nature 207: 642–643. Warr, W. B. (1966) Fiber degeneration following lesions in the anterior ventral cochlear nucleus of the cat. Exp. Neurol. 14: 453–474. Warr, W. B. (1969) Fiber degeneration following lesions in the posteroventral cochlear nucleus of the cat. Exp. Neurol. 23: 140–155. Warr, W. B. (1972) Fiber degeneration following lesions in the multipolar and globular cell areas in the ventral cochlear nucleus of the cat. Brain Res. 40: 247–270. Warr, W. B. (1982) Parallel ascending pathways from the cochlear nucleus; neuroanatomical evidence of functional specialization. Contr. Sens. Physiol. 7: 1–38. Yin, T. C. T., L. H. Carney, and P. X. Joris (1990) Interaural time sensitivity in the inferior colliculus of the albino cat. J. Comp. Neurol. 295: 438–448. Ziai, R., Y.-C. Pan, J. D. Hulmes, L. Sangameswaran, and J. I. Morgan (1986) Isolation, sequence, and developmental profile of a brain-specific polypeptide, PEP-19. PNAS 83: 8420–8423. Citing Literature Volume368, Issue122 April 1996Pages 100-120 ReferencesRelatedInformation
Referência(s)