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

  • John H. Casseday
  • John M. Zook
  • Nobuyuki Kuwabara
Part of the NATO ASI series book series (NSSA, volume 239)

Abstract

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.

Keywords

Inferior Colliculus Cochlear Nucleus Good Frequency Echolocation Call Interaural Level Difference 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Adams, J.C., 1979, Ascending projections to the inferior colliculus, J. Comp. Neurol. 183:519–538.PubMedCrossRefGoogle Scholar
  2. Adams, J.C., and Mugnaini, E., 1990, Immunocytochemical evidence for inhibitory and disinhibitory circuits in the superior olive, Hearing Res., 49: 281–298.CrossRefGoogle Scholar
  3. Bledsoe, S.C.J., Snead, C.R., Helfert, R.H., Prasad, V., Wenthold, R.J., and Atlshuler, R.A., 1990, immunocytochemical and lesion studies support the hypothesis that the projection from the medial nucleus of the trapezoid body to the lateral superior olive is glycinergic, Brain Res., 517:189–194.PubMedCrossRefGoogle Scholar
  4. Brunso-Bechtold, J.K., Henkel, C.K., and Linville, C., 1990, Synaptic organization in the adult ferret medial superior olive., J. Comp. Neurol., 294:389–398.PubMedCrossRefGoogle Scholar
  5. Caird, D., and Klinke, R., 1983, Processing of binaural stimuli by cat superior olivary complex neurons, Exp. Brain Res., 52:385–399.PubMedCrossRefGoogle Scholar
  6. Cant, N.B., and Casseday, J.H., 1986, Projections from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei, J. Comp. Neurol., 247:457–476.PubMedCrossRefGoogle Scholar
  7. Casseday J.H., and Covey E., 1987, Central auditory pathways in directional hearing, in: “Directional Hearing,” W. Yost, and G. Gourevitch, ed., Springer, New York.Google Scholar
  8. Casseday, J.H., Covey, E., and Vater, M., 1988, Connections of the superior olivary complex in the Rufous Horseshoe Bat, Rhinolophus rouxi, J. Comp. Neurol., 278:313–329.PubMedCrossRefGoogle Scholar
  9. Casseday, J.H., and Neff, W.D., 1975, Auditory localization: Role of auditory pathways in the brain stem of the cat, J. Neurophysiol., 38:842–858.PubMedGoogle Scholar
  10. Clark, G. M., 1969, The ultrastructure of nerve endings in the medial superior olive of the cat, Brain Res., 14:293–305.PubMedCrossRefGoogle Scholar
  11. Covey, E., Vater, M., and Casseday, J.H., 1991, Binaural properties of single units in the superior olivary complex of the mustached bat, J. Neurophysiol., 66:1080–1094.PubMedGoogle Scholar
  12. Friauf, E., and Ostwald, J., 1988, Divergent projections of physiologically characterized rat ventral cochlear nucleus neurons as shown by intra-axonal injection of horseradish peroxidase, Exp. Brain. Res., 73:263–284.Google Scholar
  13. Fuzessery, Z.M., and Pollak, G.D., 1985, Determinants of sound location selectivity in bat inferior colliculus: A combined dichotic and free-field stimulation study, J. Neurophysiol., 54:757–781.PubMedGoogle Scholar
  14. Galambos, R., Schwartzkopff, J., and Rupert, A., 1959, Microelectrode study of superior olivary nuclei, Am. J. Physiol., 197:527–536.PubMedGoogle Scholar
  15. Goldberg, J.M., and Brown, P.B., 1968, Functional organization of the dog superior olivary complex: An anatomical and electrophysiological study, J. Neurophysiol., 31:639–656.PubMedGoogle Scholar
  16. Goldberg, J.M., and Brown, P.B., 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.PubMedGoogle Scholar
  17. Grothe, B., 1990, “Versuch einer Definition des medialen Kernes des oberen Olivenkomplexes bei der Neuwelt fledermaus Pteronotus p. parnellii,” Ph.D. dissertation, Ludwig-Maximilians-Universität, Munich.Google Scholar
  18. Guiñan, J.J. Jr., Noms, B.E., and Guiñan, S.S., 1972, Single auditory units in the superior olivary complex. II: Locations of unit categories and tonotopic organization, Int. J. Neurosci., 4:147–166.CrossRefGoogle Scholar
  19. Guiñan, J.J., and Li, R.Y.-S., 1990, Signal processing in brainstem auditory neurons which receive giant endings (calyces of Held) in the medial nucleus of the trapezoid body of the cat, Hearing Res., 49:321–334.CrossRefGoogle Scholar
  20. Hall, J.L., 1965, Binaural interaction in the accessory superior olivary nucleus of the cat, J. Acoust. Soc. Am., 37:814–823.PubMedCrossRefGoogle Scholar
  21. Harrison J.M., and Feldman M.M., 1970, Anatomical aspects of the cochlear nucleus and superior olivary complex, in: “Contributions to Sensory Physiology, Vol. 4,” W. D. Neff, ed., Academic, New York.Google Scholar
  22. Harrison, J.M., and Irving, R., 1966, Visual and nonvisual auditory systems in mammals, Science, 154:738–743.PubMedCrossRefGoogle Scholar
  23. Helfert, R.H., Bonnueau, J.M., Wenthold, R.J., and Altschuler, R. A., 1989, GABA and glycine immunoreactivity in the guinea pig superior olivary complex, Brain Res., 501:269–286.PubMedCrossRefGoogle Scholar
  24. Inbody, S.B., and Feng, A.S., 1981, Binaural response characteristics of single neurons in the medial superior olivary nucleus of the albino rat, Brain Res., 210:361–366.PubMedCrossRefGoogle Scholar
  25. Irving, R., and Harrison, J.M., 1967, Superior olivary complex and audition: A comparative study, J. Comp. Neurol., 130:77–86.PubMedCrossRefGoogle Scholar
  26. Jeffress, L.A., 1948, A place theory of sound localization, J. Comp. Physiol. Psychol., 41:35–39.PubMedCrossRefGoogle Scholar
  27. Kiss, A., and Majorossy, K., 1983, Neuron morphology and synaptic architecture in the medial superior olivary nucleus, Exp. Brain Res., 52:315–327.PubMedCrossRefGoogle Scholar
  28. Kuwabara, N., DiCaprio, R.A., and Zook, J.M., 1991, Afferents to the medial nucleus of the trapezoid body and their collateral projections, J. Comp. Neurol., 314:684–706.PubMedCrossRefGoogle Scholar
  29. Kuwabara, N., and Zook, J.M., 1992, Projections to the medial superior olive from the medial and lateral nuclei of the trapezoid body in rodents and bats, J. Comp. Neurol., in press.Google Scholar
  30. Kuwada, S., and Yin, T.C.T., 1987, Physiological studies of directional hearing, in: “Directional Hearing,” W. A. Yost, and G. Gourevitch, ed., Springer-Verlag, New York.Google Scholar
  31. Lindsey, B.G., 1974, Fine structure and distribution of axon terminals from the cochlear nucleus on neurons in the medial superior olivary nucleus of the cat, J. Comp. Neurol., 16:81–104.Google Scholar
  32. Masterton, B., Jane, J.A., and Diamond, LT., 1967, Role of brain stem auditory structures in sound localization. I. Trapezoid body, superior olive, and lateral lemniscus, J. Neurophysiol., 30:341–359.PubMedGoogle Scholar
  33. Moore, C.N., Casseday, J.H., and Neff, W.D., 1974, Sound localization: The role of the commissural pathways of the auditory system of the cat, Brain Res., 82:13–26.PubMedCrossRefGoogle Scholar
  34. Moore, J.K., 1980. The primate cochlear nuclei: loss of lamination as a phylogenetic process, J. Comp. Neurol., 193:609–629.PubMedCrossRefGoogle Scholar
  35. Moore, M.M., and Caspary, D.M., 1983, Strychnine blocks binaural inhibition in lateral superior olivary neurons, J. Neurosci., 3:237–242.PubMedGoogle Scholar
  36. 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.PubMedCrossRefGoogle Scholar
  37. Peyret, D., Campistron, G., Geffard, M., and Aran, J.-M.,1987, Glycine immunoreactivity in the brainstem auditory and vestibular nuclei of the guinea pig, Acta Otolaryngol., 104:71–76.PubMedCrossRefGoogle Scholar
  38. Peyret, D., Geffard, M., and Aran, J.-M., 1986, GABA immunoreactivity in the primary nuclei of the auditory central nervous system, Hearing Res., 23:115–121.CrossRefGoogle Scholar
  39. Reed, M.C., and Blum, J.J., 1990, A model for the computation and encoding of azimuthal information by the lateral superior olive, J. Acoust. Soc. Am., 88:1442–1453.PubMedCrossRefGoogle Scholar
  40. Ross, L.S., and Pollak, G.D., 1989, Differential ascending projections to aural regions in the 60 kHz contour of the mustache bat’s inferior colliculus, J. Neurosci., 9:2819–2834.PubMedGoogle Scholar
  41. Ross L.S., Pollak G.D., and Zook J.M., 1988, Origin of ascending projections to an isofrequency region of the mustache bat’s inferior colliculus, J. Comp. Neurol., 270:488–505.PubMedCrossRefGoogle Scholar
  42. Rouiller, E.M., and Ryugo, D.K., 1984, Intracellular marking of physiologically characterized cells in the ventral cochlear nucleus of the cat. J. Comp. Neurol. 225:167–186.PubMedCrossRefGoogle Scholar
  43. Sanes, D.H., 1990, An in vitro analysis of sound localization mechanisms in the gerbil lateral superior olive, J. Neurosci., 10:3494–3506.PubMedGoogle Scholar
  44. Schwartz, I.R., 1980, The differential distribution of synaptic terminal on marginal and central cells in the cat medial superior olivary nucleus, Am. J. Anat., 159:25–31.PubMedCrossRefGoogle Scholar
  45. Schwartz I.R., 1984, Axonal organization in the cat medial superior olivary nucleus, in: “Contributions to Sensory Physiology, Vol. 8,” W. D. Neff, ed., New York.Google Scholar
  46. Simmons, J.A., and Lawrence, B.D., 1982, Echolocation in bats: the external ear and perception of the vertical positions of targets, Science, 218:481–483.PubMedCrossRefGoogle Scholar
  47. Smith, P.H., Joris, P.X., Carney, L.H., and Yin, T.C.T., 1991, Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat, J. Comp. Neurol., 304:387–407.PubMedCrossRefGoogle Scholar
  48. Spangler, K.M., Warr, W.B., and Henkel, C.K., 1985, The projections of principal cells of the medial nucleus of the trapezoid body in the cat, J. Comp. Neurol., 238:249–262.PubMedCrossRefGoogle Scholar
  49. Spirou, G.A., Brownell, W.E., and Zidanic, M., 1990, Recordings from cat trapezoid body and HRP labeling of globular bushy cell axons, J. Neurophysiol., 63:1169–1190.PubMedGoogle Scholar
  50. 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.PubMedCrossRefGoogle Scholar
  51. Strominger, N.L., and Strominger, A.I., 1971, Ascending brain stem projections of the anteroventral cochlear nucleus in the rhesus monkey, J. Comp. Neurol., 143:217–242.PubMedCrossRefGoogle Scholar
  52. Tolbert, L.P., Morest, D.K., and Yurgelun-Todd, D.A., 1982, The neuronal architecture of the anteroventral cochlear nucleus of the cat in the region of the cochlear nerve root: Horseradish peroxidase labelling of identified cell types, Neurosci., 7:3031–3052.CrossRefGoogle Scholar
  53. Tsuchitani, C., 1977, Functional organization of lateral cell groups of cat superior olivary complex, J. Neurophysiol., 40:296–318.PubMedGoogle Scholar
  54. Tsuchitani, C., and Boudreau, J.C., 1966, Single unit analysis of cat superior olive S segment with tonal stimuli, J. Neurophysiol., 29:684–697.PubMedGoogle Scholar
  55. Vater, M., and Feng, A.S., 1990, Functional organization of ascending and descending connections of the cochlear nucleus of horseshoe bats, J. Comp. Neurol., 292:373–395.PubMedCrossRefGoogle Scholar
  56. Warr, W.B., 1966, Fiber degeneration following lesions in the anterior ventral cochlear nucleus of the cat, Exp. Neurol., 14:453–474.PubMedCrossRefGoogle Scholar
  57. 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.PubMedCrossRefGoogle Scholar
  58. Warr W.B., 1982, Parallel ascending pathways from the cochlear nucleus: Neuroanatomical evidence of functional specialization, in: “Contributions to Sensory Physiology, Vol. 7,” W. D. Neff, ed., Academic, New York.Google Scholar
  59. Wenthold, R.J., Huie, D., Altschuler, R.A., and Reeks, K.A., 1987, Glycine immunoreactivity localized in the cochlear nucleus and superior olivary complex, Neurosci., 22:897–912.CrossRefGoogle Scholar
  60. Yin, T.C.T., and Chan, J.C.K., 1990, Interaural time sensitivity in medial superior olive of cat, J. Neurophysiol., 64:465–488.PubMedGoogle Scholar
  61. Zook, J.M., and Casseday, J.H., 1982a, Cytoarchitecture of auditory system in lower brainstem of the mustache bat, Pteronotus parnellii, J. Comp. Neurol., 207:1–13.PubMedCrossRefGoogle Scholar
  62. Zook J.M., and Casseday J.H., 1982b, Origin of ascending projections to inferior colliculus in the mustache bat, Pteronotus parnellii, J. Comp. Neurol., 207:14–28.PubMedCrossRefGoogle Scholar
  63. Zook, J.M., and Casseday, J.H., 1985, Projections from the cochlear nuclei in the mustache bat, Pteronotusparnellii, J. Comp. Neurol., 237:307–324.PubMedCrossRefGoogle Scholar
  64. Zook, J.M., and DiCaprio, R.A., 1988, Intracellular labeling of afferents to the lateral superior olive in the bat, Eptesicus fuscus, Hearing Res., 34:141–148.CrossRefGoogle Scholar
  65. Zook, J.M., and Leake, P.A., 1989, Connections and frequency representation in the auditory brainstem of the mustache bat, Pteronotus parnelli, J. Comp. Neurol., 290:243–261.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1993

Authors and Affiliations

  • John H. Casseday
    • 1
  • John M. Zook
    • 2
  • Nobuyuki Kuwabara
    • 2
  1. 1.Department of NeurobiologyDuke University Medical CenterDurhamUSA
  2. 2.Department of Zoological and Biomedical Sciences & OUCOMOhio UniversityAthensUSA

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