Animal Sonar pp 197-223 | Cite as

Parallel Auditory Pathways: II — Functional Properties

  • George D. Pollak
  • John H. Casseday
Part of the NATO ASI Science book series (NSSA, volume 156)


In the previous chapter the wiring diagram of the auditory system was described and we pointed out the functional consequences of these connectional patterns, especially how they preserve the cochlear tonotopic organization. In this chapter we discuss the physiological characteristics of the brainstem auditory nuclei in echolocating bats, considering two major challenges bats face: 1) The evaluation of target range coded by the temporal interval between an emitted pulse and echo; and 2) The localization of a sound in space which is computed from interaural intensity disparities.


Inferior Colliculus Sound Localization Auditory Nerve Fiber Lateral Superior Olive Superior Olivary Complex 
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  1. Aitkin, L.M. (1976) Tonotopic organization at higher levels of the auditory pathway. Inter. Rev. Physiol. Neurophysiol. 10: 249–279.Google Scholar
  2. Blauert, J. (1969/70) Sound localization in the median plane. 22: 205–213.Google Scholar
  3. Bodenhamer, R.D., Pollak, G.D. and Marsh, D. (1979) Coding of fine frequency information by echoranging neurons in the inferior colliculus of Mexican free-tailed bats. Brain Res. 171: 530–535.PubMedCrossRefGoogle Scholar
  4. Bodenhamer, R.D. and Pollak, G.D. (1981) Time and frequency domain processing in the inferior colliculus of echolocating bats. Hearing Res. 5: 317–335.CrossRefGoogle Scholar
  5. Boudreau, J.C., and C. Tsuchitani (1968) Binaural interaction in the cat superior olive s-segment. J. Neurophysiol. 31: 442–454.PubMedGoogle Scholar
  6. Butler, R.A. (1974) Does tonotopy subserve the perceived elevation of a sound? Federation Proc. 33: 1920–1923.Google Scholar
  7. Cant, N.B. (1984) The fine structure of the lateral superior olivary nucleus of the cat. J. Comp. Neurol. 227: 63–77.PubMedCrossRefGoogle Scholar
  8. Cant, N.B. and D.K. Morest (1984) The structural basis for stimulus coding in the cochlear nucleus of the cat. In: Hearing Science. C. Berlin (Ed.), College-Hill Press, San Diego, California, pp. 423–460.Google Scholar
  9. Caird, D. and R. Klinke (1983) Processing of binaural stimuli by cat olivary complex neurons. Exp. Brain Res. 52: 385–399.PubMedCrossRefGoogle Scholar
  10. Cajal, S. Ramon Y., 1909, “Le system nerveus de l’homme et des vertebres,” Instituto Ramon y Cajal, Madrid.Google Scholar
  11. Casseday, J.H., and Covey, E., 1986, Central auditory pathways in directional hearing in: “Directional Hearing,” W.A. Yost and G. Gourevitch, eds., Springer Verlag, New York (in press).Google Scholar
  12. Casseday, J.H., Diamond, I.T., and Harting, J.K., 1976, Auditory pathways to the cortex in Tupaia glis. J. Comp. Neurol., 166: 303–340.Google Scholar
  13. Covey, E., and Casseday, J.H., 1986, Connectional basis for frequency representation in the nuclei of the lateral lemniscus of the bat, Eptesicus fuscus. J. Neurosci., in press.Google Scholar
  14. Erulkar, S.D. (1972) Comparative aspects of spatial localization of sound. Physiol. Rev. 52: 237–360.PubMedGoogle Scholar
  15. Feng, A.S. and M. Vater (1985) Functional organization of the cochlear nucleus of Rufous horseshoe bats: Frequencies and internal connections are arranged in slabs. J. Comp. Neurol. 235: 529–553.PubMedCrossRefGoogle Scholar
  16. Fuzessery, Z.M. and G.D. Pollak (1984) Neural mechanisms of soundGoogle Scholar
  17. localization in an echolocating bat. Science 225:725–728.Google Scholar
  18. Fuzessery, Z.M., J.J. Wenstrup, and G.D. Pollak (1985) A representation of horizontal sound location in the inferior colliculus of the mustache bat (Pteronotus p. parnellii). Hear. Res. 20: 85–89.PubMedCrossRefGoogle Scholar
  19. Fuzessery, Z.M. and G.D. Pollak (1985) Determinants of sound location selectivity in the bat inferior colliculus: a combined dichotic and free-field stimulation study. J. Neurophysiol. 54: 757–781.PubMedGoogle Scholar
  20. Goldberg, J.M. and P.B. Brown (1968) Responses of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: some physiological mechanisms of sound localization. J. Neurophysiol. 32: 613–636.Google Scholar
  21. Goldberg, J.M. (1975) Physiological studies of auditory nuclei of the pons. In: Handbook of Sensory Physiology, Vol. V/2, B.D. Keidel and W.D. Neff (Eds.), Springer Verlag, New York, pp. 109–144.Google Scholar
  22. Grinnell, A.D. and V.S. Grinnell (1965) Neural correlates of vertical sound localization by echolocating bats. J. Physiol London 181: 830–851.PubMedGoogle Scholar
  23. Guinan, J.J., Jr., B.E. Norris, and S.S. Guinan (1972) Single units in superior olivary complex II. Locations of unit categories and tonotopic organization. Internat. J. Neurosci. 4: 147–166.Google Scholar
  24. Harnischfeger, G., G. Neuweiler, and P. Schlegel (1985) Interaural time and intensity coding in superior olivary complex and inferior colliculus of the bat, Molossus ater. J. Neurophysiol. 53: 89–109.PubMedGoogle Scholar
  25. Harrison, J.M. and R. Irving (1966) Visual and non-visual auditory systems in mammals. Science 154: 738–743.PubMedCrossRefGoogle Scholar
  26. Helfert, F.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: 533–550.PubMedCrossRefGoogle Scholar
  27. Irving, R. and J.M. Harrison (1967) The superior olivary complex and audition: A comparative study. J. Comp. Neurol. 130: 77–86.PubMedCrossRefGoogle Scholar
  28. Jen, P.H.S. (1980) Coding of directional information by single neurons in the S-segment of the FM bat, Myotis lucifugus. J. Exp. Biol. 87: 203–216.PubMedGoogle Scholar
  29. Masterson, B.R. and I.T. Diamond (1973) Hearing: Central neural mechanisms: In: Handbook of Perception, E. Carterette and M. Freedman (Eds.), Academic Press, New York.Google Scholar
  30. Masterton, B.R., G.C. Thompson, J.K. Brunso-Bechtold, and M.J. Robarts (1975) Neuroanatomical basis of binaural phase-difference analysis for sound localization. A comparative study. J. Comp. Physiol. Psychol. 89: 379–386.PubMedCrossRefGoogle Scholar
  31. Metzner, W. and S. Radkhe-Schuller (1985) The lateral lemniscus in Rufous horseshoe bat. Abstract in SIBRC, Aberdeen.Google Scholar
  32. Morest, D.K., 1964, The neuronal architecture of the medial geniculate body of the cat. J. Anat. Lond. 98: 611–630.Google Scholar
  33. Morest, D.K., and Oliver, D.L., 1984, The neuronal architecture of the inferior colliculus in the cat: defining the functional anatomy of the auditory midbrain. J. Comp. Neurol. 222: 209–236.PubMedCrossRefGoogle Scholar
  34. Musicant and Butler (1985) Influence of monaural spectral cues on binaural localization. J. Acoust. Soc. Am. 77: 202–208.CrossRefGoogle Scholar
  35. Novick, A. (1977) Acoustic orientation. In: Biology of Bats, Vol. III. W.A. Wimsatt (Ed.) Academic Press, N.Y. pp. 74–273.Google Scholar
  36. Oliver, D.L., and Morest, D.K., 1984, The central nucleus of the inferior colliculus in the cat. J. Comp. Neurol. 222: 237–264.CrossRefGoogle Scholar
  37. O’Neill, W.E. (1985) Responses to pure tones and linear frequency components of CF-FM biosonar signal by single units in the inferior colliculus of the mustache bat. J. Comp. Physiol. 157: 797–816.CrossRefGoogle Scholar
  38. O’Neill, W.E. (1986) The processing of temporal information in the auditory system of echolocating bats. In: Myotis, P.A. Racey (ed.), SIBRC, Averdeen Symposium (in press)Google Scholar
  39. Papez, J.W., 1929, “Central acoustic tract in cat and man,” Anat. Rec., 42: 60.Google Scholar
  40. Poljak, S., 1926, Untersuchungen am Oktavussystem der Saugetiere und an den mit diesem koordinierten motorischen Apparaten des Hirnstammes. J. f. Psychol. u. Neurol. 32: 170–231.Google Scholar
  41. Pollak, G.D. (1980) Organizational and encoding features of neurons in the inferior colliculus of bats. In: Animal Sonar System. Busnel, R.-G, and J. Fish, (Eds.) Plenum, N.Y. pp. 549–587.Google Scholar
  42. Pollak, G.D., Marsh, D., Bodenhamer, R.D. and Souter A. (1977) Characteristics of phasic-on neurons in the inferior colliculus of bats with observation relating to mechanisms for echo-ranging. J. Neurophysiol. 40: 926–942.PubMedGoogle Scholar
  43. Pollak, G.D., D.S. Marsh, R. Bodenhamer, and A. Souther (1978) A single unit analysis of the inferior colliculus in unanesthetized bats: Response patterns and spike-count functions by constant-frequency and frequency-modulated sounds. J. Neurophysiol. 41: 677–691.PubMedGoogle Scholar
  44. Pollak, G.D. and Schuller, G. (1981) Tonotopic organization and encoding features of single units in the inferior colliculus of horseshoe bats: functional implications for prey identification. J. Neurophysiol. 45: 208–226.PubMedGoogle Scholar
  45. Pollak, G.D., Bodenhamer, R.D. and Zook, J.M (1983) Cochleotopic organization of mustache bat’s inferior colliculus. In: Advances in Vertebrate Neuroethology. J.-P Ewert, R.R. Capranica and D.J. Ingle (eds). Plenum, N.Y. pp. 925–935.CrossRefGoogle Scholar
  46. Pollak, G.D., J.J. Wenstrup, and Z.M. Fuzessery (in press) Auditory processing in the mustache bat’s inferior colliculus. Trends in Neurosci.Google Scholar
  47. Pumphrey, D.J. (1947) The sense organs of birds. Ibis 90: 171–199.CrossRefGoogle Scholar
  48. Ross, L.S., J.J. Wenstrup, and G.D. Pollak (1985) AnatomicalGoogle Scholar
  49. projections to an isofrequency region: Basis for an organization of binaural response properties in mustache bats. Soc. Neurosci. Abst. 11, Part 1, pg. 734.Google Scholar
  50. Ross. L.S., G.D. Pollak, and J.M. Zook (submitted) AscendingGoogle Scholar
  51. projections to an isofrequency region in the mustache bat’s inferior colliculus. J. Comp. Neurol.Google Scholar
  52. Ross, L.S., and G.D. Pollak (1986) Differential projections to monaural and binaural regions of one isofrequency contour in mustache bat’s inferior colliculus. Soc. Neurosci. Abstr.Google Scholar
  53. Schlegel, P. (1977) Directional coding by binaural brainstem units of the CF-FM bat, Rhinolophus ferrumequinum. J. Comp. Physiol. 118: 327–357.CrossRefGoogle Scholar
  54. Schweizer, H. (1981) The connections of the inferior colliculus and the organization of the auditory brainstem nuclei in the greater horseshoe bat. J. Comp. Neurol. 201: 25–49.PubMedCrossRefGoogle Scholar
  55. Schweizer, H., and Radtke, S., 1980, The auditory pathway of the greater horseshoe bat Rhinolophus ferrumequinum, in: Animal Sonar Systems, R.G. Busnel and J.E. Fish, eds., Plenum Press, New York, pp. 987 –989.Google Scholar
  56. Simmons, J.A. (1973) The resolution of target range by bats. J. Acoust. Soc. Am. 54: 157–173.PubMedCrossRefGoogle Scholar
  57. Simmons, J.A, 1971, Echolocation in bats: signal processing of echoes for target range. Science. 171: 925–928.PubMedCrossRefGoogle Scholar
  58. Simmons, J.A., 1979, Perception of echo pase information in bat sonar. Science. 204: 1336–1338.PubMedCrossRefGoogle Scholar
  59. Simmons, J.A., Howell, D.J. and Suga, N. (1975) Information content of bat sonar echoes. Am. Sci. 63: 204–215.PubMedGoogle Scholar
  60. Stevens, S.S. and E.B. Newman (1936) The localization of actual sources of sound. Amer. J. Psych. 48: 297–306.CrossRefGoogle Scholar
  61. Suga, N. (1964) Single unit activity in cochlear nucleus and inferior colliculus of echolocating bats. J. Physiol. ( London ) 172: 449–474.Google Scholar
  62. Suga, N. (1970) Echo-ranging neurons in the inferior colliculus of bats. Science 170: 449–452.PubMedCrossRefGoogle Scholar
  63. Suga, N., J.A. Simmons and P.H.-S. Jen (1975) Peripheral specialization for fine analysis of Doppler-Shifted echoes in CF-FM bat, Pteronotus parnelli, J. Exp. Biol. 63: 161–192.PubMedGoogle Scholar
  64. Suga, N., G. Neuweiler, and P. Schlegel (1976) Peripheral auditory tuning for fine frequency analysis by CF-FM bat Rhinolopus ferrumequinum J. Comp. Physiol. 106: 111–125.CrossRefGoogle Scholar
  65. Suga, N., and P.H.-S. Jen (1977) Further studies on the peripheral auditory system of CF-FM bats specialized for fine frequency analysis of Dopplershifted echoes. J. Exp. Biol. 69: 207–232.PubMedGoogle Scholar
  66. Suga, N. and K. Tsuzuki (1985) Inhibition and level-tolerant frequency tuning in the auditory cortex of the mustached bat. J. Neurophysiol. 53: 1109–1145.PubMedGoogle Scholar
  67. Tsuchitani, C. and J.C. Boudreau (1966) Single unit analysis of cat superior olive S-segment with tonal stimuli. J. Neurophysiol. 29: 694–697.Google Scholar
  68. Tsuchitani, C. (1977) Functional organization of lateral cell groups of cat superior olivary complex. J. Neurophysiol. 40: 296–318.PubMedGoogle Scholar
  69. Tsuchitani, C. and D.H. Johnson (1985) The effect of ipsilateral tone burst stimulus level on the discharge patterns of cat lateral superior olivary units. J. Acoust. Soc. Am. 77: 1484–1496.PubMedCrossRefGoogle Scholar
  70. Vater, M. and D. Schlegel (1979) Comparative neurophysiology of the inferior colliculus of two molosid bats Molossus ater and Molossus molossus. II. single unit reponses to frequency modulated signals and signal and noise combination. J. Comp. Physiol. 131: 147–160.CrossRefGoogle Scholar
  71. 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, eds., Academic Press, New York.Google Scholar
  72. Wenstrup, J.J., L.S. Ross, and G.D. Pollak (1985) A functional organization of binaural reponses in the inferior colliculus. Hear. Res. 17: 191–195.PubMedCrossRefGoogle Scholar
  73. Wenstrup, J.J, L.S. Ross, and G.D. Pollak (1986) Binaural reponse organization within a frequency-band representation of the inferior colliculus: Implications for sound localization. J. Neurosci. 6: 962–973.PubMedGoogle Scholar
  74. Zook, J.M., and Casseday, J.H., 1980, Ascending auditory pathways in the brain stem of the bat, Pteronotus parnellii, in: Animal SonarGoogle Scholar
  75. Systems, R.G. Busnel and J.E. Fish, eds., Plenum Press, New York, pp. 1005–1006.Google Scholar
  76. Zook, J.M., and Casseday, J.H., 1980, Identification of auditory centers in lower brain stem of two species of echolocating bats: Evidence from injection of horseradish peroxidase into inferior colliculus. In D.E. Wilson and A.L. Gardner (eds): Proc. Fifth Int. Bat Res. Conference. Lubbock, TX: Texas Tech Press, pp. 51–60.Google Scholar
  77. Zook, J.M. and J.H. Casseday (1982a) Cytoarchitecture of auditory system in lower brainstem of the mustache bat, Pteronotus parnellii. J. Comp. Neurol. 207: 1–13.PubMedCrossRefGoogle Scholar
  78. Zook, J.M. and J.H. Casseday (1982b) Origin of ascending projections to inferior colliculus in the mustache bat, Pteronotus parnellii. J. Comp. Neurol. 207: 14–28.PubMedCrossRefGoogle Scholar
  79. Zook, J.M., J.A. Winer, G.D. Pollak, and R.D. Bodenhamer (1985) Topology of the central nucleus of the mustache bat’s inferior colliculus: Correlation of single unit properties and neuronal architecture. J. Comp. Neurol. 231: 530–546.PubMedCrossRefGoogle Scholar
  80. Zook, J.M. and Casseday, J.H., 1985, Projections from the cochlear nuclei in the mustache bat, Pteronotus parnellii. J. Comp. Neurol. 237: 307–324.PubMedCrossRefGoogle Scholar
  81. Zook, J.M., and Casseday, J.H., 1986, Convergence of ascending pathways at the inferior colliculus of the mustache bat, Pteronotus parnellii, submitted for publication.Google Scholar

Copyright information

© Plenum Press, New York 1988

Authors and Affiliations

  • George D. Pollak
    • 1
  • John H. Casseday
    • 2
  1. 1.Department of ZoologyUniversity of Texas AustinUSA
  2. 2.Department of SurgeryPsychology Duke UniversityDurhamUSA

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