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The Auditory Thalamus in Bats

  • Jeffrey J. Wenstrup
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 5)

Abstract

During the past several years, studies of the auditory cortex in bats have revealed striking examples of functional specializations in the analysis of biosonar pulses and echoes (see O’Neill, Chapter 9). By means of sharp timing or frequency selectivities, some bat cortical neurons encode particular features of sonar targets, and these features are mapped across the cortical surface. Target range is one such feature. Much of the cortical analysis of sonar signals may depend on neural interactions that occur in the medial geniculate body (MGB), the thalamic relay in the ascending pathway to the auditory cortex. For example, combination-sensitive neurons, selective for combinations of spectrally or temporally distinct signal elements in the sonar pulse and echo, have been well described in regions of the auditory cortex; physiological studies suggest that these responses may be created in the medial geniculate body (Olsen and Suga 1991a,b). Thus, the auditory thalamus in bats may provide new insights into the processing of complex sounds, as well as furthering our understanding of biosonar mechanisms in these animals.

Keywords

Auditory Cortex Inferior Colliculus Tuning Curve Thalamic Reticular Nucleus Medial Geniculate Body 
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. Aitkin LM, Webster WR (1972) Medial geniculate body of the cat: organization and responses to tonal stimuli of neurons in ventral division. J Neurophysiol (Bethesda) 35:365–380.Google Scholar
  2. Andersen RA, Roth GL, Aitkin LM, Merzenich MM (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.PubMedCrossRefGoogle Scholar
  3. Andreeva NG, Lang TT (1977) Evoked responses of the superior olive to amplitude-modulated signals. Neurosci Behav Physiol 8:306–310.PubMedCrossRefGoogle Scholar
  4. Aoki E, Semba R, Keino H, Kato K, Kashiwamata S (1988) Glycine-like immuno-reactivity in the rat auditory pathway. Brain Res 442:63–71.PubMedCrossRefGoogle Scholar
  5. Ayrapet’yants ES, Konstantinov AI (1974) Echolocation in Nature. Arlington, VA: Joint Publications Research Service.Google Scholar
  6. Baron G (1974) Differential phylogenetic development of the acoustic nuclei among chiroptera. Brain Behav Evol 9:7–40.PubMedCrossRefGoogle Scholar
  7. Bodenhamer RD, Pollak GD (1983) Response characteristics of single units in the inferior colliculus of mustache bats to sinusoidally frequency modulated signals. J Comp Physiol 153:67–79.CrossRefGoogle Scholar
  8. Butman JA (1992) Inhibitory and excitatory mechanisms of coincidence detection in delay tuned neurons of the mustache bats. In: Proceedings of the 3d International Congress in Neuroethology. McGill University, Montreal.Google Scholar
  9. Butman JA, Suga N (1989) Bicuculline modifies the delay-tuning of FM-FM neurons in the mustached bat. Soc Neurosci Abstr 15:1293.Google Scholar
  10. Butman JA, Suga N (1990) NMDA receptors are essential for delay-dependent facilitation in FM-FM neurons in the mustached bat. Soc Neurosci Abstr 16:795.Google Scholar
  11. Calford MB (1983) The panellation of the medial geniculate body of the cat defined by the auditory response properties of single units. J Neurosci 3:2350–2364.PubMedGoogle Scholar
  12. Calford MB, Aitkin LM (1983) Ascending projections to the medial geniculate body of the cat: evidence for multiple, parallel auditory pathways through thalamus. J Neurosci 3:2365–2380.PubMedGoogle Scholar
  13. Casseday JH, Pollak GD (1988) Parallel auditory pathways: I. Structure and connections. In: Nachtigall PE, Moore PWB (eds) Animal Sonar: Processes and Performance. New York: Plenum, pp. 169–196.Google Scholar
  14. Casseday JH, Kobler JB, Isbey SF, Covey E (1989) Central acoustic tract in an echolocating bat: an extralemniscal auditory pathway to the thalamus. J Comp Neurol 287:247–259.PubMedCrossRefGoogle Scholar
  15. Celio MR (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375–475.PubMedCrossRefGoogle Scholar
  16. Clarey JC, Barone P, Imig TJ (1992) Physiology of thalamus and cortex. In: Popper AN, Fay RR (eds) Springer Handbook of Auditory Research, Vol. 2, The Mammahan Auditory Pathway: Neurophysiology. New York: Springer-Verlag, pp. 232–334.CrossRefGoogle Scholar
  17. Clerici WJ, Coleman JR (1990) Anatomy of the rat medial geniculate body: I. Cytoarchitecture, myeloarchitecture and neocortical connectivity. J Comp Neurol 297:14–31.PubMedCrossRefGoogle Scholar
  18. Clerici WJ, McDonald AJ, Thompson R, Coleman JR (1990) Anatomy of the rat medial geniculate body: II. Dendritic morphology. J Comp Neurol 297:32–54.PubMedCrossRefGoogle Scholar
  19. Conley M, Kupersmith AC, Diamond IT (1991) The organization of projections from subdivisions of the auditory cortex and thalamus to the auditory sector of the thalamic reticular nucleus in Galago. Eur J Neurosci 3:1089–1103.PubMedCrossRefGoogle Scholar
  20. Covey E, Hall WC, Kobler JB (1987) Subcortical connections of the superior colliculus in the mustache bat, Pteronotusparnellii. J Comp Neurol 263:179–197.PubMedCrossRefGoogle Scholar
  21. Edeline J-M, Weinberger NM (1991) Subcortical adaptive filtering in the auditory system: associative receptive field plasticity in the dorsal medial geniculate body. Behav Neurosci 105:154–175.PubMedCrossRefGoogle Scholar
  22. Fitzpatrick DC, Kanwal JS, Butman JA, Suga N (1993) Combination-sensitive neurons in the primary auditory cortex of the mustached bat. J Neurosci 13:931–940.PubMedGoogle Scholar
  23. Frisina RD, O’Neill WE, Zettel ML (1989) Functional organization of mustached bat inferior colliculus: II. Connections of the FM2 region. J Comp Neurol 284:85–107.PubMedCrossRefGoogle Scholar
  24. Hashikawa T, Rausell E, Molinari M, Jones EG (1991) Parvalbumin- and calbindin-containing neurons in the monkey medial geniculate complex: differential distribution and cortical layer specific projections. Brain Res 544:335–341.PubMedCrossRefGoogle Scholar
  25. Hattori T, Suga N (1989) Delay lines in the inferior colliculus of the mustached bat. Soc Neurosci Abstr 15:1293.Google Scholar
  26. Henkel CK (1983) Evidence of sub-collicular auditory projections to the medial geniculate nucleus in the cat: an autoradiographic and horseradish peroxidase study. Brain Res 259:21–30.PubMedCrossRefGoogle Scholar
  27. Houser CR, Vaughn JE, Barber RP, Roberts E (1980) GABA neurons are the major cell type of the nucleus reticularis thalami. Brain Res 200:345–354.CrossRefGoogle Scholar
  28. Jenkins WM, Masterton RB (1982) Sound localization: effects of unilateral lesions in central auditory system. J Neurophysiol (Bethesda) 47:987–1016.Google Scholar
  29. Jenkins WM, Merzenich MM (1984) Role of cat primary auditory cortex for sound-localization behavior. J Neurophysiol (Bethesda) 52:819–847.Google Scholar
  30. Jones EG (1975) Some aspects of the organization of the thalamic reticular complex. J Comp Neurol 162:285–308.PubMedCrossRefGoogle Scholar
  31. Jones EG, Powell TPS (1971) An analysis of the posterior group of thalamic nuclei on the basis of its afferent connections. J Comp Neurol 143:185–216.PubMedCrossRefGoogle Scholar
  32. Kavanagh GL, Kelly JB (1987) Contribution of auditory cortex to sound localization by the ferret (Mustela putorius). J Neurophysiol (Bethesda) 57:1746–1766.Google Scholar
  33. Kobler JB, Isbey SF, Casseday JH (1987) Auditory pathways to the frontal cortex of the mustache bat, Pternontus parnellii. Science 236:824–826.PubMedCrossRefGoogle Scholar
  34. Kudo M, Niimi K (1978) Ascending projections of the inferior colliculus onto the medial geniculate body in the cat studied by anterograde and retrograde tracing techniques. Brain Res 155:113–117.PubMedCrossRefGoogle Scholar
  35. Kudo M, Niimi K (1980) Ascending projections of the inferior colliculus in the cat: an autoradiographic study. J Comp Neurol 191:545–556.PubMedCrossRefGoogle Scholar
  36. Kuwabara N, Suga N (1993) Delay lines and amplitude selectivity are created in subthalamic auditory nuclei: the brachium of the inferior colliculus of the mustached bat. J Neurophysiol (Bethesda) 69:1713–1724.Google Scholar
  37. Majorossy K, Kiss A (1976) Specific patterns of neuron arrangement and of synaptic articulation in the medial geniculate body. Exp Brain Res 26:1–17.PubMedGoogle Scholar
  38. Mitani A, Itoh K, Mizuno N (1987) Distribution and size of thalamic neurons projecting to layer I of the auditory cortical fields of the cat compared to those projecting to layer IV. J Comp Neurol 257:105–121.PubMedCrossRefGoogle Scholar
  39. Mittmann DH, Wenstrup JJ (1994) Combination-sensitive neurons in the inferior colliculus of the mustached bat. In: Proceedings of the 17th Midwinter Meeting of the Association for Research in Otolaryngology, p 93. Association for Research in Otolaryngology, Des Moines.Google Scholar
  40. Morest DK (1964) The neuronal architecture of the medial geniculate body of the cat. J Anat (Lond) 98:611–630.Google Scholar
  41. Morest DK (1965) The laminar structure of the medial geniculate body of the cat. J Anat (Lond) 99:143–160.Google Scholar
  42. Morest DK (1975) Synaptic relationships of golgi type II cells in the medial geniculate body of the cat. J Comp Neurol 162:157–193.PubMedCrossRefGoogle Scholar
  43. Morest DK, Winer JA (1986) The comparative anatomy of neurons: homologous neurons in the medial geniculate body of the opossum and the cat. Adv Anat Embryol Cell Biol 97:1–96.PubMedGoogle Scholar
  44. Niimi K, Naito F (1974) Cortical projections of the medical geniculate body in the cat. Exp Brain Res 19:326–342.PubMedCrossRefGoogle Scholar
  45. Ohlemiller KK, Kanwal JS, Suga N (1992) Responses of cortical and thalamic FM-FM and CF/CF neurons of the mustached bat to species-specific communication sounds. Soc Neurosci Abstr 18:883.Google Scholar
  46. Oliver DL (1982) A Golgi study of the medial geniculate body in the tree shrew (Tupaia glis). J Comp Neurol 209:1–16.PubMedCrossRefGoogle Scholar
  47. Olsen JF (1986) Processing of biosonar information by the medial geniculate body of the mustached bat, Pteronotus parnellii. Ph.D. dissertation, Washington University, St. Louis, MO.Google Scholar
  48. Olsen JF, Rauschecker JP (1992) Medial geniculate neurons in the squirrel monkey sensitive to combinations of components in a species-specific vocalization. Soc Neurosci Abstr 18:883.Google Scholar
  49. Olsen JF, Suga N (1991a) Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding of relative velocity information. J Neurophysiol (Bethesda) 65:1254–1274.Google Scholar
  50. Olsen JF, Suga N (1991b) Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding of target range information. J Neurophysiol (Bethesda) 65:1275–1296.Google Scholar
  51. O’Neill WE (1985) Responses to pure tones and linear FM components of the CF-FM biosonar signal by single units in the inferior colliculus of the mustached bat. J Comp Physiol A 157:797–815.PubMedCrossRefGoogle Scholar
  52. O’Neill WE, Suga N (1982) Encoding of target range and its representation in the auditory cortex of the mustached bat. J Neurosci 2:17–31.PubMedGoogle Scholar
  53. Papez JW (1929) Central acoustic tract in cat and man. Anat Rec 42:60.Google Scholar
  54. Park TJ, Pollak GD (1993) GABA shapes a topographic organization of response latency in the mustache bat’s inferior colliculus. J Neurosci 13:5172–5187.PubMedGoogle Scholar
  55. Pollak GD, Bodenhamer RD (1981) Specialized characteristics of single units in inferior colliculus of mustache bat: frequency representation, tuning, and discharge patterns. J Neurophysiol (Bethesda) 46:605–620.Google Scholar
  56. Riquimaroux H, Gaioni SJ, Suga N (1991) Cortical computational maps control auditory perception. Science 251:565–568.PubMedCrossRefGoogle Scholar
  57. Rodrigues-Dagaeff C, Simm G, de Ribaupierre Y, Villa A, de Ribaupierre F, Rouiller EM (1989) Functional organization of the ventral division of the medial geniculate body of the cat: evidence for a rostro-caudal gradient of response properties and cortical projections. Hear Res 39:103–126.PubMedCrossRefGoogle Scholar
  58. Rouiller EM, de Ribaupierre F (1985) Origin of afferents to physiologically defined regions of the medial geniculate body of the cat: ventral and dorsal divisions. Hear Res 19:97–114.PubMedCrossRefGoogle Scholar
  59. Rouiller EM, Rodrigues-Dagaeff C, Simm G, DeRibaupierre Y, Villa A, DeRibaupierre F (1989) Functional organization of the medial division of the medial geniculate body of the cat: tonotopic organization, spatial distribution of response properties and cortical connections. Hear Res 39:127–142.PubMedCrossRefGoogle Scholar
  60. Rouiller EM, Capt M, Hornung JP, Streit P (1990) Correlation between regional changes in the distributions of GABA-containing neurons and unit response properties in the medial geniculate body of the cat. Hear Res 49:249–258.PubMedCrossRefGoogle Scholar
  61. Scheibel ME, Scheibel AB (1966) The organization of the nucleus reticularis thalami: a Golgi study. Brain Res 1:43–62.PubMedCrossRefGoogle Scholar
  62. Schuller G (1979) Coding of small sinusoidal frequency and amplitude modulations in the inferior colliculus of ‘CF-FM’ bat, Rhinolophusferrumequinum. Exp Brain Res 34:117–132.PubMedCrossRefGoogle Scholar
  63. Schweizer H (1981) The connections of the inferior colliculus and the organization of the brainstem auditory system in the greater horseshoe bat (Rhinolophus ferrumequinum). J Comp Neurol 201:25–49.PubMedCrossRefGoogle Scholar
  64. Shannon S, Wong D (1987) Interconnections between the medial geniculate body and the auditory cortex in an FM bat. Soc Neurosci Abstr 13:1469.Google Scholar
  65. Shosaku A, Kayama Y, Sumitomo I, Sugitani M, Iwama K (1989) Analysis of recurrent inhibitory circuit in rat thalamus: neurophysiology of the thalamic reticular nucleus. Prog Neurobiol 32:77–102.PubMedCrossRefGoogle Scholar
  66. Simm GM, de Ribaupierre F, de Ribaupierre Y, Rouiller EM (1990) Discharge properties of single units in auditory part of reticular nucleus of thalamus in cat. J Neurophysiol (Bethesda) 63:1010–1021.Google Scholar
  67. Sousa-Pinto A (1973) Cortical projections of the medial geniculate body of the cat. Adv Anat Embryol Cell Biol 48:1–42.Google Scholar
  68. Suga N, Horikawa J (1986) Multiple time axes for representation of echo delays in the auditory cortex of the mustached bat. J Neurophysiol (Bethesda) 55:776–805.Google Scholar
  69. Suga N, Jen PH-S (1977) Further studies on the peripheral auditory system of the CF-FM bats specialized for fine frequency analysis of Doppler-shifted echoes. J Exp Biol 69:207–232.PubMedGoogle Scholar
  70. Suga N, Manabe T (1982) Neural basis of amplitude-spectrum representation in auditory cortex of the mustached bat. J Neurophysiol (Bethesda) 47:225–254.Google Scholar
  71. Suga N, Olsen JF, Butman JA (1990) Specialized subsystems for processing biologically important complex sounds: cross-correlation analysis for ranging in the bat’s brain. Cold Spring Harbor Symp Quant Biol 55:585–597.PubMedGoogle Scholar
  72. Suga N, Tsuzuki K (1985) Inhibition and level-tolerant frequency tuning in the auditory cortex of the mustached bat. J Neurophysiol (Bethesda) 53:1109–1145.Google Scholar
  73. Suga N, Simmons JA, Jen PH-S (1975) Peripheral specialization for fine analysis of doppler-shifted echoes in the auditory system of the “CF-FM” bat Pteronotus parnellii. J Exp Biol 63:161–192.PubMedGoogle Scholar
  74. Suga N, O’Neill WE, Kujirai K, Manabe T (1983) Specificity of combination-sensitive neurons for processing of complex biosonar signals in auditory cortex of the mustached bat. J Neurophysiol (Bethesda) 49:1573–1626.Google Scholar
  75. Takahashi TT, Carr CE, Brecha N, Konishi M (1993) Calcium binding protein-like immunoreactivity labels the terminal field of nucleus laminaris of the barn owl. J Neurosci 7:1843–1856.Google Scholar
  76. Taniguchi I, Niwa H, Wong D, Suga N (1986) Response properties of FM-FM combination-sensitive neurons in the auditory cortex of the mustached bat. J Comp Physiol A 159:331–337.PubMedCrossRefGoogle Scholar
  77. Vasil’ev AG, Andreeva NG (1972) Characteristics of electrical responses by the medial geniculate bodies in vespertilionidae and rhinolophidae to ultrasonic stimuli with different frequencies. Neurophysiology 3:104–109.CrossRefGoogle Scholar
  78. Vater M, Braun K (1994) Parvalbumin, calbindin D-28k, and calretinin immuno-reactivity in the ascending auditory pathway of horseshoe bats. J Comp Neurol 341:534–558.PubMedCrossRefGoogle Scholar
  79. Vater M, Kössl M, Horn AKE (1992) GAD- and GABA-immunoreactivity in the ascending auditory pathway of horseshoe and mustached bats. J Comp Neurol 325:183–206.PubMedCrossRefGoogle Scholar
  80. Wenstrup JJ (1992a) Monaural and binaural regions of the mustached bat’s inferior colliculus project differently to targets in the medial geniculate body and pons. In: Proceedings of the 16th Midwinter Meeting of the Association for Research in Otolargnology, p. 77.Google Scholar
  81. Wenstrup JJ (1992b) Inferior colliculus projections to the medial geniculate body: a study of the anatomical basis of combination-sensitive neurons in the mustached bat. Soc Neurosci Abstr 18:1039.Google Scholar
  82. Wenstrup JJ, Grose CD (1993) Inputs to combination-sensitive neurons in the medial geniculate body of the mustached bat. Soc Neurosci Abstr 19:1426.Google Scholar
  83. Wenstrup JJ, Grose CD Inputs to combination-sensitive neurons in the medial geniculate body of the mustached bat: the missing fundamental. J Neurosci (in press).Google Scholar
  84. Wenstrup JJ, Ross LS, Pollak GD (1986) Binaural response organization within a frequency-band representation of the inferior colliculus: implications for sound localization. J Neurosci 6:962–973.PubMedGoogle Scholar
  85. Wenstrup JJ, Larue DT, Winer JA (1994) Projections of physiologically defined subdivisions of the inferior colliculus in the mustached bat: targets in the medial geniculate body and extrathalamic nuclei. J Comp Neurol 346:207–236.PubMedCrossRefGoogle Scholar
  86. Wenthold RJ, Hunter C (1990) Immunocytochemistry of glycine and glycine receptors in the central auditory system. In: Ottersen OP, Storm-Mathisen J (eds) Glycine Neurotransmission. Chichester: Wiley, pp. 391–416.Google Scholar
  87. Whitfield IC, Purser D (1972) Microelectrode study of the medial geniculate body in unanaesthetized free-moving cats. Brain Behav Evol 6:311–322.CrossRefGoogle Scholar
  88. Winer JA (1984) The human medial geniculate body. Hear Res 15:225–247.PubMedCrossRefGoogle Scholar
  89. Winer JA (1985) The medial geniculate body of the cat. Adv Anat Embryol Cell Biol 86:1–98.PubMedGoogle Scholar
  90. Winer JA (1992) The functional architecture of the medial geniculate body and the primary auditory cortex. In: Webster DB, Popper AN, Fay RR (eds) Springer Handbook of Auditory Research, Vol. 1, The Mammalian Auditory Pathway: Neuroanatomy. New York: Springer-Verlag, pp. 222–409.Google Scholar
  91. Winer JA, Larue DT (1988) Anatomy of glutamic acid decarboxylase (GAD) immunoreactive neurons and axons in the rat medial geniculate body. J Comp Neurol 278:47–68.PubMedCrossRefGoogle Scholar
  92. Winer JA, Morest DK (1983) The medial division of the medial geniculate body of the cat: implications for thalamic organization. J Neurosci 3:2629–2651.PubMedGoogle Scholar
  93. Winer JA, Wenstrup JJ (1994a) Cytoarchitecture of the medial geniculate body in the mustached bat (Pteronotus parnellii). J Comp Neurol (346:161–182).Google Scholar
  94. Winer JA, Wenstrup JJ (1994b) The neurons of the medial geniculate body in the mustached bat (Pteronotus parnellii). J Comp Neurol (346:183–206).Google Scholar
  95. Winer JA, Morest DK, Diamond IT (1988) A cytoarchitectonic atlas of the medial geniculate body of the opossum, Didelphys virginiana, with a comment on the posterior intralaminar nuclei of the thalamus. J Comp Neurol 274:422–448.PubMedCrossRefGoogle Scholar
  96. Winer JA, Wenstrup JJ, Larue DT (1992) Patterns of GABAergic immunoreactivity define subdivisions of the mustached bat’s medial geniculate body. J Comp Neurol 319:172–190.PubMedCrossRefGoogle Scholar
  97. Yang L, Pollak GD, Resler C (1992) GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus. J Neurophysiol (Bethesda) 68:1760–1774.Google Scholar
  98. Zettel ML, Carr CE, O’Neill WE (1991) Calbindin-like immunoreactivity in the central auditory system of the mustached bat, Pteronotus parnellii. J Comp Neurol 313:1–16.PubMedCrossRefGoogle Scholar
  99. Zook JM, Winer JA, Pollak GD, Bodenhamer RD (1985) Topology of the central nucleus of the mustache bat’s inferior colliculus: correlation of single unit response properties and neuronal architecture. J Comp Neurol 231:530–546.PubMedCrossRefGoogle Scholar

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© Springer-Verlag New York, Inc. 1995

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  • Jeffrey J. Wenstrup

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