Anatomical basis for audio-vocal integration in echolocating horseshoe bats

Journal of Comparative Neurology

Volumn 368, Issue 2, 1996, Pages 252-269

  Metzner, Walter ^a,b  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Doppler shift compensation; nuclei of the lateral lemniscus; paralemniscal tegmentum; sensory motor interface; vocalization

Indexed keywords

HORSERADISH PEROXIDASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY NERVOUS SYSTEM; BAT; BRAIN MAPPING; ECHOLOCATION; NEUROANATOMY; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; TISSUE DISTRIBUTION; TISSUE SPECIFICITY; VOCALIZATION;

ANIMALS; AUDITORY PATHWAYS; CATS; CHIROPTERA; ECHOLOCATION; NEURAL PATHWAYS; TEGMENTUM MESENCEPHALI; WHEAT GERM AGGLUTININ-HORSERADISH PEROXIDASE CONJUGATE;

EID: 0030006056     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960429)368:2<252::AID-CNE6>3.0.CO;2-2     Document Type: Article

References (117)

1. Adams. J.C. (1977) Technical considerations on the use of horseradish peroxidase as a neuronal marker. Neuroscience 2:142-145.
2. Altafulla, I., C. Shipley, and J.S. Buchwald (1988) Voiced calls evoked by hypothalamic stimulation in the cat. Exp. Brain Res. 72:21-32.
3. Altschuler, S.M., X.M. Bao, and R.R. Miselis (1992) Dendritic architecture of ambiguus motoneurons projecting to the upper alimentary tract in the rat. J. Comp. Neurol. 309:402-414.
4. Andrezik, J.A., and A.J. Beitz (1985) Reticular formation, central gray and related tegmental nuclei. In G. Paxinos (ed): The Rat Nervous System, Vol. 2. New York: Academic Press, pp. 1-28.
5. Appell. P.P., and M. Behan (1990) Sources of GABAergic projections to the superior colliculus of the cat. J. Comp. Neurol. 302:145-158.
6. Barrilot, J.C , A.L. Bianchi, and P. Gogan (1984) Laryngeal respiratory motoneurons: Morphology and electrophysiological evidence of separate sites for excitatory and inhibitory synaptic inputs. Neurosci. Lett. 47:107-112.
7. Barris, R.W., and H.R. Schuman (1953) Bilateral anterior cingulate gyrus lesions. Neurology 3:44-53.
8. Bazett. H.D., and W.G. Penfield (1922) A study of the Sherrington decerebrate animal in the chronic as well as acute condition. Brain 45: 185-265.
9. Broca, P. (1861) Le Cortex Cérébral (cited by J. de Ajuriaguerra and H. Hécaen, 1964). Paris: Masson.
10. Brunso-Bechthold, J.K., G.C. Thompson, and R.B. Masterton (1981) HRP study of the organization of auditory afferents to central nucleus of inferior colliculus in cat. J. Comp. Neurol. 197:705-722.
11. Buge, A., R. Escourolle, G. Rancurel, and M. Poisson (1975) Mutism akinétique et ramolissememnt bicingulaire. Trois observations anatomo-cliniques. Rev. Neurol. (Paris) 131:121-137.
12. Cajál. S. Ramon y (1911) Histologie du Système Nerveux de l'Homme and des Vertébrés, Tome II. Paris: Maloine.
13. Casseday, J.H., D.R. Jones, and I.T. Diamond (1979) Projections from the cortex to the tectum in the tree shrew, Tupaia glis. J. Comp. Neurol. 185:253-292.
14. Casseday, J.H., E. Covey, and M. Vater (1988) Connections of the superior olivary complex in the rufous horseshoe bat, Rhinolophus rouxi. J. Comp. Neurol. 275:313-329.
15. Casseday, J.H., J.B. Kobler, S.F. Isbey, and E. Covey (1989) Central acoustic tract in an echolocating bat: An extralemniscal auditory pathway to the thalamus. J. Comp. Neurol. 287:247-259.
16. Courville, J. (1966) The nucleus of the facial nerve. The relation between cellular groups and peripheral branches of the nerve. Brain Res. 1:338-354.
17. Covey E. (1993) Response properties of single units in the dorsal nucleus of the lateral lemniscus and paralemniscal zone of an echolocating bat. J. Neurophysiol. 69:842-859.
18. Covey E., and J.H. Casseday (1986) Connectional basis for frequency representation in the nuclei of the lateral lemniscus of the bat, Eptesicus fuscus. J. Neurosci. 6:2926-2940.
19. Covey. E., W.C. Hall, and J.B. Kobler (1987) Subcortical connections of the superior collieulus in the mustache bat, Pteronotus parnellii. J. Comp. Neurol. 263:179-197.
20. Davis, P.J., and B.S. Nail (1984) On the location and size of laryngeal motoneurons in the cat and rabbit. J, Comp. Neurol. 230:13-32.
21. Dressnandt, J., and U. Jürgens (1992) Brain stimulation-induced changes of phonation in the squirrel monkey. Exp. Brain Res. 89:549-559.
22. Feng, A., and M. Vater (1985) Functional organization of the cochlear nucleus of rufous horseshoe bats, Rhinolophus rouxi: Frequencies and internal connections are arranged in slabs. J. Comp. Neurol. 235:529-503.
23. Fernandez de Molina, A., and R, W. Hunsperger (1962) Organization of the subcortical system governing defence and flight reactions in the cat. J. Physiol. 160:200-213.
24. Gaioni, S.J., N. Suga, and H. Riquimaroux (1988) Effects of bilateral ablation of the auditory cortex and/or cingulate cortex on the biosonar behavior of the mustache bat. 18th Annual Meeting, Am. Soc. Neurosci. (Abstr.) 442:7.
25. Glendenning, K.K., G.C. Thompson, and R.B. Masterton (1981) Ascending auditory afferents to the nuclei of the lateral lemniscus. J. Comp. Neurol. 197:673-703.
26. Gooler, D.M., and W.E. O'Neill (1987) Topographic representation of vocal frequency demonstrated by microstimulation of anterior cingulate cortex in the echolocating bat, Pteronotus parnellii parnellii. J. Comp. Physiol. A 161:283-294.
27. Grinnell, A.D. (1989) Listening to the voice within. Nature 341:488-189.
28. Henkel, C.K. (1983) Evidence of sub-collicular projections to medial geniculate nucleus in the cat: An autoradiographic and horseradish peroxidase study. Brain Res. 259:21-30.
29. Henkel, C.K., and S.B. Edwards (1978) The superior colliculus control of pinna movements in the cat: Possible anatomical connections. J. Comp. Neurol. 182:763-776.
30. Hinrichsen, C.F., and A.T. Ryan (1981) Localization of laryngeal motoneurons in the rat: Morphological evidence for dual innervation? Exp. Neurol. 74:341-355.
31. Hisa, Y., F. Sato, K. Fukui, Y. Ibata, and O. Mizukoshi (1984) Nucleus ambiguus motoneurons innervating the canine intrinsic laryngeal muscles by the fluorescent labeling technique. Exp. Neurol. 84:441-449.
32. Holstege. G. (1989) Anatomical study of the final common pathway for vocalization in the cat. J. Comp. Neurol. 284:242-252.
33. Holstege, G. (1991) Descending motor pathway and spinal motor system: Limbic and nonlimbic components. Progr. Brain Res. 87:307-421.
34. Jürgens, U. (1976) Projections from the cortical larynx area in the squirrel monkey. Exp. Brain Res. 25:401-411.
35. Jürgens, U. (1982) Afferents to the cortical larynx area in the monkey. Brain Res. 239:377-389.
36. Jürgens, U., and C.-L. Lu (1993) The effects of periaqueductally injected transmitter antagonists on forebrain-elicited vocalization in the squirrel monkey. Eur. J. Neurosci. 5:735-741.
37. Jürgens, U., and P. Müller-Preuss (1977) Convergent projections of different limbic vocalization areas in the squirrel monkey. Exp. Brain Res. 29:75-83.
38. Jürgens, U., and D. Ploog (1981) On the neural control of mammalian vocalization. TINS 4:135-137.
39. Jürgens. U., and R. Pratt (1979) The cingular vocalization pathway in the squirrel monkey. Exp. Brain Res. 34:499-559.
40. Jürgens, U., M. Hast, and R. Pratt (1978) Effects of laryngeal nerve transection on squirrel monkey calls. J. Comp. Physiol. A 123:23-29.
41. Kanai, T., and S.C. Wang (1962) Localization of the central vocalization mechanism in the brainstem of the cat. Exp. Neurol. 6:426-434.
42. Kane, E.S., and L.M. Barone (1980) The dorsal nucleus of the lateral lemniscus in the cat: Neuronal types and their distribution. J. Comp. Neurol. 192:797-826.
43. Kelly, A.H., L.E. Beaton, and H.W. Magoun (1946) A midbrain mechanism for facio-vocal activity. J. Neurophysiol. 9:181-189.
44. Kirzinger, A., and U. Jürgens (1982) Cortical lesion effects and vocalization in the squirrel monkey. Brain Res. 233:299-315.
45. Kirzinger, A., and U. Jürgens (1985) The effects of brainstem lesions on vocalization in the squirrel monkey. Brain Res. 358:150-162.
46. Kirzinger, A., and U. Jürgens (1991) Vocalization-correlated single-unit activity in the brainstem of squirrel monkeys. Exp. Brain Res. 84:545-560.
47. Kobler, J.B., S.F. Isbey, and J.H. Casseday (1987) Auditory pathways to the frontal cortex of the mustache bat, Pteronotus parnellii. Science 236: 824-826.
48. Kudo, M. (1981) Projections of the lateral lemniscus in the cat: An autoradiographic study. Brain Res. 221:57-69.
49. Larson, C.R., G.B. Kempster, and M.K. Kistler (1987) Changes in voice fundamental frequency following discharges of single motor units in cricothyroid and thyroarytenoid muscles. J. Speech Hearing Res. 30: 552-558.
50. Larson, C.R., and M.K. Kistler (1986) The relationship of periaqueductal gray neurons to vocalization and laryngeal EMG in the behaving monkey. Exp. Brain Res. 63:396-606.
51. Magoun, H.W., D. Atlas, E.H. Ingersoll, and S.W. Ranson (1937) Associated facial. vocal, and respiratory components of emotional expression: An experimental study. J. NeuroL Psychopathol. 17:241-255.
52. Martin, G.F., R. Waltzer, and R.P. Vertes (1985) Major projections of the reticular formation. In G. Paxinos (ed): The Rat Nervous System, Vol. 2. Sydney: Academic Press, pp. 29-42.
53. Mesulam, M.M. (1978) Tetramethyl benzidine for horseradish peroxidase neurochemistry: Incubation parameters and visibility. J. Histochem. Cytochem. 24:1273-1280.
54. Metzner, W. (1989) A possible neuronal basis for Doppler-shift compensation in echolocating horseshoe bats. Nature 341:529-532.
55. Metzner, W. (1993) An audio-vocal interface in echolocating horseshoe bats. J. Neurosci. 13:1899-1915.
56. Metzner, W., and S. Radtke-Schuller (1987) The nuclei of the lateral lemniscus in the rufous horseshoe bat, Rhinolophus rouxi. J. Comp. Physiol. A 160:395-411.
57. Metzner, W., and S. Radtke-Schuller (1989) Differences in the connection patterns of the three nuclei of the lateral lemniscus in horseshoe bats. In N. Elsner and W. Singer (eds): Dynamics and Plasticity in Neural Systems. Stuttgart: Thieme, p. 290.
58. Morest, O.K., and D.L. Oliver (1984) The neuronal cytoarchitecture of the inferior colliculus in the cat: Defining the functional anatomy of the auditory midbrain. J. Comp. Neurol. 222:209-236.
59. Movchan, E.V. (1984) Participation of auditory centers in echolocative tracking of a moving target by greater horseshoe bat (in Russian). Neirofiziologyia 16:737-745.
60. Mugnaini, E., and W.H. Oertel (1985) An atlas of the distribution of GABAergic neurons and terminals in the rat CNS as revealed by GAD immunohistochemistry. In A. Björklund and T. Hökfelt (eds): Handbook of Chemical Neuroanatomy, Vol. 4: GABA and Neuropeptides in the CNS. Amsterdam: Elsevier, pp. 436-608.
61. Müller-Preuss, P., and D. Ploog (1983) Central control of sounds production in mammals. In B. Lewis (ed): Bioaeoustics - A Comparative Approach. New York: Academic Press, pp. 125-146.
62. Neuweiler, G. (1970) Neurophysiologische Untersuchungen zum Echoortungssystem der Grossen Hufeisennase Rhinolophus femimequinum. Z. Vergl. Physiol. 67:273-306.
63. Neuweiler, G. (1990) Auditory adaptations for prey capture in echolocating bats. Physiol. Rev. 70:615-641.
64. Neuweiler, G., W. Metzner, U. Heilmann, R. Rübsamen, M. Eckrich, and H.H. Costa (1987) Foraging behavior and echolocation in the rufous horseshoe bat (Rhinolophua rouxi) of Sri Lanka. Behav. Ecol. Sociobiol. 20:53-67.
65. Novick, A., and D.R. Griffin (1961) Laryngeal mechanism in bats for the production of orientation sounds. J. Exp. Zool. 148:125-145.
66. Okubo, J., S. Kitamura, K. Ogata, and A. Sakai (1987) Localization of rabbit laryngeal motoneurons in the nucleus ambiguus. Exp. Neurol. 96: 528-539.
67. Oliver, D.L., and M.F. Huerta (1992) Inferior and superior colliculi. In D.B. Webster, A.N. Popper, and R.R. Fay (eds): The Mammalian Auditory System - Neuroanatomy. New York: Springer-Verlag, pp. 168-221.
68. Panneton, W.M., and G.F. Martin (1979) Midbrain projections to the trigeminal, facial and hypoglossal nuclei in the opossum. A study using axonal transport techniques. Brain Res. 165:493-511.
69. Panneton, W.M., and G-F. Martin (1983) Brainstem projections to the facial nucleus of the opossum. A study using axonal transport techniques-Brain Res. 267:19-83.
70. Papez, J.W. (1929) Central acoustic tract in cat and man. Anat. Rec. 42:60.
71. Paxinos, G., and C. Watson (1986) The Rat Brain in Stereotaxic Coordinates, 2nd ed. Sydney: Academic Press.
72. Pollak, G.D., and J.H. Casseday (1989) Echolocation: The functional organization of the auditory brainstem of bats. Berlin: Springer Verlag.
73. Popper, A.N., and R.R. Fay (1992) The Mammalian Auditory Pathway. Berlin: Springer-Verlag.
74. Prechtl, H. (1991) Akustische Eigenschaften von Neuronen des rostralen Colliculus Inferior bei der Hufeisennasen-Fledermaus Rhinolophus rouxi. Diploma Thesis, University of Munich.
75. Reimer. K. (1989a) Dissertation Thesis. Faculty of Biology, University of Munich.
76. Reimer, K. (1989b) Retinofugal projections in the rufous horseshoe bat, Rhinolophus rouxi. Anat. Embryol. 180:89-98.
77. Robinson, B.W. (1967) Vocalization evoked from forebrain in Macaco, mulatto. Physiol. Behav. 2:345-354.
78. Rübsamen, R., and M. Betz ( 1986) Control of echolocation pulses by neurons of the nucleus ambiguus in the rufous horseshoe bat, Rhinolophus rouxi (I). J. Comp. Physiol. A 159:675-687.
79. Rübsamen, R., and G. Schuller (1981) Laryngeal nerve activity during pulse emission of the CF-FM bat, Rhinolophus ferrumequinum. J. Comp. Physiol. 143:323-327.
80. Rübsamen, R., and H. Schweizer (1986) Control of echolocation pulses by neurons of the nucleus ambiguus in the rufous horseshoe bat, Rhinolpohus rouxi. II. Afferent and efferent connections of the motor nucleus of the laryngeal nerve. J. Comp. Physiol. A 159:689-699.
81. Schnitzler, H.U. (1968) Die Ultraschallortungslaute der Hufeisen-Fledermä-use (Chiroptera, Rhinolophidae) in verschiedenen Orientierungssituationen. Z. Vergl. Physiol. 57:376-408.
82. Schuller, G. (1986) Influence of echolocation pulse rate on Doppler shift compensation control system in the greater horseshoe bat. J. Comp. Physiol. A 158:239-246.
83. Schuller, G., and S. Radtke-Schuller (1990) Neural control of vocalization in bats: Mapping of brainstem areas with electrical microstimulation eliciting species-specific echolocation calls in the rufous horseshoe bat. Exp. Brain Res. 79:192-206.
84. Schuller, G., and R. Rübsamen (1981) Laryngeal nerve activity during pulse emission in the CF-FM bat, Rhinolophus ferrumequinum. I. Superior laryngeal nerve (external motor branch). J. Comp. Physiol. 143:317-321.
85. Schuller, G., and N. Suga (1976) Laryngeal mechanism for the emission of CF-FM sounds in the Doppler-shifl compensating bat, Rhinolophus ferrumequinum. J. Comp. Physiol. 107:253-262.
86. Schuller, G., K. Beuter, and H.U. Schnitzler (1974) Response to frequency shifted artificial echoes in the bat Rhinolophus ferrumequinum. J. Comp. Physiol. 89:275-286.
87. Schuller, G., K. Beuter, and R. Rübsamen (1975) Dynamic properties of the compensation system for Doppler shifts in the bat Rhinolophus ferrumequinum. J. Comp. Physiol. 97:113-125.
88. Schuller, G., S. Radtke-Schuller, and M. Betz (1986) A stereotaxic method for small animals using experimentally determined reference profiles. J. Neurosci. Methods 18:339-350.
89. Schwartz, I.R. (1992) The superior olivary complex and lateral lemniscal nuclei. In D.B. Webster, A.N. Popper, and R.R. Fay (eds): The Mammalian Auditory System - Neuroanatomy. New York :Springer-Verlag, pp. 117-167.
90. 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.
91. Schweizer, H., R. Rübsamen, and C. Rühle (1981) Localization of brainstem motoneurons innervating the laryngeal muscles in the rufous horseshoe bat, Rhinolophus rouxi. Brain Res. 230:41-50.
92. Skultety, F.M. (1958) The behavioral effects of destructive lesions of the periaqueductal gray matter in adult cats. J. Comp. Neurol. 110:337-365.
93. Suga, N., and P. Schlegel (1972) Neural attenuation of responses to emitted sounds in echolocating bats. Science 177:82-84.
94. Suga, N., and T. Shimozawa (1974) Site of neural attenuation of responses to self-vocalized sounds in echolocating bats. Science 183:1211-1213.
95. Suga, N., and Y. Yajima (1989) Auditory-vocal integration in the midbrain of the mustached bat: Periaqueductal gray and reticular formation. In J.D. Newman (ed): The Physiological Control of Mammalian Vocalization. New York: Plenum Press, pp. 87-98.
96. Suga, N., P. Schlegel, T. Shimozawa, and J. Simmons (1973) Orientation sounds evoked from echolocating bats by electrical stimulation of the brain. J. Acoust. Soc. Am. 54:793-797.
97. Suthers, R.A., and J.M. Fattu (1973) Mechanism of sound production by echolocating bats. Am. Zool. 13:1215-1226.
98. Swanson, L.W. (1992) Brain Maps: Structure of the Rat Brain. Amsterdam: Elsevier.
99. Tanaka, K., K. Otani, A. Tokunaga, and S. Sughita (1985) The organization of neurons in the nucleus of the lateral lemniscus projecting to the superior and inferior colliculus. Brain Res. 341:252-260.
100. Thorns, G., and U. Jürgens (1987) Common input of the cranial motor nuclei involved in phonation in squirrel monkey. Exp. Neurol. 95:85-99.
101. Travers, J.B., and R. Norgren (1983) Afferent projections to the oral motor nuclei in the rat. J. Comp. Neurol. 220:280-298.
102. Vartanyan, I.A., and T.V. Chernigovskaya (1990) Vocalization and speech systems of the brain: An evolutionary-neurobiological analysis. J. Evol. Biochem. Physiol. 26:627-636.
103. Vater, M., and K. Braun (1994) Parvalbumin, calbindin D-28k, and calretin immunoreactivity in the ascending auditory pathway of horseshoe bats. J. Comp. Neurol. 341:534-558.
104. Vater, M., M. Kössl, and A.K.E. Horn (1992) GAD- and GABA-immunoreactivity in the ascending auditory pathway of horseshoe and mustached bats. J. Comp. Neurol. 325:183-206.
105. Veazey, R.B., and C.M. Severin (1980a) Efferent projections of the deep mesencephalic nucleus (pars lateralis) in the rat. J. Comp. Neurol. 190:231-244.
106. Veazey, R.B., and C.M. Severin (1980b) Efferent projections of the deep mesencephalic nucleus (pars medialis) in the rat. J. Comp. Neurol. 190:245-258.
107. Veazey, R.B., and C.M. Severin (1982) Afferent projections of the deep mesencephalic nucleus in the rat. J. Comp. Neurol. 204:134-150.
108. Vernov, J.J., and J. Sutin (1983) Brainstem projections to the normal and noradrenergically hyperinnervated trigeminal motor nucleus. J. Comp. Neurol. 214:198-208.
109. Vogt, B.A., and H. Barbas (1988) Structure and connections of the cingulate vocalization region in the rhesus monkey. In J.D. Newman (ed): The Physiological Control of Mammalian Vocalization. New York: Plenum Press, pp. 203-225.
110. Webster. D.B., A.N. Popper, and R.R. Fay (1992; eds) The Mammalian Auditory Pathway: Neuroanatomy. New York: Springer-Verlag.
111. Yajima, Y., and Y. Hayashi (1983) Ambiguus motoneurons discharging synchronously with ultrasonic vocalization in rats. Exp. Brain Res. 50:359-366.
112. Yajima, Y., and C.R. Larson (1993) Multifunctional properties of ambiguus neurons identified electrophysiologically during vocalization in the awake monkey. J. Neurophysiol. 70:529-540.
113. Yoshida, Y., T. Miyazaki, M. Hirano, T. Shin, and T. Kanaseki (1982) Arrangement of motoneurons innervating the intrinsic laryngeal muscles of cats as demonstrated by horseradish peroxidase. Acta Otolaryngol. 94:329-334.
114. Zhang, S., X. Sun, and P.H.S. Jen (1987) Anatomical study of neural projections to the superior colliculus of the big brown bat, Eptesicus fuscus. Brain Res. 416:375-380.
115. Zook, J.M., and J.H. Casseday (1982) Origin of ascending projections to inferior colliculus of mustache bat, Pteronotus parnellii. 3. Comp. Neurol. 207:14-28.
116. Zook, J.M., and J.H. Casseday (1985) Projections from the cochlear nucleus in the mustache bat, Pteronotus parnellii. J. Comp. Neurol. 237:307-324.
117. Zook, J.M., and J.H. Casseday (1987) Convergence of ascending pathways at the inferior colliculus of the mustache bat, Pteronotus parnellii. J. Comp. Neurol. 267:347-361.