Portal de Periódicos da CAPES

Sonic/vocal-acousticolateralis pathways in teleost fishes: A transneuronal biocytin study in mochokid catfish

1996; Wiley; Volume: 374; Issue: 4 Linguagem: Inglês

10.1002/(sici)1096-9861(19961028)374

1096-9861

Friedrich Ladich, Andrew H. Bass,

Ichthyology and Marine Biology

Journal of Comparative NeurologyVolume 374, Issue 4 p. 493-505 Sonic/vocal-acousticolateralis pathways in teleost fishes: A transneuronal biocytin study in mochokid catfish Friedrich Ladich, Friedrich Ladich Institute of Zoology, University of Vienna, Vienna, AustriaSearch for more papers by this authorAndrew H. Bass, Corresponding Author Andrew H. Bass ahb3@ cornell.edu Section of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853 UC Bodega Marine Laboratory, Bodega Bay, California 94923Section of Neurobiology and Behavior, Cornell University, Seeley G. Mudd Hall, Ithaca, NY 14853.Search for more papers by this author Friedrich Ladich, Friedrich Ladich Institute of Zoology, University of Vienna, Vienna, AustriaSearch for more papers by this authorAndrew H. Bass, Corresponding Author Andrew H. Bass ahb3@ cornell.edu Section of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853 UC Bodega Marine Laboratory, Bodega Bay, California 94923Section of Neurobiology and Behavior, Cornell University, Seeley G. Mudd Hall, Ithaca, NY 14853.Search for more papers by this author First published: 28 October 1996 https://doi.org/10.1002/(SICI)1096-9861(19961028)374:4 3.0.CO;2-XCitations: 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 Mochokid catfish have two sound-producing (sonic) organs—a pectoral spine stridulatory apparatus and a swimbladder whose vibration is established by nearby "drumming" muscles. Dextran-biotin or biocytin application to sonic nerves or muscles identified topographically separated motoneuron pools. Pectoral spine-related motoneurons are located within the ventral motor column whereas swimbladder motoneurons lie just ventral to the central canal or fourth ventricle. Axons of both groups of motoneurons exit the brain and spinal cord via ventral roots of occipital (swimbladder and pectoral) and spinal (swimbladder only) nerves. Transneuronal biocytin transport identified an extensive premotor network only for the swimbladder motor nuclei. Premotoneuron somata are located ipsilaterally in 1) a dorsolateral region of the sonic motor nucleus (SMN); motoneurons were clustered in the ventromedial region of the SMN and 2) the ventromedial medulla at the rostral pole of the SMN. Biocytin-filled fibers and less frequently premotoneuron somata were also found in the contralateral SMN. Biocytin-labeled fibers were continuous farther rostrally with 1) a commissural bundle that terminated bilaterally in the medial reticular formation near the caudal pole of the descending octaval nucleus and 2) a lateral brainstem bundle that terminated ipsilaterally in regions of the medulla and cerebellum considered to subserve acoustic and lateral line functions. Together with other data in distantly related teleost fishes, the results support the hypotheses that 1) central pathways linking sound-generating (sonic or vocal) and acoustic regions of the brain are traits common to both teleosts fishes and tetrapods that actively generate sounds, and 2) sonic/vocal pathways in teleosts have a conserved pattern of organization suggestive of common developmental origins. © 1996 Wiley-Liss, Inc. Literature Cited Abu-Gideiri, J. B., and D. H. Nasr (1973) Sound production by Synodontis schall (Bloch-Schneider). Hydrobiologia 43: 415–428. Baron, V. D., K. S. Morshev, V. M. Olshansky, and A. A. Orlov (1994) Electric organ discharges of two species of African catfish (Synodontis) during social behaviour. Anim. Behav. 48: 1472–1475. Bass, A. H. (1982) Evolution of the vestibulolateral lobe of the cerebellum in electroreceptive and nonelectroreceptive teleosts. J. Morphol. 174: 335–348. Bass, A. H., and R. Baker (1990) Sexual dimorphisms in a vocal control system of a teleost fish: morphology of physiologically identified neurons. J. Neurobiol. 21: 1155–1168. Bass, A., and R. Baker (1991) Evolution of homologous vocal control traits. Brain Behav. Evol. 38: 240–254. Bass, A. H., and R. Baker (1997) Phenotypic specification of hindbrain rhombomeres and the origins of rhythmic circuits in vertebrates. Brain Behav. Evol. (in press). Bass, A. H., M. A. Marchaterre, and R. Baker (1993) Transneuronal biocytin delineates species differences in a brainstem vocal-acoustic circuit in sound producing fish. Soc. Neurosci. 19: 1202 (Abstract). Bass, A. H., M. A. Marchaterre, and R. Baker (1994) Vocal-acoustic pathways in a teleost fish. Soc. Neurosci. 14: 4025–4039. Bleckmann, H., U. Neimann, and B. Fritzsch (1991) Peripheral and central aspects of the acoustic and lateral line system of a bottom dwelling catfish, Ancistrus sp. J. Comp. Neurol. 314: 452–466. Cohen, M., and H. Winn (1967) Electrophysiological observations on hearing and sound production in the fish, Porichthys notatus. J. Exp. Zool. 165: 355–369. Fine, M. L., H. E. Winn, and B. L. Olla (1977) Communication in fishes. In T. A. Sebeok (ed): How Animals Communicate. Bloomington, IN: Indiana University Press, pp. 472–518. Finger, T. E., and K. Kalil (1985) Organization of motoneuronal pools in the rostral spinal cord of the sea robin Prionotus carolinus. J. Comp. Neurol. 239: 384–390. Finger, T. E., and S.-L. Tong (1984) Central organization of eighth nerve and mechanosensory lateral line systems in the brainstem of Ictalurid catfish. J. Comp. Neurol. 229: 129–151. Fritzsch, B., U. Niemann, and H. A. Bleckmann (1990) Discrete projection of the sacculus and lagena to a distinct brainstem nucleus in a catfish. Neurosci. Lett. 111: 7–11. Furukawa, T. (1981) Effects of efferent stimulation on the saccule of goldfish. J. Physiol. (Lond.) 315: 203–215. Gainer, H. (1967) Neuromuscular mechanisms of sound production and pectoral spine locking in the banjo catfish Bunocephalus species. Physiol. Zool. 40: 296–306. Gainer, H., K. Kusano and R. F. Mathewson (1965) Electrophysiological and mechanical properties of squirrelfish sound-producing muscle. Comp. Biochem. Physiol. 14: 661–671. Hagedorn, M., M. Womble, and T. E. Finger (1990) Synodontid catfish: a new group of weakly electric fish. Behaviour and anatomy. Brain Behav. Evol. 35: 268–277. Kastberger, G. (1977) Der Trommelapparat der Doradiden. (Siluriformes, Pisces). Zool. Jb. Physiol. 81: 281–309. Kratochvil, H. (1978) Der Bau des Lautapparates vom Knurrenden Gurami (Trichopsis vittatus Cuvier & Valenciennes) (Anabantidae, Belontiidae). Zoomorphologie 91: 91–99. Ladich, F. (1996) Agonistic behaviour and signficance of sounds in vocalizing fish. Mar. Fresw. Behav. Physiol. (in press). Ladich, F., and M. L. Fine (1992) Localization of pectoral fin motoneurons (sonic and hovering) in the croaking gourami Trichopsis vittatus. Brain Behav. Evol. 39: 1–7. Ladich, F., and M. L. Fine (1994) Localization of swimbladder and pectoral motoneurons involved in sound production in pimelodid catfish. Brain Behav. Evol. 44: 86–100. Ladich, F., M. A. Marchaterre, L. Goldstein, and A. H. Bass (1995) Vocoalacoustic pathways in mochokidand arrid catfish. Soc. Neurosci. Abstr. 21: 1451. Lin, J. -W., and D. S. Faber (1988) An efferent inhibition of auditory afferents mediated by the goldfish Mauthner cell. Neuroscience 24: 829–836. Lindholm, M. M., and A. H. Bass (1993) Early events in myofibrillogenesis and innervation of skeletal, sound-generating muscle in a teleost fish. J. Morphol. 216: 225–239. McCormick, C. A., and M. R. Braford (1993) The primary octaval nuclei and inner ear afferent projections in the otophysan Ictalurus punctatus. Brain Behav. Evol. 42: 48–68. McCormick, C. A., and D. V. Hernandez (1996) Connections of octaval and lateral line nuclei of the medulla in the goldfish, including the cytoarchitecture of the secondary octaval population in goldfish and catfish. Brain Behav. Evol. 47: 113–137. Myrberg, A. A. (1981) Sound communication and interception in fishes. In W. N. Tavolga, A. N. Popper, and R. R. Fay, (eds): Hearing and Sound Communication in Fishes. New York: Springer-Verlag, pp. 395–426. Pereda, A. E., T. D. Bell, and D. S. Faber (1995) Retrograde synaptic communication via gap junctions coupling auditory afferents to the Mauthner cell. J. Neurosci. 15: 5943–5955. Pfeiffer, W., and J. F. Eisenberg (1965) Die Lauterzeugung der Dorwelse (Doradidae) und der Fiederbartwelse (Mochokidae). Z. Morphol. Oekol. Tiere 54: 669–679. Popper, A. N., and R. R. Fay (1993) Sound detection and processing by fish: critical review and major research questions. Brain Behav. Evol. 41: 14–38. Russell, I. J. (1971) The role of the lateral-line efferent system in Xenopus laevis. J. Exp. Biol. 54: 621–641. Salmon, M., H. E. Winn, and N. Sorgente (1968) Sound production and acoustical behavior in triggerfish. Pac. Sci. 12: 11–20. Schachner, G., and F. Schaller (1981) Schallerzeugung und Schallreaktionen beim Antennenwels (Mandim) Rhamdia sebae sebae Val. Zool. Beitr. 27: 375–392. Sörensen, W. (1895) Are the extrinsic muscles of the air-bladder in some Siluroidae and the "elastic spring" apparatus of others subordinate to the volunatary production of sound? What is, according to our present knowledge, the function of the Weberian ossicles?. J. Anat. Physiol. 29: 205–229, 399–423, 518–552. Tavolga, W. N. (1962) Mechanisms of sound production in the ariid catfishes Galeichthys and Bagre. Bull. Am. Mus. Nat. Hist. 24: 1–30. Tong, S. -L., and T. E. Finger (1983) Central organization of the electrosensory lateral line system in bullhead catfish Ictalurus nebulosus. J. Comp. Neurol. 217: 1–16. Tracy, H. C. (1959) Stages in the development of the anatomy of motility of the toadfish (Opsanus tau). J. Comp. Neurol. 11: 27–81. Weiser, M., N. Bennett, M. V. L. Bennett, and R. Baker (1985) Toadfish sonic motor system. II. Morphology. Biol. Bull. 169: 556–557. Citing Literature Volume374, Issue428 October 1996Pages 493-505 ReferencesRelatedInformation