The paratympanic organ (PTO) in the middle ear has been described in numerous bird species, but little is known about the distribution of this presumed lateral line remnant in other vertebrate classes. Here we provide evidence for a PTO in juvenile alligators, and make the first detailed description of its location and relation to ligaments in the reptilian middle ear. The alligator PTO measures about 450 µm in diameter. The alligator PTO contains hair cells whose cilia extend into a mucous substance within the lumen. The PTO connects though a ligament to the ear drum, suggesting that pressure onto the tympanic membrane might induce fluid movement in the PTO. Labeling of innervating nerve fibers with the fluorescent dye, DiI, indicates that the alligator PTO is connected with the vestibular brainstem. Because all bird species examined possess a PTO except for owls and possibly parakeets, we verified the absence of a PTO in parakeets by examination of serial sections combined with GABA immunolabeling for potential hair cells. Bird species with significant upper beak movement lack a PTO, suggesting that PTO function is incompatible with upper beak movement. We also examined the middle ear of an armadillo, a mammal that has a very basal position within the eutherian phylogenetic tree. A small vesicle with ciliated cells was found, but did not label with a hair-cell specific marker, antibodies to myosin VIIa, and thus is not likely to represent a true PTO. Our evidence for a PTO in a non-avian species, the alligator, together with previous reports suggesting the presence of a PTO in some mammals, indicates that ancestral stem amniotes possessed a PTO, and that the PTO was not a de novo invention of birds.

1.
Arnason, U., A. Gullberg, and A. Janke (1997) Phylogenetic analyses of mitochondrial DNA suggest a sister group relationship between Xenartha (Edentata) and Ferungulates. Mol. Biol. Evol., 14: 762–768.
2.
Barry, M.A., and R.L. Boord (1984) The spiracular organ of sharks and skates: Anatomical evidence indicating a mechanoreceptive role. Science, 226: 990–992.
3.
Barry, M.A., and M.V.L. Bennett (1989) Specialized lateral line receptor systems in elasmobranchs: the spiracular organs and vesicles of Savi. In The Mechanosensory Lateral Line: Neurobiology and Evolution (ed. by S. Coombs, P. Görner and H. Münz), Springer, New York, pp. 591–606.
4.
Benjamins, C.E. (1926) Y a-t-il une relation entre l’organe paratympanique de Vitali et le vol des oiseaux? Arch. Neerl. Physiol., 11: 215–222.
5.
Benjamins, C.E. (1939) L’ organe paratympanique de Vitali, soi-disant organe du vol des oiseaux, chez le Pingouin. Acta Otolaryngol. (Stockh.), 27: 266–270.
6.
Borg, E., and S.A. Counter (1989) The middle ear muscles. Sci. Am., 261: 74–80.
7.
Butler, A.B., and W. Hodos (1996) Comparative Vertebrate Neuroanatomy. Evolution and Adaptation. Wiley, New York.
8.
Buttemer, W.A. (1985) Energy relations of winter roost-site utilization by American goldfinches (Carduelis tristis). Oecologia, 68: 126–132.
9.
Clack, J.A. (1989) Discovery of the earliest known tetrapod stapes. Nature, 342: 425–427.
10.
Clack, J.A. (1990) Nos ancêtres respiraient-ils par les oreilles? (Did our ancestors breathe through their ears?). Recherche, 21: 770–772.
11.
Clack, J.A. (1994) Earliest known tetrapod braincase and the evolution of the stapes and fenestra ovalis. Nature, 369: 392–394.
12.
Counter, S.A., and E. Borg (1979) Physiological activation of the stapedius muscle in Gallus gallus. Acta Otolaryngol., 403: 13–19.
13.
Delius, J.D., and J. Emmerton (1978) Sensory mechanisms related to homing in pigeons; In Animal Migration, Navigation and Homing (ed. by K. Schmidt-Koenig and W.T. Keeton), Springer, Berlin, pp. 35–41.
14.
Delsuc, F., F.M. Catzeflis, M.J. Stanhope, and E.J.P. Douzery (2001) The evolution of armadillos, anteaters and sloths depicted by nuclear and mitochondrial phylogenies: Implications for the status of the enigmatic fossil Eurotamandua. P. Roy. Soc. Lond. Ser. B-Biol. Sci., 268: 1605–1615.
15.
Federici, F. (1927) Über die Innervation des von Vitali entdeckten Sinnesorgans im Mittelohr der Vögel (sogen. paratympanisches Organ). Anat. Anz., 62: 241–254.
16.
Giannessi, F., and L. Pera (1986) The ultrastructure of the paratympanic organ in the domestic fowl (Gallus gallus domesticus). J. Anat., 147: 191–199.
17.
Giannessi, F., and R. Ruffoli (1996) The ultrastructure of the sensory hairs of the paratympanic organ receptor cells in chicken. Anat. Embryol. (Berl), 193: 569–575.
18.
Giannessi, F., B. Fattori, R. Ruffoli, and A. Gagliardo (1996) Homing experiments on pigeons subjected to bilateral destruction of the paratympanic organ. J. Exp. Biol., 199: 2035–2039.
19.
Golubeva, T.B. (1972) The reflex activity of the tympanal muscle in the owl Asio otus. Zhurn. Evol. Biochem. Fisiol., 8: 173–181. (J. Evol. Biochem. Physiol., 8: 149–155).
20.
Grassi, S., F. Magni, and F. Ottaviani (1983) Identification of the motoneurons innervating the stapedius muscle in Gallus gallus: A horseradish peroxidase study. Arch. Ital. Biol., 121: 37–45.
21.
Grassi, S., F. Magni, and F. Ottaviani (1988) Mechanisms controlling vocalization-evoked stapedius muscle activity in chickens (Gallus gallus). J. Comp. Physiol. A, 162: 525–532.
22.
Griffin, D.R. (1969) The physiology and geophysics of bird navigation. Q. Rev. Biol., 44: 255–276.
23.
Hasson, T., M.B. Heintzelman, J. Santos-Sacchi, D.P. Corey, and M.S. Mooseker (1995) Expression in cochlea and retina of myosin VIIa, the gene product defective in Usher syndrome type1B. Proc. Natl. Acad. Sci. U.S.A., 92:9815–9819.
24.
Hedges, S.B., and L.L. Poling (1999) A molecular phylogeny of reptiles. Science, 283: 998–1001.
25.
Hofmann, M.H., and H. Bleckmann (1999) Effect of temperature and calcium on transneuronal diffusion of DiI in fixed brain preparations. J. Neurosci. Methods, 88: 27–31.
26.
Jacobson, M. (1978) Developmental Neurobiology, 2nd ed., Plenum Press, New York.
27.
Jørgensen, J.M. (1984) Fine structure of the paratympanic organ in the avian middle ear. Acta Zool., 65: 89–94.
28.
Kreithen, M.L., and W.T. Keeton (1974) Detection of changes in atmospheric pressure by the homing pigeon, Columba livia. J. Comp. Physiol., 89: 73–82.
29.
Manley, G.A. (2000) Cochlear mechanisms from a phylogenetic viewpoint. Proc. Natl. Acad. U.S.A., 97: 11736–11743.
30.
Miyamoto, M.M., and M. Goodman (1986) Biomolecular systematics of eutherian mammals – phylogenetic patterns and classification. Syst. Zool., 35: 230–240.
31.
Neeser, J.A., and C.S. von Bartheld (2001) Evidence for a paratympanic organ (presumed lateral line remnant) in the middle ear of juvenile alligators: implications for the phylogeny of hearing. Brain Behav. Evol., 57: 229.
32.
Oeckinghaus, H., and J. Schwartzkopff (1975) Elektrische Aktivierung des Mittelohrmuskels beim Star. Naturwissenschaften, 62: 582.
33.
Oeckinghaus, H., and J. Schwartzkopff (1983) Electrical and acoustical activiation of the middle ear muscle in a songbird. J. Comp. Physiol., 150: 61–67.
34.
Oldenstam, R.A. (1925) Over het z.g.n. vliegeorgaan van Vitali in het middenoor der vogels. Ph.D. dissertation. University of Groningen, Groningen.
35.
Petrash, E.W., K.H. Andres, M. Von Düring, and J.D. Delius (1983) Morphologische Aspekte des Vitali-Organs bei der Taube. Anat. Anz., 153: 288.
36.
Platner, F. (1839) Bemerkungen über das Quadratbein und die Paukenhöhle der Vögel. Gerhard Fleischer, Leipzig.
37.
Pohlman, A.G. (1921) The position and functional interpretation of the elastic ligaments in the middle ear region of Gallus. J. Morphol., 35: 229–262.
38.
Pohlman, A.G. (1922) The problem of middle ear mechanics. Ann. Otol. Rhinol. Laryngol., 31: 1–45.
39.
Popper, A.N., and B. Hoxter (1987) Sensory and nonsensory ciliated cells in the ear of the sea lamprey, Petromyzon marinus. Brain Behav. Evol., 30: 43–61.
40.
Ranzi, S. (1926) L’organo di senso spiracolare dei selaci. Pubbl. Staz. Zool. Napoli, 7: 37–76.
41.
Ruffini, A. (1920) Sull’organo nervoso paratimpanico di G. Vitali od organo del volo degli uccelli. Boll. Sci. med. Soc. med.-chir.Bologna, pp. 141–154/ Archo ital. Otol. Rhinol. Lar., 31: 397–413.
42.
Simonetta, A. (1953) L’organo di senso dello spiracolo e l’organo paratimpanico nella sistematica dei vertebrati. Arch. Ital. Anat. Embryol., 58:266–294.
43.
Stellbogen, E. (1930) Über das äussere und mittlere Ohr des Waldkauzes (Syrnium aluco, L.). Z. Morphol. Okol. Tiere, 19: 686–731.
44.
Usami, S., M. Igarashi, and G.C. Thompson (1987) GABA-like immunoreactivity in the chick vestibular end organs. Brain Res., 418: 383–387.
45.
Vitali, G. (1911) Di un interessante derivato della prima fessura branchiale nel passero. Anat. Anz., 39: 219–224.
46.
Vitali, G. (1914) Di un nuovo organo nervoso di senso nell’orecchio medio degli uccelli. Ulteriore destino dell’organo della prima fessura branchiale. Int. Msch. Anat. Physiol., 30: 363–428.
47.
Vitali, G. (1920) Sulla presenza nei chirotteri dell’organo nervoso di senso da me scoperto nell’orecchio medio degli uccelli. Atti R. Acad. d. Fisiocritici in Siena, 12: 521–524.
48.
Vitali, G. (1921) L’organo nervoso paratimpanico e la sua funzione. Riv. Biol., 3: 302–316.
49.
Vitali, G. (1923) Sul comportamento dell’organo della prima fessura branchiale in Athene noctua. Richerche Morfol., 3: 153–168.
50.
Vitali, G. (1924) Il compartamento dell’organo della prima fessura branchiale negli anfibi, nei rettili e nei mammiferi. Richerche Morfol., 4:191–221.
51.
Vitali, G. (1925) Il comportamento dell’organo della prima fessura branchiale (placode epibranchiale) nei selaci. Monitore Zool. Ital., 36: 122–130.
52.
Vitali, G. (1941) Alcune considerazioni sulla pubblicazione del Prof. Benjamins della presenza dell’organo paratimpanico nel Pinguino. Anat. Anz., 91: 364–368.
53.
von Bartheld, C.S. (1990) Development and innervation of the paratympanic organ (Vitali organ) in chick embryos. Brain Behav. Evol., 35: 1–15.
54.
von Bartheld, C.S. (1994) Functional morphology of the paratympanic organ in the middle ear of birds. Brain Behav. Evol., 44: 61–73.
55.
von Bartheld, C.S., and E.W. Rubel (1990) Paratympanic and spiracular sense organs: Phylogenetic distribution and theories of function, including hearing. In Evolutionary Biology of Hearing (ed. by D.B. Webster, R.R. Fay and A.N. Popper), Springer, New York, pp. 582–583.
56.
von Bartheld, C.S., D.E. Cunningham, and E.W. Rubel (1990) Neuronal tracing with DiI: Decalcification, cryosectioning, and photoconversion for light and electron microscopic analysis. J. Histochem. Cytochem., 38: 725–733.
57.
von Bartheld, C.S., W. Yang, and E.W. Rubel (1992) Normal and abnormal pathfinding of facial nerve fibers in the chick embryo. J. Neurobiol., 23: 1021–36.
58.
Wada, Y. (1924) Beiträge zur vergleichenden Physiologie des Gehörorganes. Pflüg. Arch., 202: 46–69.
59.
Wallraf, H.G. (1972) Homing of pigeons after extirpation of their cochleae and lagenae. Nature New Biol. (London), 236: 223–224.
60.
Webb J.F., and R.G. Northcutt (1991) Ciliated epidermal-cells in non-teleost actinopterygian fish. Acta Zool. (Stockholm), 72: 107–111.
61.
Wever, E.G. (1978) The Reptile Ear: Its Structure and Function. Princeton University Press, Princeton, N.J.
62.
Yntema, C.L. (1944) Experiments on the origin of the sensory ganglia of the facial nerve in the chick. J. Comp. Neurol., 81: 147–167.
63.
Zardoya, R., and A. Meyer (2001) The evolutionary position of turtles revised. Naturwissenschaften, 88: 193–200.
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.