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Ultrastructural study of the neural microcircuits in the sensory epithelium of the paratympanic organ of the chicken

F. Giannessi, L. Ryskalin, R. Ruffoli

Abstract


The paratympanic organ (PTO) is a sensory organ located in the medial wall of the tympanic cavity of birds. The organ looks like a small tapering vesicle, and is equipped with a sensory epithelium formed by supporting cells (SCs) and Type II hair cells (Type II-HCs). The function of the PTO has not yet been precisely defined. The prevailing current hypothesis is that the PTO assesses the air pressure exerted on the external surface of the tympanic membrane. The PTO could may thus function as a barometer and, in flying birds, also as an altimeter. The afferent synapses of the PTO of chicken were described in detail in a previous paper. Reciprocal synapses between efferent nerve endings (ENEs) and the HCs were also observed, suggesting the existence of local microcircuits. The aim of this work was to provide a more detailed ultrastructural description of these microcircuits in the PTO of chicken. We observed for the first time: (1) reciprocal synapses between the HCs and the afferent nerve endings (ANEs); (2) presence of two distinct types of ENEs; (3) reciprocal synapses between the HCs and both types of ENEs. Overall, these results indicate that a complex processing of the incoming sensory signals may occur in the PTO. This thus suggests that the PTO may perform more complex functions than those supposed until now. We hypothesize that the PTO could have a role in the low-frequency sound perception.

Keywords


paratympanic organ, hair cells, innervation, ultrastructure

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Baker C.V., O'Neill P., McCole R.B. Lateral line, otic and epibranchial placodes: developmental and evolutionary links? J. Exp. Zool. B. Mol. Dev. Evol., 310: 70-83, 2008.

Castellano-Muñoz M., Israel S.H., Hudspeth A.J. Efferent control of the electrical and mechanical properties of hair cells in the bullfrog’s sacculus. PLoS One, 5: e13777, 2010.

Dunn R.F. Reciprocal synapses between hair cells and first order afferent dendrites in the crista ampullaris of the bullfrog. J. Comp. Neurol., 193: 255-264, 1980.

Engström H., Bergström B., Ades H.W. Macula utriculi and macula sacculi in the squirrel monkey. Acta Otolaryngol. Suppl., 301: 75, 1972.

Ekström D.K.J. Ultrastructure of the Lateral-line Sense Organs of the Ratfish, Chimera montrosa. Cell Tissue Res., 215: 651-665, 1981.

Flock Ǻ. Structure of the macula utriculi with special references to directional interplay of sensory responses as revealed by morphological polarization. J. Cell Biol., 22: 413-431, 1964.

Flock Ǻ. Electron microscopic and electrophysiological studies on the lateral-line canal-organ. Acta oto-laryng. (Stockh.), 199: 1-90, 1965.

Francis H.W. and Nadol J.B. Jr. Patterns of innervation of outer hair cells in a chimpanzee: I. Afferent and reciprocal synapses. Hear Res., 64: 184-190, 1993.

Giannessi F. and Pera L. The ultrastructure of the paratympanic organ in the domestic fowl (Gallus gallus domesticus). J. Anat., 147: 191-199, 1986.

Giannessi F. On the presence of reciprocal synapses in the paratympanic organ of the chicken. Anat. Embryol., 180: 175-178, 1989.

Giannessi F. and Ruffoli R. The ultrastructure of the sensory hair cells of the paratympanic organ receptor cells in chicken. Anat. Embryol., 193: 569-575, 1996a.

Giannessi F. and Ruffoli R. Fine structure of the afferent synapses in the paratympanic organ of the chicken, with special reference to the synaptic bodies. Ann. Anat., 178: 127-131, 1996b.

Giannessi F., Fattori B., Ruffoli R., Gagliardo A. Homing experiments on pigeons subjected to bilateral destruction of the paratympanic organ. J. Exp. Biol., 199: 2035-2039, 1996c.

Giannessi F., Ruffoli R., von Bartheld C.S. Giovanni Vitali: Discoverer of the paratympanic organ. Ann. Anat., 195: 5-10, 2013.

Griffin D.R. The physiology and geophysics of bird navigation. Q. Rev. Biol., 44: 255-276, 1969.

Jordan P.M., Fettis M., Holt J.C. Efferent innervation of turtle semicircular canal cristae: comparisons with bird and mouse. J. Comp. Neurol., 523: 1258-1280, 2015.

Hagstrum J.T. Infrasound and the avian navigational map. J. Exp. Biol., 203: 1103-1111, 2000.

Hagstrum J.T. Atmospheric propagation modeling indicates homing pigeons use loft-specific infrasonic 'map' cues. J. Exp. Biol., 216: 687-699, 2013.

Hama K. A study on the fine structure of the saccular macula of the gold fish. Z. Zellforsch., 94: 155, 1969.

Higgs D.M. and Radford C.A. The contribution of the lateral line to 'hearing' in fish. J. Exp. Biol., 216: 1484-1490, 2013.

Hill E.M., Koay G., Heffner R.S., Heffner H.E. Audiogram of the chicken (Gallus gallus domesticus) from 2 Hz to 9 kHz. J. Comp. Physiol., 200: 863-870, 2014.

Holstein G.R., Martinelli G.P., Boyle R., Rabbitt R.D., Highstein S.M. Ultrastructural observations of efferent terminals in the crista ampullaris of the toadfish, Opsanus tau. Exp. Brain Res., 157: 128-136, 2004.

Konishi M. Comparative neurophysiological studies of hearing and vocalization in songbirds. Zeitscrifth fur vergleichend Physiologie, 66: 257-272, 1970.

Kreithen M.L. and Quine D.B. Infrasound detection by the homing pigeon. J. Comp. Physiol., 129: 1-4, 1979.

Lysakowski A. and Goldberg J.M. Ultrastructural analysis of the cristae ampullares in the squirrel monkey (Saimiri sciureus). J. Comp. Neurol., 511: 47-64, 2008.

Mirjany M. and Faber D.S. Characteristics of the anterior lateral line nerve input to the Mauthner cell. J. Exp. Biol., 214: 3368-3377, 2011.

Mirjany M., Preuss T., Faber D.S. Role of the lateral line mechanosensory system in directionality of goldfish auditory evoked escape response. J. Exp. Biol., 214: 3358-3367, 2011.

Nadol J.B. Jr. Reciprocal synapses at the base of outer hair cells in the organ of Corti of man. Ann. Otol. Rhinol. Laryngol., 90: 12-17, 1981.

Nadol J.B. Jr. Incidence of reciprocal synapses on outer hair cells of the human organ of Corti. Ann. Otol. Rhinol. Laryngol., 93: 247-250, 1984.

Nadol J.B. Jr. and Burgess B.J. Morphology of synapses at the base of hair cells in the organ of Corti of the chimpanzee. Ann. Otol. Rhinol. Laryngol., 99: 215-220, 1990.

Nagai T. Innervation of the tympanic membrane. Acta Otorhinolaryngol. Belg., 49: 117-120, 1995.

Nakajima Y. and Wang D.W. Morphology of afferent and efferent synapses in hearing organ of the goldfish. J. Comp. Neurol., 156: 403-416, 1974.

Neeser J.A. and von Bartheld C.S. Comparative anatomy of the paratympanic organ (Vitali organ) in the middle ear of birds and non-avian vertebrates: focus on alligators, parakeets and armadillos. Brain Behav. Evol., 60: 65-79, 2002.

O'Neill P., Mak S.S., Fritzsch B., Ladher R.K., Baker C.V. The amniote paratympanic organ develops from a previously undiscovered sensory placode. Nat. Commun., 3: 1041, 2012.

Quine D.B. and Kreithen M.L. Frequency Shift Discrimination: Can Homing Pigeons Locate lnfrasounds by Doppler Shifts? J. Comp. Physiol., 141: 153-155, 1981.

Quine D.B. Infrasounds: a potential navigational cue for homing pigeons. pp. 373-376. In: Papi F., Wallraff H.G. (Eds.). Avian Navigation. Berlin, Springer, Heidelberg, 1982.

Radford C.A. and Mensinger A.F. Anterior lateral line nerve encoding to tones and play-back vocalisations in free-swimming oyster toadfish, Opsanus tau. J. Exp. Biol., 217: 1570-1579, 2014.

Rockley T.J. and Hawke W.M. The middle ear as a baroreceptor. Acta Otolaryngol., 112: 816-823, 1992.

Ross M.D., Roger C.M., Donovan K.M. Innervation patterns in rat saccular macula. A structural basis for complex sensory processing. Acta Otolaryngol., 102: 75-86, 1986.

Ross M.D. Morphological evidence for local microcircuits in rat vestibular macula. J. Comp. Neurol., 379: 333-346, 1997.

Ruffoli R., Giambelluca M.A., Giannessi F. Ultrastructure of the supporting cells in the paratympanic organ of chicken, Gallus gallus domesticus. J. Morphol., 236: 65-73, 1998.

Sato M., Henson M.M., Smith D.W. Synaptic specializations associated with the outer hair cells of the Japanese macaque. Hear Res., 108: 46-54, 1997.

Schermuly L. and Klinke R. Infrasound sensitive neurones in the pigeon cochlear ganglion. J. Comp. Physiol., 166: 355-363, 1990.

Simmons D.D., Bertolotto C., Narins P.M. Morphological gradients in sensory hair cells of the amphibian papilla of the frog. Hear Res., 80: 71-78, 1994.

Simmons D.D. Development of the inner ear efferent system across vertebrate species. J. Neurobiol., 53: 228-250, 2002.

Sobkowicz H.M., Slapnick S.M., August B.K. Reciprocal synapses between inner hair cell spines and afferent dendrites in the organ of Corti of the mouse. Synapse, 50: 53-66, 2003.

Sobkowicz H.M., August B.K., Slapnick S.M. Synaptic arrangements between inner hair cells and tunnel fiber in the mouse cochlea. Synapse, 15: 299-315, 2004.

Spoendlin H. and Schrott A. The spiral ganglion and the innervation of the human organ of Corti. Acta Otolaryngol., 105: 403-410, 1988.

Theurich M., Langner G., Scheich H. Infrasound responses in the midbrain of the guinea fowl. Neurosci. Lett., 49: 81-86, 1984.

Thiers F.A., Nadol J.B. Jr., Liberman M.C. Reciprocal synapses between outer hair cells and their afferent terminals: evidence for a local neural network in the mammalian cochlea. J. Assoc. Res. Otolaryngol., 9: 477-489, 2008.

Vitali G. Di un interessante derivato dell’ectoderma della prima fessura branchiale nel passero. Un organo nervoso di senso nell’orecchio medio degli uccelli. Anat. Anz., 40: 631-639, 1912.

Vitali G. Di un nuovo organo nervoso di senso nell’orecchio medio degli uccelli. Ulteriore destino dell’organo della prima fessura branchiale. Int. Mschr. Anat. Physiol., 30: 363-428, 1913.

Vitali G. Sur les troubles fonctionnels et sur les lesions histologiques dépendant de la destruction de l’organe nerveux de sense que j’ai décrit dans l’oreille moyenne des oiseaux. Arch. It. Biol., 64: 17-44, 1915.

Vitali G. L’organo nervoso paratimpanico e la sua funzione. Riv. Biol., 3: 302-316, 1921.

von Bartheld C.S. Development and innervation of the paratympanic organ (Vitali organ) in chick embryos. Brain Behav. Evol., 35: 1-15, 1990.

von Bartheld C.S. Functional morphology of the paratympanic organ in the middle ear of birds. Brain Behav. Evol., 44: 61-73, 1994.

von Bartheld C.S. and Giannessi F. The paratympanic organ: a barometer and altimeter in the middle ear of birds? J. Exp. Zool. B. Mol. Dev. Evol., 316: 402-408, 2011.

Yodlowski M.L., Kreithen M.L., Keeton W.T. Detection of atmospheric infrasound by homing pigeons. Nature, 265: 725-726, 1977.

Zetes D.E. and Steele C.R. Fluid-structure interaction of the stereocilia bundle in relation to mechanotransduction. J. Acoust. Soc. Am., 101: 3593-3601, 1997.


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