Paratympanic Organ Research Articles

Expression patterns of prosaposin and neurotransmitter-related molecules in the chick paratympanic organ

The paratympanic organ (PTO) is a small sense organ in the middle ear of birds that contains hair cells similar to those found in vestibuloauditory organs and receives afferent fibers from the geniculate ganglion. To consider the histochemical similarities between the PTO and vestibular hair cells, we examined the expression patterns of representative molecules in vestibular hair cells, including prosaposin, G protein-coupled receptor (GPR) 37 and GPR37L1 as prosaposin receptors, vesicular glutamate transporter (vGluT) 2 and vGluT3, nicotinic acetylcholine receptor subunit α9 (nAChRα9), and glutamic acid decarboxylase (GAD) 65 and GAD67, in the postnatal day 0 chick PTO and geniculate ganglion by in situ hybridization. Prosaposin mRNA was observed in PTO hair cells, supporting cells, and geniculate ganglion cells. vGluT3 mRNA was observed in PTO hair cells, whereas vGluT2 was observed in a small number of ganglion cells. nAChRα9 mRNA was observed in a small number of PTO hair cells. The results suggest that the histochemical character of PTO hair cells is more similar to that of vestibular hair cells than that of auditory hair cells in chicks.

The “Organ of flight”: Paratympanic Organ (PTO) of Vitali in Wild Birds as Biological Barometer-Altimeter

The “Organ of flight”: Paratympanic Organ (PTO) of Vitali in Wild Birds as Biological Barometer-Altimeter

Infrasonic hearing in birds: a review of audiometry and hypothesized structure-function relationships.

The perception of airborne infrasound (sounds below 20 Hz, inaudible to humans except at very high levels) has been documented in a handful of mammals and birds. While animals that produce vocalizations with infrasonic components (e.g. elephants) present conspicuous examples of potential use of infrasound in the context of communication, the extent to which airborne infrasound perception exists among terrestrial animals is unclear. Given that most infrasound in the environment arises from geophysical sources, many of which could be ecologically relevant, communication might not be the only use of infrasound by animals. Therefore, infrasound perception could be more common than currently realized. At least three bird species, each of which do not communicate using infrasound, are capable of detecting infrasound, but the associated auditory mechanisms are not well understood. Here we combine an evaluation of hearing measurements with anatomical observations to propose and evaluate hypotheses supporting avian infrasound detection. Environmental infrasound is mixed with non-acoustic pressure fluctuations that also occur at infrasonic frequencies. The ear can detect such non-acoustic pressure perturbations and therefore, distinguishing responses to infrasound from responses to non-acoustic perturbations presents a great challenge. Our review shows that infrasound could stimulate the ear through the middle ear (tympanic) route and by extratympanic routes bypassing the middle ear. While vibration velocities of the middle ear decline towards infrasonic frequencies, whole-body vibrations - which are normally much lower amplitude than that those of the middle ear in the 'audible' range (i.e. >20 Hz) - do not exhibit a similar decline and therefore may reach vibration magnitudes comparable to the middle ear at infrasonic frequencies. Low stiffness in the middle and inner ear is expected to aid infrasound transmission. In the middle ear, this could be achieved by large air cavities in the skull connected to the middle ear and low stiffness of middle ear structures; in the inner ear, the stiffness of round windows and cochlear partitions are key factors. Within the inner ear, the sizes of the helicotrema and cochlear aqueduct are expected to play important roles in shunting low-frequency vibrations away from low-frequency hair-cell sensors in the cochlea. The basilar papilla, the auditory organ in birds, responds to infrasound in some species, and in pigeons, infrasonic-sensitive neurons were traced back to the apical, abneural end of the basilar papilla. Vestibular organs and the paratympanic organ, a hair cell organ outside of the inner ear, are additional untested candidates for infrasound detection in birds. In summary, this review brings together evidence to create a hypothetical framework for infrasonic hearing mechanisms in birds and other animals.

Chicken embryos share mammalian patterns of apoptosis in the posterior placodal area.

In the posterior placodal area (PPA) of C57BL/6N mice and primate-related Tupaia belangeri (Scandentia), apoptosis helps to establish morphologically separated otic and epibranchial placodes. Here, we demonstrate that basically identical patterns of apoptosis pass rostrocaudally through the Pax2+ PPA of chicken embryos. Interplacodal apoptosis eliminates unneeded cells either between the otic anlage and the epibranchial placodes 1, 2 and/or 3, respectively (type A), or between neighbouring epibranchial placodes (type B). These observations support the idea that in chicken embryos, as in mammals, interplacodal apoptosis serves to remove vestigial lateral line placodes (Washausen & Knabe, 2018, Biol Open 7, bio031815). A special case represents the recently discovered Pax2- /Sox2+ paratympanic organ (PTO) placode that has been postulated to be molecularly distinct from and developmentally independent of the ventrally adjacent first epibranchial (or 'geniculate') placode (O'Neill etal. 2012, Nat Commun 3, 1041). We show that Sox2+ (PTO placodal) cells seem to segregate from the Pax2+ geniculate placode, and that absence of Pax2 in the mature PTO placode is due to secondary loss. We further report that, between Hamburger-Hamilton (HH) stages HH14 and HH26, apoptosis in the combined anlage of the first epibranchial and PTO placodes is almost exclusively found within and/or immediately adjacent to the dorsally located PTO placode. Hence, apoptosis appears to support decision-making processes among precursor cells of the early developing PTO placode and, later, regression of the epibranchial placodes 2 and 3.

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

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.

Giovanni Vitali: Discoverer of the paratympanic organ

One-hundred years ago, the Italian anatomist Giovanni Vitali reported the discovery of the paratympanic organ, a sense organ in the middle ear of birds, in two issues of the Anatomischer Anzeiger (1911, 1912). In this minireview, we summarize Vitali's biography, and examine the scientific impact of his discovery of this sense organ. We also compile – for the first time – the entire bibliography of published papers on the paratympanic organ. Vitali described the ontogenetic development of this sense organ, examined its distribution among species, recognized its evolutionary relationship with the spiracular sense organ of fishes, and he developed the theory that it functions as a detector of changes in air pressure. He was the first to postulate that the paratympanic and spiracular sense organs were homologous organs that originate from homologous placodes – currently a hotly debated topic. His morphological work indicating the sensory nature of the PTO was validated by subsequent ultrastructural studies. Vitali's discovery of the paratympanic organ prompted his nomination for the Nobel Prize in 1934. Nevertheless, the paratympanic organ and the presumed barometric sense of hundreds of billions of living birds have failed to receive the recognition they deserve. Conclusive evidence of the function of the paratympanic organ remains a formidable challenge in vertebrate sensory physiology.

The amniote paratympanic organ develops from a previously undiscovered sensory placode

The paratympanic organ (PTO), a mechanosensory hair cell-containing pouch in the amniote middle ear, was first described 100 years ago yet its origins remain unresolved. Homology with the anamniote spiracular organ is supported by association with homologous skeletal elements and similar central targets of afferent neurons, suggesting it might be a remnant of the water-dependent lateral line system, otherwise lost during the amniote transition to terrestrial life. However, this is incompatible with studies suggesting it arises from the first epibranchial (geniculate) placode. Here we show that a previously undiscovered Sox2-positive placode, immediately dorsal to the geniculate placode, forms the PTO and its afferent neurons, which are molecularly and morphologically distinct from geniculate neurons. These data remove the only obstacle to accepting the homology of the PTO and spiracular organ. We hypothesise that the PTO/spiracular organ represents an ancient head ectoderm module, developmentally and evolutionarily independent of both lateral line and epibranchial placodes.

The paratympanic organ: a barometer and altimeter in the middle ear of birds?

A century has passed since the discovery of the paratympanic organ (PTO), a mechanoreceptive sense organ in the middle ear of birds and other tetrapods. This luminal organ contains a sensory epithelium with typical mechanosensory hair cells and may function as a barometer and altimeter. The organ is arguably the most neglected sense organ in living tetrapods. The PTO is believed to be homologous to a lateral line sense organ, the spiracular sense organ of nonteleostean fishes. Our review summarizes the current state of knowledge of the PTO and draws attention to the astounding lack of information about the unique and largely unexplored sensory modality of barometric perception.

09-P084 A role for BMP signalling in paratympanic organ development

09-P084 A role for BMP signalling in paratympanic organ development

Lateral line, otic and epibranchial placodes: developmental and evolutionary links?

Two embryonic cell populations, the neural crest and cranial ectodermal placodes, between them give rise to many of the unique characters of vertebrates. Neurogenic placode derivatives are vital for sensing both external and internal stimuli. In this speculative review, we discuss potential developmental and evolutionary relationships between two placode series that are usually considered to be entirely independent: lateral line placodes, which form the mechanosensory and electroreceptive hair cells of the anamniote lateral line system as well as their afferent neurons, and epibranchial placodes (geniculate, petrosal and nodose), which form Phox2b(+) visceral sensory neurons with input from both the external and internal environment. We illustrate their development using molecular data we recently obtained in shark embryos, and we describe their derivatives, including the possible geniculate placode origin of a mechanosensory sense organ associated with the first pharyngeal pouch/cleft (the anamniote spiracular organ/amniote paratympanic organ). We discuss how both lateral line and epibranchial placodes can be related in different ways to the otic placode (which forms the inner ear and its afferent neurons), and how both are important for protective somatic reflexes. Finally, we put forward a highly speculative proposal about the original function of the cells whose evolutionary descendants today include the derivatives of the lateral line, otic and epibranchial placodes, namely that they produced sensory receptors and neurons for Phox2b-dependent protective reflex circuits. We hope this review will stimulate both debate and a fresh look at possible developmental and evolutionary relationships between these seemingly disparate and independent placodes.

Class III ?-tubulin expression in sensory and nonsensory regions of the developing avian inner ear

A previous study showed that class III beta-tubulin, a widely used neuron-specific marker, is expressed in mature and regenerating hair cells but not the support cells of the avian inner ear. We investigated the expression of this marker in the developing avian inner ear. We found that class III beta-tubulin is not neuron-specific in the avian embryo, but appears to accumulate in neuronal cell types, including hair cells, about the time of their differentiation. In the developing inner ear, some degree of class III beta-tubulin immunoreactivity is found in all regions of the otic epithelium from its formation as the otic placode (stage 10 [embryonic day, E1.5]) until about stage 21 (E3.5), when the prospective tegmentum vasculosum begins to lose its staining. By stage 35 (E8-9), most of the nonsensory epithelia have lost their class III beta-tubulin staining, leaving distinct regions of staining between the morphological compartments of the inner ear. Concurrent with the loss of staining from nonsensory regions, the hair cells of the sensory epithelia accumulate class III beta-tubulin, whereas the supporting cells decrease their staining. We also observed a similar pattern of development in another hair cell organ, the paratympanic organ. Double labeling with the 275 kD hair cell antigen (HCA) indicated that the majority of hair cells identifiable with class III beta-tubulin are HCA-positive. Additionally, presumptive hair cells were identified which were not within defined sensory epithelia. Our findings show that class III beta-tubulin can be used as an early marker for hair cell differentiation in all hair cell sensory epithelia in the chicken.

Ultrastructure of the supporting cells in the paratympanic organ of chicken, Gallus gallus domesticus

The paratympanic organ is a specialized sensory organ of birds located in the medial wall of the tympanic cavity. It possesses a sensory epithelium formed by type II hair cells and supporting cells. The supporting cells are tall, narrow units that extend from the basement membrane to the free epithelial surface. They show a fine structure characterized by numerous mitochondria, a conspicuous Golgi complex and a well-developed RER. Moreover, some uncommon structures, probably formed by heaped RER cisternae, are frequently present in the cytoplasm. Adjacent supporting cells are connected by numerous and extensive gap junctions; moreover, small gap junctions between hair cell and supporting cells are to be found. The possible mechanical and metabolical functions of the paratympanic organ supporting cells are discussed. J. Morphol. 236:65–73, 1998. © 1998 Wiley-Liss, Inc.

Ultrastructure of the supporting cells in the paratympanic organ of chicken, Gallus gallus domesticus.

The paratympanic organ is a specialized sensory organ of birds located in the medial wall of the tympanic cavity. It possesses a sensory epithelium formed by type II hair cells and supporting cells. The supporting cells are tall, narrow units that extend from the basement membrane to the free epithelial surface. They show a fine structure characterized by numerous mitochondria, a conspicuous Golgi complex and a well-developed RER. Moreover, some uncommon structures, probably formed by heaped RER cisternae, are frequently present in the cytoplasm. Adjacent supporting cells are connected by numerous and extensive gap junctions; moreover, small gap junctions between hair cell and supporting cells are to be found. The possible mechanical and metabolical functions of the paratympanic organ supporting cells are discussed.

Homing experiments on pigeons subjected to bilateral destruction of the paratympanic organ

The paratympanic organ (PO) in birds is a specialised sensory organ whose function is still unknown. G. Vitali, who first described the PO from observations of the behaviour of PO-lesioned pigeons, proposed that this organ was needed to maintain normal wing muscle function and called it the 'organ of flight'. This interpretation has since been disputed. To solve this controversy and to test whether the PO is involved in flight and navigation, we performed release tests on homing pigeons subjected to bilateral destruction of this organ. No impairment of either flight or navigation was observed in the lesioned pigeons.

The ultrastructure of the sensory hairs of the paratympanic organ receptor cells in chicken.

The hair bundle of the receptor cells in the paratympanic organ of the chicken was studied by TEM, after fixation in aldehydes/osmium tetroxide or in aldehydes/osmium tetroxide/tannic acid. The bundles are formed by a kinocilium and by 40-70 stereocilia. The stereocilia are linked to each other by an extensive network of filaments. Three types of these connectors are present: basal, shaft and apical; the latter consist of side-to-side and tip-to-side connectors. We observed that the shaft connectors are well-highlighted only when tannic acid was used, while the other connectors are to be found in the conventionally fixed specimens also. The tip-to-side connector consists of a filament which joins the tip of a stereocilium with the side of an adjacent taller stereocilium; we suggest that the distortion of this filament would give rise to the mechanosensory transduction. The other connectors probably serve to maintain the regular spatial arrangement of the hair bundle and the mechanical coupling of the stereocilia. Our study shows that the general conformation of the hair bundle and the stereociliary links of the hair cells in the paratympanic organ of chicken are similar to those previously described in the hair cells of the acoustico lateralis system.

Fine structure of the afferent synapses in the paratympanic organ of the chicken, with special reference to the synaptic bodies

The afferent synapses of the paratympanic organ in the chicken were studied by TEM. These synapses were formed by non-myelinated fibres which reached the basal part of the hair cells. The fibres contained a number of irregular mitochondria and a few pale vesicles. In the hair cells, near the presynaptic membrane, typical synaptic bodies formed by an electron-dense core surrounded by several small pale vesicles were present. The core was connected with the vesicles by numerous thin filaments, and at same time with the presynaptic membrane by some dense projections. Moreover, we have observed that the connections between the core and the adjacent vesicles also consisted of similar structures to the dense projections. We suggest that this device is involved in the movement of the vesicles towards the presynaptic membrane. Our hypothesis is in agreement with that formulated by some authors who believe that the electron-dense core of the synaptic bodies is able to channel the vesicles to the presynaptic membrane (conveyor-belt hypothesis). Moreover, our work showed that the synaptic bodies of the paratympanic organ in the chicken are variable in density and in shape. These morphological aspects might be linked to regression-reconstitution cycles of the SBs and to the functional level of the afferent synapses.

Functional Morphology of the Paratympanic Organ in the Middle Ear of Birds

The paratympanic organ (PTO) is a small sense organ in the middle ear of birds. This luminal organ contains mechanoreceptors (hair cells) with afferent and efferent innervation and may function as a baroreceptor. The hypothesis that elastic ligaments of the middle ear may be involved in the transduction of barometric pressure was tested. Two elastic ligaments are shown to attach to the PTO. The columellar-squamosal ('Platner's') ligament inserts at its caudal pole; the superior portion of the superior drum-tubal ligament attaches at the rostral tip of the organ. To determine if pressure to the tympanic membrane and tension of ligaments may cause lumen changes in the PTO, the length of elastic ligaments, and the length, volume and configuration of the PTO were measured in normal animals and in animals following application of positive or negative pressure to the tympanic membrane. The rostral pole of the PTO changes its shape differentially as a function of the tension of the superior drum-tubal ligament, resulting in volume shifts of about 10% of the total volume in the PTO. With negative pressure, volume moves from the rostral pole to the caudal half of the PTO; with positive pressure, volume shifts rostrally. Displacement of fluid in the lumen of the PTO thus may stimulate the paratympanic hair cells. Tracing of efferent projections to the PTO with the fluorescent compound DiI reveals a cluster of about 40 labeled neurons at the caudal pole of the ventral facial motor nucleus adjacent to the superior olive. These findings support the notion that the PTO may be part of a neural circuit that controls the position of the tympanic membrane and may mediate barometric perception in birds.

Development and Innervation of the Paratympanic Organ (Vitali Organ) in Chick Embryos

The paratympanic organ (Vitali organ) is a small sensory organ in the middle ear of birds. It possesses a sensory epithelium with hair cells similar to those of the inner ear. Injections of fluorescent carbocyanine tracers into the paratympanic organ of 9- to 11-day-old chick embryos labeled ganglion cells in the facial ganglia. Paratympanic nerve fibers enter the brainstem with the facial nerve but proceed to vestibular brainstem nuclei. A dorsal branch terminates in ventral areas of the cerebellum, while a ventral component projects to the descending vestibular nucleus, with some fibers turning medially into lateral parts of the medial vestibular nucleus. No fibers were labeled in the motor or sensory facial nucleus or in auditory brainstem nuclei. This projection pattern suggests a function of the paratympanic organ in equilibrium rather than audition. Projections similar to those of the paratympanic nerve have been reported for the lagenar nerve. Immunocytochemical techniques using an antiserum to gamma-aminobutyric acid (GABA) demonstrate that hair cells in the paratympanic organ develop GABA immunoreactivity at 5 days of incubation (E5), 2-4 days earlier than GABA immunoreactivity can be detected in hair cells of the inner ear, i.e. in the saccule (E6.5-7.0), the utricle (E7), the cristae (E8-9) and the cochlea (E9-9.5). Afferent fibers that are transiently GABAergic are rare in the paratympanic organ (1-2 fibers), though present from E6 to E7.5. The early onset of GABA immunoreactivity in the paratympanic organ may indicate that this organ matures (and possibly functions) earlier in ontogenetic development than its counterparts located in the inner ear. The present findings are consistent with the hypothesis that the paratympanic organ is homologous with the spiracular sense organ of fishes. The paratympanic organ of birds may represent a sense organ that is derived phylogenetically and ontogenetically from the lateral-line system.

On the presence of reciprocal synapses in the paratympanic organ of the chicken.

The innervation pattern of the paratympanic organ was studied by TEM. The paraympanic organ is a small tapering vesicle, typical of birds, situated in the medial wall of the tympanic cavity; it contains hair cells which are similar to type II receptors of the acoustic-lateral system; these cells are characterised by synapses which are not only afferent and efferent, as previously described, but also reciprocal with efferent fibers. Our observation revealed some efferent nerve fibers which form a relationship with hair cells containing synaptic bodies situated next to the plasma membrane and near the fibers themselves. Since synaptic bodies are commonly considered to be the site where the transmission of the impulse from the receptor to the nerve fiber takes place, our pictures suggest that the efferent fibers and hair cells may be either presynaptic or postsynaptic with respect to each other in the paratympanic organ. The hypothesis is formulated that reciprocal synapses allow interaction between hair cells, thus determining an increase in the contrast of information sent by the paratympanic organ to the CNS.

Fine Structure of The Paratympanic Organ in the Avian Middle Ear

AbstractLight and electron microscopical examination of the paratympanic organ of 8 avian species reveals a sensory epithelium with hair cells and supporting cells, covered by a gelatinous cupula with numerous non‐crystalline deposits. The position of the organ is in agreement with previous suggestions of its function as an air pressure detector.