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

Abstract

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.

From shared lineage to distinct functions: the development of the inner ear and epibranchial placodes

“…Some clear examples can also be found in terrestrial vertebrates. In birds, for example, the first epibranchial placode (geniculate) generates the paratympanic organ (PTO), which is a small baroreceptor located in the middle ear that is thought to act as an altimeter during flight (D'Amico-Martel and Noden, 1983;von Bartheld, 1990;von Bartheld, 1994;Nesser and von Bartheld, 2002). Importantly, it contains mechanosensory hair cells similar to those of the inner ear (Giannessi and Ruffoli, 1996), and is innervated by neurons of the geniculate ganglion (von Bartheld, 1990).…”

Comparative Anatomy of the Paratympanic Organ (Vitali Organ) in the Middle Ear of Birds and Non-Avian Vertebrates: Focus on Alligators, Parakeets and Armadillos

“…In the avian PTO, the sensory epithelium is innervated by afferent ganglion cells located in the facial ganglion that project to the facial/vestibular brainstem [von Bartheld, 1990] as well as efferent neurons in the vicinity of the facial motor nucleus [von Bartheld, 1994]. To determine if the hair cells in the alligator PTO are innervated, the lipophilic fluorescent tracer DiI was applied to the vestibular brainstem, and 3 months later, the middle ear was sectioned and analyzed for DiI-labeled fibers and terminals.…”

“…Nevertheless, some regression does not preclude the possibility that the PTO still has a functional role in reptiles. The primary role is probably the detection of changes in barometric or hydrostatic pressure as suggested in fishes for the spiracular sense organ (SSO) and in birds for the PTO [Ranzi, 1926;von Bartheld, 1994]. The crocodilian middle ear is not thought to flood when the head is submerged in water [Wever, 1978], similar to aquatic birds that contain welldeveloped PTOs, presumably for detection of hydrostatic pressure [Vitali, 1941].…”

“…Neither owls nor parakeets have a lifestyle that would make PTOs particularly advantageous, unlike small birds that rely on barometric information for weather changes and upcoming (winter) storms [Buttemer, 1985]. Migratory birds might require barometers for choosing favorable weather conditions [Kreithen and Keeton, 1974] and could utilize the PTO as an altimeter to maintain altitudes when flying considerable distances at night or in cloud cover [Griffin, 1969;Kreithen and Keeton, 1974;von Bartheld, 1994]. Absence of a PTO in owls and parakeets may present no major disadvantage, owing to the lifestyles of these birds that do not migrate and do not need to change their behavior much with upcoming winterstorms, unlike smaller birds whose life might depend on a functional PTO [Buttemer, 1985].…”

“…Thus, it is likely that with changing functions of the hyomandibula/columella from breathing assistance to hearing assistance, the associated sense organ underwent its first change in function. In birds, the PTO appears to have undergone a second transformation into an organ with the possible function of detection of barometric pressure [Vitali, 1921[Vitali, , 1941Ranzi, 1926;Federici, 1927;Griffin, 1969;Delius and Emmerton, 1978;Jørgensen, 1984;Giannessi and Pera, 1986;von Bartheld, 1994], and it is possibly used in addition as an 'altimeter' in some birds [Griffin, 1969;Kreithen and Keeton, 1974;von Bartheld, 1990von Bartheld, , 1994.…”