The middle ear is part of the ear in all terrestrial vertebrates. It provides an interface between two media, air and fluid. How does it work? In mammals, the middle ear is traditionally described as increasing gain due to Helmholtz’s hydraulic analogy and the lever action of the malleus-incus complex: in effect, an impedance transformer. The conical shape of the eardrum and a frequency-dependent synovial joint function for the ossicles suggest a greater complexity of function than the traditional view. Here we review acoustico-mechanical measurements of middle ear function and the development of middle ear models based on these measurements. We observe that an impedance-matching mechanism (reducing reflection) rather than an impedance transformer (providing gain) best explains experimental findings. We conclude by considering some outstanding questions about middle ear function, recognizing that we are still learning how the middle ear works.
more »
« less
A monotreme-like auditory apparatus in a Middle Jurassic haramiyidan
Among extant vertebrates, mammals are distinguished by having a chain of three auditory ossicles (the malleus, incus and stapes) that transduce sound waves and promote an increased range of audible—especially high—frequencies. By contrast, the homologous bones in early fossil mammals and relatives also functioned in chewing through their bony attachments to the lower jaw. Recent discoveries of well-preserved Mesozoic mammals have provided glimpses into the transition from the dual (masticatory and auditory) to the single auditory function for the ossicles, which is now widely accepted to have occurred at least three times in mammal evolution. Here we report a skull and postcranium that we refer to the haramiyidan Vilevolodon diplomylos (dating to the Middle Jurassic epoch (160 million years ago)) and that shows excellent preservation of the malleus, incus and ectotympanic (which supports the tympanic membrane). After comparing this fossil with other Mesozoic and extant mammals, we propose that the overlapping incudomallear articulation found in this and other Mesozoic fossils, in extant monotremes and in early ontogeny in extant marsupials and placentals is a morphology that evolved in several groups of mammals in the transition from the dual to the single function for the ossicles.
more »
« less
- Award ID(s):
- 1654949
- PAR ID:
- 10248811
- Date Published:
- Journal Name:
- Nature
- Volume:
- 590
- ISSN:
- 0028-0836
- Page Range / eLocation ID:
- 279-283
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
ABSTRACT The study of primate auditory morphology is a significant area of interest for comparative anatomists, given the phylogenetic relationships that link primate hearing and the morphology of these auditory structures. Extensive literature addresses the form‐to‐function relationship of the auditory system (outer, middle, and inner ear) in primates and, by extension, provides insight into the auditory system of extinct primates and even modern humans. We add to this literature by describing the ontogenetic trajectory of the middle ear cavity and ossicular chain (malleus, incus, and stapes) due to their critical role in relaying auditory stimuli for interpretation. We examined middle ear morphology in neonatal primates and adult primates using a taxonomically broad sample. We focused primarily on nocturnal primate taxa (Daubentonia,Loris,Galago,Aotus, andTarsier), which are underrepresented in the literature. However, we also included three diurnal taxa (Macaca,Lemur, andSaguinus). Using 3D Slicer, we visualized middle ear structures in three dimensions using conventional micro CT data informed by diffusible iodine‐based contrast‐enhanced CT (diceCT) data. We illustrated how spatial relationships between otic elements, such as the various epitympanic sinuses of the middle ear and the auditory ossicles, vary throughout ontogeny. Our major findings include that the central tympanic cavity scaled with negative allometry in all taxa and that the accessory cavities scaled with isometry or positive allometry in most taxa. Despite these changes in chamber size, the size of the ear ossicles remained relatively consistent through ontogeny in most taxa. We confirmed our expectation that anthropoids exhibit an increase in the complexity of accessory cavities throughout ontogeny, mirroring the exponential pneumatization of the face in anthropoids. These findings provide an ontogenetic perspective and reveal further functional complexities of the middle ear as a conduit for sound proliferation and as a pressure regulator.more » « less
-
The end-Cretaceous extinction triggered the collapse of ecosystems and a drastic turnover of mammalian communities. During the Mesozoic, mammals were ecologically diverse, but less so than extant species. Modern ecological richness was established by the Eocene, but questions remain about the ecology of the first wave of mammals radiating after the extinction.Postcranial fossils are often used to determine locomotor behavior; however, the semicircular canals of theinner ear also represent a reliable proxy. These canals detect the angular acceleration of the head duringl ocomotion and transmit neuronal signals to the brain to allow stabilization of the eyes and head. Accordingly, vestibular sensitivity to rapid rotational head movements is higher in species with a larger canal radius of curvature and more orthogonal canals. We used high-resolution computed tomography scanning to obtain inner ear virtual endocasts for 30 specimens. We supplemented these with data from the literature to constructa database of 79 fossil from the Jurassic to the Eocene and 262 extant mammals. We compared data on canal morphology and another lifestyle proxy, the size of the petrosal lobules, which have a role in maintaining eyes’ movements and position. We find that Paleocene mammals exhibited a lower average and more constricted range of Agility Indices (AI), a new measure of canal radius size relative to body size, compared to Mesozoic, Eocene and extant taxa. Inthe early Paleocene, body mass and canal radius increased, but the former outpaced the latter leading to an AIdecline. Similarly, their petrosal lobules were relatively smaller on average compared to other temporal groups, which suggests less ability for fast movements. Additionally, Paleocene mammals had similar AIs to extant scansorial and terrestrial quadrupeds. In contrast, the lack of canal orthogonality change from the Mesozoic to the Paleocene indicates no trend toward lower vestibular sensitivity regardless of changes in body size. This result may reflect functional differences between canal orthogonality and radius size. Our results support previous work on tarsal morphology and locomotor behavior ancestral state reconstruction suggesting that ground dwelling mammals were more common than arboreal taxa during the Paleocene. Ultimately, this pattern may indicate that the collapse of forested environments immediately after extinction led to the preferential survivorship of more terrestrially adapted mammals.more » « less
-
The end-Cretaceous extinction triggered the collapse of ecosystems and a drastic turnover of mammalian communities. During the Mesozoic, mammals were ecologically diverse, but less so than extant species. Modern ecological richness was established by the Eocene, but questions remain about the ecology of the first wave of mammals radiating after the extinction.Postcranial fossils are often used to determine locomotor behavior; however, the semicircular canals of theinner ear also represent a reliable proxy. These canals detect the angular acceleration of the head duringl ocomotion and transmit neuronal signals to the brain to allow stabilization of the eyes and head. Accordingly, vestibular sensitivity to rapid rotational head movements is higher in species with a larger canal radius of curvature and more orthogonal canals. We used high-resolution computed tomography scanning to obtain inner ear virtual endocasts for 30 specimens. We supplemented these with data from the literature to constructa database of 79 fossil from the Jurassic to the Eocene and 262 extant mammals. We compared data on canal morphology and another lifestyle proxy, the size of the petrosal lobules, which have a role in maintaining eyes’ movements and position. We find that Paleocene mammals exhibited a lower average and more constricted range of Agility Indices (AI), a new measure of canal radius size relative to body size, compared to Mesozoic, Eocene and extant taxa. Inthe early Paleocene, body mass and canal radius increased, but the former outpaced the latter leading to an AIdecline. Similarly, their petrosal lobules were relatively smaller on average compared to other temporal groups, which suggests less ability for fast movements. Additionally, Paleocene mammals had similar AIs to extant scansorial and terrestrial quadrupeds. In contrast, the lack of canal orthogonality change from the Mesozoic to the Paleocene indicates no trend toward lower vestibular sensitivity regardless of changes in body size. This result may reflect functional differences between canal orthogonality and radius size. Our results support previous work on tarsal morphology and locomotor behavior ancestral state reconstruction suggesting that ground dwelling mammals were more common than arboreal taxa during the Paleocene. Ultimately, this pattern may indicate that the collapse of forested environments immediately after extinction led to the preferential survivorship of more terrestrially adapted mammals.more » « less
-
Abstract Two‐toed (Choloepus sp.) and three‐toed (Bradypus sp.) sloths possess short, rounded pisiforms that are rare among mammals and differ from other members of Xenarthra like the giant anteater (Myrmecophaga tridactyla) which retain elongated, rod‐like pisiforms in common with most mammals. Using photographs, radiographs, and μCT, we assessed ossification patterns in the pisiform and the paralogous tarsal, the calcaneus, for two‐toed sloths, three‐toed sloths, and giant anteaters to determine the process by which pisiform reduction occurs in sloths and compare it to other previously studied examples of pisiform reduction in humans and orangutans. Both extant sloth genera achieve pisiform reduction through the loss of a secondary ossification center and the likely disruption of the associated growth plate based on an unusually porous subchondral surface. This represents a third unique mechanism of pisiform reduction among mammals, along with primary ossification center loss in humans and retention of two ossification centers with likely reduced growth periods in orangutans. Given the remarkable similarities between two‐toed and three‐toed sloth pisiform ossification patterns and the presence of pisiform reduction in fossil sloths, extant sloth pisiform morphology does not appear to represent a recent convergent adaptation to suspensory locomotion, but instead is likely to be an ancestral trait of Folivora that emerged early in the radiation of extant and fossil sloths.more » « less
An official website of the United States government

