Cochlea The cochlea is the part of the inner ear involved in hearing. It is a spiral-shaped cavity in the bony labyrinth, in humans making 2.75 turns around its axis, the modiolus. A core component of the cochlea is the Organ of Corti, the sensory or ...

is Latin for “snail, shell or screw” and originates from the Greek word κοχλίας ''kokhlias''. The modern definition, the auditory portion of the inner ear, originated in the late 17th century. Within the mammalian cochlea exists the

organ of Corti The organ of Corti, or spiral organ, is the receptor organ for hearing and is located in the mammalian cochlea. This highly varied strip of epithelial cells allows for transduction of auditory signals into nerve impulses' action potential. Transd ...

, which contains

hair cell Hair cells are the sensory receptors of both the auditory system and the vestibular system in the ears of all vertebrates, and in the lateral line organ of fishes. Through mechanotransduction, hair cells detect movement in their environment. ...

s that are responsible for translating the vibrations it receives from surrounding fluid-filled ducts into electrical impulses that are sent to the

brain A brain is an organ that serves as the center of the nervous system in all vertebrate and most invertebrate animals. It is located in the head, usually close to the sensory organs for senses such as vision. It is the most complex organ in a ve ...

to process sound. This spiral-shaped cochlea is estimated to have originated during the early

Cretaceous Period The Cretaceous ( ) is a geological period that lasted from about 145 to 66 million years ago (Mya). It is the third and final period of the Mesozoic Era, as well as the longest. At around 79 million years, it is the longest geological period of t ...

, around 120 million years ago. Further, the auditory innervation of the spiral-shaped cochlea also traces back to the Cretaceous period. The

evolution Evolution is change in the heritable characteristics of biological populations over successive generations. These characteristics are the expressions of genes, which are passed on from parent to offspring during reproduction. Variation ...

of the human cochlea is a major area of scientific interest because of its favourable representation in the

fossil A fossil (from Classical Latin , ) is any preserved remains, impression, or trace of any once-living thing from a past geological age. Examples include bones, shells, exoskeletons, stone imprints of animals or microbes, objects preserved ...

record. During the last century, many scientists such as evolutionary biologists and

paleontologist Paleontology (), also spelled palaeontology or palæontology, is the scientific study of life that existed prior to, and sometimes including, the start of the Holocene epoch (roughly 11,700 years before present). It includes the study of fossi ...

s strove to develop new methods and techniques to overcome the many obstacles associated with working with ancient, delicate artifacts. In the past, scientists were limited in their ability to fully examine specimens without causing damage to them. In more recent times, technologies such as

micro-CT X-ray microtomography, like tomography and X-ray computed tomography, uses X-rays to create cross-sections of a physical object that can be used to recreate a virtual model (3D model) without destroying the original object. The prefix ''micro-'' ...

scanning became available. These technologies allow for the visual differentiation between fossilized animal materials and other sedimentary remains. With the use of

X-ray An X-ray, or, much less commonly, X-radiation, is a penetrating form of high-energy electromagnetic radiation. Most X-rays have a wavelength ranging from 10 picometers to 10 nanometers, corresponding to frequencies in the range 30&nb ...

technologies, it is possible to ascertain some information about the auditory capabilities of extinct creatures, giving insight to human ancestors as well as their contemporary species.

Comparative anatomy

While the basic structure of the inner ear in

lepidosaurs The Lepidosauria (, from Greek meaning ''scaled lizards'') is a subclass or superorder of reptiles, containing the orders Squamata and Rhynchocephalia. Squamata includes snakes, lizards, and amphisbaenians. Squamata contains over 9,000 species ...

(lizards and snakes),

archosaurs Archosauria () is a clade of diapsids, with birds and crocodilians as the only living representatives. Archosaurs are broadly classified as reptiles, in the cladistic sense of the term which includes birds. Extinct archosaurs include non-avia ...

(birds and crocodilians) and

mammals Mammals () are a group of vertebrate animals constituting the class Mammalia (), characterized by the presence of mammary glands which in females produce milk for feeding (nursing) their young, a neocortex (a region of the brain), fur o ...

is similar, and the organs are considered to be homologous, each group has a unique type of auditory organ. The hearing organ arose within the lagenar duct of stem reptiles, lying between the saccular and lagenar

epithelia Epithelium or epithelial tissue is one of the four basic types of animal tissue, along with connective tissue, muscle tissue and nervous tissue. It is a thin, continuous, protective layer of compactly packed cells with a little intercellula ...

. In lepidosaurs, the hearing organ, the basilar papilla, is generally small, with at most 2000 hair cells, whereas in archosaurs the basilar papilla can be much longer (>10mm in

owl Owls are birds from the order Strigiformes (), which includes over 200 species of mostly solitary and nocturnal birds of prey typified by an upright stance, a large, broad head, binocular vision, binaural hearing, sharp talons, and feathers a ...

s) and contain many more hair cells that show two typical size extremes, the short and the tall hair cells. In mammals, the structure is known as the

and shows a unique arrangement of hair cells and supporting cells. All mammalian organs of Corti contain a supporting tunnel made up of pillar cells, on the inner side of which there are inner hair cells and outer hair cells on the outer side. The definitive mammalian middle ear and the elongated cochlea allows for better sensitivity for higher frequencies.

Lepidosaurs

As in all lepidosaurs and archosaurs, the single-

ossicle The ossicles (also called auditory ossicles) are three bones in either middle ear that are among the smallest bones in the human body. They serve to transmit sounds from the air to the fluid-filled labyrinth (cochlea). The absence of the auditory ...

(columellar) middle ear transmits sound to the footplate of the

columella Lucius Junius Moderatus Columella (; Arabic: , 4 – ) was a prominent writer on agriculture in the Roman Empire. His ' in twelve volumes has been completely preserved and forms an important source on Roman agriculture, together with the wo ...

, which sends a pressure wave through the inner ear. In snakes, the basilar papilla is roughly 1mm long and only responds to frequencies below about 1 kHz. In contrast, lizards tend to have two areas of

s, one responding below and the other above 1 kHz. The upper frequency limit in most lizards is roughly 5–8 kHz. The longest lizard papillae are about 2mm long and contain 2000 hair cells and their afferent innervating fibers can be very sharply tuned to frequency.

Archosaurs

In birds and crocodilians, the similarity of the structure of the basilar papilla betrays their close evolutionary relationship. The basilar papilla is up to about 10mm long and contains up to 16,500 hair cells. While most birds have an upper hearing limit of only about 6 kHz, the barn owl can hear up to 12 kHz and thus close to the human upper limit.

Mammals

Egg-laying mammals, the monotremes (

echidna Echidnas (), sometimes known as spiny anteaters, are quill-covered monotremes (egg-laying mammals) belonging to the family Tachyglossidae . The four extant species of echidnas and the platypus are the only living mammals that lay eggs and the ...

and

platypus The platypus (''Ornithorhynchus anatinus''), sometimes referred to as the duck-billed platypus, is a semiaquatic, egg-laying mammal endemic to eastern Australia, including Tasmania. The platypus is the sole living representative or mono ...

), do not have a spiral cochlea, but one shaped more like a banana, up to about 7 mm long. Like in lepidosaurs and archosaurs, it contains a lagena, a vestibular sensory epithelium, at its tip. Only in

theria Theria (; Greek: , wild beast) is a subclass of mammals amongst the Theriiformes. Theria includes the eutherians (including the placental mammals) and the metatherians (including the marsupials) but excludes the egg-laying monotremes. ...

n mammals (

marsupial Marsupials are any members of the mammalian infraclass Marsupialia. All extant marsupials are endemic to Australasia, Wallacea and the Americas. A distinctive characteristic common to most of these species is that the young are carried in a ...

s and

placental Placental mammals (infraclass Placentalia ) are one of the three extant subdivisions of the class Mammalia, the other two being Monotremata and Marsupialia. Placentalia contains the vast majority of extant mammals, which are partly distinguishe ...

s) is the cochlea truly coiled 1.5 to 3.5 times. Whereas in monotremes there are many rows of both inner and outer hair cells in the organ of Corti, in therian (marsupial and placental) mammals the number of inner hair-cell rows is one, and there are generally only three rows of outer hair cells.

Amphibians

Amphibians have unique inner ear structures. There are two sensory papillae involved in hearing, the basilar (higher frequency) and amphibian (lower frequency) papillae, but it is uncertain whether either is homologous to the hearing organs of lepidosaurs, archosaurs and mammals and we have no idea when they arose.

Fish

Fish Fish are aquatic, craniate, gill-bearing animals that lack limbs with digits. Included in this definition are the living hagfish, lampreys, and cartilaginous and bony fish as well as various extinct related groups. Approximately 95% of ...

have no dedicated auditory epithelium, but use various

vestibular The Vestibular (from pt, vestíbulo, "entrance hall") is a competitive examination and is the primary and widespread entrance system used by Brazilian universities to select the students admitted. The Vestibular usually takes place from Nove ...

sensory organs that respond to sound. In most teleost fishes it is the saccular macula that responds to sound. In some, such as

goldfish The goldfish (''Carassius auratus'') is a freshwater fish in the family Cyprinidae of order Cypriniformes. It is commonly kept as a pet in indoor aquariums, and is one of the most popular aquarium fish. Goldfish released into the wild have bec ...

es, there is also a special bony connection to the gas bladder that increases sensitivity allowing hearing up to about 4 kHz.

Neanderthals to modern humans

The size of cochlea has been measured throughout its evolution based on the fossil record. In one study, the basal turn of the cochlea was measured, and it was hypothesized that cochlear size correlates with body mass. The size of the basal turn of the cochlea was not different in

Neanderthal Neanderthals (, also ''Homo neanderthalensis'' and erroneously ''Homo sapiens neanderthalensis''), also written as Neandertals, are an extinct species or subspecies of archaic humans who lived in Eurasia until about 40,000 years ago. While the ...

s and

Holocene The Holocene ( ) is the current geological epoch. It began approximately 11,650 cal years Before Present (), after the Last Glacial Period, which concluded with the Holocene glacial retreat. The Holocene and the preceding Pleistocene togeth ...

humans, however it became larger in early modern humans and

Upper Paleolithic The Upper Paleolithic (or Upper Palaeolithic) is the third and last subdivision of the Paleolithic or Old Stone Age. Very broadly, it dates to between 50,000 and 12,000 years ago (the beginning of the Holocene), according to some theories coin ...

humans. Furthermore, the position and orientation of the cochlea is similar between Neanderthals and Holocene humans, relative to plane of the lateral canal, whereas early modern and upper Paleolithic humans have a more superiorly placed cochlea than Holocene humans. When comparing hominins of the

Middle Pleistocene The Chibanian, widely known by its previous designation of Middle Pleistocene, is an age in the international geologic timescale or a stage in chronostratigraphy, being a division of the Pleistocene Epoch within the ongoing Quaternary Period. Th ...

, Neanderthals and Holocene humans, the apex of the cochlea faces more inferiorly in the

hominin The Hominini form a taxonomic tribe of the subfamily Homininae ("hominines"). Hominini includes the extant genera ''Homo'' (humans) and '' Pan'' (chimpanzees and bonobos) and in standard usage excludes the genus ''Gorilla'' (gorillas). The ...

s than the latter two groups. Finally, the cochlea of European middle Pleistocene hominins faces more inferiorly than Neanderthals, modern humans, and Homo erectus. Human beings, along with

ape Apes (collectively Hominoidea ) are a clade of Old World simians native to sub-Saharan Africa and Southeast Asia (though they were more widespread in Africa, most of Asia, and as well as Europe in prehistory), which together with its sister g ...

s, are the only mammals that do not have high frequency (>32 kHz) hearing. Humans have long cochleae, but the space devoted to each frequency range is quite large (2.5mm per octave), resulting in a comparatively reduced upper frequency limit. The human cochlea has approximately 2.5 turns around the modiolus (the axis). Humans, like many mammals and birds, are able to perceive auditory signals that displace the eardrum by a mere picometre.

The ear

Because of its prominence and preserved state in the fossil record, until recently, the ear had been used to determine

phylogeny A phylogenetic tree (also phylogeny or evolutionary tree Felsenstein J. (2004). ''Inferring Phylogenies'' Sinauer Associates: Sunderland, MA.) is a branching diagram or a tree showing the evolutionary relationships among various biological spe ...

. The ear itself contains different portions, including the

outer ear The outer ear, external ear, or auris externa is the external part of the ear, which consists of the auricle (also pinna) and the ear canal. It gathers sound energy and focuses it on the eardrum (tympanic membrane). Structure Auricle Th ...

, the

middle ear The middle ear is the portion of the ear medial to the eardrum, and distal to the oval window of the cochlea (of the inner ear). The mammalian middle ear contains three ossicles, which transfer the vibrations of the eardrum into waves in the ...

, and the inner ear and all of these show evolutionary changes that are often unique to each lineage 4 It was the independent evolution of a tympanic middle ear in the

Triassic period The Triassic ( ) is a geologic period and system which spans 50.6 million years from the end of the Permian Period 251.902 million years ago ( Mya), to the beginning of the Jurassic Period 201.36 Mya. The Triassic is the first and shortest period ...

that produced strong selection pressures towards improved hearing organs in the separate lineages of land

vertebrate Vertebrates () comprise all animal taxa within the subphylum Vertebrata () (chordates with backbones), including all mammals, birds, reptiles, amphibians, and fish. Vertebrates represent the overwhelming majority of the phylum Chordata, with c ...

Evolutionary perspective

The cochlea is the tri-chambered auditory detection portion of the ear, consisting of the

scala media Scala or SCALA may refer to: Automobiles * Renault Scala, multiple automobile models * Škoda Scala, a Czech compact hatchback Music * Scala (band), an English electronic music group * Escala (group), an electronic string quartet formerly known ...

, the

scala tympani The tympanic duct or scala tympani is one of the perilymph-filled cavities in the inner ear of humans. It is separated from the cochlear duct by the basilar membrane, and it extends from the round window to the helicotrema, where it continues as ...

, and the

scala vestibuli The vestibular duct or scala vestibuli is a perilymph-filled cavity inside the cochlea of the inner ear that conducts sound vibrations to the cochlear duct. It is separated from the cochlear duct by Reissner's membrane and extends from the vesti ...

. Regarding mammals, placental and marsupial cochleae have similar cochlear responses to auditory stimulation as well as DC resting potentials. This leads to the investigation of the relationship between these therian mammals and researching their ancestral species to trace the origin of the cochlea. This spiral-shaped cochlea that is in both marsupial and placental mammals is traced back to approximately 120 million years ago. The development of the most basic basilar papilla (the auditory organ that later evolved into the Organ of Corti in mammals) happened at the same time as the water-to-land transition of vertebrates, approximately 380 million years ago. The actual coiling or spiral nature of the cochlea occurred to save space inside the

skull The skull is a bone protective cavity for the brain. The skull is composed of four types of bone i.e., cranial bones, facial bones, ear ossicles and hyoid bone. However two parts are more prominent: the cranium and the mandible. In humans, th ...

. The longer the cochlea, the higher is the potential resolution of sound frequencies given the same hearing range. The oldest of the truly coiled mammalian cochleae were approximately 4 mm in length. The earliest evidence available for primates depicts a short cochlea with prominent laminae, suggesting that they had good high-frequency sensitivity as opposed to low-frequency sensitivity. After this, over a period of around 60 million years, evidence suggests that primates developed longer cochleae and less prominent laminae, which means that they had an improvement in low-frequency sensitivity and a decrease in high-frequency sensitivity. By the early

Miocene period The Miocene ( ) is the first geological epoch of the Neogene Period and extends from about (Ma). The Miocene was named by Scottish geologist Charles Lyell; the name comes from the Greek words (', "less") and (', "new") and means "less recen ...

, the cycle of the elongation of the cochleae and the deterioration of the laminae was completed. Evidence shows that primates have had an increasing cochlear volume to body mass ratio over time. These changes in the cochlear

labyrinth In Greek mythology, the Labyrinth (, ) was an elaborate, confusing structure designed and built by the legendary artificer Daedalus for King Minos of Crete at Knossos. Its function was to hold the Minotaur, the monster eventually killed by t ...

volume negatively affect the highest and lowest audible frequencies, causing a downward shift. Non-primates appear to have smaller cochlear labyrinth volumes overall when compared to

primate Primates are a diverse order of mammals. They are divided into the strepsirrhines, which include the lemurs, galagos, and lorisids, and the haplorhines, which include the tarsiers and the simians ( monkeys and apes, the latter including ...

s. Some evidence also suggests that selective forces for the larger cochlear labyrinth may have started after the basal primate node. Mammals are the subject of a substantial amount of research not only because of the potential knowledge to be gained regarding humans, but also because of their rich and abundant representation in the fossil record. The spiral shape of the cochlea evolved later on in the evolutionary pathway of mammals than previously believed, just before the therians split into the two lineages marsupials and placentals, about 120 million years ago.

The evolution of prestin

Parallel to the evolution of the cochlea,

prestin Prestin is a protein that is critical to sensitive hearing in mammals. It is encoded by the ''SLC26A5'' (solute carrier anion transporter family 26, member 5) gene. Prestin is the motor protein of the outer hair cells of the inner ear of the mamm ...

shows an increased rate of evolution in therian mammals.

Prestin Prestin is a protein that is critical to sensitive hearing in mammals. It is encoded by the ''SLC26A5'' (solute carrier anion transporter family 26, member 5) gene. Prestin is the motor protein of the outer hair cells of the inner ear of the mamm ...

is the motor protein of the outer hair cells of the inner ear of the mammalian cochlea. It is found in the hair cells of all vertebrates, including fish, but are thought to have initially been membrane transporter molecules. A high concentration of prestin are found only in the lateral membranes of therian outer hair cells (there is uncertainty with regard to concentrations in monotremes). This high concentration is not found in inner hair cells, and is also lacking in all hair cell types of non-mammals. Prestin also has a role in motility, which evolved a greater importance in the motor function in land vertebrates, but this developed vastly differently in different lineages. In certain birds and mammals, prestin function as both transporters and motors, but the strongest evolution to robust motor dynamics only evolved in therian mammals. It is hypothesized that this motor system is significant to the therian cochlea at high frequencies because of the distinctive cellular and bony composition of the organ of Corti that allows prestin to intensify the movements of the whole structure. Modern ultra-sound echolocating species such as

bat Bats are mammals of the order Chiroptera.''cheir'', "hand" and πτερόν''pteron'', "wing". With their forelimbs adapted as wings, they are the only mammals capable of true and sustained flight. Bats are more agile in flight than most ...

s and

toothed whale The toothed whales (also called odontocetes, systematic name Odontoceti) are a parvorder of cetaceans that includes dolphins, porpoises, and all other whales possessing teeth, such as the beaked whales and sperm whales. Seventy-three species of ...

s show highly evolved prestin, and this prestin shows identical sequence alterations over time. Unusually, the sequences thus apparently evolved independent from each other during different time periods. Furthermore, the evolution of neurotransmitter receptor systems ( acetylcholine) that regulate the motor feedback of the outer hair cells coincides with prestin evolution in therians. This suggests that there was a parallel evolution of a control system and a motor system in the inner ear of therian mammals.

Homoplasies (convergent evolution)

Land vertebrates evolved middle ears independently in each major lineage, and are thus the result of parallel evolution. The configurations of the middle ears of monotreme and therian mammals can thus be interpreted as convergent evolution or

homoplasy Homoplasy, in biology and phylogenetics, is the term used to describe a feature that has been gained or lost independently in separate lineages over the course of evolution. This is different from homology, which is the term used to characterize ...

. Thus evidence from fossils demonstrate homoplasies for the detachment of the ear from the jaw. Furthermore, it is apparent that the land-based eardrum, or tympanic membrane, and connecting structures such as the Eustachian tube evolved convergently in multiple different settings as opposed to being a defining

morphology Morphology, from the Greek and meaning "study of shape", may refer to: Disciplines * Morphology (archaeology), study of the shapes or forms of artifacts * Morphology (astronomy), study of the shape of astronomical objects such as nebulae, galaxies ...

References

{{reflist, refs= {{cite journal, last1=Luo, first1=Z, last2=Ruf, first2=I, last3=Schultz, first3=JA, last4=Martin, first4=T, title=Fossil evidence on evolution of inner ear cochlea in Jurassic mammals, journal=Proceedings of the Royal Society B, date=July 2010, volume=282, issue=1806, pages=28–34, doi=10.1098/rspb.2010.1148, pmc=2992725, pmid=20667879 {{cite journal, last1=Clack, first1=JA, title=Patterns and Processes in the Early Evolution of the Tetrapod Ear, journal=Journal of Neurobiology, date=November 2002, volume=53, issue=2, pages=251–64, doi=10.1002/neu.10129, pmid=12382279 {{cite journal, last1=Manley, first1=GA, title=Evolutionary Paths to Mammalian Cochleae, journal=Journal of the Association for Research Otolaryngology, date=August 2012, pages=733–43, doi=10.1007/s10162-012-0349-9, volume=13, issue=6 , pmc=3505590, pmid=22983571 {{cite journal, last1=Ladevèze, first1=S, last2=de Muizon, first2=C, last3=Colbert, first3=M, last4=Smith, first4=T, title=3D computational imaging of the petrosal of a new multituberculate mammal from the Late Cretaceous of China and its paleobiologic inferences, journal=Comptes Rendus Palevol, date=2010, volume=9, issue=6, pages=319–330, doi=10.1016/j.crpv.2010.07.008 {{cite journal, last1=Armstrong, first1=SD, last2=de Bloch, first2=JI, last3=Houde, first3=P, last4=Silcox, first4=MT, title=Cochlear labyrinth volume in euarchontoglirans: implications for the evolution of hearing in primates, journal=The Anatomical Record, date=2011, volume=294, issue=2, pages=263–266, doi=10.1002/ar.21298, pmid=21235000 , doi-access=free {{cite journal, last1=Fernández, first1=C, last2=Schmidt, first2=RS, title=The opossum ear and evolution of the coiled cochlea, journal=Journal of Comparative Neurology, date=1963, volume=121, issue=1, pages=151–59, doi=10.1002/cne.901210111, pmid=14051841, s2cid=44589070 {{cite journal, last1=Manley, first1=GA, last2=Köppl, first2=C, title=Phylogenetic development of the cochlea and its innervation, journal=Current Opinion in Neurobiology, date=1998, volume=8, issue=4, pages=468–474, doi=10.1016/s0959-4388(98)80033-0, pmid=9751658 , s2cid=8688145 {{cite journal, last1=Koeppl, first1=C, title=Birds - same thing, but different? Convergent evolution in the avian and mammalian auditory systems provides informative comparative models, journal=Hearing Research, date=2011, volume=273, issue=1, pages=65–71, doi=10.1016/j.heares.2010.03.095, pmid=20430083, s2cid=39751724 {{cite journal, last1=Coleman, first1=MN, last2=Boyer, first2=DM, title=Inner ear evolution in primates through the Cenozoic: implications for the evolution of hearing, journal=The Anatomical Record, date=2012, volume=295, issue=4, pages=615–631, doi=10.1002/ar.22422, pmid=22282428 , doi-access=free {{cite journal, last1=Luo, first1=ZX, title=Developmental patterns in Mesozoic evolution of mammal ears, journal=Annual Review of Ecology, Evolution, and Systematics, date=2011, volume=42, pages=355–380, doi=10.1146/annurev-ecolsys-032511-142302 {{cite journal, last1=Romer, first1=AS, last2=Parsons, first2=TS, title=The Vertebrate Body, date=1977 {{cite journal, last1=Koeppl, first1=C, last2=Forge, first2=A, last3=Manley, first3=GM, title=Low density of membrane particles in auditory hair cells of lizards and birds suggests an absence of somatic motility, journal=Journal of Comparative Neurology, date=2004, volume=479, issue=1, pages=149–155, doi=10.1002/cne.20311, pmid=15452826, s2cid=25637434 {{cite journal, last1=Drake, first1=R, last2=Vogl, first2=AW, last3=Mitchell, first3=AW, title=Gray's anatomy for students, journal=Nature, date=1997, volume=390, issue=6656, pages=137–142, doi=10.1038/36505, bibcode=1997Natur.390..137H, pmid=9367151, s2cid=205025005 {{cite journal, last1=Spoor, first1=F, last2=Hublin, first2=J, last3=Braun, first3=M, last4=Zonneveld, first4=F, title=The Bony Labyrinth of Neanderthals, journal=Journal of Human Evolution, date=2002, volume=44, issue=2003, pages=141–165, doi=10.1016/s0047-2484(02)00166-5, pmid=12662940 {{cite web, url=https://www.nlm.nih.gov/medlineplus/ency/anatomyvideos/000063.htm, title=Hearing and the Cochlea, last=Dugdale, first=DC, date=2012, website=MedlinePlus {{cite journal, last1= Kitazawa , first1=T, last2=Takechi, first2=M, last3=Hirasawa, first3=T, last4=Adachi, first4=N, last5=Narboux-Nâme, first5=N, last6=Kume, first6=H, last7=Maeda, first7=K, last8=Hirai, first8=T, last9=Miyagawa-Tomita, first9=S, last10=Kurihara, first10=Y, last11=Hitomi, first11=J, last12=Levi, first12=GL, last13=Kuratani, first13=S, last14=Kurihara, first14=H, title= Developmental genetic bases behind the independent origin of the tympanic membrane in mammals and diapsids, journal=Nature Communications, date=2015, volume=6, issue=6853, pages=6853, doi=10.1038/ncomms7853, pmid=25902370, pmc=4423235, bibcode=2015NatCo...6E6853K

Auditory system Otology Audiology