Morphology of the Inner Ear in Mammals with Different Ecological Peculiarities in Ontogeny
The inner ear is the first to form, as the core, phylogenetically most ancient formation of the peripheral auditory system both in phylogenesis and in ontogenesis. As the development of the inner ear continues, the other parts of the peripheral auditory system of different evolutionary age start to...
Збережено в:
| Дата: | 2010 |
|---|---|
| Автор: | |
| Формат: | Стаття |
| Мова: | English |
| Опубліковано: |
Інститут зоології ім. І.І. Шмальгаузена НАН України
2010
|
| Назва видання: | Вестник зоологии |
| Теми: | |
| Онлайн доступ: | http://dspace.nbuv.gov.ua/handle/123456789/65686 |
| Теги: |
Додати тег
Немає тегів, Будьте першим, хто поставить тег для цього запису!
|
| Назва журналу: | Digital Library of Periodicals of National Academy of Sciences of Ukraine |
| Цитувати: | Morphology of the Inner Ear in Mammals with Different Ecological Peculiarities in Ontogeny / G.N. Solntseva // Вестник зоологии. — 2010. — Т. 44, № 3. — С. 227–244. — Бібліогр.: 20 назв. — англ. |
Репозитарії
Digital Library of Periodicals of National Academy of Sciences of Ukraine| id |
irk-123456789-65686 |
|---|---|
| record_format |
dspace |
| spelling |
irk-123456789-656862014-07-01T03:01:42Z Morphology of the Inner Ear in Mammals with Different Ecological Peculiarities in Ontogeny Solntseva, G.N. Морфология The inner ear is the first to form, as the core, phylogenetically most ancient formation of the peripheral auditory system both in phylogenesis and in ontogenesis. As the development of the inner ear continues, the other parts of the peripheral auditory system of different evolutionary age start to be formed, and the outer ear is the evolutionary youngest among them. All parts of the peripheral auditory system are multicomponent formations. As opposed to the outer and middle ears, which are characterized by different structural variations and a wide spectrum of adaptable transformations connected with the peculiarities of species ecology, the inner ear possesses a variety of functions in the repre-sentatives of different ecological groups and, therefore, keeps a similar structural organization. Usually, both in the cochlear and vestibular analyzers the topography, form and size of separate components vary. Basically, the anatomic formation of the structures of the inner ear finishes in the early prefetal period, while the cellular differentiation of the sensory epithelium of the cochlea, maculas and cristae in immature-born species continues up to the early stages of postnatal ontogenesis. In mature-born species (cetaceans, ungulates), the differentiation of the inner ear structures is complete by the moment of birth. Как в филогенезе, так и в онтогенезе прежде всего формируется внутреннее ухо как стержневое, филогенетически наиболее древнее образование периферического отдела слуховой системы. По мере развития внутреннего уха начинают формироваться другие звенья периферической слуховой системы разного эволюционного возраста, из которых филогенетически молодым является наружное ухо. В отличие от наружного и среднего уха, которые характеризуются самыми разнообразными структурными вариациями и широким спектром адаптационных преобразований, связанных с особенностями экологии вида, внутреннее ухо у представителей различных экологических групп при многообразии функций сохраняет однообразную структурную организацию. Как в кохлеарном, так и в вестибулярном анализаторах обычно варьируют топография, форма и размеры отдельных компонентов. Анатомическое формирование структур внутреннего уха в основном заканчивается в раннем предплодном периоде, в то время как клеточная дифференцировка чувствующего эпителия улитки, макул и крист у незрелорождающихся видов продолжается вплоть до ранних стадий постнатального онтогенеза. У зрелорождающихся видов (китообразные, копытные) дифференцировка структур внутреннего уха в основном завершается к моменту рождения. 2010 Article Morphology of the Inner Ear in Mammals with Different Ecological Peculiarities in Ontogeny / G.N. Solntseva // Вестник зоологии. — 2010. — Т. 44, № 3. — С. 227–244. — Бібліогр.: 20 назв. — англ. 0084-5604 http://dspace.nbuv.gov.ua/handle/123456789/65686 591.485:591.3:599 en Вестник зоологии Інститут зоології ім. І.І. Шмальгаузена НАН України |
| institution |
Digital Library of Periodicals of National Academy of Sciences of Ukraine |
| collection |
DSpace DC |
| language |
English |
| topic |
Морфология Морфология |
| spellingShingle |
Морфология Морфология Solntseva, G.N. Morphology of the Inner Ear in Mammals with Different Ecological Peculiarities in Ontogeny Вестник зоологии |
| description |
The inner ear is the first to form, as the core, phylogenetically most ancient formation of the peripheral auditory system both in phylogenesis and in ontogenesis. As the development of the inner ear continues, the other parts of the peripheral auditory system of different evolutionary age start to be formed, and the outer ear is the evolutionary youngest among them. All parts of the peripheral auditory system are multicomponent formations. As opposed to the outer and middle ears, which are characterized by different structural variations and a wide spectrum of adaptable transformations connected with the peculiarities of species ecology, the inner ear possesses a variety of functions in the repre-sentatives of different ecological groups and, therefore, keeps a similar structural organization. Usually, both in the cochlear and vestibular analyzers the topography, form and size of separate components vary. Basically, the anatomic formation of the structures of the inner ear finishes in the early prefetal period, while the cellular differentiation of the sensory epithelium of the cochlea, maculas and cristae in immature-born species continues up to the early stages of postnatal ontogenesis. In mature-born species (cetaceans, ungulates), the differentiation of the inner ear structures is complete by the moment of birth. |
| format |
Article |
| author |
Solntseva, G.N. |
| author_facet |
Solntseva, G.N. |
| author_sort |
Solntseva, G.N. |
| title |
Morphology of the Inner Ear in Mammals with Different Ecological Peculiarities in Ontogeny |
| title_short |
Morphology of the Inner Ear in Mammals with Different Ecological Peculiarities in Ontogeny |
| title_full |
Morphology of the Inner Ear in Mammals with Different Ecological Peculiarities in Ontogeny |
| title_fullStr |
Morphology of the Inner Ear in Mammals with Different Ecological Peculiarities in Ontogeny |
| title_full_unstemmed |
Morphology of the Inner Ear in Mammals with Different Ecological Peculiarities in Ontogeny |
| title_sort |
morphology of the inner ear in mammals with different ecological peculiarities in ontogeny |
| publisher |
Інститут зоології ім. І.І. Шмальгаузена НАН України |
| publishDate |
2010 |
| topic_facet |
Морфология |
| url |
http://dspace.nbuv.gov.ua/handle/123456789/65686 |
| citation_txt |
Morphology of the Inner Ear in Mammals with Different Ecological Peculiarities in Ontogeny / G.N. Solntseva // Вестник зоологии. — 2010. — Т. 44, № 3. — С. 227–244. — Бібліогр.: 20 назв. — англ. |
| series |
Вестник зоологии |
| work_keys_str_mv |
AT solntsevagn morphologyoftheinnerearinmammalswithdifferentecologicalpeculiaritiesinontogeny |
| first_indexed |
2025-07-05T16:05:03Z |
| last_indexed |
2025-07-05T16:05:03Z |
| _version_ |
1836823613411426304 |
| fulltext |
UDC 591.485:591.3:599
MORPHOLOGY OF THE INNER EAR
IN MAMMALS WITH DIFFERENT ECOLOGICAL
PECULIARITIES IN ONTOGENY
G. N. Solntseva
A. N. Severtsov Institute of Problem Ecology and Evolution, Russian Academy of Sciences,
33, Leninsky Prospekt, Moscow, 119071 Russia
E-mail: g-solntseva@yandex.ru; g-solntseva@mail.ru
Received 3 August 2009
Accepted 7 September 2009
Morphology of the Inner Ear in Mammals with Different Ecological Peculiarities in Ontogeny.
Solntseva G. N. — The inner ear is the first to form, as the core, phylogenetically most ancient
formation of the peripheral auditory system both in phylogenesis and in ontogenesis. As the
development of the inner ear continues, the other parts of the peripheral auditory system of different
evolutionary age start to be formed, and the outer ear is the evolutionary youngest among them. All
parts of the peripheral auditory system are multicomponent formations. As opposed to the outer and
middle ears, which are characterized by different structural variations and a wide spectrum of adaptable
transformations connected with the peculiarities of species ecology, the inner ear possesses a variety of
functions in the repre-sentatives of different ecological groups and, therefore, keeps a similar structural
organization. Usually, both in the cochlear and vestibular analyzers the topography, form and size of
separate components vary. Basically, the anatomic formation of the structures of the inner ear finishes
in the early prefetal period, while the cellular differentiation of the sensory epithelium of the cochlea,
maculas and cristae in immature-born species continues up to the early stages of postnatal ontogenesis.
In mature-born species (cetaceans, ungulates), the differentiation of the inner ear structures is complete
by the moment of birth.
Ke y wo r d s: cochlea, vestibular apparatus, sacculus, utriculus, semicircular canals, utricular macula,
saccular macula, crista ampullaris, receptor cells, organ of Corti.
Ìîðôîëîãè÷åñêèå îñîáåííîñòè îíòîãåíåçà âíóòðåííåãî óõà ìëåêîïèòàþùèõ ñ ðàçëè÷íûì îáðàçîì
æèçíè. Ñîëíöåâà Ã. Í. — Êàê â ôèëîãåíåçå, òàê è â îíòîãåíåçå ïðåæäå âñåãî ôîðìèðóåòñÿ
âíóòðåííåå óõî êàê ñòåðæíåâîå, ôèëîãåíåòè÷åñêè íàèáîëåå äðåâíåå îáðàçîâàíèå ïåðèôåðè-
÷åñêîãî îòäåëà ñëóõîâîé ñèñòåìû. Ïî ìåðå ðàçâèòèÿ âíóòðåííåãî óõà íà÷èíàþò ôîðìèðîâàòüñÿ
äðóãèå çâåíüÿ ïåðèôåðè÷åñêîé ñëóõîâîé ñèñòåìû ðàçíîãî ýâîëþöèîííîãî âîçðàñòà, èç êîòîðûõ
ôèëîãåíåòè÷åñêè ìîëîäûì ÿâëÿåòñÿ íàðóæíîå óõî.  îòëè÷èå îò íàðóæíîãî è ñðåäíåãî óõà,
êîòîðûå õàðàêòåðèçóþòñÿ ñàìûìè ðàçíîîáðàçíûìè ñòðóêòóðíûìè âàðèàöèÿìè è øèðîêèì
ñïåêòðîì àäàïòàöèîííûõ ïðåîáðàçîâàíèé, ñâÿçàííûõ ñ îñîáåííîñòÿìè ýêîëîãèè âèäà,
âíóòðåííåå óõî ó ïðåäñòàâèòåëåé ðàçëè÷íûõ ýêîëîãè÷åñêèõ ãðóïï ïðè ìíîãîîáðàçèè ôóíêöèé
ñîõðàíÿåò îäíîîáðàçíóþ ñòðóêòóðíóþ îðãàíèçàöèþ. Êàê â êîõëåàðíîì, òàê è â âåñòèáóëÿðíîì
àíàëèçàòîðàõ îáû÷íî âàðüèðóþò òîïîãðàôèÿ, ôîðìà è ðàçìåðû îòäåëüíûõ êîìïîíåíòîâ.
Àíàòîìè÷åñêîå ôîðìèðîâàíèå ñòðóêòóð âíóòðåííåãî óõà â îñíîâíîì çàêàí÷èâàåòñÿ â ðàííåì
ïðåäïëîäíîì ïåðèîäå, â òî âðåìÿ êàê êëåòî÷íàÿ äèôôåðåíöèðîâêà ÷óâñòâóþùåãî ýïèòåëèÿ
óëèòêè, ìàêóë è êðèñò ó íåçðåëîðîæäàþùèõñÿ âèäîâ ïðîäîëæàåòñÿ âïëîòü äî ðàííèõ ñòàäèé
ïîñòíàòàëüíîãî îíòîãåíåçà. Ó çðåëîðîæäàþùèõñÿ âèäîâ (êèòîîáðàçíûå, êîïûòíûå)
äèôôåðåíöèðîâêà ñòðóêòóð âíóòðåííåãî óõà â îñíîâíîì çàâåðøàåòñÿ ê ìîìåíòó ðîæäåíèÿ.
Êëþ÷åâûå ñ ëîâ à: óëèòêà, âåñòèáóëÿðíûé àïïàðàò, êîðòèåâ îðãàí, ñàêêóëþñ, óòðèêóëþñ,
àìïóëÿðíàÿ êðèñòà, ïîëóêðóæíûå êàíàëû, ñàêêóëÿðíàÿ ìàêóëà, óòðèêóëÿðíàÿ ìàêóëà.
Introduction
The question on evolutionary origin of a labyrinth in vertebrates still remains open, despite the existing
hypotheses explaining its evolution beginning from a lancelet up to mammals. A well-known hypothesis is
that the labyrinth has appeared on the basis of the organs of a lateral line, which are openly located on the
Vestnik zoologii, 44(3): 227–244, 2010 Ìîðôîëîãèÿ
surface of an animal’s body and have a direct contact with the environment. Complication of structures and
functions of the lateral line organ has caused an appearance of a new structural formation — the vestibular
apparatus. However, nobody among the researchers succeeded to trace how the evolution was progressing
from an open labyrinth to a closed one, which is located deeply in the cranium.
The present research does not give a direct answer to this question, but it essentially contributes to its
solution and is devoted to comparative analysis of an early embryogenesis of the vestibular and cochlear parts
of the inner ear in terrestrial, semi-aquatic and aquatic mammals, since the sensory systems, in particular,
brightly demonstrate the range of evolutionary and adaptive transformations, which have appeared in
mammals during their transition from terrestrial to aquatic way of life.
The inner ear of mammals, in contrast to that of the lower vertebrates (amphibians, reptilians, birds)
reveals the features of the progressive evolution which become apparent in the spiral torsion of the cochlea
and the presence of the structurally complicated organ of Corti. Whereas the lagena papilla still remains in
the representatives of the monotremats, the organ of Corti develops in the marsupials and in the placental
animals.
The aim of the present research is to study the species and adaptive features of the cochlear and
vestibular organs of mammals with different ecologies in pre- and postnatal ontogeny.
Material and methods
The following species of mammals (in postnatal ontogeny) were studied: Insectivora (Talpa europaea
Linnaeus, 1758); Chiroptera (Rhinolophus ferrumequinum Schreber, 1774); Rodentia (Myicastor coypus
Molina, 1782); Cetacea (Odontoceti: Tursiops truncatus Montagu, 1821, Delphinus delphis Lacepede, 1758,
Phocoena phocoena Linnaeus, 1758; Mysticeti: Balaenoptera acutorostrata Lacepede, 1804, Balaenoptera
physalus Lacepede, 1758); Carnivora (Vulpes vulpes Linnaeus, 1758, Enhydra lutris Linnaeus, 1758, Mustela
vison Schreber, 1777); Pinnipedia (Otariidae: Callorchinus ursinus Linnaeus, 1758, Eumetopias jubatus
Schreber, 1776; Phocidae: Pagophilus groenlandicus Erxleben, 1777, Phoca vitulina Linnaeus, 1758, Phoca
insularis Belkin, 1967, Erignathus barbatus Erxleben, 1777, Pusa hispida Schreber, 1775, Pusa caspica Gmelin,
1788; Odobenidae: Odobenus rosmarus divergens Linnaeus, 1758).
For comparative ecological and embryological study were used the following species of mammals:
terrestrial forms: Rodentia — laboratory rat (Rattus norvegicus Pallas, 1779), guinea pig (Cavia porcellus
Linnaeus, 1758), Artiodactyla — pig (Sus scrofa domestica Linnaeus, 1758); semi-aquatic forms:
Pinnipedia — Otariidae: Steller sea lion (Eumetopias jubatus); Phocidae: ringed seal (Phoca hispida), bearded
seal (Erignathus barbatus); and Odobenidae: walrus (Odobenus rosmarus divergens); aquatic forms: Cetacea —
Odontoceti: spotted dolphin (Stenella attenuata Gray, 1846), bottlenose dolphin (Tursiops truncatus),
common dolphin (Delphinus delphis), harbor porpoise (Phocoena phocoena), beluga (Delphinapterus leucas
Pallas, 1776); Mysticeti: minke whale (Balaenoptera acutorostrata).
Specimens were fixed in 10% buffered formalin and Wittmaak fixative then dehydrated and treated in
an increasing series of ethanol, embedded in celloidin, and sectioned at 10–15 micron thickness in a
dorsoventral plane. The sections were stained with hematoxylin-eosin, according to the methods of Mallory
and Kulchitsky, and impregnated with silver nitrate.
The duration of gestation and length of embryos an diverse stages of embryogenesis vary widely among
mammals. To examine embryos of different species, I compared developing structures of the vestibular
apparatus with the development of acoustic structures at the same stage of development. For convenience, I
used the stages of development described in certain terrestrial species (Dyban et al., 1975).
Results
It is known that the inner ear, in which the cochlea and the vestibular apparatus
are located, is placed in a petrous part (pyramid) of a temporal bone. Because of the
complexity of its structure, it is also called a labyrinth. There are two labyrinths: osseous
and membranaceous. The osseous labyrinth includes a cochlea, a vestibule and three
semicircular canals. The vestibule looks like a cavity of an oval form. It is located
between the cochlea and the semicircular canals. The membranaceous labyrinth is
located inside the osseous labyrinth and its form usually repeats the form of a labyrinth,
but is significantly smaller in size. The walls of a membranaceous labyrinth are formed
by a dense connective tissue.
The inner ear of mammals, in contrast to that of the lower vertebrates (amphib-
ians, reptilians, birds), reveals the features of the progressive evolution which become
apparent in the spiral torsion of the cochlea and the presence of the structurally com-
plicated organ of Corti. While the lagena papilla still remains in the representatives of
228 G. N. Solntseva
the monotremats, the organ of Corti develops in the marsupials and in the placental
animals.
The periotic bone in which the cochlea of mammals is located in the majority of
mammals knits to the tympanic bone (rodents, carnivores, pinnipeds etc.). In the odon-
tocetes, it only partially knits to the tympanic bone and it is located outside the tym-
panum.
In the inner ear, the principle of the cochlea’s structure reveals similarities in
almost all mammals. The number of the turns which form the cochlea can vary from
0.5 in monotremats to 4.5–5 turns in some rodents (fig. 1).
The increase of the number of cochlea’s turns is explained by its morphological
progress (Fleischer, 1973). However, in such echolocating animals as dolphins the
cochlea is flat and forms 1.5–2.0 turns only, while in bats the number of its turns
amounts to 3.5. Such variability in the number of cochlea’s turns in echolocating forms
proves that the cochlea’s height caused by the turns’ increase doesn’t influence the per-
ceptible frequency band.
Big cochlea is characteristic for all species of dolphins. The cochlear bones are
localized in periotic, in the thickness of which a cochlea channel is extended. In
Amazon river dolphin (Inia geoffrensis) a cochlea is half-covered with medial lobe of
tympanic bone. In marine dolphins the cochlea is separated from the other bones and
229Morphology of the Inner ear in mammals with different ecological peculiarities in ontogeny
Fig. 1. The cochlea of Myocastor coypus. Slit through the cochlea axis. 4.5 turns of the cochlea are shown.
Staining with hematoxylin-eosin. Magnification x25. 1 — cochlear canal; 2 — vestibular scala; 3 — tympanic
scala; 4 — cochlear nerve.
Ðèñ. 1. Óëèòêà íóòðèè (Myocastor coypus). Ïîïåðå÷íûé ðàçðåç ÷åðåç îñü óëèòêè. Ïîêàçàíû 4,5 îáîðîòà
óëèòêè. Îêðàñêà ãåìàòîêñèëèí-ýîçèíîì. Óâåëè÷åíèå x25. 1 — óëèòêîâûé êàíàë; 2 — âåñòèáóëÿðíàÿ
ëåñòíèöà; 3 — áàðàáàííàÿ ëåñòíèöà; 4 — êîõëåàðíûé íåðâ.
is an independent structure. Cochlear canal in river dolphin is weakly traced, and crista
transversalis is almost twice as small as in marine dolphins, in which the crista transver-
salis is opened, and cochlear canal is well-traced.
In the majority of mammals the size of the cochlea’s basal turn slightly differs from
that of the turn which is located above. For the representatives of some genera the dras-
tic enlarging of the cochlea’s basal turn is typical (shrews, bats, odontocetes and pin-
nipeds).
The comparative analysis shows that in echolocating forms one of the important
cochlea’s adaptations, which provide high-frequency hearing: the increasing of the
cochlea’s basal turn. For example, the surface of the basal turn of dolphins is increased
due to the “untwisting” of the cochlea up to 1.5–2.0 turns (fig. 2). The bat’s cochlea
reveals just the same, in spite of the fact that its promptness is increased up to 3.5.
During the comparison of the primary and the secondary osseous spiral laminas
some peculiarities are revealed in the cochlea’s basal and apical turns. The extension of
the primary lamina along the cochlea’s passage varies significantly less than such of the
secondary lamina (Fleischer, 1973).
The structure of the primary osseous spiral lamina is dissimilar in different species.
The vestibular and the tympanal osseous leaves which form the primary lamina can be
thick and compact, as well as less developed. For example, in a man both leaves of the
primary spiral lamina have a spongy structure, while in the Loxodonta a great loosen-
ing of the tympanal leaf is observed (Fleischer, 1973).
In the majority of mammals the secondary osseous spiral lamina is more developed
in the cochlea’s basal part than in the apical part, where it becomes thin.
In the Chiroptera and Odontocetes the secondary lamina occupies the whole
cochlea’s passage stretching from its basal to the apical turn. In the majority of mam-
mals and in a man in the cochlea’s basal part the secondary lamina is well-marked, and
in the apical part it quickly disappears.
230 G. N. Solntseva
Fig. 2. The cochlea of Delphinus delphis. 1.5 turns of the cochlea are shown. Staining according to Kampas.
Magnification õ25. a — cochlea, anatomical preparation; b — histological preparation, slit through the axis
of the cochlea. 1 — cochlear canal; 2 — vestibular scala; 3 — tympanic scala; 4 — cochlear nerve. 5 —
semicircular canal
Ðèñ. 2. Óëèòêà îáûêíîâåííîãî äåëüôèíà. Ïîêàçàíû 1,5 îáîðîòà óëèòêè. Îêðàñêà ïî Êàìïàñó.
Óâåëè÷åíèå õ25. à — óëèòêà, àíàòîìè÷åñêèé ïðåïàðàò; á — ãèñòîëîãè÷åñêèé ïðåïàðàò, ïðîäîëüíûé
ðàçðåç ÷åðåç îñü óëèòêè. 1 — óëèòêîâûé êàíàë; 2 — âåñòèáóëÿðíàÿ ëåñòíèöà; 3 — áàðàáàííàÿ
ëåñòíèöà; 4 — êîõëåàðíûé íåðâ; 5 — ïîëóêðóæíûé êàíàë.
The comparison of two spiral lamina’s structure shows that the species which pos-
sess a thick secondary lamina have a well-developed primary lamina. It is basically typ-
ical in the forms with the narrow basilar membrane. In the forms with the underdevel-
oped secondary osseous lamina the distance between two laminas is bigger.
Another important peculiarity of the cochlea’s structure in echolocating mammals
is a well-developed secondary spiral bone lamella. The lesser a distance between prima-
ry and secondary spiral bone lamellas is, the narrower the width of the basilar mem-
brane becomes, and the secondary spiral bone lamella turns out to be more developed,
its rigidity is continuously and evenly decreasing from the cochlea’s basal turn to the
apical turn.
In all mammals the cochlea’s basilar membrane heterogeneously widens along its
length. For example, in a guinea pig the basilar membrane is wide in the cochlea’s basal
part, narrow in the medial part and widens again in the apical part. In the Odontocetes
(porpoises) the diameter of the basilar membrane changes from the basal to the apical
turn in 5.4 times (Kolmer, 1908) and in a Baird’s beaked whale — in 10 times (Yama-
da, 1953).
In the majority of mammals the membrane is up to 29 micrometers thick. In bats
and Odontocetes the basilar membrane is the narrowest and the thinnest. For example,
in dolphins its thickness amounts to 6.5 μm.
The structure of the organ of Corti, as well as the quantity of its receptor elements,
reveals similar features. Usually, the outer hair cells are located in three rows, the inner
hair cells — in one row. The total number of the hair cells in a man amounts to 14 975,
in a guinea pig — to 8939, in a cat — to 12 500, in a rabbit — to 7800, in a seal — to
17 972, in a ringed seal — to 21 792, in a bottlenose dolphin — to 17 384, in a pacif-
ic white-sided dolphin — 12 899 (Ramprashad et al., 1976).
Usually the number of the hair cells decreases in the direction from the basal to
the cochlea’s apical turn. Usually the volume of the nuclei of the organ of Corti hair
cells increases in the same direction, as well as in the direction from the inner row of
the outer hair cells to the periphery (Akimov, 1976).
In most mammals the structure of the organ of Corti reveals patterns of similari-
ty. The number of receptor cells in echolocating and non-echolocating forms doesn’t
change. However, some researchers observed certain peculiarities in the structure of the
organ of Corti bearing elements in dolphins and bats, in which these cells are enlarged
in size and compactly located (Wever et al., 1971). The increasing number of the spi-
ral ganglion’s cells (3 times) and the enlargement of their size compared to a man tes-
tify in favour of the data concerning dolphins’ and bats’ high abilities to process acous-
tical information starting from the peripheral part of the auditory analyzer (Firbas,
Welleschik, 1973).
The most interesting facts are revealed during the study of the inner ear’s structure
in mammals. First of all, this is the existence of two types of receptors belonging to a
different evolutional age (outer and inner hair cells), which are spatially separated from
each other (fig. 3). What is more, it has an extremely small number of the receptor cells
and a sufficient stability in animals of the very variable hearing specializations. The
auditory system of echolocating species and animals with low-frequency hearing pos-
sesses approximately equal quantities of the hair cells and the identical character of their
distribution upon the basilar membrane.
According to our point of view, the fact that most mammals, even the species with
extraordinarily broad hearing abilities, have relatively little number of receptors as well
as auditory nerve’s fibres, is connected with a temporary specificity of the acoustic sig-
nal’s perception and processing. It is a consequent receipt of information that allows
simultaneous use of comparatively little quantity of parallel canals in the periphery of
the auditory system (Bogoslovskaya, Solntseva, 1979).
231Morphology of the Inner ear in mammals with different ecological peculiarities in ontogeny
Due to two partitions, the cochlea’s tunnel is divided into three independent canals
(canals of cochlea): tympanic, vestibular and middle, or cochlear. The first two canals
are filled with a perilymph and communicate with each other through an opening on
the cochlea’s top — helicotrema. The middle canal is filled with an endolymph and ends
blindly, widening in the cochlea’s apical part and spirally repeating the number of the
turns which form the cochlea. On the cross-sections the cochlear canal has three walls:
inferior, superior and external.
232 G. N. Solntseva
Fig. 3. The organ of Corti of Delphinus delphis. Slit through the cochlea axis at the level of the basal turn.
Staining with hematoxylin-eosin (immersion objective 90, ocular 7). a — general view; b, c, d — cells of the
organ of Corti. IHC — inner hair cells; OHC — outer hair cells; ICC — inner columnar cells; SG — cells
of spiral ganglion.
Ðèñ. 3. Êîðòèåâ îðãàí îáûêíîâåííîãî äåëüôèíà. Ïðîäîëüíûé ðàçðåç ÷åðåç îñü óëèòêè íà óðîâíå
áàçàëüíîãî îáîðîòà. Îêðàñêà ãåìàòîêñèëèí-ýîçèíîì (îá. èì. 90, îê. 7). à — îáùèé âèä; b, c, d —
êëåòêè êîðòèåâà îðãàíà OHC — íàðóæíûå âîëîñêîâûå êëåòêè; IHC — âíóòðåííèå âîëîñêîâûå
êëåòêè; ICC — âíóòðåííèå êëåòêè-ñòîëáû; SG — êëåòêè ñïèðàëüíîãî ãàíãëèÿ.
The inferior wall is the continuation of the spiral lamina, which starts from modi-
olus and consists of two layers. The spiral ganglion’s dendrites pass between them in
the radial canals. The upper layer of the osseous lamina turns into a spiral limb and the
lower one — into a basilar membrane. The inferior wall of the cochlear canal divides
the spiral canal into vestibular (scala vestibuli) and tympanic (scala tympani) scalae of
the cochlea. On the cochlea’s top the osseous lamina ends with a peculiar curve in the
form of a hook (hamulus cochleae).
The superior wall of the cochlea’s canal is formed by the Reisner’s membrane,
which isolates it from the vestibular canal of the cochlea. The external wall is the thick-
est and covers the upper part of the spiral ligament; it takes part in the endolymph pro-
duction, which fills the cochlear canal (ductus cochlearis).
The Reissner’s membrane looks like a thin membrane which, from the cochlear
canal’s side, is covered with a flat polygonal epithelium, and from the vestibular canal’s
side it is covered with a thin endothelium of a mesenchymal origin. The layer is formed
by thin elastic fibers. During the basilar membrane’s oscillations and the perilymph’s
displacements in the vestibular canal the oscillations of the Reissner’s membrane occur,
which, in their turn, are transmitted to the cochlear canal’s endolymph. The basilar
membrane (membrana basilaris) forms the inferior wall of the cochlear canal. The organ
of Corti is situated on its surface. From the side of the tympanic canal the surface of
the basilar membrane is covered with the same endothelium, under which blood ves-
sels are situated. The basilar membrane passes through the whole cochlear canal in the
form of a connective-tissue spiral. The inner edge of the basilar membrane begins from
the upper leaf of the osseous spiral lamina of habenula perforata, and the external one
is fastened in the area of lamina spiralis ossea. The basilar membrane is subdivided into
two zones: inner and outer. In the inner zone the tunnel, inner and outer hair cells of
the organ of Corti are located, and in the outer zone there are mainly the Hensen’s
cells.
At the basis of the outer cells-columns the inner zone turns into the outer zone.
The collagen fibers which form the structure of the basilar membrane are the shortest
at the cochlea’s basis and while moving to the apical part they greatly lengthen and
widen. The width of the basilar membrane depends on the distance between primary
and secondary osseous spiral laminas. The secondary osseous spiral lamina (lamina spi-
ralis ossea secundaria) is connected with the vestibular fibres of the basilar membrane.
It was experimentally shown that the flexible basilar membrane and the rigid osseous
spiral lamina form the oscillating system of the cochlea.
The organ of Corti is located on the vestibular surface of the basilar membrane;
from its inner side the organ of Corti is adjoined by a connective-tissue structure — a
vestibular, or spiral, labium, which passes on the inner spiral incisure.
The tectorial membrane starts from the spiral labium and is located above the ele-
ments of the organ of Corti in the form of a jelly-like lamina and stretches spirally along
the organ of Corti.
In the tectorial membrane the following structures are discerned: the axial part,
which adjoins to the top of the epithelial cells of the spiral labium, the middle part,
which is freely located above the organ of Corti, and the external part, which, as it is
supposed, is connected with the Hensen’s cells (Titova, 1968).
The organ of Corti of mammals is formed by supporting and receptor elements.
The supporting elements are represented by inner frontier cells, inner cells- phalanxes,
inner and outer cells-columns and Deuters’s, Hensen’s, Claudius’s supporting cells.
The inner frontier cells border upon the inner side of the inner hair cells and form
1–2 rows of elements. With their tops they adjoin to the tops of the inner cells-pha-
lanxes. The narrow and flat head of the inner frontier cells is tightly connected with the
233Morphology of the Inner ear in mammals with different ecological peculiarities in ontogeny
structural elements of the reticular membrane. The basal part of the cell is located in
the area of habenula perforata. The nucleus is located in the basal part of the cell.
The inner cells-phalanxes form one row. Their upper end is connected with the
reticular membrane and has the form of a phalanx, with the help of which the inner
hair cells are separated from each other. The middle part of the inner cell-phalanx is
flattened out and narrowed. The external side of the inner hair cells is adjacent to the
cell’s body. The basal part of the cell is located in the area of habenula perforata, as
well as the inner frontier cells. Between these cells the dendrites of the spiral ganglion
are located. The nucleus lies in the basal part of the cell. Between the inner cells-pha-
lanxes and the frontier cells there is an isolated intercellular cavity, in the apical part
of which the inner hair cells are located (Titova, 1968).
The outer and the inner cells-columns adjoin to each other by their tops and form
a three-cornered tunnel which is filled with an endolymph. This tunnel spirally passes
through the whole the organ of Corti. With the help of their basis the cells-columns
contact with the basilar membrane. The cells-columns are located at the sharp angle
facing each other; as a result their tops adjoin to each other. At that the outer cells-
columns form the bigger angle of inclination than the inner cells-columns.
In the place of their contact the cells-columns form a peculiar arch (arcus spiralis).
The apical part of the inner cells-columns forms a head lamina. In the aggregate these
laminas enable the formation of the space between the inner hair cells and the first row
of the outer hair cells. In the area of the contact with the inner hair cells the head lam-
inas have inner incisures. The outer cells-columns adjoin to the head lamina of the
inner cells-columns from below and give outward from themselves long oar-like pro-
cesses, which contact with each other and thus isolate the lateral sides of the first row
of the outer hair cells from each other, as well as the second row of the outer hair cells
from the first row. The number of the inner cells-columns exceeds the number of the
outer cells-columns. For example, in a man the number of the inner cells-columns
amounts to 5600, and the number of the outer cells-columns amounts to 3850.
The supporting cells-columns locating on the basilar membrane stretch it and,
together with the other supporting elements, transmit the basilar membrane’s oscilla-
tions to the receptor cells.
The Deiters’s cells are located on the basilar membrane; usually they form three
rows and lie close to the inner cells-columns. These cells are the supporting cells for
the outer hair cells. The Deiters’s cells have a polygonal cylindrical form with a big
rounded nucleus which is located in the basal part of the cell. In its upper part the
Deiters’s cell forms a phalanx-shaped incisure — the upper head, which, together with
other laminas, phalanxes and outgrowths of the cells-columns takes part in the forma-
tion of the reticular membrane. Also, from the Deiters’s cell the lower head begins, the
bowl-shaped bottom of which gives support to the basis of the outer hair cell.
The Hensen’s cells, in contrast to the Deiters’s cells, are not connected to the
reticular membrane’s structures. They adjoin to the Deiters’s cells and form a wide row
fastening to the basal part of the basilar membrane. The nucleus is big and rounded. It
is supposed, that the transportation of the nutrients to the hair cells and to the Deiters’s
cells from the vascular stria is provided with the help of the Hensen’s cells (Titova,
1968).
The Claudius’s cells are located behind the Hensen’s cells and have a cubical form
with distinct intercellular borders. It is supposed, that the functional role of the
Claudius’s cells, as well as the role of the Hensen’s cells, is a trophic one.
The outer (OHC) and the inner (IHC) hair cells are the receptor elements of the
organ of Corti. According to the Retzius’s assessment (Retzius, 1884), there are about
12000 outer and 3500 inner hair cells in a man’s cochlea — slightly less than in the
cochlea of a cat and a guinea-pig. The inner hair cells (IHC) lie in one row with an
234 G. N. Solntseva
inclination from modiolus and the outer hair cells (OHC), which are isolated from IHC
by the tunnel, lie in three rows with an inclination to the opposite side. In different
turns of the cochlea the OHC slightly differ in shape, while the IHC’s shape is invari-
able in all cochlea’s turns.
The height of the cylindrical OHC’s increases in the direction from the basal to
the apical turn (20 and 50 μ, accordingly) and their diameter is practically invariable
(5 μ). The OHC’s stability is provided by the system of the Deiters’s supporting cells
and the space between them, which is filled with a liquid (Nuel’s space). The receptor
pole of the hair cells is formed by a cuticular lamina and sensitive flagellums.
The flagellums are represented by peculiar rigid rods which in their narrowest part,
a neck, near the cuticular membrane, have the diameter of about 0.05 μ, and in the rest
part — about 0.2 μ. The fine structure of the flagellums is known: there is a bundle of
fibrils inside, which is 30–40 A thick (collateral line of fishes). The flagellum’s mem-
brane is the part of the receptor cell’s membrane and each of the flagellums is fixed on
the cuticular lamina with the help of a peculiar rootlet.
Each OHC is provided with 100–120 flagellums which are located in three paral-
lel rows in the form of the letter W, the top of which is turned towards modiolus. The
flagellum’s length in the cochlea’s basal part amounts approximately to 2 μ and increas-
es towards the top up to 6 μ. In a guinea-pig, a cat, a rat and a man the flagellums of
the middle and modiolus row are shorter than those of the distant row; as the investi-
gations with the application of the electron microscope showed, the flagellums only
touch the tectorial membrane, at that the longest of them can be pressed in it.
The OHC contains a lot of organelles: mitochondrions, ribosomes and some spe-
cific inclusions. The mitochondrions are concentrated in the subapical and the basal
part of the cell, as well as along the cell walls. Cytoplasmic membranes form flat cis-
terns which are parallel to the cell walls; the nucleus is located close to the OHC’s basis.
Directly behind the nucleus the central part of the cell’s cylinder contains also
numerous microtubules and vesicles — features, which are typical for the presynaptic
endings.
The inner hair cells (IHC) turned out to be less specialized elements as compared
with the OHC. The basic differences from the latter are: a pear-shaped form, location
of the filaments, distribution of the cytoplasmic organelles and the type of contact with
nerve endings. Besides, the IHC’s body is totally surrounded by the supporting ele-
ments. Sensory filaments, as it is in the OHC, are situated in three rows in the form of
the greatly flattened letter W, the number of the filaments in average amounts to 60,
and in the apical turn they are longer than in the basal one. The distribution of the
mitochondrions in the IHC’s body is not as irregular as it is in the OHC; the nucleus
is located in the center of the cell. In the upper, relative to the nucleus, cytoplasm’s
part numerous Golgi vacuoles can be met, under the nucleus the membranes of the
granular endoplasmic reticulum can be found, as well as mitochondrions. The smooth
endoplasmic reticulum is concentrated in the subapical part mainly, where it has the
form of small tubules and cisterns. The receptor-neuronal contacts are not limited by
the basal part of the cell only, but are irregularly located in the area of the lower two
thirds of the cell. The basal part of the IHC is quite often irregularly shaped with
numerous and noticeable outgrowths.
The most interesting facts are revealed during the study of the inner ear’s structure
in mammals. First of all, this is the existence of two types of receptors belonging to a
different evolutional age (outer and inner hair cells), which are spatially separated from
each other. What is more, it has an extremely small number of the receptor cells and
a sufficient stability in animals of the very variable hearing specializations. The audito-
ry system of echolocating species and animals with low-frequency hearing possesses
235Morphology of the Inner ear in mammals with different ecological peculiarities in ontogeny
approximately equal quantities of the hair cells and the identical character of their dis-
tribution upon the basilar membrane.
According to our point of view, the fact that most mammals, even the species with
extraordinarily broad hearing abilities, have relatively little number of receptors as well
as auditory nerve’s fibres, is connected with a temporary specificity of the acoustic sig-
nal’s perception and processing. This is a consequent receipt of information that allows
simultaneous use of comparatively little quantity of parallel canals in the periphery of
the auditory system (Bogoslovskaya, Solntseva, 1979).
The neurons which innervate the auditory receptor cells form a spiral ganglion: a
nerve-knot of the VIII pair’s acoustic part of the craniocerebral nerves. The ganglion
fills the Rosental’s canal in the cochlea’s axis and repeats the number of its spiral turns.
The ganglionic neuron has, as a rule, a much widened body with two processes: periph-
eral and central. The body is covered with a special, complicatedly constructed myeli-
nated membrane or capsule.
The peripheral process (dendrite) penetrates to the Corti’s organ through an aper-
ture in habenula perforata; cat has 2500 of such apertures (Spoendlin, 1972). The den-
drite is covered with a myelin (medullated) membrane which disappears only at the
entrance of the habenula’s aperture. In the terms of electrophysiology the peripheral
process as well as the central one is an axon since the place of the myelin membrane’s
termination is morphologically similar to the Ranvie’s interception (Engstrom, Wersall,
1958) and according to the existent conceptions this is exactly the area, which is anal-
ogous to the initial neuron’s segment, where the action potential is generated. The cen-
tral processes (axons) form the auditory nerve, which fibres, combined with vestibular
ones, enter the CNS in the area of the medulla’s and pons’s boundary (Bogoslovskaya,
Solntseva, 1979).
There is no consensus of opinion in the literature about how many types of cells
can be distinguished among the spiral ganglion’s neurons. Depending on methods and
purposes of investigation so many different criterions were used that the obtained
results, in spite of their fundamental character, are very hard to coordinate between
each other. We believe that it is very important to quote here the basic points of view
on this question.
The oldest and the most generally accepted discerning of the ganglionic cells is
their division into two types according to their peripheral processes’ distribution. The
neurons with the radial distribution of dendrites innervate the inner hair cells (IHC)
only, at that every neuron contacts with one or two IHC only, but at the same time
each of these cells interacts with many neurons. Such “radial” cells form the over-
whelming majority of the spiral ganglion’s neurons and carry out the projection of the
cochlea to the cerebral centers according to the principle “point to point”. The cells of
the second type have dendrites which go spirally for the major space of the cochlea
turn’s passage and contact with a great amount of the outer hair cells (OHC) which,
in their turn, are connected with the spiral dendrites of many neurons (Smith,
Sjostrand, 1961).
Thereby, two or three (and may be more) neuron types exist in the spiral ganglion
of mammals. However, during the analysis of the different authors’ data it remains
unclear, how are the cell’s types marked out on the basis of different structural criteri-
ons, correlate with each other, since none of them coincide completely with another
by the quantitative indices. The correspondence between the morphological types of the
spiral ganglion’s cells and the characteristics of their reactions and the responses of the
auditory nerve’s fibres which were electrophysiologically registered is not specified up
to now (Bogoslovskaya, Solntseva, 1979).
Such characteristics as the neurons number, their size, the distribution density
along the cochlea’s turns and the correlation with the hair cell’s number are important
236 G. N. Solntseva
indices of the spiral ganglion general structural organization and the auditory function’s
intensity. Unfortunately, because of the difficulties with the material processing the data
have been so far obtained only for several mammalian species.
In mammals of a different hearing specialization the difference in the ganglionic
neurons number is much more significant than in the receptors number. Man and dol-
phins, for example, possess approximately equal quantity of the hair cells while the spi-
ral neurons number increases in echolocating forms in 2–3 times. On average the neu-
ron’s relation to the receptor cells amounts to 4–5.5 : 1 in dolphins, 3 : 1 in a seal and
a cat, and 2 : 1 in a man. For the bat from the Vespertilionidae family it is found to be
6 : 1 (Firbas, Wellenschick, 1973). However, this correlation is inconstant along the
whole of the cochlea’s length and usually gradually decreases from 6 : 1 in the basal
turn to 3 : 1 in the apical end of the organ of Corti.
The auditory nerve represents a complex fibrous system which consists of several
components. Its main part is formed out of the axons or the central processes of the
spiral ganglion’s cells. They transmit the specific information to the primary acoustic
centers, which are located in the CNS (Echandia, 1967). After leaving the cell’s body
the axon passes inside the Rosenthal’s canal where it is usually impossible to track it at
a long distance among other processes. Sometimes in young animals the axon is subdi-
vided into several branches, which are not observed in the adult individuals.
It was shown that the fibres from the apical turn are passing in the center of the
nerve, but beginning from the basal part they are located on the periphery of the nerve
trunk (Sando, 1965).
Consequently, the comparatively-morphological analysis of the mammals’ cochlea
shows that there are two types of its structure. The first structural type can be found in
the mammals whose habitat conditions are not connected with the usage of ultrasonic
orientation. The following features are typical for this type: less developed cochlea’s
basal turn, wide and thick basilar membrane, large distance between the primary and
the secondary osseous spiral laminas, weak development of the secondary lamina and
its disappearance in the cochlea’s apical turns.
The second structural type of the cochlea is present in the species which use ultra-
sonic orientation and echolocation (shrews, rats, bats, fur seals, dolphins). For this type
the following features are typical: noticeable enlarging of the cochlea’s basal turn, nar-
row and thin basilar membrane, small distance between the spiral laminas and well
developed secondary osseous spiral lamina.
The vestibular apparatus of the investigated species consists of the system of mem-
branaceous saccules and closed among themselves canals, which are filled with
endolymph. This system is referred to as a membranaceous labyrinth, which includes a
round sacculus, an oval utriculus, and also three semicircular canals located in three
mutually perpendicular planes. In each of the semicircular canals, there are widenings
(ampullae), which form connections with utriculus. In ampullae, the receptor struc-
tures — ampullar cristae — are located. The receptor structures of sacculus and utricu-
lus are represented by the auditory spots (maculae): saccular macula, located on the
lateral wall of sacculus, utricular macula, located at the basis of utriculus, and macula
neglecta, which is located in the inner ear on the medial wall of utriculus, but in many
species of mammals it is absent. In terrestrial, semi-aquatic and aquatic mammals all
structures of the membranaceous labyrinth differ among themselves in their location in
the inner ear, as well as in their size and form. However, for all species the presence
in maculae of the otolithic membrane of a gelatinous consistence is typical, as well as
the presence of the gelatinous cupula on the tops of the auditory cristae. Macula is the
receptor formation, consisting of the sensory cells, which are covered with the otolith-
ic membrane with small crystals — otoconias, plunged into the otolithic membrane.
237Morphology of the Inner ear in mammals with different ecological peculiarities in ontogeny
The auditory cristae have the similar structure, but opposed to the maculas, the surface
layer of the cristae’ receptor epithelium is covered with a gelatinous cupula.
Other receptor formation of the inner ear is papilla basilaris, which in higher rep-
tilians and birds develops into the auditory organ (papilla acustica basilaris) and in
mammals — into the organ of Corti, which is located in the closed cochlear canal,
involuted into a spiral cochlea.
Relative to each other, the receptor spots of the saccular and utricular maculae
form a right angle. There is an assumption that there are no basic distinctions in the
structure of these maculas (Burlet, de, 1934), however, the electron-microscopic
researches have shown, that the sensory epithelium of the organ of equilibrium consists
of the receptor hair cells of two types. The cells of the first type have a jug-like form
and the cells of the second type — a cylindrical form; more significant distinctions
between both types of the sensory cells are revealed in the connection with the features
of their innervation (Wersall et al., 1965). Studies of other authors have shown that dur-
ing the evolution the receptor cells of the first type have appeared in the inner ear of
mammals in connection with the change of position of the animal’s body in a gravita-
tional field after their coming out on land (Titova, 1968).
As the comparative analysis of the inner ear’s development has shown, in most of
mammals at the stage of 20 pairs of somites (forelimb bud, stage 13), an acoustic vesi-
cle develops.
Both in terrestrial mammals, pinnipeds and cetaceans at the 14–15th stages of
development, the acoustic vesicle is divided into the superior and inferior saccules.
From the inferior saccule, the sacculus and a cochlear canal are formed, and, from the
superior saccule, the utriculus and semicircular canals develop. Both parts are surround-
ed by a condensed mesenchyme. The wall of the acoustic vesicle consists of a single-
layered epithelium. The epithelial thickening of the medial wall of the acoustic vesicle
is an anlage of terminal organs of a labyrinth — macula communis. Macula and the
acoustic vesicle increase in size and are simultaneously divided into superior and infe-
rior parts. By means of an epithelial bridge, these parts are temporarily connected with
each other. Further, the epithelial bridge is replaced by an indifferent epithelium and
two neuroepithelial spots are formed, one of which is located in pars superior and the
other — in pars inferior. The anlage of terminal organs is located in pars superior and
gives rise to the development of macula utriculi and ampullar cristae of the anterior ver-
tical and horizontal semicircular canals. The anlage of terminal organs in pars inferior
forms a process inward and backward in the ampulla of the posterior vertical semicir-
cular canal, forming the ampullar crista.
The other part of this anlage grows in length and is divided into two anlages: a
small top and a big bottom. Out of the top anlage, the saccular macula is formed; the
bottom anlage develops further, forming the anlage of Corti’s organ.
At the 16th stage, the cochlear canal twists spirally, forming a lower, or basal turn
of the cochlea, which is surrounded with an aural capsule, consisting of a condensed
mesenchyme. At the given stage, the formation of the cochlea in terrestrial and semi-
aquatic species maintains behind the formation of the equilibrium organ.
In most investigated species the semicircular canals are very narrow in diameter.
Sacculus and utriculus are of a small size and have a roundish or an oval form.
At the same stage of development, in representatives of different ecological groups,
the sites of the upper part of the wall of the superior saccule thicken, and flat recesses
are formed from them; their opposite walls adjoin each other. Later on, these places of
the adhesion resolve and, from the external parts of the recesses, the semicircular canals
are formed. The inferior and posterior vertical semicircular canals develop from a com-
mon anlage, their back ends fall into the middle part of utriculus. The other ends of
238 G. N. Solntseva
the semicircular canals fall directly into utriculus, as a result of what the widenings
(ampullae) are formed.
At the 17th stage of development, the lumens of the semicircular canals, as well as
the size of sacculus, utriculus and the auditory cristae increase. In otariids, as well as
in terrestrial species, the initial cellular differentiation of the sensory epithelium into
receptor and supporting cells is marked in the utricular macula. In odontocetes and
mysticetes the earlier differentiation of the sensory epithelium is marked in saccular
macula, while in phocids and in a walrus the cellular differentiation is marked neither
in saccular macula, nor in utricular macula.
At the given stage of development, in all investigated species, the cochlear appa-
ratus is represented by a cochlear canal of a slit-like form, whose basis, formed by a
columnar epithelium, and a roof, consisting of cells of a cuboidal epithelium, are well-
discernable.
In terrestrial species, otariids and in a walrus, the size of the vestibular apparatus
surpasses the size of the cochlear part of the inner ear twice, the lumens of the semi-
circular canals are wide, utriculus has an oval form and sacculus has a roundish form
(fig. 4). In phocids, the size of the cochlear and vestibular parts of the inner ear reveals
similar size, while the form and size of sacculus, utriculus and semicircular canals keeps
similarity with terrestrial species. In cetaceans, the vestibular apparatus is extraordinary
small. The connection between utriculus and sacculus is carried out by means of a nar-
row canal (ductus utriculosaccularis), which opens into ductus endolymphaticus.
Utriculus is connected with sacculus by means of a sacculo-endolymphatic canal. In
the cochlear part of the inner ear, the medial turn of the cochlea is formed. Structures
of the cochlear canal are not formed; the cellular differentiation of Corti’s organ is
absent.
In all studied species of mammals, at the 18th stage of development, an increase
in the size of structures of the vestibular apparatus occurs proportionally to the growth
of a prefetus. In otariids, as well as in the species, whose way of life is in a greater
degree connected with the stay on a firm substratum, the increase of size of all struc-
tures of the vestibular apparatus occurs proportionally to the increase of the cochlea’s
size. In absolute hydrobionts (cetaceans), the increase of the cochlea’s size consider-
ably outstrips the growth of structures of the organ of equilibrium. The receptor spot of
the utricular macula acquires the more horizontal position in relation to the receptor
spot of the saccular macula, which lies almost vertically. As a result, both spots form a
right angle relative to each other. Maculas represent the receptor formations covered by
a columnar epithelium. Each of them carries a strongly specific function.
In cetaceans and pinnipeds, as well as in terrestrial species, in the formed ampul-
lae of the semicircular canals, the ampullar cristae are located; their receptor epitheli-
um according to its structure is similar to the receptor epithelium of maculae. Above
the surface of the sensory epithelium, the otolithic membrane, which in aquatic species
is much thinner than in terrestrial and semiaquatic mammals, is located. In cetaceans,
the ampullar crista is big and occupies a significant part of the ampullar space of the
semicircular canals. The receptor epithelium covers the whole surface of the crista. At
the given stage, contrary to the anterior and posterior vertical semicircular canals, the
formation of the horizontal semicircular canal continues in all studied species. In
humans, the growth of the horizontal and posterior vertical semicircular canals comes
to an end by the 7th month of the prenatal life, while the growth of the anterior verti-
cal semicircular canal — only by the moment of birth. The author connects it with the
fact that in comparison with the posterior vertical and horizontal semicircular canals,
the anterior vertical semicircular canal is vitally important to the developing fetus, as
this structure takes part in the fixation of a body in a vertical position.
239Morphology of the Inner ear in mammals with different ecological peculiarities in ontogeny
The differentiation of the sensory epithelium of maculas and cristae is marked in
all investigated animals. In a walrus, the initial cellular differentiation is observed in the
utricular macula, as well as in terrestrial species. Phocids are characterized by the
simultaneous differentiation of the sensory epithelium in the utricular and saccular
maculae. In cetaceans, the initial cellular differentiation of the sensory epithelium is
marked only in one site of the saccular macula.
At the given stage, the formation of the cochlea finishes with the formation of the
last apical turn. In representatives of odontocetes (Stenella attenuata, Delphinapterus
leucas), the height of the cochlea amounts to 2.0 turns; in pinnipeds (Eumetopias juba-
tus, Erignathus barbatus, Pusa hispida, Odobenus rosmarus divergens) and in representa-
240 G. N. Solntseva
Fig. 4. Histotopography of the peripheral part of the auditory system in dorsoventral sections of prefetal heads
of Sus scrofa domestica, stages 18,19. The cochlea is formed, as in definitive forms; an anatomical formation
of the vestibular apparatus is completed. 1 — cochlear canal; 2 — scala vestibuli; 3 — scala tympani; 4 —
cochlea; 5 — cochlear nerve; 6 — auditory capsule; 7 — sacculus; 8 — utriculus; 9 — semicircular canal; 10 —
musculus stapedius; 11 — stapes; 12 — incus; 13 — malleus; 14 — membrane tympani; 15 — external auditory
meatus; 16 — cerebrum.
Ðèñ. 4. Ãèñòîòîïîãðàôèÿ ïåðèôåðè÷åñêîãî îòäåëà ñëóõîâîé ñèñòåìû â äîðñîâåíòðàëüíûõ ñðåçàõ
ãîëîâû ó ïðåäïëîäîâ äîìàøíåé ñâèíüè (Sus scrofa domestica), ñòàäèè 18–19. Óëèòêà ñôîðìèðîâàíà,
êàê è ó äåôèíèòèâíûõ ôîðì; çàêîí÷èëîñü àíàòîìè÷åñêîå ôîðìèðîâàíèå âåñòèáóëÿðíîãî àïïàðàòà.
1 — óëèòêîâûé êàíàë; 2 — âåñòèáóëÿðíàÿ ëåñòíèöà; 3 — áàðàáàííàÿ ëåñòíèöà; 4 — óëèòêà; 5 —
êîõëåàðíûé íåðâ; 6 — óøíàÿ êàïñóëà; 7 — ñàêêóëþñ; 8 — óòðèêóëþñ; 9 — ïîëóêðóæíûé êàíàë; 10 —
ñòðåìåííàÿ ìûøöà; 11 — ñòðåìÿ; 12 — íàêîâàëüíÿ; 13 — ìîëîòî÷åê; 14 — áàðàáàííàÿ ïåðåïîíêà;
15 — íàðóæíûé ñëóõîâîé ïðîõîä; 16 — ìîçã.
tives of mysticetes (Âàlaenoptera acutorostrata) — 2.5 turns. In terrestrial species (Sus
scrofa domestica, Rattus norvegicus), the cochlea is formed by 3 turns and in bats
(Rhinolophus ferrumequinum) — by 3.5 turns. In some terrestrial mammals, the height
of the cochlea reaches 4.5 turns (Cavia porcellus). The elements of the cochlear canal
are not formed and the cells of Corti’s organ are at the same stage of differentiation in
all turns of the cochlea. From the columnar epithelium of the cochlear canal, two
thickenings are formed: axial and lateral; from them the structures of the cochlear canal
and the cells of the organ of Corti develop.
At the 19th stage of development, in saccular macula, the differentiation of the
sensory epithelium into receptor and supporting cells occurs simultaneously in several
sites of maculas and cristae, spreading over the most part of their surface. The struc-
ture of the cells, which, as well as the cells of the organ of Corti, form a mosaic dis-
tribution pattern, is well-discernable. The neurons of the vestibular ganglion contain big
nuclei of an oval form with expressed nucleoli. The size of all structures of the organ
of equilibrium is considerably increased. In otariids and in a walrus, as well as in ter-
restrial mammals, the size of utriculus surpasses the size of sacculus. In cetaceans, the
utriculus and sacculus are similar in size with that in phocids.
In cochlea, formation of the elements of the cochlear canal is marked (fig. 5). The
flattening of the cells of a cuboidal epithelium and the loosening of connective tissue,
adjacent to this epithelium, occurs. In this place, the tympanic and vestibular scalae are
formed. The Reissner’s membrane is formed. The differentiation of the cells of the
organ of Corti begins in the basal turn of cochlea from the moment when the cells of
a columnar epithelium start to move apart, and is spread gradually over the turns locat-
ed above. As a result, in all turns of the cochlea a different degree of anatomic and cel-
lular differentiation is observed.
241Morphology of the Inner ear in mammals with different ecological peculiarities in ontogeny
Fig. 5. Histotopography of the peripheral part of the auditory system in dorsoventral sections of the head of
a prefetal Eumetopias jubatus, stages 18, 19. An initial differentiation of the elements of the cochlear canal is
marked in the cochlea. 1 — cochlear canal; 2 — cochlear ganglion; 3 — cochlea; 4 — cochlear nerve; 5 —
auditory capsule; 6 — sacculus; 7 — utriculus; 8 — vestibular nerve; 9 — acoustic nerve; 10 — musculus
stapedius; 11 — cerebrum.
Ðèñ. 5. Ãèñòîòîïîãðàôèÿ ïåðèôåðè÷åñêîãî îòäåëà ñëóõîâîé ñèñòåìû â äîðñîâåíòðàëüíûõ ñðåçàõ
ãîëîâû ó ïðåäïëîäà ñèâó÷à (Eumetopias jubatus), ñòàäèè 18, 19.  óëèòêå îòìå÷åíà íà÷àëüíàÿ äèôôå-
ðåíöèðîâêà ýëåìåíòîâ óëèòêîâîãî õîäà. 1 — óëèòêîâûé êàíàë; 2 — êîõëåàðíûé ãàíãëèé; 3 — óëèòêà;
4 — êîõëåàðíûé íåðâ; 5 — óøíàÿ êàïñóëà; 6 — ñàêêóëþñ; 7 — óòðèêóëþñ; 8 — âåñòèáóëÿðíûé íåðâ;
9 — ñëóõîâîé íåðâ; 10 — ñòðåìåííàÿ ìûøöà; 11 — ìîçã.
In otariids and in a walrus, at the 20th stage of development, the vestibular appa-
ratus is twice bigger than the cochlear part, as well as it is in terrestrial mammals; in
phocids their size reveals similarities. In cetaceans, the vestibular apparatus is twice
smaller than the cochlea. The cellular differentiation of the sensory epithelium of mac-
ulae, cristae and the organ of Corti continues. The cochlear and vestibular branches of
the auditory nerve are formed.
In the cochlear canal, a spiral limb, a vascular stria and a tectorial membrane are
formed. The differentiation of the cells of the organ of Corti continues. The size of the
cochlea is increased. At the given stage, the basic process of anatomic formation of the
structures of the inner ear has ended.
Discussion
Both in phylogenesis and in ontogenesis the inner ear is the first to form, as it is
the core, phylogenetically most ancient formation of the peripheral auditory system. As
the development of the inner ear continues, the other parts of the peripheral auditory
system of different evolutionary age start to be formed, the most evolutionary young
among them is the outer ear.
The comparative analysis of development of the auditory and vestibular structures
in representatives of terrestrial, semi-aquatic and aquatic mammals has shown that the
formation of these structures occurs in an early prefetal period and is extended in time
that is caused by the presence of the heterochrony in the development of the inner ear
(Solntseva, 1999, 2002).
In representatives of different ecological groups, in an early embryogenesis, the
auditory and vestibular structures are simultaneously separated from each other and
reveal similar features in structure. In most of mammals, in the first half of an early
prefetal period (stages 13–15), both auditory and vestibular formations have common
features in structure. Specific features in the structural organization of the hearing and
equilibrium organs are formed in the second half of an early prefetal period (stages
16–20) at similar stages of development and in a certain sequence. Basically, in imma-
ture-born species, the anatomic formation of structures of the inner ear comes to an
end in an early prefetal period, while the cellular differentiation of the sensory epithe-
lium of the cochlea, maculae and cristae continues up to the early stages of a postna-
tal ontogenesis. In mature-born species (cetaceans), the differentiation of structures of
the inner ear finishes by the moment of birth.
In studied groups of mammals, the features, which are connected with the stages
of differentiation of the sensory epithelium of maculae and cristae into the receptor and
supporting cells, are revealed. In terrestrial and semi-aquatic mammals (otariids, a wal-
rus), whose way of life to a greater degree is connected with the stay on a firm substra-
tum, the initial cellular differentiation of the sensory epithelium occurs in the utricular
macula that indicates the important role of the organ of gravitation in the vital activi-
ty of these mammals. The simultaneous cellular differentiation of the sensory epitheli-
um in the saccular and utricular maculae, as well as the similarity of size of the cochlear
and vestibular parts of the inner ear in phocids allow for assumption that for these
species the organs of gravitation and vibration are equally vitally important. Each of
these organs is adapted for functioning in the habitat with certain physical properties.
In absolute hydrobionts (cetaceans), the initial cellular differentiation of the saccular
macula indicates that in aquatic mammals the organ of vibration carries out a more
important function in comparison with the organ of gravitation.
All parts of the peripheral auditory system are multicomponent formations. As
against the outer and middle ear, which are characterized by very diverse structural vari-
ations and a wide spectrum of the adaptable transformations connected with peculiar-
242 G. N. Solntseva
ities of the species ecology, the inner ear in representatives of different ecological
groups, in spite of the variety of functions, keeps a monotonous structural organization.
Usually, both in the cochlear and vestibular analyzers the topography, form and size of
separate components vary.
In the echolocating mammals, the substantial growth of the cochlea’s size in com-
parison with the size of the vestibular apparatus, as well as other features in the struc-
ture of the cochlear canal and the cells of Corti’s organ’s, serves as the adaptation of
the cochlea to the perception of frequencies of a wide range, including ultrasounds
(dolphins, bats). At the same time, a huge cochlea and extraordinary small size of the
vestibular apparatus in absolute hydrobionts with a various orientation of hearing can
serve as the adaptations of the inner ear to aqueous medium, as hearing in the aquat-
ic mammals dominates among distant analyzers, thus providing the survival of these
animals in conditions of constant dwelling in aquatic environment.
Comparative study of the peripheral auditory system’s development allowed to
reveal the general regularities of its formation in ontogenesis of representatives of vari-
ous ecological groups: (1) in most mammals at the early stages of development (st.
13–16), the peripheral auditory system has common basic features in structure; (2)
species-specific features in the structural organization of the peripheral auditory system
are formed in the early prefetal period, depending on the frequency tuning of the audi-
tory system in each species; (3) these structural features are caused by habitat peculiar-
ities and develop in parallel from the homologous anlages of the peripheral auditory sys-
tem in phylogenetically distant and close forms; (4) in mammals, the morphological
features of the peripheral auditory system, which were formed in an early prefetal peri-
od, continue to develop in a fetal period and during the whole period of a postnatal
development.
This work was supported by the International Science Foundation (Project NF 3000). Embryos of
cetaceans and pinnipeds were obtained from colleagues at several institutes of the Russian Ministry of Fish
Industry (Moscow, Vladivostok, Kaliningrad, Archangelsk, Astrachan). The unique collection of Stenella
attenuata was passed to me by the well-know American researcher of marine mammals, Dr. William F. Perrin
(La Jolla, USA). I am grateful to all colleagues for providing the embryological material.
Akimov V. N. About morphological and functional heterogeneity of the rows of outer hair cells of the cochlear
spiral ganglion in guinea pig // Vestnik otorinolaryngologii — 1976. — 3. — P. 16–19. — Russian :
Àêèìîâ Â. Í. Î ìîðôîëîãè÷åñêîé è ôóíêöèîíàëüíîé íåîäíîðîäíîñòè ðÿäîâ íàðóæíûõ âîëîñ-
êîâûõ êëåòîê ñïèðàëüíîãî óëèòêè ìîðñêîé ñâèíêè // Âåñòíèê îòîðèíîëàðèíãîëîãèè.
Bogoslovskaya L. S., Solntseva G. N. The Auditory system of mammals. — Moscow : Nauka, 1979. —
238 p. — Russian : Áîãîñëîâñêàÿ Ë. Ñ., Ñîëíöåâà Ã. Í. Ñëóõîâàÿ ñèñòåìà ìëåêîïèòàþùèõ.
Burlet H. M. de Vergleichende Anatomie des statoakustischen organs // Handb. Vergl. Anat. Wirb. — 1934. —
2, N 2. — P. 1293.
Dyban A. P., Puchkov V. F., Baranov V. S. et al. The laboratory mammals: a mouse Mus musculus, a rat
Rattus norvegicus, a rabbit Oryctolagus cuniculus, a hamster Cricetus griseous // Subjects of
Developmental Biology. — Moskow : Nauka, 1975. — P. 505–563. — Russian : Äûáàí À. Ï., Ïó÷-
êîâ Â. Ô., Áàðàíîâ Â. Ñ. è äð. Ëàáîðàòîðíûå ìëåêîïèòàþùèå: ìûøü Ìus musculus, êðûñà Rattus
norvegicus, êðîëèê Oryctolagus cuniculus, õîìÿ÷îê Cricetus griseous. // Î6úåêòû áèîëîãèè
ðàçâèòèÿ.
Echandia R. L. R. An electron microscopic study on the cochlear innervation. I. The recepto-neural junctions
at the outer hair cells // Z. Zellforsch. — 1967. — 78. — P. 30–46.
Engstrom H., Wersall J. Structure and innervation of the inner ear sensory epithelia // Intern. Rev. of
Cytol. — 1958. — 7. — P. 535.
Firbas W., Welleschik B. A quantitative study on the spiral ganglion of the chiroptera // Period.
Biologorum. — 1973. — 75, N 1 — P. 67—70.
Fleischer G. Studien am Skelett des Gehororgans der Saugetiere, einschliesslich des Menschen // Saugetierk.
Mitt. — 1973. — 21, H. 2—3 — P. 131.
Gagloeva K. E. Topographo-anatomical relations of the peripheral part of the auditory analyzer in a
comparative-anatomical aspect // Functional and Structural Foundations of Systemic Functioning and
the Mechanisms of Brain Plasticity. — Moscow : Medgiz, 1976. — P. 14–17. — Russian : Ãàãëîåâà Ê. Å.
Òîïîãðàôî-àíàòîìè÷åñêèå âçàèìîîòíîøåíèÿ ïåðèôåðè÷åñêîãî çâåíà ñëóõîâîãî àíàëèçàòîðà â ñðàâ-
243Morphology of the Inner ear in mammals with different ecological peculiarities in ontogeny
íèòåëüíî-àíàòîìè÷åñêîì àñïåêòå // Ôóíêöèîíàëüíûå ñòðóêòóðíûå îñíîâû ñèñòåìíîé äåÿòåëüíîñ-
òè è ìåõàíèçìû ïëàñòè÷íîñòè ìîçãà.
Kolmer W. Uber das hautige Labyrinth des Delphins // Anat. Anz. — 1908. — 32. — S. 295–300.
Ramprashad F., Ronald K., Geraci J., Smith T. G. A comparative study of surface preparations of the organ
of Corti of the harp seal (Pagophilus groenlandicus, Erxleben, 1777) and the ringed seal (Pusa hispida).
I. Sensory cell population and density // Canad. J. Zool. — 1976. — 54, N 1. — P. 1–9.
Sando I. The anatomical interrelationships of the cochlear nerve fibers // Acta oto-laryngol. — 1965. — 59. —
P. 417–436.
Smith C. A., Sjostrand F. S. A sinaptic structure in the hair cells of the guinea pig cochlea // J. Ultrastruct.
Res. — 1961. — 5. — P. 184–192.
Solntseva G. N. Development of the auditory organ in terrestrial, semi-aquatic, and aquatic mammals //
J. Aquatic Mammals — 1999. — 25, N 3. — P. 135–148.
Solntseva G. N. Early embryogenesis of the vestibular apparatus in mammals with different ecologies //
J. Aquatic Mammals. — 2002. — 28, N 2. — P. 159–169.
Spoendlin H. Innervation densities of the cochlea // Acta otolaryngol. — 1972. — 73. — P. 235–247.
Titova L. K. Development of receptor structures in the inner ear of vertebrates. — Leningrad : Nauka,
1968. — 217 p. — Russian : Òèòîâà Ë. Ê. Ðàçâèòèå ðåöåïòîðíûõ ñòðóêòóð âíóòðåííåãî óõà
ïîçâîíî÷íûõ.
Wever E. G., McCormick J. G., Ðàlin J., Ridgway S. H. The cochlea of the dolphin, Tursiops truncatus: hair
cells and ganglion cells // Proc. Nat. Acad. Sci. USA — 1971. — 68. — P. 2908–2912.
Wersall J., Frock A., Lundquist P. G. Sructural basis for directional sensitivity in cochlear and vestibular
sensory receptors // Cold spring Harbor Symp. Quant. Biol. — 1965. — 30. — P. 115–145.
Yàmàdà M. Contribution to the anatomy of the organ of hearing of Whales // Sci. Repts Whales Res. Inst. —
1953. — 8. — P. 1–79.
244 G. N. Solntseva
|