Lagenar Nerve Research Articles

Inner ear morphology of Adalatherium hui (Mammalia, Gondwanatheria) from the Late Cretaceous of Madagascar

ABSTRACT The cochlear canal of Adalatherium hui, from the Late Cretaceous of Madagascar, exhibits a combination of features previously unknown among mammaliaforms. The cochlear canal of Adalatherium is short and ‘C’-shaped (curved through at least 210°). A presumptive lagenar nerve canal extends from the apex of the cochlea to the internal acoustic meatus. In conjunction with an apical expansion of the cochlear canal, this morphology suggests that Adalatherium retained a lagenar macula. Adalatherium is derived among mammaliaforms in possessing primary and secondary osseous laminae, a cribriform plate, and a distinct cochlear ganglion canal. Strikingly, Adalatherium shows a single-layered primary osseous lamina that lacks internal, radially oriented canaliculi for auditory nerve fibers. In this respect, the primary lamina of Adalatherium is structurally different from the double-layered primary lamina containing habenulae perforatae of extant therians. Furthermore, Adalatherium resembles the gondwanatherian Vintana in possessing a secondary canal running parallel to the cochlear ganglion canal. Although its exact role and homology are uncertain, the morphology of this secondary canal and its tributary canaliculi is most consistent with a vascular function. The inner ear of Adalatherium augments a growing list of characters (or character combinations) in which gondwanatherians are not only different from the inferred plesiomorphic condition for mammaliaforms but also distinct from the derived characters of therians. Collectively, the new morphological and phylogenetic data support homoplastic transformation of such structures as the cribriform plate and primary osseous lamina in mammals and independent loss of the lagenar macula within gondwanatherians.

Inner ear labyrinth anatomy of monotremes and implications for mammalian inner ear evolution.

The monophyletic clade Monotremata branches early from the rest of the mammalian crown group in the Jurassic and members of this clade retain many ancestral mammalian traits. Thus, accurate and detailed anatomical descriptions of this group can offer unique insight into the early evolutionary history of Mammalia. In this study, we examine the inner ear anatomy of two extant monotremes, Ornithorhynchus anatinus and Tachyglossus aculeatus, with the primary goals of elucidating the ancestral mammalian ear morphology and resolving inconsistencies found within previous descriptive literature. We use histological serial sections and high-resolution microcomputed tomography (µCT) for correlating soft tissue features of the vestibule and cochlea to the osseous labyrinth endocast. We found that in both monotremes the scala tympani coils to a lesser degree than scala vestibuli and scala media, although all three scalae show an apical coil inside the osseous cochlear tube. The helicotrema (conduit between scala tympani and scala vestibuli) is in subapical position, and the cochlear and lagenar ganglia and their associated nerve fibers are not enclosed by bone. In comparison, in extant therian mammals (i.e., marsupials and placentals) the helicotrema is located at the apex of the osseous cochlear canal, the three scalae coil to the same degree and the cochlear ganglion is enclosed by the primary bony lamina. Whether the lagenar ganglion is lost in therian mammals or integrated into the cochlear ganglion is still debated. The presence of a sensory lagenar macula at the apex of the membranous cochlear duct, innervated by a separate lagenar nerve and ganglion is a plesiomorphic condition of amniotes that monotremes share. A separate osseous lagenar canaliculus for the lagenar nerve, and the coiling of the distended lagenar sac at the end of the cochlear duct are autapomorphies of monotremes. Based on our findings we hypothesize that the ancestral inner ear of stem mammaliaforms is characterized by a straight or slightly curved osseous cochlear canal, a lagenar macula, lagenar nerve fibers separated from a larger bundle of cochlear nerve fibers, the presence of an organ of Corti and an intra-otic cochlear ganglion suspended by membranous connective tissue. Among the major Mesozoic clades of crown mammals, cladotherians and gondwanatherians most likely acquired a fully functioning organ of Corti but lost the sensory lagenar macula, like extant therians. However, Mesozoic spalacotherioids, multituberculates and eutriconodonts likely retained the mammaliaform condition. J. Morphol. 278:236-263, 2017. © 2016 Wiley Periodicals,Inc.

Reinvestigation of the basicranium of Haldanodon exspectatus (Mammaliaformes, Docodonta)

ABSTRACT The docodont Haldanodon exspectatus, a mammaliaform from the Late Jurassic of Portugal, is a crucial taxon for studying higher-level relationships of mammaliaforms and their morphological evolution. Based on high-resolution computed tomography scanning of three specimens of Haldanodon, we developed a new reconstruction of the basicranium including the petrosal and the inner ear. Our study confirms that Haldanodon and other basal mammaliaforms, such as Morganucodon and Sinoconodon, are similar in the main characteristics of their external anatomy of the petrosal. However, Haldanodon shows several derived features that support a phylogenetic position of docodonts more derived than Morganucodon and Sinoconodon: (1) elongated and curved cochlear canal (nearly 180°), (2) single lateral flange foramen of petrosal, (3) absence of anterior paroccipital process, and (4) squamosal constriction. The bony labyrinth reveals a secondary crus commune, which is regarded to be a plesiomorphic feature of the mammaliaform groundplan. The cochlear canal shows an apical inflation connected to a distinct sulcus and a separate notch in the internal acoustic meatus, supporting the existence of a lagenar nerve and macula as in monotremes. Haldanodon is unique among Mesozoic mammaliaforms in having a hypertrophied paroccipital region that is excavated into large tympanic pneumatic recesses, which are connected with the extensive porous and probably also pneumatic internal structures of the surrounding bones. The curved cochlear canal and the pneumatized middle ear region support the hypothesis that Haldanodon had more effective low-frequency hearing as an adaptation to a fossorial mode of life.

Dipole source encoding and tracking by the goldfish auditory system

In goldfish and other otophysans, the Weberian ossicles mechanically link the saccule of the inner ear to the anterior swimbladder chamber (ASB). These structures are correlated with enhanced sound-pressure sensitivity and greater sensitivity at high frequencies (600-2000 Hz). However, surprisingly little is known about the potential impact of the ASB on other otolithic organs and about how auditory responses are modulated by discrete sources that change their location or orientation with respect to the ASB. In this study, saccular and lagenar nerve fiber responses and conditioned behaviors of goldfish were measured to a small, low-frequency (50 Hz) vibrating sphere (dipole) source as a function of its location along the body and its orientation with respect to the ASB. Conditioned behaviors and saccular nerve fiber activity exhibited response characteristics nearly identical to those measured from a hydrophone in the same relative position as the ASB. By contrast, response patterns from lagena fibers could not be predicted by pressure inputs to the ASB. Deflation of the ASB abolished the characteristic spatial response pattern of saccular but not lagena fibers. These results show that: (1) the lagena is not driven by ASB-mediated pressure inputs to the ear; (2) the ASB-saccule pathway dominates behavioral responsiveness, operating effectively at frequencies as low as 50 Hz; and (3) behavioral and neural (saccular) responses are strongly modulated by the position and orientation of the dipole with respect to the ASB.

Second-order vestibular neurons form separate populations with different membrane and discharge properties.

Membrane and discharge properties were determined in second-order vestibular neurons (2 degrees VN) in the isolated brain of grass frogs. 2 degrees VN were identified by monosynaptic excitatory postsynaptic potentials after separate electrical stimulation of the utricular nerve, the lagenar nerve, or individual semicircular canal nerves. 2 degrees VN were classified as vestibulo-ocular or -spinal neurons by the presence of antidromic spikes evoked by electrical stimulation of the spinal cord or the oculomotor nuclei. Differences in passive membrane properties, spike shape, and discharge pattern in response to current steps and ramp-like currents allowed a differentiation of frog 2 degrees VN into two separate, nonoverlapping types of vestibular neurons. A larger subgroup of 2 degrees VN (78%) was characterized by brief, high-frequency bursts of up to five spikes and the absence of a subsequent continuous discharge in response to positive current steps. In contrast, the smaller subgroup of 2 degrees VN (22%) exhibited a continuous discharge with moderate adaptation in response to positive current steps. The differences in the evoked spike discharge pattern were paralleled by differences in passive membrane properties and spike shapes. Despite these differences in membrane properties, both types, i.e., phasic and tonic 2 degrees VN, occupied similar anatomical locations and displayed similar afferent and efferent connectivities. Differences in response dynamics of the two types of 2 degrees VN match those of their pre- and postsynaptic neurons. The existence of distinct populations of 2 degrees VN that differ in response dynamics but not in the spatial organization of their afferent inputs and efferent connectivity to motor targets suggests that frog 2 degrees VN form one part of parallel vestibulomotor pathways.

Acoustic response properties of lagenar nerve fibers in the sleeper goby, Dormitator latifrons

Auditory and vestibular functions of otolithic organs vary among vertebrate taxa. The saccule has been considered a major hearing organ in many fishes. However, little is known about the auditory role of the lagena in fishes. In this study we analyzed directional and frequency responses from single lagenar fibers of Dormitator latifrons to linear accelerations that simulate underwater acoustic particle motion. Characteristic frequencies of the lagenar fibers fell into two groups: </=50 Hz and 80-125 Hz. We observed various temporal response patterns: strong phase-locking, double phase-locking, phase-locked bursting, and non-phase-locked bursting. Some bursting responses have not been previously observed in vertebrate otolithic nerve fibers. Lagenar fibers could respond to accelerations as small as 1.1 mm s(-2). Like saccular fibers, lagenar fibers were directionally responsive and decreased directional selectivity with stimulus level. Best response axes of the lagenar fibers clustered around the lagenar longitudinal axis in the horizontal plane, but distributed in a diversity of axes in the mid-sagittal plane, which generally reflect morphological polarizations of hair cells in the lagena. We conclude that the lagena of D. latifrons plays a role in sound localization in elevation, particularly at high stimulus intensities where responses of most saccular fibers are saturated.

Peripheral origins and functional characteristics of vibration-sensitive VIIIth nerve fibers in the frog Rana temporaria

1) The peripheral origins of vibration-sensitive VIIIth nerve fibers in European grassfrogs (Rana temporaria) were investigated by recording from individual nerve branchlets within the inner ear. Furthermore, the fibers' responses to both pulsed and continuous, dorsoventral, sinusoidal vibrations were studied. 2) Vibration-sensitive fibers were found in both the anterior and posterior branch of the VIIIth nerve. 3) No vibration-sensitive fibers were found in the lagenar nerve. 4) The vibration-sensitive fibers in the posterior branch probably innervated the amphibian papilla and many of these fibers also responded to low-frequency sound. 5) The vibration-sensitive fibers in the anterior branch probably innervated the sacculus and the utriculus. 6) Hence, the grassfrog has at least two, and probably three, vibration-sensitive organs in the inner ear. 7) All fibers had V-shaped vibrational tuning curves. In the posterior branch best frequencies (BFs) ranged from 10 to 300 Hz, in the anterior branch from 10 to 100 Hz. In the posterior branch spike-rate thresholds at BF ranged from 0.04 to 1.28 cm/s2, in the anterior branch from 0.02 to 1.28 cm/s2. All fibers showed strong synchronization to the stimulus waveform, particularly at low frequencies.

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

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

On the Polarization and Innervation of the Pars Inferior Sensory Epithelia of the Herring Labyrinth

AbstractThe macula sacculi and the macula lagenae of the herring, Clupea harengus L., were examined by light microscopy, the macula lagenae is large compared to what is normal among non‐ostariophysan fishes, the morphological polarization of the hair cells in the inferior maculae shows a pattern which is similar to that usually seen in teleost fishes. The fibres in the nerves supplying the macula sacculi and the macula lagenae were counted and their diameters measured. The ramulus saccularis is divided in two separate ramuli innervating populations of hair cells with different morphological polarization. The saccular rostral nerve trunk contains 1800–2300 fibres, with 1300–1800 fibres in the caudal nerve trunk. The lagenar nerve is composed of 2100–4000 fibres. The fibre diameters are 1–14 μm in all ramuli. Silver staining of the nerve axoplasm reveals a unique differentiation of the maculae, which can be divided into a central area surrounded by a peripheral part. The hair cells in the central area are innervated by thick nerve fibres (5–14 μm diameter) as well as a few thin nerve fibres (about 1 μm diameter), while the receptor cells in the peripheral area are exclusively innervated by thin fibres having diameters of 2 μm or less.

Response patterns of neurons in the lagenar branch of the goldfish auditory nerve

The response of single fibers of the goldfish lagenar nerve were recorded extracellularly in response to tonal stimuli generated by a loudspeaker. Measures were made of both the average impulse rate and the degree of phase locking at a number of different stimulus frequencies and sound pressure levels. Phase locking was determined to be a more sensitive and reliable measure of sound pressure sensitivity than impulse rate. Unit tuning curves constructed using phase-locking criteria showed low-pass characteristics above 150 Hz. Wide variability was observed in sensitivity, bandwidth, spontaneous activity and adaptation. Lagenar fibers overlap in sensitivity with type II saccular neurons described by Fay [J. Acoust. Soc. Am. 60, S80 (A) (1976)]. The discharge patterns of lagenar and saccular neurons were analyzed in response to direct vibration of the head and were found to have quite similar directional sensitivities. The results are discussed in terms of the information available to the fish for auditory localization and distance perception. [Work supported by the NSF.]