Determinants of spatial and temporal coding by semicircular canal afferents

The vestibular semicircular canals are internal sensors that signal the magnitude, direction, and temporal properties of angular head motion. Fluid mechanics within the 3-canal labyrinth code the direction of movement and integrate angular acceleration stimuli over time. Directional coding is accomplished by decomposition of complex angular accelerations into 3 biomechanical components-one component exciting each of the 3 ampullary organs and associated afferent nerve bundles separately. For low-frequency angular motion stimuli, fluid displacement within each canal is proportional to angular acceleration. At higher frequencies, above the lower corner frequency, real-time integration is accomplished by viscous forces arising from the movement of fluid within the slender lumen of each canal. This results in angular velocity sensitive fluid displacements. Reflecting this, a subset of afferent fibers indeed report angular acceleration to the brain for low frequencies of head movement and report angular velocity for higher frequencies. However, a substantial number of afferent fibers also report angular acceleration, or a signal between acceleration and velocity, even at frequencies where the endolymph displacement is known to follow angular head velocity. These non-velocity-sensitive afferent signals cannot be attributed to canal biomechanics alone. The responses of non-velocity-sensitive cells include a mathematical differentiation (first-order or fractional) imparted by hair-cell and/or afferent complexes. This mathematical differentiation from velocity to acceleration cannot be attributed to hair cell ionic currents, but occurs as a result of the dynamics of synaptic transmission between hair cells and their primary afferent fibers. The evidence for this conclusion is reviewed below.     

Spatial orientation of semicircular canals and afferent sensitivity vectors in pigeons

Rotational head motion in vertebrates is detected by the semicircular canal system, whose innervating primary afferent fibers carry information about movement in specific head planes. The semicircular canals have been qualitatively examined over a number of years, and the canal planes have been quantitatively characterized in several animal species. The present study first determined the geometric relationship between individual semicircular canals and between the canals and the stereotactic head planes in pigeons. Stereotactic measurements of multiple points along the circumference of the bony canals were taken, and the measured points fitted with a three-dimensional planar surface. Direction normals to the plane's surface were calculated and used to define angles between semicircular canal pairs. Because of the unusual shape of the anterior semicircular canals in pigeons, two planes, a major and a minor, were fitted to the canal's course. Calculated angle values for all canals indicated that the horizontal and posterior semicircular canals are nearly orthogonal, but the anterior canals have substantial deviations from orthogonality with other canal planes. Next, the responses of the afferent fibers that innervate each of the semicircular canals to 0.5 Hz sinusoidal rotation about an earth-vertical axis were obtained. The head orientation relative to the rotation axis was systematically varied so that directions of maximum sensitivity for each canal afferent could be determined. These sensitivity vectors were then compared with the canal plane direction normals. The afferents that innervated specific semicircular canals formed homogeneous clusters of sensitivity vectors in different head planes. The horizontal and posterior afferents had average sensitivity vectors that were largely coincident with the innervated canal plane direction normals. Anterior canal afferents, however, appeared to synthesize contributions from the major and minor plane components of the bony canal structure to produce a resultant sensitivity vector that was positioned between the canal planes. Calculated angles between the average canal afferent sensitivity vectors revealed that direction orthogonality is preserved at the afferent signal level, even though deviations from canal plane orthogonality exist.     

Principles of linear and angular vestibuloocular reflex organization in the frog.

We compared the spatial organization patterns of linear and angular vestibuloocular reflexes in frogs by recording the multiunit spike activity from cranial nerve branches innervating the lateral rectus, the inferior rectus, or the inferior obliquus eye muscles. Responses were evoked by linear horizontal and/or vertical accelerations on a sled or by angular accelerations about an earth-vertical axis on a turntable. Before each sinusoidal oscillation test in darkness, the static head position was systematically altered to determine those directions of horizontal linear acceleration and those planes of angular head oscillation that were associated with minimal response amplitudes. Inhibitory response components during angular accelerations were clearly present, whereas inhibitory response components during linear accelerations were absent. Likewise was no contribution from the vertical otolith organs (i.e., lagena and saccule) observed during vertical linear acceleration. Horizontal linear acceleration evoked responses that originated from eye muscle-specific sectors on the contralateral utricular macula. The sectors of the inferior obliquus and lateral rectus muscles on the utricle had an opening angle of 45 and 60 degrees, respectively and overlapped to a large extent in the laterorostral part of the utricle. Both sectors were coplanar with the horizontal semicircular canals. The sector of the inferior rectus muscle was narrow (opening 5 degrees), laterocaudally oriented, and slightly pitched up by 6 degrees. Angular acceleration evoked maximal responses in the inferior obliquus muscle nerve that originated from the ipsilateral horizontal and the contralateral anterior vertical canals in a ratio of 50:50. Lateral rectus excitation originated from the contralateral horizontal and anterior vertical semicircular canals in a ratio of 80:20. The excitatory responses of the inferior rectus muscle nerve originated exclusively from the contralateral posterior vertical canal. Measured data and known semicircular canal plane vectors were used to calculate the spatial orientation of maximum sensitivity vectors for the investigated eye muscle nerves in semicircular canal coordinates. Comparison of the directions of maximal sensitivity vectors of responses evoked by linear or angular accelerations in a given eye muscle nerve showed that the two vector directions were oriented about orthogonally with respect to each other. With this arrangement the linear and the angular vestibuloocular reflex can support each other dynamically whenever they are co-activated without a change in the spatial response characteristics. The mutual adaptation of angular and linear vestibuloocular reflexes as well as the differences in their organization described here for frogs may represent a basic feature common for vertebrates in general.     

Anatomy of the lamprey ear: morphological evidence for occurrence of horizontal semicircular ducts in the labyrinth of Petromyzon marinus

In jawed (gnathostome) vertebrates, the inner ears have three semicircular canals arranged orthogonally in the three Cartesian planes: one horizontal (lateral) and two vertical canals. They function as detectors for angular acceleration in their respective planes. Living jawless craniates, cyclostomes (hagfish and lamprey) and their fossil records seemingly lack a lateral horizontal canal. The jawless vertebrate hagfish inner ear is described as a torus or doughnut, having one vertical canal, and the jawless vertebrate lamprey having two. These observations on the anatomy of the cyclostome (jawless vertebrate) inner ear have been unchallenged for over a century, and the question of how these jawless vertebrates perceive angular acceleration in the yaw (horizontal) planes has remained open. To provide an answer to this open question we reevaluated the anatomy of the inner ear in the lamprey, using stereoscopic dissection and scanning electron microscopy. The present study reveals a novel observation: the lamprey has two horizontal semicircular ducts in each labyrinth. Furthermore, the horizontal ducts in the lamprey, in contrast to those of jawed vertebrates, are located on the medial surface in the labyrinth rather than on the lateral surface. Our data on the lamprey horizontal duct suggest that the appearance of the horizontal canal characteristic of gnathostomes (lateral) and lampreys (medial) are mutually exclusive and indicate a parallel evolution of both systems, one in cyclostomes and one in gnathostome ancestors.     

Geometry of the semicircular canals and extraocular muscles in rodents,lagomorphs, felids and modern humans

The vestibulo‐ocular reflex (VOR) exacts compensatory movements of the extraocular muscles in response to stimulation of the semicircular canals to allow gaze fixation during head movements. In this study, the spatial relationships of these muscles and canals were investigated to assess their relative alignments in mammalian species commonly used in studies of the VOR. The head region of each specimen was scanned using magnetic resonance imaging and 28 anatomical landmarks were recorded from the images to define the six extraocular muscles and the anatomical planes of the three semicircular canals. The vector rotation of a semicircular canal that does not stimulate either of its two sister canals, referred to as the prime direction, was also calculated as an estimate of the maximal response plane. Significant misalignments were found between the extraocular muscles and the canals by which they are principally stimulated in most of the species under study. The deviations from parallel orientation were most pronounced in the human and rabbit samples. There were also significant departures from orthogonality between the semicircular canals in most species. Only the guinea pig displayed no significant difference from 90° in any of its three inter‐canal angles, although humans and rabbits deviated from orthogonality in just one semicircular canal pair – the anterior and posterior canals. The prime directions were found to deviate considerably from the anatomical canal planes (by over 20° in rats). However, these deviations were not always compensatory, i.e. prime planes were not always more closely aligned with the muscle planes. Results support the view that the vestibular frame remains relatively stable and that the spatial mismatch with the extraocular co‐ordinate frame is principally driven by realignment of the muscles as a result of changes in the position of the orbits within the skull (orbital convergence and frontation).     

Spatial and temporal response properties of the vestibulocollic reflex in decerebrate cats

Vestibulocollic reflex responses of several neck muscles in decerebrate cats were studied during angular rotations of the whole body in a large number of vertical and horizontal rotation planes, at frequencies from 0.07 to 1.6 Hz. Vestibulocollic responses were compared to eye muscle and forelimb muscle vestibular responses. Electromyographic activity was recorded by fine wires inserted in biventer cervicis, complexus, longus capitis, obliquus capitis inferior, occipitoscapularis, rectus capitis major, splenius, lateral rectus, and triceps brachii. At frequencies of approximately 0.5 Hz and above, neck muscle electromyographic response gains were sinusoidal functions of stimulus orientation within a set of vertical or horizontal planes, and a muscle's response phase remained constant across rotation planes, or reversed by 180 degrees. Response patterns at high frequencies were consistent with vestibulocollic reflex activation by semicircular canals through brain circuitry that modifies canal dynamics. At frequencies of approximately 0.5 Hz and above, the stimulus orientation in which a given neck muscle's response was maximal remained nearly constant across frequencies. Thus, we used responses to rotations at high frequencies to calculate axes of maximal response of each muscle in three-dimensional space. Lateral rectus, obliquus, and to a lesser extent, splenius and longus capitus were activated predominantly by horizontal rotations. Biventer was activated predominantly by pitch, triceps predominantly by roll, and complexus, occipitoscapularis, and rectus major significantly excited by rotations in all three coordinate planes. In some cases, at frequencies less than 0.5 Hz, neck muscle response phase varied depending on the vertical plane in which the cat was rotated, and the optimal response plane was poorly defined and varied with frequency. These responses indicated that, at some frequencies, neck muscle activity can result from summation of inputs with differing spatial orientation and dynamics (spatial-temporal convergence). Differences between responses to vertical and horizontal rotations suggested that low-frequency spatial-temporal convergence behavior of the vestibulocollic reflex during vertical rotations was due to convergent semicircular canal and otolith receptor inputs.(ABSTRACT TRUNCATED AT 400 WORDS)     

The human semicircular canal model of galvanic vestibular stimulation

A vector summation model of the action of galvanic stimuli on the semicircular canals has been shown to explain empirical balance and perceptual responses to binaural-bipolar stimuli. However, published data suggest binaural-monopolar stimuli evoke responses that are in the reverse direction of the model prediction. Here, we confirm this by measuring balance responses to binaural-monopolar stimulation as movements of the upper trunk. One explanation for the discrepancy is that the galvanic stimulus might evoke an oppositely directed balance response from the otolith organs that sums with and overrides the semicircular canal response. We tested this hypothesis by measuring sway responses across the full range of head pitch. The results showed some modulation of sway with pitch such that the maximal response occurred with the head in the primary position. However, the effect fell a long way short of that required to reverse the canal sway response. This indicates that the model is incomplete. Here, we examine alterations to the model that could explain both the bipolar and monopolar-evoked behavioural responses. An explanation was sought by remodelling the canal response with more recent data on the orientation of the individual canals. This improved matters but did not reverse the model prediction. However, the model response could be reversed by either rotating the entire labyrinth in the skull or by altering the gains of the individual canals. The most parsimonious solution was to use the more recent canal orientation data coupled with a small increase in posterior canal gain.     

Influence of surgical plugging on horizontal semicircular canal mechanics and afferent response dynamics.

Mechanical occlusion of one or more of the semicircular canals is a surgical procedure performed clinically to treat certain vestibular disorders and used experimentally to assess individual contributions of separate canals and/or otoliths to vestibular neural pathways. The present experiments were designed to determine if semicircular canal afferent nerve modulation to angular head acceleration is blocked by occlusion of the endolymphatic duct, and if not, what mechanism(s) might account for a persistent afferent response. The perilymphatic space was opened to gain acute access to the horizontal canal (HC) in the oyster toadfish, Opsanus tau. Firing rate responses of HC afferents to sinusoidal whole-body rotation were recorded in the unoccluded control condition, during the process of duct occlusion, and in the plugged condition. The results show that complete occlusion of the duct did not block horizontal canal sensitivity; individual afferents often exhibited a robust firing rate modulation in response to whole-body rotation in the plugged condition. At high stimulus frequencies (about >8 Hz) the average sensitivity (afferent gain; spikes/s per degrees /s of head velocity) in the plugged condition was nearly equal to that observed for unoccluded controls in the same animals. At low stimulus frequencies (about <0.1 Hz), the average sensitivity in the plugged condition was attenuated by more than two orders of magnitude relative to unoccluded controls. The peak afferent firing rate for sinusoidal stimuli was phase advanced approximately 90 degrees in plugged canals relative to their control counterparts for stimulus frequencies approximately 0.1-2 Hz. Data indicate that afferents normally sensitive to angular velocity in the control condition became sensitive to angular acceleration in the plugged condition, whereas afferents sensitive to angular acceleration in the control condition became sensitive to the derivative of acceleration or angular jerk in the plugged condition. At higher frequencies (>8 Hz), the phase of afferents in the plugged condition became nearly equal, on average, to that observed in controls. A three-dimensional biomechanical model of the HC was developed to interpret the residual response in the plugged condition. Labyrinthine fluids were modeled as incompressible and Newtonian; the membranous duct, osseous canal and temporal bone were modeled as visco-elastic materials. The predicted attenuation and phase shift in cupular responses were in close agreement with the observed changes in afferent response dynamics after canal plugging. The model attributes the response of plugged canals to labyrinthine fluid pressure gradients that lead to membranous duct deformation, a spatial redistribution of labyrinthine fluids and cupular displacement. Validity of the model was established through its ability to predict: the relationship between plugged canal responses and unoccluded controls (present study), the relationship between afferent responses recorded during mechanical indentation of the membranous duct and physiological head rotation, the magnitude and phase of endolymphatic pressure generated during HC duct indentation, and previous model results for cupular gain and phase in the rigid-duct case. The same model was adjusted to conform to the morphology of the squirrel monkey and of the human to investigate the possible influence of canal plugging in primates. Membranous duct stiffness and perilymphatic cavity stiffness were identified as the most salient model parameters. Simulations indicate that canal plugging may be the most effective in relatively small species having small labyrinths, stiff round windows, and stiff bony perilymphatic enclosures.     

人内耳半规管嵴顶时间常数的定量分析

目的 通过数值仿真和实验定量探究人内耳前庭半规管中的嵴顶时间常数,明确半规管编码角运动的时间过程。方法 建立人双耳半规管数值模型,通过流固耦合数值模拟嵴顶的生物力学响应,进而计算嵴顶的力学松弛时间常数。同时,对志愿者进行前庭眼反射实验,根据志愿者的眼震慢相角速度计算嵴顶的时间常数。结果 通过人内耳半规管数值模型计算得出的嵴顶力学松弛时间常数为3.75 s。通过实验测量得出平均嵴顶时间常数约为4.86 s。数值模型和实验中的结果近似保持一致。结论 人内耳前庭半规管中的嵴顶时间常数大约为4.86 s,反映了嵴顶力学松弛和半规管传入神经适应性的联合作用效果,体现了半规管编码角运动的时间过程。     

A quantitative analysis of the spatial organization of the vestibulo-ocular reflexes in lateral- and frontal-eyed animals--I. Orientation of semicircular canals and extraocular muscles

The spatial relationship between extraocular muscles and semicircular canals was evaluated in cat (frontal-eyed animal) and rabbit (lateral-eyed animal). Semicircular canal orientations in the rabbit were determined by a principal components analysis of data points obtained from the exposed osseous canals using a three-axis micromanipulator. Canal orientations were presented in terms of unit sensitivity vectors. Orientation of extraocular muscles in rabbits and cats was derived from measurements of the insertion and origin of each muscle with respect to a reference point on the skull and a calculated estimate of the center of the eye. Muscle orientations were presented in terms of unit action vectors. Semicircular canal planes of the rabbit labyrinth were not orthogonal, having deviations up to 14 degrees. Pairs of antagonistically acting vertical semicircular canals, left (right) anterior-right (left) posterior deviated from coplanarity by 16 degrees, while the deviation for the horizontal canals was 9 degrees. In both animals, muscles of an antagonistic pair were coplanar to within 8 degrees, with the exception of the oblique muscles in the rabbit for which the deviation was 19 degrees. The three pairs of antagonistic muscles were almost orthogonal to each other, the maximum deviation between any of the pairs being 8 degrees in the cat and 18 degrees in the rabbit. Comparing extraocular muscle planes and semicircular canal planes reveals that they are roughly aligned. However, there were slight but consistent differences between a given semicircular canal plane and the planes of the muscles to which this canal is connected by the classical three-neuron-arc (principal vestibulo-ocular reflex circuits).(ABSTRACT TRUNCATED AT 250 WORDS)     

Excitation of the extraocular muscles in decerebrate cats during the vestibulo-ocular reflex in three-dimensional space

Summary (1) Vestibulo-ocular reflex excitation of the six extraocular muscles was studied by recording their electromyographic activity in decerebrate cats during oscillations about horizontal and vertical axes, at frequencies from 0.07 to 4 Hz. Animals were oriented in many different positions and rotated about axes that lay in the horizontal, frontal, or sagittal planes defined by our coordinate system. (2) The strengths of modulation (gains) of the responses of all extraocular muscles were a sinusoidal function of the orientation of the rotation axis within a coordinate plane, and this function was nearly independent of rotation frequency. (3) The responses were used to determine an axis of maximal excitation for each of the extraocular muscles by the vestibulo-ocular reflex. Antagonistic muscle pairs were found to have best axes in nearly opposite directions, confirming their operation as pairs. (4) Excitation of the medial and lateral rectus could be explained by input from the paired horizontal semicircular canals, with essentially no convergent input from vertical canals. (5) Excitation of the vertical rectus and oblique muscles could be explained by convergent inputs from the vertical canals with little or no horizontal canal input.     

Response of pontomedullary reticulospinal neurons to vestibular stimuli in vertical planes. Role in vertical vestibulospinal reflexes of the decerebrate cat.

1. To investigate the neural substrate of vestibulospinal reflexes in decerebrate cats, we studied the responses of pontomedullary reticulospinal neurons to natural stimulation of the labyrinth in vertical planes. Our principal aim was to determine whether reticulospinal neurons that terminate in, or are likely to give off collaterals to, the upper cervical segments had properties similar to those of the vestibulocollic reflex (VCR). 2. Antidromic stimulation was used to determine whether the neurons projected to the neck, lower cervical, thoracic, or lumbar levels. Dynamics of the responses of spontaneously firing neurons were studied with sinusoidal stimuli delivered at 0.05-1 Hz and aligned to the plane of body rotation, that produced maximal modulation of the neuron (response vector orientation). Each neuron was assigned a vestibular input classification of otolith, vertical canal, otolith + canal, or spatial-temporal convergence (STC). 3. We found, in agreement with previous studies, that the largest fraction of pontomedullary reticulospinal neurons projected to the lumbar cord, and that only a small number ended in the neck segments. Neurons projecting to all levels of the spinal cord had similar responses to labyrinth stimulation. 4. Reticulospinal neurons that received only vertical canal inputs were rare (1 of 67 units). Most reticulospinal neurons (48%) received predominant otolith inputs, 18% received otolith + canal input, and only 9% had STC behavior. These data are in sharp contrast to the results of our previous studies of vestibulospinal neurons. A considerable portion of vestibulospinal neurons receives vertical canal input (38%), fewer receive predominantly otolith input (22%), whereas the proportion that have otolith + canal input or STC behavior is similar to our present reticulospinal data. 5. The response vector orientations of our reticulospinal neurons, particularly those with canal inputs (canal, otolith + canal, STC) were predominantly in the roll quadrants. There was no evidence of convergence of inputs from like canals across the midline (e.g., right anterior + left anterior). 6. Two characteristics of the VCR, STC behavior and bilateral input from symmetric vertical canals (in some muscles), cannot be accounted for by the reticulospinal neurons that we studied. Because these characteristics are also not seen in vestibulocollic neurons, they are likely to be the result of the appropriate convergence of vestibular signals in the spinal cord. 7. Pontomedullary reticulospinal neurons seem particularly well suited to play a role in gravity-dependent postural reflexes of neck and limbs.     

Spatial properties of central vestibular neurons

We studied the spatial characteristics of 45 vestibular-only (VO) and 12 vestibular-plus-saccade (VPS) neurons in two cynomolgus monkeys using angular rotation and static tilt. The purpose was to determine the contribution of canal and otolith-related inputs to central vestibular neurons whose activity is associated with the central velocity storage integrator. Lateral canal-related neurons responded maximally during vertical axis rotation when the head was tilted 25 +/- 6 and 22 +/- 3 degrees forward relative to the axis of rotation in the two animals, and vertical canal-related neurons responded maximally with the head tilted back 63+/- 5 and 57 +/- 7 degrees . The origin of the vertical canal-related input was verified by rotation about a spatial horizontal axis. Thirty-one percent of cells received input in a single canal plane. Sixty-seven percent of canal-related cells received otolith input, 31% of vertical canal neurons had lateral canal input, and 43% of lateral canal neurons had vertical canal input. Twenty percent of neurons had convergent input from the lateral canals, the vertical canals, and the otolith organs. Some VO and VPS cells had spatial-temporal convergent (STC) properties; more of these cells had STC properties at lower frequencies of rotation. Thus VO and VPS neurons associated with velocity storage receive a broad range of convergent inputs from each portion of the vestibular labyrinth. This convergence could provide the basis for gravity-dependent eye velocity orientation induced through velocity storage.     

Origin of orientation-dependent asymmetries in vestibulo-ocular reflexes evoked by caloric stimulation

A caloric stimulus evokes primarily a horizontal vestibulo-ocular reflex (VOR) when subjects are in a supine or prone orientation with the horizontal semicircular canal plane oriented vertically. In both monkeys and humans, the magnitude of VOR eye movements is greater in the supine than in the prone orientation, indicating that some factor or factors, other than the conventionally accepted convective stimulation of the horizontal canals, contributes to the generation of the VOR. We used long-duration caloric irrigations and mathematical models of canal-otolith interactions to investigate factors contributing to the prone/supine asymmetry. Binaural caloric irrigations were applied for 7.5 or 9.5 min with subjects in a null orientation with horizontal canals in the earth-horizontal plane (control trial), or with the subject's pitch orientation periodically changing between null, supine, and prone positions with each orientation held for 30 s (caloric step trial). The control trial responses identified a small response attributable to a direct thermal effect on vestibular afferent activity that accounted for only 15% of the observed prone/supine asymmetry. We show that the gravito-inertial force resolution hypothesis for sensory integration of canal and otolith information predicts that the central processing of canal and otolith information produces an internal estimate of motion that includes both a rotational motion component and a linear acceleration component. These components evoke a horizontal angular VOR and linear VOR, which combine additively in the supine orientation, but subtract in the prone orientation, thus accounting for the majority of the observed prone/supine asymmetry.     

基于内耳体素模型的膜迷路三维可视化

目的探讨基于内耳体素模型三维可视化膜迷路。方法磁共振显微成像颞骨扫描影像数据使用3D Slicer软件进行表面模型体裁剪,将内耳体素模型通过表面绘制和体绘制混合成像三维显示膜迷路。结果通过内耳体素模型可以三维可视化膜迷路,且内耳体素模型文件较表面模型文件容量更小。结论内耳体素模型对于内耳解剖学习和研究有重要意义。     

The organogenesis of the membranous labyrinth in Polypterus senegalus Cuvier, 1829 (Pisces, Holostei, Polypteridae)

The organogenesis of the membranous labyrinth of Polypterus senegalus is described. 1. The otocyst seems to be formed by the invagination of a thick portion of the deeper layer of the epidermis. 2. The 3 semi-circular canals are formed by 3 pairs of invaginations of the wall of the otocyst and at the expense of its volume; the anterior vertical canal is completed first, followed by the horizontal and then the posterior vertical one; the ampullae, not very developed, appear a long time after the formation of their corresponding canals: that of the horizontal canal appears first, followed by that of the posterior and finally that of the anterior one. 3. The sensory areas derive from a common macula which subsequently divides into 2 zones, the anterior one giving rise to the utricular macula and the anterior and horizontal cristae, the posterior one giving rise to the posterior crista and the saccular macula; from the latter subsequently develops the lagenar macula. 4. The otoconiae appear as soon as the otocyst forms; the otoliths are agglomerations of otoconias brought together by an interstitial cement. 5. The endolymphatic primordium is formed before that of the semi-circular canals; the endolymphatic sack becomes voluminous and spreads over the brain as far as the sagittal plane.     

A Morphometric Study of the Semicircular Canals Using Micro‐CT Images in Three‐Dimensional Reconstruction

It is generally accepted that the three semicircular canals are set at right angles to each other and the lateral semicircular canal is smaller than the anterior and posterior semicircular canals. Precise knowledge of the size and spatial relationships of the semicircular canals is vital, and so the 40 petrous parts of the temporal bones were scanned by micro‐CT at a slice thickness of 35 µm. The micro‐CT images were used in reconstructing three‐dimensional models of the bony labyrinth using computer software. Various dimensions of the semicircular canals were measured using the software, and statistical analysis was performed. The anterior semicircular canal was slightly wider than the posterior semicircular canal, and their heights were similar. The radius of curvature of the lateral semicircular canal was 20% smaller than those of the anterior and posterior semicircular canals. The angles between the three canals were not exactly 90 degrees: they were 92.1, 84.4, and 86.2 degrees between the anterior and posterior, anterior and lateral, and posterior and lateral semicircular canals, respectively. We obtained high‐resolution images of the semicircular canals using three‐dimensional reconstruction software, and these were used to precisely measure the angles between the semicircular canals and the area of the distorted circle formed by each semicircular canal. Anat Rec, 296:834–839, 2013. © 2013 Wiley Periodicals, Inc.     

Ontogenetic Variation in the Bony Labyrinth of Monodelphis domestica (Mammalia: Marsupialia) Following Ossification of the Inner Ear Cavities

Ontogeny, or the development of an individual from conception to death, is a major source of variation in vertebrate morphology. All anatomical systems are affected by ontogeny, and knowledge of the ontogenetic history of these systems is important to understand when formulating biological interpretations of evolutionary history and physiology. The present study is focused on how variation affects the bony labyrinth across a growth series of an extant mammal after ossification of the inner ear chambers. Digital endocasts of the bony labyrinth were constructed using CT data across an ontogenetic sequence of Monodelphis domestica, an important experimental animal. Various aspects of the labyrinth were measured, including angles between the semicircular canals, number of turns of the cochlea, volumes of inner ear constituents, as well as linear dimensions of semicircular canals. There is a strong correlation between skull length and age, but from 27 days after birth onward, there is no correlation with age among most of the inner ear measurements. Exceptions are the height of the arc of the lateral semicircular canal, the angular deviation of the lateral canal from planarity, the length of the slender portion of the posterior semicircular canal, and the length of the canaliculus cochleae. Adult dimensions of several of the inner ear structures, such as the arcs of the semicircular canals, are achieved before the inner ear is functional, and the non‐ontogenetic variation in the bony labyrinth serves as an important source for behavioral, physiological, and possibly phylogenetic information. Anat Rec, 2010. © 2010 Wiley‐Liss, Inc.     

Spatial tuning and dynamics of vestibular semicircular canal afferents in rhesus monkeys

Rotational head motion in vertebrates is detected by the three semicircular canals of the vestibular system whose innervating primary afferent fibers encode movement information in specific head planes. In order to further investigate the nature of vestibular central processing of rotational motion in rhesus monkeys, it was first necessary to quantify afferent information coding in this species. Extracellular recordings were performed to determine the spatial and dynamic properties of semicircular canal afferents to rotational motion in awake rhesus monkeys. We found that the afferents innervating specific semicircular canals had maximum sensitivity vectors that were mutually orthogonal. Similar to other species, afferent response dynamics varied, with regular firing afferents having increased long time constants (t ₁), decreased cupula velocity time constants (t _v), and decreased fractional order dynamic operator values (s ^k) as compared to irregular firing afferents.     

Bony labyrinth shape variation in extant Carnivora: a case study of Musteloidea

The bony labyrinth provides a proxy for the morphology of the inner ear, a primary cognitive organ involved in hearing, body perception in space, and balance in vertebrates. Bony labyrinth shape variations often are attributed to phylogenetic and ecological factors. Here we use three‐dimensional (3D) geometric morphometrics to examine the phylogenetic and ecological patterns of variation in the bony labyrinth morphology of the most species‐rich and ecologically diversified traditionally recognized superfamily of Carnivora, the Musteloidea (e.g. weasels, otters, badgers, red panda, skunks, raccoons, coatis). We scanned the basicrania of specimens belonging to 31 species using high‐resolution X‐ray computed micro‐tomography (μCT) to virtually reconstruct 3D models of the bony labyrinths. Labyrinth morphology is captured by a set of six fixed landmarks on the vestibular and cochlear systems, and 120 sliding semilandmarks, slid at the center of the semicircular canals and the cochlea. We found that the morphology of this sensory structure is not significantly influenced by bony labyrinth size, in comparisons across all musteloids or in any of the individual traditionally recognized families (Mephitidae, Procyonidae, Mustelidae). PCA (principal components analysis) of shape data revealed that bony labyrinth morphology is clearly distinguishable between musteloid families, and permutation tests of the Kmult statistic confirmed that the bony labyrinth shows a phylogenetic signal in musteloids and in most mustelids. Both the vestibular and cochlear regions display morphological differences among the musteloids sampled, associated with the size and curvature of the semicircular canals, angles between canals, presence or absence of a secondary common crus, degree of lateral compression of the vestibule, orientation of the cochlea relative to the semicircular canals, proportions of the cochlea, and degree of curvature of its turns. We detected a significant ecological signal in the bony labyrinth shape of musteloids, differentiating semi‐aquatic taxa from non‐aquatic ones (the taxa assigned to terrestrial, arboreal, semi‐arboreal, and semi‐fossorial categories), and a significant signal for mustelids, differentiating the bony labyrinths of terrestrial, semi‐arboreal, arboreal, semi‐fossorial and semi‐aquatic species from each other. Otters and minks are distinguished from non‐aquatic musteloids by an oval rather than circular anterior canal, sinuous rather than straight lateral canal, and acute rather than straight angle between the posterior and lateral semicircular canals – each of these morphological characters has been related previously to animal sensitivity for detecting head motion in space.