Angular Head Research Articles

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.

Biomechanics and neuropathology of adult and paediatric head injury

The objective of this study was to understand the biomechanics in age-related primary traumatic brain injuries (TBI) causing initial severity and secondary progressive damage and to develop strategy reducing TBI outcome variability using biomechanical reconstruction to identify types of causal mechanisms prior to clinical trials of neuro-protective treatment. The methods included the explanation of TBI biomechanics and physiopathological mechanisms from dual perspectives of neurosurgery and biomechanical engineering. Scaling of tolerances for skull failure and brain injuries in infants, children and adults are developed. Diagnostic assumptions without biomechanical considerations are critiqued. Methods for retrospective TBI reconstruction for prevention are summarized. Mechanisms of TBI are based on the differences between the mechanical properties of the head and neck related to age. Skull fracture levels correlate with increasing cranial bone thickness and in the development of the cranial sutures in infants and in adults. Head injury tolerance levels at three age categories for cerebral concussion, skull fracture and three grades of diffuse axonal injuries (DAI) are presented. Brain mass correlates inversely for TBI caused by angular head motions and locations of injurious stresses are predictable by centripetal theory. Improved quantitative diagnosis of TBI type and severity levels depend primarily on age and biomechanical mechanisms. Reconstruction of the biomechanics is feasible and enables quantitative stratification of TBI severity. Experimental treatment has succeeded in preventing progressive damage in animal TBI models. In humans this has failed, because the animal model received biomechanically controlled TBI and humans did not. Clinical similarities of human TBI patients do not necessarily predict equivalent biomechanics because such trauma can be produced in various ways. We recommend 'reverse engineering' for in-depth reconstruction of the TBI injury mechanism for qualitative diagnoses and reduction of outcome variability.

Bayeritheca hughesii gen. et sp. nov., a new Eucommiidites -bearing pollen organ from the Cenomanian of Bohemia

A new pollen organ, Bayeritheca hughesii gen. et sp. nov. with in situ Eucommiidites pollen grains, is described from the Cenomanian of Bohemia in Central Europe. It is based on a single lignified specimen which is the largest Eucommiidites -producing pollen structure described so far. It shows whorls of microsporangiate units attached to a massive main axis forming a cone-like structure. Each microsporangiate unit forms distally an angular head bearing trichomes and centrally arranged mucronate tubercles. The head is attached to a short stalk. Proximal sides of heads display radially arranged synangia. Each synangium contains an unknown number of pollen sacs with numerous Eucommiidites pollen grains.Bayeritheca is the only genus of Erdtmanithecales in which synangia instead of sporangia are found. Bayeritheca differs from Eucommiiditheca Friis & Pedersen in the whorled arrangement of microsporangiate units, which are densely spaced forming a cone-like structure. It differs from Erdtmanitheca Pedersen, Crane & Friis in the elongate shape of the whole organ, slender main axis, shorter pollen sacs, and different Eucommiidites pollen.

Signal processing by vestibular nuclei neurons is dependent on the current behavioral goal.

The vestibular sensory apparatus and associated vestibular nuclei are generally thought to encode angular head velocity during our daily activities. However, in addition to direct inputs from vestibular afferents, the vestibular nuclei receive substantial projections from cortical, cerebellar, and other brainstem structures. Given this diversity of inputs, the question arises: How are the responses of vestibular nuclei neurons to head velocity modified by these additional inputs during naturally occurring behaviors? Here we have focused on the signal processing done by two specific classes of neurons in the vestibular nuclei: (1) position-vestibular-pause (PVP) neurons that mediate the vestibulo-ocular reflex (VOR), and (2) vestibular-only (VO) neurons that are thought to mediate, at least in part, the vestibulo-collic reflex (VCR). We first characterized neuronal responses to passive rotation in the head-restrained condition, and then released the head to record the discharges of the same neurons during self-generated head movements. VOR interneurons (i.e., PVP neurons) faithfully transmitted head velocity signals when the animal stabilized its gaze, regardless of whether the head motion was actively or passively generated; their responses were attenuated only when the monkey's behavioral goal was to redirect its axis of gaze relative to space. In contrast, VCR interneurons (i.e., VO neurons) faithfully transmitted head velocity signals during passive head motion, but their responses were greatly (and similarly) attenuated during all behaviors (i.e., gaze shifts, gaze pursuit, gaze stabilization) during which the monkey's behavioral goal was to move its head relative to the body. To characterize the mechanism(s) that underlie this differential processing, we tested neurons during passive rotation of the head relative to the body, as well as during a task in which a monkey actively "drove" both its head and body together in space. We conclude that neither passive activation of neck proprioceptors nor knowledge of self-generated head-in-space motion directly mediate the observed reductions in head-velocity-related modulation. Instead, we propose that the VOR and VCR pathways use efference copies of oculomotor and neck movement commands, respectively, for the differential processing of vestibular information.

Evaluating eye-body coordination during unrestrained functional activity in older persons.

Traditional paradigms for the study of ocular-motor control restrain subject motion and have not adequately quantified the sensorimotor strategies used by older persons to control gaze while performing activities of daily living. The purpose of our study was to describe eye-head-trunk coordination during a functional activity in freely moving community-dwelling older persons. Thirty-five community-dwelling older persons (age range 71-92 years) participated in this study. Surface electro-oculography was used with an electromagnetic tracking device to measure vertical eye movement and linear and angular head position while each subject performed a stand-from-chair task. Standing from a chair involved low-frequency head motion (median z = 0.25 Hz; median pitch = 0.32 Hz). The distribution of phase for eyes versus vertical body motion were skewed toward head-trunk leading, suggesting that eye motion follows vertical body motion. Vertical gaze, however, was in phase with and moved in the same direction as head pitch. Gaze (eye position in space) was an active, integrated component of the standing motion. The results imply that both the oculomotor system and the head motor system in older persons are coordinated to direct gaze and, when necessary, work to suppress the vestibuloocular reflex. The interaction of eye-head-trunk motion provides a basis for understanding how a breakdown in the gaze control mechanisms in older persons might contribute to the risk of falling and fall-related injuries.

Relationship between inner-ear fluid pressure and semicircular canal afferent nerve discharge.

The present study was designed to determine (1) the transcupular fluid pressure (deltaP) generated across the semicircular canal cupula in response to sinusoidal head rotation, (2) the translabyrinthine dilational pressure (P0) generated across the membranous labyrinth in response to an increase in endolymph fluid volume (hydrops), (3) afferent nerve discharge patterns generated by these distinct pressure stimuli and, (4) threshold values of deltaP and P0 required to elicit afferent neural responses. The experimental model was the oyster toadfish, Opsanus tau. Micromechanical indentation of the horizontal canal (HC) duct and utricular vestibule was used to simulate sinusoidal head rotation and fluid volume injection. Single-unit neural spike trains and endolymph pressure within the ampulla, on both sides of the cupula, were recorded simultaneously. deltaP averaged 0.013 Pa per 1 degrees/s of sinusoidal angular head velocity and P0 averaged 0.2 Pa per 1 nL of endolymph volume injection. The most responsive afferents had a threshold sensitivity to deltaP of 10(-3) Pa and to P0 of 5 x 10(-2) Pa based on a discharge modulation criterion of 1 impulse/s per cycle for 2 Hz pressure stimuli. Neural sensitivity to AP was expected on the basis of transverse cupular and hair bundle deflections. Analysis of mechanics of the end organ, neuronal projections into the crista, and individual neural firing patterns indicates that P0 sensitivity resulted from pressure-induced distension of the ampulla that led to a nonuniform cupular deformation pattern and hair bundle deflections. This explanation is consistent with predictions of a finite element model of the end organ. Results have implications regarding the role of deltaP in angular motion transduction and the role of P0 under transient hydropic conditions.

Neural Correlates for Angular Head Velocity in the Rat Dorsal Tegmental Nucleus

Many neurons in the rat lateral mammillary nuclei (LMN) fire selectively in relation to the animal's head direction (HD) in the horizontal plane independent of the rat's location or behavior. One hypothesis of how this representation is generated and updated is via subcortical projections from the dorsal tegmental nucleus (DTN). Here we report the type of activity in DTN neurons. The majority of cells (75%) fired as a function of the rat's angular head velocity (AHV). Cells exhibited one of two types of firing patterns: (1) symmetric, in which the firing rate was positively correlated with AHV during head turns in both directions, and (2) asymmetric, in which the firing rate was positively correlated with head turns in one direction and correlated either negatively or not at all in the opposite direction. In addition to modulation by AHV, some of the AHV cells (40.1%) were weakly modulated by the rat's linear velocity, and a smaller number were modulated by HD (11%) or head pitch (15.9%). Autocorrelation analyses indicated that with the head stationary, AHV cells displayed irregular discharge patterns. Because afferents from the DTN are the major source of information projecting to the LMN, these results suggest that AHV information from the DTN plays a significant role in generating the HD signal in LMN. A model is proposed showing how DTN AHV cells can generate and update the LMN HD cell signal.

Aerial somersault performance under three visual conditions.

Experiments were designed to examine the visual contributions to performance of back aerial double somersaults by collegiate acrobats. Somersaults were performed on a trampoline under three visual conditions: (a) NORMAL acuity; (b) REDUCED acuity (subjects wore special contacts that blocked light reflected onto the central retina); and (c) NO VISION. Videotaped skill performances were rated by two NCAA judges and digitized for kinematic analyses. Subjects' performance scores were similar in NORMAL and REDUCED conditions and lowest in the NO VISION condition. Control of body movement, indicated by time-to-contact, was most variable in the NO VISION condition. Profiles of angular head and neck velocity revealed that when subjects could see, they slowed their heads prior to touchdown in time to process optical flow information and prepare for landing. There was not always enough time to process vision associated with object identification and prepare for touchdown. It was concluded that collegiate acrobats do not need to identify objects for their best back aerial double somersault performance.

Angular velocity and head direction signals recorded from the dorsal tegmental nucleus of gudden in the rat: Implications for path integration in the head direction cell circuit.

When a rat navigates through space, head direction (HD) cells provide an ongoing signal of the rat's directional heading. It is thought that these cells rely, in part, on angular path integration of the rat's head movements. This integration requires that the HD cell system receive information about angular head movements and that this information be combined with the current directional signal, to generate the next "predicted" direction. Recent data suggest that the dorsal tegmental nucleus (DTN) may play a critical role in helping to generate the HD cell signal. To test this, recordings were made from cells in the DTN in freely moving rats. The following cell types were found: (a) "classic" HD cells, (b) angular velocity cells, and (c) cells that fired as a function of both head direction and angular velocity. Thus, DTN cells exhibit firing characteristics that are critical to the neural circuit hypothesized for generation of the HD cell signal.

Perception of angular head position during attempted alignment with eccentric visual objects.

The perception of angular head position with respect to a visual object was investigated using three different methods: Pointer indication (P); in the dark, subjects' (Ss') heads were horizontally turned to various positions (range +/- 54 degrees); Ss then rotated a pointer carrying a light emitting diode (LED) so as to align it with head position. Active head pointing (A); again in darkness, the pointer was rotated to various positions; Ss then turned their heads so as to align them with the pointer. Reading from visible scale (V); Ss viewed a degrees scale on a circular screen; Ss' heads were turned as in P, and Ss reported head position in terms of this scale. The results obtained with all three methods indicate that head position is overestimated with respect to the visual object (LED, scale mark): object position exceeded head position by 6, 18, and 7% when measured with the P-, A-, and V-methods, respectively (median values). The observed misalignment between head and object suggests that subjective primary eye position is shifted in the direction of head rotation by a cross-talk of head position. Whether a functional advantage or merely a tolerated side-effect of other constraints, this behavior confers the impression of looking "straight ahead" in the literal sense when gaze is shifted by coordinated eye-head movements with a 10% eye and a 90% head share in total lateral displacement. In an attempt to probe a hypothesized internal representation of head position implied in head-to-object alignment, Ss were also to estimate head position in space using only neck proprioceptive information. In complete darkness, responses were often non-linear functions of head position with overestimation of large eccentricities. When a head-centered LED was added (which conveyed no position information), responses became more linear, suggesting that the mere presence of visual afferents may improve the perceptual interpretation of proprioceptive information.

Combined intertrochanteric valgus and rotational acetabular osteotomy.

Results are reported for combined intertrochanteric valgus and rotational acetabular osteotomies in 18 dysplastic hips (17 patients), involving two types of femoral head and neck deformities, after an average followup of 13 years (range, 8.9-22.6 years). The mean age of the patients at the time of surgery was 25 years (range, 11-36 years). Pain was the indication for surgery in all patients. The preoperative deformities were classified into two groups. Hips in Group I had an angular head and a normal or valgus neck. Hips in Group II had an ovoid head, a short neck in varus angulation, and relative overgrowth of the greater trochanter. There were seven hips (seven patients) in Group I, and 11 hips (10 patients) in Group II. The sum of the most recent pain score and gait score of Merle d'Aubigné (a full score of 12 points) was 11 to 12 points for seven of 11 hips of Group II, and 11 to 12 points for only one of the seven hips of Group I. For patients with hip pain in Group II, this operation fairly consistently relieves pain for at least an average of 13 years, but whether the rate of development of osteoarthrosis is retarded is not known.

Angular velocity and head direction signals recorded from the dorsal tegmental nucleus of gudden in the rat: Implications for path integration in the head direction cell circuit.

Angular velocity and head direction signals recorded from the dorsal tegmental nucleus of gudden in the rat: Implications for path integration in the head direction cell circuit.

Central Versus Peripheral Origin of Vestibuloocular Reflex Recovery Following Semicircular Canal Plugging in Rhesus Monkeys

We have previously shown that there is a slowly progressing, frequency-specific recovery of the gain and phase of the horizontal vestibuloocular reflex (VOR) in rhesus monkeys following plugging of the lateral semicircular canals. The adapted VOR response exhibited both dynamic and spatial characteristics that were distinctly different from responses in intact animals. To discriminate between adaptation or recovery of central versus peripheral origin, we have tested the recovered vestibuloocular responses in three rhesus monkeys in which either one or both coplanar pairs of vertical semicircular canals had been plugged previously by occluding the remaining semicircular canals in a second plugging operation. We measured the spatial tuning of the VOR in two or three different mutually orthogonal planes in response to sinusoidal oscillations (1.1 Hz, +/-5 degrees, +/-35 degrees /s) over a period of 2-3 and 12-14 mo after each operation. Apart from a significant recovery of the torsional/vertical VOR following the first operation we found that these recovered responses were preserved following the second operation, whereas the responses from the newly operated semicircular canals disappeared acutely as expected. In the follow-up period of up to 3 mo after the second operation, responses from the last operated canals showed recovery in two of three animals, whereas the previously recovered responses persisted. The results suggest that VOR recovery following plugging may depend on a regained residual sensitivity of the plugged semicircular canals to angular head acceleration.

Real-Time Assessment of Secondary Task Intrusiveness upon Real-World Driver Steering Performance using a Fiber-Optic Gyroscope

Lateral steering stability is a critical parameter of driving performance from both a theoretical as well as applied perspective. The measurement of lateral steering stability in a driving simulation environment is both straightforward and ubiquitous. However, the ability to measure this performance parameter in real-time during real-world driving has typically been fraught with technical challenges. The recent introduction of low cost fiber-optic gyroscope devices appears to have addressed many of the traditional difficulties associated with the real-time measurement of steering performance. State-of-the-art fiber-optic gyroscopes are capable of providing continuous data representing the rate of change in heading angle with a precision of 0.001 deg/sec. The current study evaluated the reliability and potential usefulness of real-time angular heading rate data collected from a instrumented research vehicle fitted with a KVH AutoGyro (fiber-optic laser gyroscope). Data from the fiber-optic gyroscope was collected and logged (at 10 Hz) via digital computer while volunteer participants performed a number of standard driving maneuvers and in-vehicle tasks involving interactions with instrument panel interfaces and controls.

Morphological identification of physiologically characterized afferents innervating the turtle posterior crista.

The turtle posterior crista consists of two hemicristae. Each hemicrista extends from the planum semilunatum to the nonsensory torus and includes a central zone (CZ) surrounded by a peripheral zone (PZ). Type I and type II hair cells are found in the CZ and are innervated by calyx, dimorphic and bouton afferents. Only type II hair cells and bouton fibers are found in the PZ. Units were intraaxonally labeled in a half-head preparation. Bouton (B) units could be near the planum (BP), near the torus (BT), or in midportions of a hemicrista, including the PZ and CZ. Discharge properties of B units vary with longitudinal position in a hemicrista but not with morphological features of their peripheral terminations. BP units are regularly discharging and have small gains and small phase leads re angular head velocity. BT units are irregular and have large gains and large phase leads. BM units have intermediate properties. Calyx (C) and dimorphic (D) units have similar discharge properties and were placed into a single calyx-bearing (CD) category. While having an irregular discharge resembling BT units, CD units have gains and phases similar to those of BM units. Rather than any single discharge property, it is the relation between discharge regularity and either gain or phase that makes CD units distinctive. Multivariate statistical formulas were developed to infer a unit's morphological class (B or CD) and longitudinal position solely from its discharge properties. To verify the use of the formulas, discharge properties were compared for units recorded intraaxonally or extracellularly in the half-head or extracellularly in intact animals. Most B units have background rates of 10-30 spikes/s. The CD category was separated into CD-high and CD-low units with background rates above or below 5 spikes/s, respectively. CD-low units have lower gains and phases and are located nearer the planum than CD-high units. In their response dynamics over a frequency range from 0.01-3 Hz, BP units conform to an overdamped torsion-pendulum model. Other units show departures from the model, including high-frequency gain increases and phase leads. The longitudinal gradient in the physiology of turtle B units resembles a similar gradient in the anamniote crista. In many respects, turtle CD units have discharge properties resembling those of calyx-bearing units in the mammalian central zone.

Initial vestibulo-ocular reflex during transient angular and linear acceleration in human cerebellar dysfunction.

During transient, high-acceleration rotation, performance of the normal vestibulo-ocular reflex (VOR) depends on viewing distance. With near targets, gain (eye velocity/head velocity) enhancement is manifest almost immediately after ocular rotation begins. Later in the response, VOR gain depends on both head rotation and translation; gain for near targets is decreased for rotation about axes anterior to the otoliths and augmented for rotation about axes posterior to the otoliths. We sought to determine whether subjects with cerebellar dysfunction have impaired modification of the VOR with target distance. Eleven subjects of average age 48 +/- 16 years (mean +/- standard deviation, SD) with cerebellar dysfunction underwent transients of directionally unpredictable whole-body yaw rotation to a peak angular acceleration of 1000 or 2800 degrees/s2 while viewing a target either 15 cm or 500 cm distant. Immediately before onset of head rotation, the lights were extinguished and were relit only after the rotation was completed. The axis of head rotation was varied so that it was located 20 cm behind the eyes, 7 cm behind the eyes (centered between the otoliths), centered between the eyes, or 10 cm anterior to the eyes. Angular eye and head positions were measured with magnetic search coils. The VOR in subjects with cerebellar dysfunction was compared with the response from 12 normal subjects of mean age 25 +/- 4 years. In the period 35-45 ms after onset of 2800 degrees/s2 head rotation, gain was independent of rotational axis. In this period, subjects with cerebellar dysfunction had a mean VOR gain of 0.5 +/- 0.2, significantly lower than the normal range of 1.0 +/- 0.2. During a later period, 125-135 ms after head rotation about an otolith-centered axis, subjects with cerebellar dysfunction had a mean VOR gain of 0.67 +/- 0.46, significantly lower than the value of 1.06 +/- 0.14 in controls. Unlike normal subjects, those with cerebellar dysfunction did not show modification of VOR gain with target distance in the early response and only one subject showed a correct effect of target distance in the later response. The effect of target distance was quantitatively assessed by subtracting gain for a target 500 cm distant from gain for a target 15 cm distant. During the period 35-45 ms after the onset of 2800 degrees/s2 head motion, only two subjects with cerebellar loss demonstrated significant VOR gain enhancement with a near target, and both of these exhibited less than half of the mean enhancement for control subjects. During the later period 125-135 ms after the onset of head rotation, when VOR gain normally depended on both target location and otolith translation, only one subject with cerebellar dysfunction consistently demonstrated gain changes in the normal direction. These findings support a role for the cerebellum in gain modulation of both the canal and otolith VOR in response to changes in distance. The short latency of gain modification suggests that the cerebellum may normally participate in target distance-related modulation of direct VOR pathways in a manner similar to that found in plasticity induced by visual-vestibular mismatch.

Early components of the human vestibulo-ocular response to head rotation: latency and gain.

To characterize vestibulo-ocular reflex (VOR) properties in the time window in which contributions by other systems are minimal, eye movements during the first 50-100 ms after the start of transient angular head accelerations ( approximately 1000 degrees /s(2)) imposed by a torque helmet were analyzed in normal human subjects. Orientations of the head and both eyes were recorded with magnetic search coils (resolution, approximately 1 min arc; 1000 samples/s). Typically, the first response to a head perturbation was an anti-compensatory eye movement with zero latency, peak-velocity of several degrees per second, and peak excursion of several tenths of a degree. This was interpreted as a passive mechanical response to linear acceleration of the orbital tissues caused by eccentric rotation of the eye. The response was modeled as a damped oscillation (approximately 13 Hz) of the orbital contents, approaching a constant eye deviation for a sustained linear acceleration. The subsequent compensatory eye movements showed (like the head movements) a linear increase in velocity, which allowed estimates of latency and gain with linear regressions. After appropriate accounting for the preceding passive eye movements, average VOR latency (for pooled eyes, directions, and subjects) was calculated as 8.6 ms. Paired comparisons between the two eyes revealed that the latency for the eye contralateral to the direction of head rotation was, on average, 1.3 ms shorter than for the ipsilateral eye. This highly significant average inter-ocular difference was attributed to the additional internuclear abducens neuron in the pathway to the ipsilateral eye. Average acceleration gain (ratio between slopes of eye and head velocities) over the first 40-50 ms was approximately 1.1. Instantaneous velocity gain, calculated as Veye(t)/Vhead(t-latency), showed a gradual build-up converging toward unity (often after a slight overshoot). Instantaneous acceleration gain also converged toward unity but showed a much steeper build-up and larger oscillations. This behavior of acceleration and velocity gain could be accounted for by modeling the eye movements as the sum of the passive response to the linear acceleration and the active rotational VOR. Due to the latency and the anticompensatory component, gaze stabilization was never complete. The influence of visual targets was limited. The initial VOR was identical with a distant target (continuously visible or interrupted) and in complete darkness. A near visual target caused VOR gain to rise to a higher level, but the time after which the difference between far and near targets emerged varied between individuals.

Eye-position dependence of three-dimensional ocular rotation-axis orientation during head impulses in humans.

If horizontal saccades or smooth-pursuit eye movements are made with the line-of-sight at different elevations, the three-dimensional (3D) angular rotation axis of the globe tilts by half the vertical eye eccentricity. This phenomenon is named "half-angle rule" and is a consequence of Listing's law. It was recently found that the ocular rotation axis during the horizontal vestibulo-ocular reflex (VOR) on a turntable also tilts in the direction of the line-of-sight by about a quarter of the eye's vertical eccentricity. This is surprising, since, in a "perfect" VOR, the angular rotation axis of the eye should be independent from the position of the eye to fully compensate for the 3D angular head rotation. We asked whether this quarter-angle strategy is a general property of the VOR or whether the 3D kinematics of ocular movements evoked by vestibular stimulation would be less eye-position dependent at higher stimulus frequencies. Nine healthy subjects were exposed to horizontal head impulses (peak velocity approximately 250 degrees /s). The line-of-sight was systematically changed along the vertical meridian of a tangent screen. Three-dimensional eye and head movements were monitored with dual search coils. The 3D orientation of the angular eye-in-head rotation axis was determined by calculating the average angular velocity vectors of the initial 10 degrees displacements. Then, the difference between the tilt angles of the ocular rotation axis during upward and downward viewing was determined and divided by the difference of vertical eccentricity ("tilt angle coefficient"). Control experiments included horizontal saccades, smooth-pursuit eye movements, and eye movements evoked by slow, passive head rotations at the same vertical eye eccentricities. On average, the ocular rotation axis during horizontal head-impulse testing at different elevations of the line-of-sight was closely aligned with the rotation axis of the head (tilt angle coefficient of pooled abducting and adducting eye movements: 0.11+/-0.17 SD). Values for slow head impulses, however, exceeded somewhat the quarter angle (0.33+/-0.12), while smooth-pursuit movements (0. 50+/-0.09) and saccades (0.44+/-0.11) were closest to the half angle. These results demonstrate that the 3D orientation of the ocular rotation axis during rapid head thrusts is relatively independent of the direction of the line-of-sight and that ocular rotations elicited by head impulses are kinematically different from saccades, despite similar movement dynamics.

A linear canal-otolith interaction model to describe the human vestibulo-ocular reflex.

A control systems model of the vestibulo-ocular reflex (VOR) originally derived for yaw rotation about an eccentric axis (Crane et al. 1997) was applied to data collected during ambulation and dynamic posturography. The model incorporates a linear summation of an otolith response due to head translation scaled by target distance, adding to a semi-circular canal response that depends only on angular head rotation. The results of the model were compared with human experimental data by supplying head angular velocity as determined by magnetic search coil recording as the input for the canal branch of the model and supplying linear acceleration as determined by flux gate magnetometer measurements of otolith position. The model was fit to data by determining otolith weighting that enabled the model to best fit the data. We fit to the model experimental data from normal subjects who were: standing quietly, walking, running, or making active sinusoidal head movements. We also fit data obtained during dynamic posturography tasks of: standing on a platform sliding in a horizontal plane at 0.2 Hz, standing directly on a platform tilting at 0.1 Hz, and standing on the tilting platform buffered by a 5-cm thick foam rubber cushion. Each task was done with the subject attending a target approximately 500, 100, or 50 cm distant, both in light and darkness. The model accurately predicted the observed VOR response during each test. Greater otolith weighting was required for near targets for nearly all activities, consistent with weights for the otolith component found in previous studies employing imposed rotations. The only exceptions were for vertical axis motion during standing, sliding, and tilting when the platform was buffered with foam rubber. In the horizontal axis, the model always fit near target data better with a higher otolith component. Otolith weights were similar with the target visible and in darkness. The model predicts eye movement during both passive whole-body rotation and free head movement in space implying that the VOR is controlled by a similar mechanism during both situations. Factors such as vision, proprioception, and efference copy that are available during head free motion but not during whole-body rotation are probably not important to gaze stabilization during ambulation and postural stabilizing movement. The linearity of the canal-otolith interaction was tested by re-analysis of the whole body rotation data on which the model is based (Crane et al. 1997). Normalized otolith-mediated gain enhancement was determined for each axis of rotation. This analysis uncovered minor non-linearities in the canal-otolith interaction at frequencies above 1.6 Hz and when the axis of rotation was posterior to the head.

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.