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I S Curthoys

Publications and source records attributed to I S Curthoys.

At least 19 recordsLinked to original sources

Physiological and anatomical study of click-sensitive primary vestibular afferents in the guinea pig.

We studied the sensitivity of primary vestibular afferents in anaesthetised guinea pigs to clicks. These vestibular neurons were also tested by their response to pitch and roll tilts and yaw-axis angular acceleration. The click intensity was referred to the threshold for evoking the auditory brainstem responses. Recording sites in the vestibular nerve were confirmed histologically using iontophoretic injection of FCF green dye. To confirm the site of labyrinthine origin of the click-sensitive neurons, we used retrograde tracing with biocytin. In all, 647 out of 2354 neurons in the vestibular nerves of 51 guinea pigs were activated by clicks. Most were irregularly discharging primary neurons, but some were regularly discharging. We studied responses to vestibular stimuli in 188 click-sensitive neurons. Of these, 86% responded to pitch and/or roll tilt, but none responded to yaw angular acceleration. Conversely we also recorded vestibular neurons which did not respond to clicks. None of 300 neurons sensitive to yaw angular acceleration were responsive to 80-90 dB SL clicks (0 dB SL = threshold for auditory brainstem response to clicks). The latencies of click-evoked action potentials of neurons in the vestibular nerve were very short (mean +/- SD = 0.82 +/- 0.22 ms). Changing click polarity caused a heterogeneous pattern of latency change. Thresholds for evoking spikes in primary vestibular neurons were high (62.0 +/- 12.2 dB SL, range 30-90 dB, n = 371). Retrograde tracing of the origin of the click-sensitive afferents using extracellular biocytin showed that most neurons originated in the medial (striola area) of the saccular macula.

Acoustic Stimulation

Response of guinea pig vestibular nucleus neurons to clicks.

Responses of single neurons in the vestibular nuclei to clicks were studied by extracellular recording in anaesthetised guinea pigs. Eighty-four neurons in the ipsilateral vestibular nuclei were activated with an average latency of 1.75 +/- 0.30 ms, which is about 0.9 ms longer than the mean latency of activation of click-sensitive vestibular afferents to intense clicks. The threshold of clicks for evoking the response of these neurons was around 70 dB above the auditory brainstem response threshold. Earlier studies have indicated that click-sensitive vestibular afferents are tilt-sensitive and likely to originate from saccular receptors, and in the present study nine of the click-sensitive vestibular nucleus neurons were tilt-sensitive, suggesting that these central neurons receive monosynaptic input from the corresponding saccular afferents. Recording sites were marked by means of iontophoretic injection of FCF green dye; they were located in the lateral portion of the descending vestibular nucleus and the caudal and ventral regions of the lateral vestibular nucleus.

Acoustic Stimulation

The three-dimensional human vestibulo-ocular reflex: response to long-duration yaw angular accelerations.

We recorded three-dimensional eye movements during angular acceleration steps from 0 to 250 degrees/s at 20 degrees/s2 about an earth-vertical axis. Experiments were performed on 27 normal subjects and on 19 patients who had recovered well from unilateral vestibular deafferentation on the right or left side. In addition to compensatory horizontal eye movements, significant vertical and torsional eye movement components were elicited. These vertical and torsional eye velocity traces led to a shift of the axis of eye velocity away from the axis of head velocity. Horizontal, vertical, and torsional velocity components showed clear differences between normals and patients with unilateral vestibular deafferentation. In normals, the axis of eye velocity tilted backward and slightly away from the axis of head velocity. Patients showed similar, but more pronounced, shifts during rotations toward the intact ear and shifts in the opposite direction for rotations toward the operated ear. Eye velocity traces were analyzed with special consideration given to the orientation of the axis of eye velocity. We speculate that the vertical and torsional velocity components may be due to the effects of Listing's plane, as well as the contributions of the otolith signals.

Adult

A neural network simulation of the vestibular system: implications on the role of intervestibular nuclear coupling during vestibular compensation.

Previous neural network simulations of the vestibular system have been based loosely on known physiology. This research involved the use of a strongly physiologically based neural network model which was used to investigate the role of the vestibular commissure in restoring the bilateral symmetry of the resting rates of the vestibular nuclei during vestibular compensation following unilateral labyrinthectomy. It was found the readjustments in the gain of the vestibular commissure were not primarily responsible for vestibular compensation, as has previously been suggested, but rather that it was modifications in extralabyrinthine sources of tone which mediated the restoration of the central symmetry between the two nuclei.

Animals

A geometric basis for measurement of three-dimensional eye position using image processing.

Polar cross correlation is commonly used for determination of ocular torsion from video images, but breaks down at eccentric positions if the spherical geometry of the eye is not considered. We have extended this method to allow three-dimensional eye position measurement over a range of +/- 20 deg by determining the correct projection of the eye onto the image plane of the camera. We also determine the orientation of the camera with respect to the eye, allowing eye position to be represented in appropriate head-fixed coordinates. These algorithms have been validated using both in vitro and in vivo measures of eye position.

Algorithms

The role of ocular torsion in visual measures of vestibular function.

This brief review highlights problems in the interpretation of results about perceived postural roll-tilt of human subjects undergoing roll-tilt around their naso-occipital axis, when visual stimuli are used as a means of indicating perception. The otolithic stimulus, which causes the changes in perceived posture, also causes the eyes to roll (or tort). In turn, the altered torsional position of the eye causes the perceived orientation of visual stimuli to change. Consequently, indicators of postural perception, which rely on visual stimuli, are a confounded combination of two factors; the person's perceived postural roll-tilt, and the effect of the otolithic stimulus on ocular torsional position. Consequently, settings of a visual stimulus do not permit direct unambiguous interpretation of a subject's perceived postural roll-tilt.

Eye Movements

The delay of the oculogravic illusion.

Previous measures of roll-tilt sensation during combined angular and linear acceleration during off-center rotation have found a heading-dependent delay in reaching a stable sensory value. This delay has been attributed to sensory conflict between the canal and otolith signals. Another possibility is that the visual indicator used to measure this sensation may have been responsible for the heading-dependent difference. This study used a somatosensory task, which is free from such artifacts and still showed a significant heading-dependent delay. We conclude that in analyzing canal-otolith interaction it is necessary to take into account the direction of the linear acceleration with respect to the activated canal.

Adult

Three-dimensional vector analysis of the human vestibuloocular reflex in response to high-acceleration head rotations. I. Responses in normal subjects.

1. The kinematics of the human angular vestibuloocular reflex (VOR) in three dimensions was investigated in 12 normal subjects during high-acceleration head rotations (head "impulses"). A head impulse is a passive, unpredictable, high-acceleration (3,000-4,000 degrees/s2) head rotation of approximately 10-20 degrees in roll, pitch, or yaw, delivered with the subject in the upright position and focusing on a fixation target. Head and eye rotations were measured with dual search coils and expressed as rotation vectors. The first of these two papers describes a vector analysis of the three-dimensional input-output kinematics of the VOR as two indexes in the time domain: magnitude and direction. 2. Magnitude is expressed as speed gain (G) and direction as misalignment angle (delta). G is defined as the ratio of eye velocity magnitude (eye speed) to head velocity magnitude (head speed). delta is defined as the instantaneous angle by which the eye rotation axis deviates from perfect alignment with the head rotation axis in three dimensions. When the eye rotation axis aligns perfectly with the head rotation axis and when eye velocity is in a direction opposite to head velocity, delta = 0. The orientation of misalignment between the head and the eye rotation axes is characterized by two spatial misalignment angles, which are the projections of delta onto two orthogonal coordinate planes that intersect at the head rotation axis. 3. Time series of G were calculated for head impulses in roll, pitch, and yaw. At 80 ms after the onset of an impulse (i.e., near peak head velocity), values of G were 0.72 +/- 0.07 (counterclockwise) and 0.75 +/- 0.07 (clockwise) for roll impulses, 0.97 +/- 0.05 (up) and 1.10 +/- 0.09 (down) for pitch impulses, and 0.95 +/- 0.06 (right) and 1.01 +/- 0.07 (left) for yaw impulses (mean +/- 95% confidence intervals). 4. The eye rotation axis was well aligned with head rotation axis during roll, pitch, and yaw impulses: delta remained almost constant at approximately 5-10 degrees, so that the spatial misalignment angles were < or = 5 degrees. delta was 9.6 +/- 3.1 (counterclockwise) and 9.0 +/- 2.6 (clockwise) for roll impulses, 5.7 +/- 1.6 (up) and 6.1 +/- 1.9 (down) for pitch impulses, and 6.2 +/- 2.2 (right) and 7.9 +/- 1.5 (left) for yaw impulses (mean +/- 95% confidence intervals). 5. VOR gain (gamma) is the product of G and cos(delta). Because delta is small in normal subjects, gamma is not significantly different from G. At 80 ms after the onset of an impulse, gamma was 0.70 +/- 0.08 (counterclockwise) and 0.74 +/- 0.07 (clockwise) for roll impulses, 0.97 +/- 0.05 (up) and 1.09 +/- 0.09 (down) for pitch impulses, and 0.94 +/- 0.06 (right) and 1.00 +/- 0.07 (left) for yaw impulses (mean +/- 95% confidence intervals). 6. VOR latencies, estimated with a latency shift method, were 10.3 +/- 1.9 (SD) ms for roll impulses, 7.6 +/- 2.8 (SD) ms for pitch impulses, and 7.5 +/- 2.9 (SD) ms for yaw impulses. 7. We conclude that the normal VOR produces eye rotations that are almost perfectly compensatory in direction as well as in speed, but only during yaw and pitch impulses. During roll impulses, eye rotations are well aligned in direction, but are approximately 30% slower in speed.

Adult

Three-dimensional vector analysis of the human vestibuloocular reflex in response to high-acceleration head rotations. II. responses in subjects with unilateral vestibular loss and selective semicircular canal occlusion.

1. We studied the three-dimensional input-output human vestibuloocular reflex (VOR) kinematics after selective loss of semicircular canal (SCC) function either through total unilateral vestibular deafferentation (uVD) or through single posterior SCC occlusion (uPCO), and showed large deficits in magnitude and direction in response to high-acceleration head rotations (head "impulses"). 2. A head impulse is a passive, unpredictable, high-acceleration (3,000-4,000 degrees/s2) head rotation through an amplitude of 10-20 degrees in roll, pitch, or yaw. The subjects were tested while seated in the upright position and focusing on a fixation target. Head and eye rotations were measured with the use of dual search coils, and were expressed as rotation vectors. A three-dimensional vector analysis was performed on the input-output VOR kinematics after uVD, to produce two indexes in the time domain: magnitude and direction. Magnitude is expressed as speed gain (G) and direction as misalignment angle (delta). 3. G. after uVD, was significantly lower than normal in both directions of head rotation during roll, pitch, and yaw impulses, and were much lower during ipsilesional than during contralesional roll and yaw impulses. At 80 ms from the onset of an impulse (i.e., near peak head velocity), G was 0.23 +/- 0.08 (SE) (ipsilesional) and 0.56 +/- 0.08 (contralesional) for roll impulses, 0.61 +/- 0.09 (up) and 0.72 +/- 0.10 (down) for pitch impulses, and 0.36 +/- 0.06 (ipsilesional) and 0.76 +/- 0.09 (contralesional) for yaw impulses (mean +/- 95% confidence intervals). 4. delta, after uVD, was significantly different from normal during ipsilesional roll and yaw impulses and during pitch-up and pitch-down impulses. delta was normal during contralesional roll and yaw impulses. At 80 ms from the onset of the impulse, delta was 30.6 +/- 4.5 (ipsilesional) and 13.4 +/- 5.0 (contralesional) for roll impulses, 23.7 +/- 3.7 (up) and 31.6 +/- 4.4 (down) for pitch impulses, and 68.7 +/- 13.2 (ipsilesional) and 11.0 +/- 3.3 (contralesional) for yaw impulses (mean +/- 95% confidence intervals). 5. VOR gain (gamma), after uVD, were significantly lower than normal for both directions of roll, pitch, and yaw impulses and much lower during ipsilesional than during contralesional roll and yaw impulses. At 80 ms from the onset of the head impulse, the gamma was 0.22 +/- 0.08 (ipsilesional) and 0.54 +/- 0.09 (contralesional) for roll impulses, 0.55 +/- 0.09 (up) and 0.61 +/- 0.09 (down) for pitch impulses, and 0.14 +/- 0.10 (ipsilesional) and 0.74 +/- 0.06 (contralesional) for yaw impulses (mean +/- 95% confidence intervals). Because gamma is equal to [G*cos (delta)], it is significantly different from its corresponding G during ipsilesional roll and yaw, and during all pitch impulses, but not during contralesional roll and yaw impulses. 6. After uPCO, pitch-vertical gamma during pitch-up impulses was reduced to the same extent as after uVD; roll-torsional gamma during ipsilesional roll impulses was significantly lower than normal but significantly higher than after uVD. At 80 ms from the onset of the head impulse, gamma was 0.32 +/- 0.13 (ipsilesional) and 0.55 +/- 0.16 (contralesional) for roll impulses, 0.51 +/- 0.12 (up) and 0.91 +/- 0.14 (down) for pitch impulses, and 0.76 +/- 0.06 (ipsilesional) and 0.73 +/- 0.09 (contralesional) for yaw impulses (mean +/- 95% confidence intervals). 7. The eye rotation axis, after uVD, deviates in the yaw plane, away from the normal interaural axis, toward the nasooccipital axis, during all pitch impulses. After uPCO, the eye rotation axis deviates in same direction as after uVD during pitch-up impulses, but is well aligned with the head rotation axis during pitch-down impulses.

Adult

Compensation of the human vertical vestibulo-ocular reflex following occlusion of one vertical semicircular canal is incomplete.

The vestibulo-ocular reflex (VOR) was studied in nine human subjects 2-15 months after permanent surgical occlusion of one posterior semicircular canal. The stimuli used were rapid, passive, unpredictable, low-amplitude (10-20 degrees), high-acceleration (3000-4000 degrees/s2) head rotations in pitch and yaw planes. The responses measured were vertical and horizontal eye rotations, and the results were compared with those from 19 normal subjects. After unilateral occlusion of the posterior semicircular canal, the gain of the head-up pitch vertical VOR--the vertical VOR generated by excitation from only one and disfacilitation from two vertical semicircular canals--was reduced to 0.61 +/- 0.06 (normal 0.92 +/- 0.06) at a head velocity of 200 degrees/s. In contrast the gain of the head-down pitch vertical VOR--the VOR still generated by excitation from two, but disfacilitation from only one vertical semicircular canal--was within normal limits: 0.86 +/- 0.11 (normal 0.96 +/- 0.04). The gain of the horizontal VOR in response to yaw head rotations--ipsilesion 0.81 +/- 0.06 (normal 0.88 +/- 0.05) and contralesion 0.80 +/- 0.11 (normal 0.92 +/- 0.11)--was within normal limits in both directions (group means +/- two-tailed 95% confidence intervals given in each case). These results show that occlusion of just one vertical semicircular canal produces a permanent deficit of about 30% in the vertical VOR gain in response to rapid pitch head rotations in the excitatory direction of the occluded canal. This observation indicates that, in response to a stimulus in the higher dynamic range, compensation of the human VOR for the loss of excitatory input from even one vertical semicircular canal is incomplete.

Adaptation, Physiological

Responses of guinea pig primary vestibular neurons to clicks.

Responses of single neurons in the vestibular nerve to high-intensity clicks were studied by extracellular recording in anaesthetised guinea pigs. One hundred and two neurons in the posterior division of the superior branch or in the inferior branch of the vestibular nerve were activated at short latency by intense clicks. The latency of activation was short (median 0.9 ms) and the threshold was high: the click intensity for evoking the response of these cells was around 60 dB above the auditory brainstem response threshold. Animals were tilted and rotated to identify physiologically the sensory region of the labyrinth from which the activated neurons originated. Seventeen neurons responded to static tilt as well as clicks. These results show that vestibular receptors, probably the otoliths, respond to clicks at intensities corresponding to those used in a new clinical test of the vestibulo-collic pathway.

Acoustic Stimulation

The human ocular torsion position response during yaw angular acceleration.

Recent results by Wearne [(1993) Ph.D. thesis] using the scleral search-coil method of measuring eye position indicate that changes in ocular torsion position (OTP) occur during yaw angular acceleration about an earth vertical axis. The present set of experiments, using an image processing method of eye movement measurement free from the possible confound of search coil slippage, demonstrates the generality and repeatability of this phenomenon and examines its possible causes. The change in torsion position is not a linear vestibulo-ocular reflex (LVOR) response to interaural linear acceleration stimulation of the otoliths, but rather the effect is dependent on the characteristics of the angular acceleration stimulus, commencing at the onset and decaying at the offset of the angular acceleration. In the experiments reported here, the magnitude of the angular acceleration stimulus was varied and the torsion position response showed corresponding variations. We consider that the change in torsion position observed during angular acceleration is most likely to be due to activity of the semicircular canals.

Acceleration

Unilateral vestibular deafferentation (UVD) causes permanent asymmetry in the gain of the yaw VOR to high acceleration head impulses in guinea pigs.

Using an acute scleral search coil technique for measuring eye position in alert animals we have shown that after UVD the yaw VOR in the guinea pig shows a permanent gain asymmetry. There is a reduced gain during the first 100 ms of brief, high acceleration horizontal head rotations ("yaw head impulses") towards the operated side, but only a small loss in gain for similar rotations towards the intact side. This result confirms that the horizontal E response during the first 100 ms of an abrupt high acceleration head rotation is a clear indicator of the function of the horizontal canal. These results are similar to those in human patients after unilateral acoustic neuroma operations. The asymmetry in response is large shortly after UVD and decreases over time but is permanent.

Acceleration

Torsional eye velocity components during yaw angular acceleration identify the side of unilateral vestibular deafferentation.

Using dual torsion scleral search coils we have recorded 3-dimensional eye position during yaw angular accelerations of 20 degrees/s2 about an earth vertical axis in healthy subjects and in patients with unilateral vestibular deafferentation (UVD). These experiments produced two interesting results: i) even in healthy subjects, the axis of eye velocity did not coincide with the (earth vertical) stimulus axis during centred rotation; ii) Patients with UVD had torsional eye velocity components that were systematically different from those in normal subjects. While in normals the direction of the torsional component of the eye velocity depended on the direction of rotation and was on average approximately symmetric for CW and CCW yaw rotation, there was a clear asymmetry in patients, which was distinctly different for left and right UVD.

Acceleration

The effect of unilateral posterior semicircular canal inactivation on the human vestibulo-ocular reflex.

The responses to rapid, passive, unpredictable, low amplitude (10-20 degrees), high acceleration (3,000-4,000 degrees/s2) head rotations were used to study the human vestibulo-ocular reflex (VOR) in pitch and yaw plane after unilateral posterior semicircular canal occlusion (uPCO) in 10 subjects. The results from these 10 uPCO subjects were compared with those from 18 normal subjects. The VOR gains at a head velocity of 200 degrees/s in the uPCO subjects were: pitch upward = 0.62 +/- 0.06, pitch downward = 0.87 +/- 0.11, yew ipsilesion = 0.78 +/- 0.06, yaw contralesion = 0.79 +/- 0.10 and in normal subjects were: pitch upward = 0.92 +/- 0.06, pitch downward = 0.96 +/- 0.04, yaw right = 0.88 +/- 0.05, yaw left = 0.91 +/- 0.12 (group means +/- twotailed 95% confidence intervals). The results showed that the pitch-vVOR gain was significantly (p < 0.05) decreased in response to upward head impulses whereas in response to downward, ipsilesion and contralesion head impulses were not significantly different (p > 0.05) from the normals. This study shows that there is 30% permanent residual deficit of the upward pitch-vVOR with an up-down asymmetry in pitch-vVOR gain following inactivation of a single posterior semicircular canal and that compensation of pitch-vVOR function is incomplete.

Adult

Ocular torsion position and the perception of visual orientation.

Previous studies have shown that in patients with unilateral vestibular deafferentation (UVD) there is a close relationship between the change in ocular torsional position consequent on the UVD, and the visually perceived orientation of short dim lines in an otherwise darkened room (1). However that result may have been confounded because the UVD may have affected both ocular torsion and sensory information about head position re gravity which must be used in making the visual perceptual judgement. Therefore we have sought a means of testing the relationship between ocular torsional position and the visual perception of orientation which was not confounded by the possible effect of changes in perceived head position.

Afferent Pathways

The effect of roll-tilt on ocular skew deviation.

Static roll-tilt of normal healthy subjects causes the ocular tilt reaction (OTR) one component of which is disconjugate vertical eye position (skew deviation). In this study the magnitude of skew was measured subjectively by the use of a computerized Hess test at three static roll-tilt angles (head erect, left ear down and right ear down) and two viewing distances (20 cm and 60 cm). The results showed that during static roll-tilt there was a small skew deviation, the magnitude of which was increased at close viewing distances.

Afferent Pathways