How does the otolith system detect three-dimensional head angular velocity?
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Animals↗
Biomedical subjects
B J Hess
Publications and source records attributed to B J Hess.
Does counterrolling violate Listing's law?
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Animals↗
Three-dimensional head angular velocity detection from otolith afferent signals.
Afferent signals from the otolith organs can produce compensatory eye position and velocity signals which has been described as linear vestibulo-ocular reflex (LVOR). The afferent otolith signals carry information about head orientation and changes of head orientation relative to gravity. A head orientation (tilt) related position signal can be obtained from population vector coding of tonic otolith afferent signals during static or dynamic head tilts, which in turn could produce compensatory eye position signals in the LVOR. On the other hand, eye angular velocity signals may be extracted, as proposed in this study, from the population response of tilt-velocity sensitive otolith afferents. Such afferents are shown to encode instantaneous head orientation relative to gravity at onset of a head movement and, as the movement continues, the projection of head angular velocity onto the earth-horizontal plane, indicating the instantaneous direction of movement relative to gravity. Angular velocity components along the earth-vertical direction which are not directly encoded by otolith afferents can be detected by central signal processing. Central reconstruction of 3D head angular velocity allows to obtain information about absolute head orientation in space even in the absence of semi-circular canal related information. Such information is important for generating compensatory eye movements as well as for dynamic control of posture.
Afferent Pathways↗
Visual suppression of torsional vestibular nystagmus in rhesus monkeys.
Juvenile rhesus monkeys, placed on a motorized turntable, were rotated at constant velocity and then decelerated about an Earth-vertical axis. The animals were implanted with dual search coils to measure eye movements in three dimensions. By changing the monkey's body position (upright, ear-down, supine), postrotatory nystagmus was elicited in the horizontal, vertical, or torsional direction. Peak slow phase eye velocity and time constant of velocity decay were compared between decelerations in the dark and in the light. In all nystagmus directions, illumination reduced the time constant (Tc) to values around 5 sec. Peak velocity (Vp) was markedly attenuated in the horizontal and vertical directions (around 50%), but the effect of light on Vp in the torsional direction was small (less than 20%). These findings were independent of the velocity step size. Our hypothesis is that the two dynamic components of optokinetic nystagmus, as they interact with postrotatory nystagmus during visual suppression, differ in their dimensionality: the early component (fast component, direct pathway, pursuit system) is mainly activated in the horizontal and vertical directions, while the late component (slow component, indirect pathway, optokinetic system) effectively operates in all three dimensions.
Animals↗
Calibration of three-dimensional eye position using search coil signals in the rhesus monkey.
A procedure is described to calibrate three-dimensional eye position with a dual-search coil implant in rhesus monkeys using a two-field magnetic system. The method allows one to determine the sensitivity of the search coils taking into account the presence of d.c. offset voltages. The orientation of the implant on the eye relative to a space-fixed reference frame is computed using fixations of targets arranged vertically. The critical steps of the procedure are discussed and documented by experimental data.
Algorithms↗
Static roll and pitch in the monkey: shift and rotation of Listing's plane.
In three rhesus monkeys three-dimensional eye positions were measured with the dual search coil technique. Recordings of spontaneous eye movements were made in the light and in the dark, with the monkeys in different static roll or pitch positions. Eye positions were expressed as rotation vectors. In all static positions eye rotation vectors were confined to a plane, i.e. Listing's plane was conserved. Tilt about the roll axis shifted the plane along this axis, i.e. a constant torsional component was added to all eye positions. Tilt about the pitch axis changed the pitch angle of Listing's plane.
Animals↗
Two- rather than three-dimensional representation of saccades in monkey superior colliculus.
Saccades are controlled by neurons in the brainstem reticular formation that receive input from the superior colliculus and cortex. Recently two quantitative models have been proposed for the role of the colliculus in the generation of three-dimensional eye movements. In order to test these models, three-dimensional eye movements were measured in the alert monkey to investigate whether the saccadic motor map of the superior colliculus is two-dimensional, representing retinal target vectors, or three-dimensional, representing three-dimensional motor error for the rotation of the eye. Electrical stimulation of the superior colliculus produced two-dimensional, not three-dimensional, eye movements. It is therefore concluded that the collicular motor map is two-dimensional.
Animals↗
Smooth pursuit eye movements obey Listing's law in the monkey.
We have tested Listing's law in the monkey using the dual search coil technique to record 3-dimensional eye positions during smooth pursuit and during spontaneous eye movements in the light. Our results indicate that during smooth pursuit the eye positions obey Listing's law with a least the same accuracy as during spontaneous eye movements or during periods of fixations.
Animals↗
Magnetic search coil system for linear detection of three-dimensional angular movements.
The design of a two-dimensional (2D) magnetic field search coil system based on the phase detection principle is described. The system was developed to record horizontal and vertical eye and head movements of small, unrestrained laboratory animals. It is also applicable for measuring three-dimensional (3D) eye and head movements in primates and man. The output is linear over 355 degrees in the horizontal plane and over +/- 60 degrees in the vertical direction. The procedure of recording 3D eye and head movements is discussed.
Animals↗
Spatial organization of linear vestibuloocular reflexes of the rat: responses during horizontal and vertical linear acceleration.
1. The spatial properties of linear vestibuloocular reflexes (LVOR) were studied in pigmented rats in response to sinusoidal linear acceleration on a sled. The orientation of the animal on the sled was altered in 15 degrees steps over the range of 360 degrees. Horizontal, vertical, and torsional components of eye movements were recorded with the magnetic field search coil technique in complete darkness. Conjugacy of the two eyes was studied in the horizontal movement plane. 2. Acceleration along the optic axis of one eye (approximately 50 degrees lateral) induced maximal vertical responses in the ipsilateral eye and, at the same time, maximal torsional responses in the contralateral eye. These vertical and torsional responses of the LVOR coincide with those obtained when the respective coplanar vertical semicircular canals are stimulated. Such a congruence suggests a common reference frame for LVOR and angular vestibuloocular reflexes (AVOR), with the result that direct combination of signals indicating apparent and real head tilt is facilitated. 3. Transformations of vertical and torsional responses into head coordinates (pitch and roll) show that these movements are compensatory in direction for any combination of apparent head tilt in pitch and roll planes. 4. Gain (rotation of the eye/apparent rotation of the gravity direction) was approximately 0.3 at 0.1 Hz and decreased to approximately 0.1 at 1.0 Hz. Vertical responses tended to have a larger gain than torsional responses. Phase lag relative to peak acceleration increased from about -9 degrees to about -47 degrees over the same frequency range. 5. Vertical linear acceleration evoked only vertical eye movements at a frequency of 1.0 Hz. 6. Horizontal responses of both eyes were symmetric or asymmetric in amplitude and in-phase (conjugate) or out-of-phase (disconjugate) with respect to each other, depending on the direction of linear acceleration. Translation in the transverse direction evoked conjugate compensatory horizontal responses. Forward-backward translation evoked movements of both eyes that were symmetric in amplitude, but 180 degrees out-of-phase. Translation along diagonal axes evoked almost no horizontal responses in the eye facing in the direction of linear motion but maximal horizontal responses in the eye facing away from the direction of linear motion. These disconjugate movements resulted in a modulation of the vergence angle of the eyes. 7. Disconjugate horizontal responses in darkness are best explained by the assumption that part of the visual consequences of a translational head displacement (i.e., change of viewing distance in light) is taken into account centrally.(ABSTRACT TRUNCATED AT 400 WORDS)
Animals↗
Generation of vertical and torsional rapid eye movement in the rostral mesencephalon. Experimental data and clinical implications.
The riMLF is a nucleus in the rostral mesencephalon whose bilateral destruction leads to a palsy of vertical and torsional rapid eye movements. A unilateral lesion leads to a loss of torsional rapid eye movements in only one direction, but vertical rapid movements can still be generated with some reduction in their velocity. Single neuron studies in monkeys and anatomy support the concept that the riMLF together with the PPRF are the critical areas in the brainstem to generate rapid eye movements in 3 dimensions.
Animals↗
Dual-search coil for measuring 3-dimensional eye movements in experimental animals.
The design and fabrication of a dual-search coil for measuring three-dimensional eye movements in experimental animals is described. The coil configuration is rigid and allows reliable precalibration in the magnetic field. It is implanted beneath the conjunctiva on the eye ball using the conventional implantation technique.
Animals↗
Caloric nystagmus in three dimensions under otolithic control in rhesus monkeys. A preliminary report.
The caloric nystagmus of rhesus monkeys in the 'optimum' supine or prone position was recorded three-dimensionally using magnetic search coils. The horizontal component of the nystagmus was in the direction expected from the convection flow theory of Bárány. The torsional component changed its direction according to the side of caloric stimulation independent of head position with regard to gravity, i.e., counterclockwise nystagmus by right ear stimulation and clockwise nystagmus by left ear stimulation both in the supine or in the prone positions. The direction of the vertical component depended upon the head position and not upon the side of stimulation, i.e., up-beating nystagmus in the supine position and down-beating nystagmus in the prone position. The durations and the contours of slow phase velocity of the horizontal, vertical and torsional components were different from each other. The origins of the first phase of caloric nystagmus in three dimensions may be explained by activation of all the three semicircular canals. As for the second phase of caloric nystagmus in the supine or in the prone position, the torsional component was comparatively strong and lasted the longest among the three components. The second phase of caloric nystagmus was markedly modified by head position with regard to gravity. These findings suggest that it is the otolithic organs that determine the moving plane of second phase caloric nystagmus.
Animals↗
Effects of kainic acid lesions of the nucleus reticularis tegmenti pontis on fast and slow phases of vestibulo-ocular and optokinetic reflexes in the pigmented rat.
The nucleus reticularis tegmenti pontis (NRTP) and adjacent pontine reticular formation were lesioned chemically using the neurotoxic agent kainic acid, and the effects of these lesions on horizontal ocular optokinetic and vestibular nystagmus were examined. Eye position was measured in the alert, NRTP-lesioned animals with the electromagnetic search coil technique. Optokinetic and vestibular stimuli consisted of steps of rotations or sinusoidal oscillations of a fullfield visual pattern surrounding the animal or of the animal in total darkness, respectively. In a first group of animals, small unilateral NRTP lesions were produced by placing a single kainic acid injection in the area of the left NRTP. In one third of the animals, ipsilateral quick phases of optokinetic and vestibular nystagmus were abolished. In the remaining animals, quick phases were deficient to various degrees or not affected at all. There were no changes in the characteristics of optokinetic step responses to ipsilateral pattern rotations which activate predominantly optokinetic pathways on the side of the brainstem lesion. In animals with ipsiversive quick phase deficits, contralateral pattern rotations elicited tonic eye deviations. In a second group of animals, large uni- or bilateral lesions were produced by injecting kainic acid into three separate rostral, middle and caudal levels of the right NRTP. These animals had uni- or bilateral quick phase deficits during optokinetic and vestibular nystagmus. Optokinetic nystagmus in response to velocity steps of pattern rotation towards the lesion side was strongly reduced in gain even in those animals that had no apparent deficits in the fast contraversive reset phases. In four out of six animals, responses to sinusoidal optokinetic pattern oscillations were reduced in gain and showed increased phase lags compared to controls. Vestibulo-ocular responses to velocity steps of head rotations were of normal gain but reduced in duration (measured from onset of stimulation to reversal of nystagmus). Sinusoidal vestibulo-ocular responses evoked by head oscillations exhibited reduced gain values and strongly increased phase leads in the frequency range below 0.5 Hz. The vestibular time constant was found to be around 4.5 s in animals with NRTP lesions compared to about 7.5 s in control animals. The present results show that large kainic acid lesions of the NRTP (and adjacent area) do not abolish optokinetic eye movements in the rat, in contrast to what has been reported after electrolytic lesions.(ABSTRACT TRUNCATED AT 400 WORDS)
Animals↗
Development of optokinetic neuronal responses in the pretectum and horizontal optokinetic nystagmus in unilaterally enucleated rats.
Responses of single units to constant-velocity rotations of the visual surround (0.25-10 degrees/s) were studied in the pretectum of unilateral enucleated rats at different ages. Enucleation was performed either in the first postnatal week ("early" enucleated rats) or in the adult stage ("late" enucleated rats). Pretectal unitary responses were recorded in early enucleated animals at postnatal day 20-21, 36-49 and, in both experimental groups, in the adult stage. Optokinetic ocular nystagmus was studied in early and late enucleated rats in the adult stage. Gain of optokinetic nystagmus in temporo-nasal stimulus direction was not changed for visual surround rotations of up to 20 degrees/s compared to controls in monocular viewing conditions. At higher stimulus velocities, however, the gain dropped. In naso-temporal stimulus direction, optokinetic nystagmus was improved in gain for optokinetic pattern motions of up to 5-10 degrees/s. There were only minor differences in the gain behaviour of optokinetic nystagmus obtained from early or late enucleated rats. The optokinetic responses of pretectal neurons obtained from early and late enucleated rats were reduced in sensitivity by more than 50%. The response patterns of neurons recorded in the contralateral pretectum relative to the intact eye were shifted by a large amount from directional selective to directional nonselective response types. No such changes were obtained in the ipsilateral pretectum. In contrast to normal rats, there were very few directional selective units responding to temporo-nasal pattern motion. On the other hand, a large proportion of directional selective units responded to naso-temporal pattern motion. These latter units were found in both early and late enucleated rats. A similar response type has previously been described for intact young rats but not for adult rats. The velocity tuning curve of pretectal units studied in the adult stage was similar in shape in early and late enucleated rats and resembled that obtained from enucleated or intact young animals. Our results show that response sensitivity, direction and velocity tuning of pretectal units depend crucially on retinal afferent input originating from both eyes. The data suggest that the response characteristics of many of the pretectal units that are considered to be important for mediating optokinetic reflexes depend on interpretectal signal processing using commissural connections. There is very little evidence for an adaptative structural plasticity of the optokinetic system following loss of one eye. The reduced asymmetry observed in gain of optokinetic responses correlated in both early and late enucleated rats with the shifts observed in the distribution of pretectal unitary response patterns.
Action Potentials↗
Dynamic characteristics of optokinetically controlled eye movements following inferior olive lesions in the brown rat.
1. The inferior olive was destroyed by the drug 3-acetylpyridine in brown rats. Spontaneous and optokinetic eye movements in response to constant-velocity rotation (5-80 deg/s) or sinusoidal oscillations (0.05 and 0.1 Hz with 15 deg/s peak velocity and 0.3, 0.5, 1.0 and 2 Hz with 5 deg/s peak velocity) of the visual surround were recorded 4-6 days, 40-50 days and 3-4 months after the lesion using the magnetic search coil technique. 2. Persistent oculomotor deficits were observed in rats with a lesion of more than 97% of inferior olive neurones. In cases with a less complete lesion, no or only transient deficits were observed. In these latter cases the bulk of surviving neurones was located in the caudal half of the inferior olive, which includes the dorsal cap of Kooy. 3. Eye position holding after saccadic gaze shifts in the light was strongly deficient, showing pronounced postsaccadic centripetal drift for several hundred milliseconds. Similar deficits were observed in slow-phase components following quick phases of optokinetic nystagmus. In the dark, eye position holding was also deficient. 4. Closed-loop gains of optokinetic step responses obtained from rats with inferior olive lesions could be as good as those obtained from control animals. There was, however, a trend towards smaller gain values over the range of stimulus velocities tested. The duration of optokinetic after-nystagmus was not changed. 5. The initial fast rise of slow-phase velocity of optokinetic step responses was reduced by about 30-50%, showing no recovery in the follow-up experiments up to 3-4 months after the lesion. 6. Optokinetic responses to sinusoidal oscillations of the visual surround exhibited an increasing drop in gain for frequencies between 0.1 to 0.5 Hz. In the range of 0.5-2.0 Hz gain was only about 0.2 compared to 0.7-0.8 in control animals. Phase lag of sinusoidal responses was shifted to larger values by about 25-35 deg for frequencies increasing from 0.1 to 0.5 Hz. At 1.0 Hz phase shift was reduced to about 15 deg and at 2.0 Hz no significant change in phase was observed. Both gain and phase of sinusoidal responses showed some recovery when tested 3-4 months after inferior olive lesion. 7. The results suggest that inferior olive lesions impair velocity-to-position integration, mainly as a consequence of the missing climbing fibre input to the cerebellar flocculi.(ABSTRACT TRUNCATED AT 400 WORDS)
Animals↗
A precise and inexpensive magnetic field search coil system for measuring eye and head movements in small laboratory animals.
The design of a magnetic field search coil system based on the phase detection principle is described. The system was developed to record eye and head movements of small, unrestrained laboratory animals. It is compact, linear over 360 degrees, has a high resolution and allows the use of minute, commercially available search coils. Potential pitfalls and critical factors in the use of the system are discussed and original movement records are presented.
Animals↗
Optokinetic nystagmus in albino rats depends on stimulus pattern.
Ocular responses to optokinetic stimulation were reexamined in adult albino rats of two different strains. Eye movements were measured in head-restrained animals using the search coil method. In contrast to some previous results, the albino rats showed optokinetic nystagmus, and some of them made responses comparable to those previously recorded from pigmented rats. However, the type of stimulus pattern used to elicit optokinetic nystagmus proved to be crucial for albino rats. The deficit is attributed to abnormalities in the albino rat's visual sensory apparatus. Inverted optokinetic nystagmus was elicited in albino rats by restricting the optokinetic stimulation to the anterior visual field of both eyes. The same phenomenon has been observed previously in albino rabbits and mice, and has been suggested to be due to the abnormally small number of uncrossed optic nerve fibers in albinos.
Albinism↗