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77 records · Page 5

Horizontal vestibuloocular reflex evoked by high-acceleration rotations in the squirrel monkey. III. Responses after labyrinthectomy

The horizontal angular vestibuloocular reflex (VOR) evoked by high-frequency, high-acceleration rotations was studied in four squirrel monkeys after unilateral labyrinthectomy. Spontaneous nystagmus was measured at the beginning and end of each testing session. During the period that animals were kept in darkness (4 days), the nystagmus at each of these times measured approximately 20 degrees /s. Within 18-24 h after return to the light, the nystagmus (measured in darkness) decreased to 2.8 +/- 1.5 degrees /s (mean +/- SD) when recorded at the beginning but was 20.3 +/- 3.9 degrees /s at the end of the testing session. The latency of the VOR measured from responses to steps of acceleration (3,000 degrees /s(2) reaching a velocity of 150 degrees /s) was 8.4 +/- 0.3 ms for responses to ipsilesional rotations and 7.7 +/- 0.4 ms for contralesional rotations. During the period that animals were kept in darkness after the labyrinthectomy, the gain of the VOR measured during the steps of acceleration was 0.67 +/- 0.12 for contralesional rotations and 0.39 +/- 0.04 for ipsilesional rotations. Within 18-24 h after return to light, the VOR gain for contralesional rotations increased to 0.87 +/- 0.08, whereas there was only a slight increase for ipsilesional rotations to 0.41 +/- 0. 06. A symmetrical increase in the gain measured at the plateau of head velocity was noted after the animals were returned to light. The VOR evoked by sinusoidal rotations of 2-15 Hz, +/-20 degrees /s, showed a better recovery of gain at lower (2-4 Hz) than at higher (6-15 Hz) frequencies. At 0.5 Hz, gain decreased symmetrically when the peak amplitude was increased from 20 to 100 degrees /s. At 10 Hz, gain was decreased for ipsilesional half-cycles and increased for contralesional half-cycles when velocity was raised from 20 to 50 degrees /s. A model incorporating linear and nonlinear pathways was used to simulate the data. Selective increases in the gain for the linear pathway accounted for the recovery in VOR gain for responses at the velocity plateau of the steps of acceleration and for the sinusoidal rotations at lower peak velocities. The increase in gain for contralesional responses to steps of acceleration and sinusoidal rotations at higher frequencies and velocities was due to an increase in the contribution of the nonlinear pathway. This pathway was driven into cutoff and therefore did not affect responses for rotations toward the lesioned side.

NASA Discipline Neuroscience↗

Adaptation of primate vestibuloocular reflex to altered peripheral vestibular inputs. II Spatiotemporal properties of the adapted slow-phase eye velocity

1. The ability of the vestibuloocular reflex (VOR) to undergo adaptive modification after selective changes in the peripheral vestibular system was investigated in rhesus monkeys by recording three-dimensional eye movements before and after inactivation of selective semicircular canals. In the preceding paper we showed that the horizontal VOR gain evoked by passive yaw oscillations after lateral semicircular canal inactivation recovers gradually over time in a frequency-specific manner. Here we present the spatial tuning of the adapted slow-phase eye velocity and describe its spatiotemporal properties as a function of time after canal inactivation. 2. The spatial organization of the VOR was investigated during oscillations at different head positions in the pitch, roll, and yaw planes, as well as in the right anterior/left posterior and left anterior/right posterior canal planes. Acutely after bilateral inactivation of the lateral semicircular canals, a small horizontal response could still be elicited that peaked during rotations in pitched head positions that would maximally stimulate vertical semicircular canals. In addition, the phase of horizontal slow-phase velocity abruptly reversed through 180 degrees at positions close to upright, similarly to torsional slow-phase velocity. These spatial response properties suggest that the small, residual horizontal response components that are present acutely after plugging of both lateral canals originate from vertical semicircular canal signals. 3. As the horizontal response amplitude increased over time, consistent changes were also observed in the spatiotemporal tuning of horizontal slow-phase velocity. 1) The spatiotemporal response properties of horizontal slow-phase velocity acquired noncosine tuning characteristics, primarily in the pitch plane, in the right anterior/left posterior and left anterior/right posterior canal planes. Accordingly, horizontal response amplitude was nonzero during rotation in any head position in these planes and response phase varied significantly as a function of head orientation. 2) The peak horizontal response amplitude shifted spatially over time, such that 5-10 mo after plugging it was maximal during rotations at head positions close to upright. 4. In parallel to these unique spatiotemporal response properties characterizing the adapted horizontal VOR, torsional slow-phase velocity also exhibited small spatiotemporal changes after lateral canal inactivation that tended to precede in time the changes associated with the horizontal response components. In contrast, vertical slow-phase velocity in the plugged animals was unaltered and continued to be characterized by cosine-tuned spatial properties in three dimensions. 5. Recovery of the horizontal response gain during yaw oscillations in upright position, as well as the unique, noncosine spatiotemporal characteristics of the adapted horizontal VOR, were also observed in an animal with all but one vertical semicircular canals inactivated. There was, however, no sign of VOR gain recovery up to 2 mo after all semicircular canals were inactivated. These results suggest that the observed recovery of horizontal VOR is at least partly due to signals originating from the remaining intact vertical canal(s). Even in the presence of a single intact vertical canal, the improvement in horizontal gaze stability is at least partly restored through spatiotemporal changes in the processing of vestibuloocular signals that improve the gain and spatial tuning of horizontal VOR at the expense of temporal response properties.

NASA Discipline Number 16-10↗

Three-dimensional organization of otolith-ocular reflexes in rhesus monkeys. III. Responses To translation

The three-dimensional (3-D) properties of the translational vestibulo-ocular reflexes (translational VORs) during lateral and fore-aft oscillations in complete darkness were studied in rhesus monkeys at frequencies between 0.16 and 25 Hz. In addition, constant velocity off-vertical axis rotations extended the frequency range to 0.02 Hz. During lateral motion, horizontal responses were in phase with linear velocity in the frequency range of 2-10 Hz. At both lower and higher frequencies, phase lags were introduced. Torsional response phase changed more than 180 degrees in the tested frequency range such that torsional eye movements, which could be regarded as compensatory to "an apparent roll tilt" at the lowest frequencies, became anticompensatory at all frequencies above approximately 1 Hz. These results suggest two functionally different frequency bandwidths for the translational VORs. In the low-frequency spectrum (<<0.5 Hz), horizontal responses compensatory to translation are small and high-pass-filtered whereas torsional response sensitivity is relatively frequency independent. At higher frequencies however, both horizontal and torsional response sensitivity and phase exhibit a similar frequency dependence, suggesting a common role during head translation. During up-down motion, vertical responses were in phase with translational velocity at 3-5 Hz but phase leads progressively increased for lower frequencies (>90 degrees at frequencies <0.2 Hz). No consistent dependence on static head orientation was observed for the vertical response components during up-down motion and the horizontal and torsional response components during lateral translation. The frequency response characteristics of the translational VORs were fitted by "periphery/brain stem" functions that related the linear acceleration input, transduced by primary otolith afferents, to the velocity signals providing the input to the velocity-to-position neural integrator and the oculomotor plant. The lowest-order, best-fit periphery/brain stem model that approximated the frequency dependence of the data consisted of a second order transfer function with two alternating poles (at 0.4 and 7.2 Hz) and zeros (at 0.035 and 3.4 Hz). In addition to clearly differentiator dynamics at low frequencies (less than approximately 0.5 Hz), there was no frequency bandwidth where the periphery/brain stem function could be approximated by an integrator, as previously suggested. In this scheme, the oculomotor plant dynamics are assumed to perform the necessary high-frequency integration as required by the reflex. The detailed frequency dependence of the data could only be precisely described by higher order functions with nonminimum phase characteristics that preclude simple filtering of afferent inputs and might be suggestive of distributed spatiotemporal processing of otolith signals in the translational VORs.

Non-NASA Center↗

Role of the flocculus of the cerebellum in motor learning of the vestibulo-ocular reflex

Structure-function studies at the systems level are an effective method for understanding the relationship of the central nervous system to behavior. Motor learning or adaptation of the vestibulo-ocular reflex is a clear example wherein this approach has been productive. During a vestibulo-ocular reflex the brain converts a head velocity signal, transduced through the vestibular semicircular canals, into an eye movement command delivered to the extraocular muscles. If the viewed target remains on the fovea of the retina, the reflex is compensatory, and its gain, eye velocity/head velocity, is one. When the image of the viewed object slips across the retina, visual acuity decreases, and the gain of the reflex, which is no longer one, is plastically adapted or adjusted until retinal stability is restored. The anatomic substrate for this plasticity thus involves brain structures in which visual-vestibular interaction can potentially occur, as well as vestibular and visual sensory and oculomotor motor structures. Further, it has been known for many years that removal of the flocculus of the cerebellum permanently precludes further vestibulo-ocular reflex adaptation, demonstrating the involvement of the cerebellum in this behavior. Maekawa and Simpson (J Neurophysiol 1973;36: 649-66) discovered that one visual input to the flocculus involved the accessory optic system and the inferior olive. Ensuing work has demonstrated that the visual signals used to adapt the vestibulo-ocular reflex are transmitted by this accessory optic system to the flocculus and subsequently to brain stem structures involved in vestibulo-ocular reflex plasticity. Presently the inclusive list of anatomic sites involved in vestibulo-ocular reflex circuitry and its adaptive plasticity is small. Our laboratory continues to believe that this behavior should be caused by interactions within this small class of neurons. By studying each class of identified neuron and its interactions with others within the list, we hope to ultimately understand the mechanisms used by the brain in the expression of this behavior.

Non-NASA Center↗

Three-dimensional ocular kinematics during eccentric rotations: evidence for functional rather than mechanical constraints

Previous studies have reported that the translational vestibuloocular reflex (TVOR) follows a three-dimensional (3D) kinematic behavior that is more similar to visually guided eye movements, like pursuit, rather than the rotational VOR (RVOR). Accordingly, TVOR rotation axes tilted with eye position toward an eye-fixed reference frame rather than staying relatively fixed in the head like in the RVOR. This difference arises because, contrary to the RVOR where peripheral image stability is functionally important, the TVOR like pursuit and saccades cares to stabilize images on the fovea. During most natural head and body movements, both VORs are simultaneously activated. In the present study, we have investigated in rhesus monkeys the 3D kinematics of the combined VOR during yaw rotation about eccentric axes. The experiments were motivated by and quantitatively compared with the predictions of two distinct hypotheses. According to the first (fixed-rule) hypothesis, an eye-position-dependent torsion is computed downstream of a site for RVOR/TVOR convergence, and the combined VOR axis would tilt through an angle that is proportional to gaze angle and independent of the relative RVOR/TVOR contributions to the total eye movement. This hypothesis would be consistent with the recently postulated mechanical constraints imposed by extraocular muscle pulleys. According to the second (image-stabilization) hypothesis, an eye-position-dependent torsion is computed separately for the RVOR and the TVOR components, implying a processing that takes place upstream of a site for RVOR/TVOR convergence. The latter hypothesis is based on the functional requirement that the 3D kinematics of the combined VOR should be governed by the need to keep images stable on the fovea with slip on the peripheral retina being dependent on the different functional goals of the two VORs. In contrast to the fixed-rule hypothesis, the data demonstrated a variable eye-position-dependent torsion for the combined VOR that was different for synergistic versus antagonistic RVOR/TVOR interactions. Furthermore, not only were the eye-velocity tilt slopes of the combined VOR as much as 10 times larger than what would be expected based on extraocular muscle pulley location, but also eye velocity during antagonistic RVOR/TVOR combinations often tilted opposite to gaze. These results are qualitatively and quantitatively consistent with the image-stabilization hypothesis, suggesting that the eye-position-dependent torsion is computed separately for the RVOR and the TVOR and that the 3D kinematics of the combined VOR are dependent on functional rather than mechanical constraints.

Non-NASA Center↗