Role of the otolith organs in generation of horizontal nystagmus: effects of selective labyrinthine lesions

Gaze stabilization in the primate

Extracellular activity from vestibular nuclei neurons and vertical eye movements were recorded in the alert cat during sinusoidal optokinetic stimulation in the vertical plane at frequencies varying from 0.0125 Hz to 0.75 Hz. Among a population of 96 vestibular units located in and around Deiters' nucleus, 73 neurons (76%) displayed a firing rate modulation which followed the input at the standard parameters of visual stimulation (0.05 Hz; 10.1 deg/s or 9.1 cm/s peak to peak velocity). Two different patterns of modulation were found. In 42 cells (57%) an increase in the firing rate was observed during motion of the visual scene in the downward direction, while 31 neurons (43%) showed the opposite behavior, with an enhanced firing rate during upward movement. The phase of the neuronal responses was close (± 45°) to the velocity peaks (+90°: downward and -90°: upward) of visual scene motion for 65 among the 73 neurons. Mean values of phase was-6.1 ± 19.5° (SD) and -3.2 ± 15.5° (SD) with respect to the +90° and -90° velocity peaks, respectively. In the frequency range 0.0125–0.75 Hz, the phase of the neuronal responses remained almost stable, with only a slight lag which reaches -22° at the 0.25 Hz visual stimulation. The firing rate modulation was found to be predominant at low frequencies (0.0125 Hz–0.25 Hz), with three distinct peaks of modulation occurring either at 0.025 Hz, 0.10 Hz or 0.25 Hz, depending on the recorded cells. Above 0.5 Hz, the cell modulation was very poorly developed or even absent. A gain attenuation was observed in all units, which was more important in cells showing a peak of modulation at 0.025 Hz as compared with the others (-20.7 dB vs -9.6 dB, respectively, in the 0.025 Hz–0.25 Hz decade). The gain of the optokinetic reflex (OKR) progressively decreased from mean values of 0.78 ± 0.15 to 0.05 ± 0.06 in the 0.025 Hz–0.5 Hz frequency range. A close correlation was observed between the OKR slow phase velocity and the modulation of the neuronal responses in the two cell populations with maximal modulations at 0.10 Hz or 0.25 Hz. No correlations were noticed in the third population characterized by a peak of modulation at 0.025 Hz. In all units, the phase of eye movement velocity and of neuronal responses were both related to the velocity of the visual surround motion. These correlations were also found when varying the amplitude of the visual stimulation at a fixed frequency. Saturation was observed in the unit responses at velocities above 68.5°/s. When considering both the gain attenuation in the frequency range and the correlation between firing rate modulation and OKR slow phase velocity, two rather different cell populations can be distinguished: one with neurons peaking at 0.025 Hz (strong gain attenuation; no correlation with OKR velocity) and one with neurons peaking at 0.10 Hz or 0.25 Hz (slight gain attenuation; correlation with OKR velocity). This study points to the influence of visual motion cues on vestibular nuclei unit activity in the low-frequency range. A velocity coding of visual — surround motion in the vertical plane is performed by vestibular neurons. Our results in the alert cat suggest that both retinal (retinal slip) and extraretinal (proprioceptive afferences from eye muscles, efference copy) inputs can be involved in this visually induced modulation of vestibular nuclei neurons.

Neuronal coding of linear motion in the vestibular nuclei of the alert cat

In the present study we have investigated in the awake cat the response dynamics of vestibular nuclei neurons to visual or/and otolith stimulation elicited by vertical linear motion. Of the 53 units tested during sinusoidal motion at 0.05 Hz (9.1 cm/s), 1 (1.9%) was responsive to the otolith input only, 13 (24.5%) were influenced by the visual input only and 23 (43.4%) responded to both modalities. Neurons were excited either during upward or downward animal or visual surround movement. Most units displayed a firing rate modulation very close to motion velocity. All the neurons receiving convergent visual and otolith inputs (0.05 Hz, 9.1 cm/s) exhibited synergistic patterns of response. Motion velocity coding was improved in terms of input-output phase relationship and response sensitivity when visual and otolith signals were combined. Depending on the units, visual-otolith interactions in single neurons could follow a linear or a nonlinear mode of summation. The dynamic characteristics of visual-otolith interactions were examined in the 0.05 Hz-0.50 Hz frequency bandwidth. Visual signals seemed to predominate over otolith signals at low stimulus frequencies (up to 0.25 Hz), while the contrary was found in the higher frequency range of movement (above 0.25 Hz). The effects of visual stabilization (VS: suppression of visual motion cues) was observed in a small sample of units. As a rule, VS induced a reduction in the amplitude of unit response as compared to visual + otolith stimulation, the lower the motion frequency, the more pronounced the attenuation. VS also decreased the amplitude of the otolith-dependent component of response. The possible modes of visual-vestibular interactions in single cells are discussed. The present study supports the hypothesis that visual and vestibular motion cues are weighted according to their internal relevance.

Neuronal coding of linear motion in the vestibular nuclei of the alert cat. III. Dynamic characteristics of visual-otolith interactions.

The effect of Coriolis, cross-coupled stimulation on the vestibuloocular reflex and the elicitation of motion sickness depends on background gravitoinertial force level (DiZio et al. 1986, 1987; Graybiel et al. 1977; Lackner and Graybiel 1984, 1986). We have explored whether this response dependency is related to the unusual patterns of sensorimotor activity present during exposure to non-terrestrial gravitoinertial force levels, to alterations in the encoding of head movements in different gravitoinertial force environments, or to some combination thereof. Blindfolded subjects were exposed to sudden stops after constant velocity, vertical z-axis rotation, sometimes with and sometimes without post-rotational head movements, in the 0 G, 1 G, and 1.8 G force phases of parabolic flight. After sudden stops without head movements, the time constant of decay of post-rotational nystagmus was significantly lower in 0 G than in 1 G and lower to a smaller extent in 1.8 G. Post-rotational head movements decreased the decay time constants in 1 G and in 1.8 G, but not in free fall. The same pattern emerged for the duration of illusory after-rotation. Systematic changes were not found in the peak slow phase velocity of nystagmus. These results suggest that tonic levels of otolithic and somatosensory activity in combination with canalicular, cervical, and motor activity regulate the velocity storage mechanism of the horizontal vestibuloocular reflex (Cohen et al. 1977; Raphan et al. 1979) and sensations of after-rotation. These same factors are likely to be important etiological elements in space motion sickness.

The effects of gravitoinertial force level and head movements on post-rotational nystagmus and illusory after-rotation.

The slow phase eye velocity (SPEV) and duration of post-rotatory nystagmus (PRN) were studied in squirrel monkeys (Saimiri sciureus) after a ramp speed rotation (0–200°/sec, with 1°/sec2 angular acceleration). When the results were compared between straight upright vertical rotation, 9° tilt rotation, and 18° tilt rotation, faster decay both in SPEV and in duration was found in the tilt rotation situations. Difference in nystagmic decay curves by tilting rotation axis could be from the convergence of macula-semicircular canal inputs. Subsequently bilateral macular ablation (two-stage) was performed. The difference in nystagmus decay curves between three different rotations was reduced; therefore, the change of gravity direction perceived through gravity receptors other than macular end organs was minimal and did not produce a difference in three different rotations.

Effect of off-vertical tilt and macular ablation on postrotatory nystagmus in the squirrel monkey

Vestibular nucleus (VN) neurons, identified by sinusoidal rotation about the vertical axis, were tested for their response to moving visual field, and to electric stimulation on the optic chiasm (OX) and super colliculus (SC). Incremental responses during the rotation were inhibited by visual stimulus in cerebellectomized animals. Single-pulse stimulation applied to the OX was ineffective in producing a positive response in these neurons as well or in any other unit. Thus, such a visual pathway to VN must be located inside the brainstem and contains multi-synapses. Effects of repetitive stimulations (60 Hz) to OX and SC were more predominant in the cerebellectomized animal than in the intact animal. Cerebellar inhibitory control on visual-vestibular linkage was suggested.

T. Kubo

Papers

Effect of off-vertical tilt and macular ablation on postrotatory nystagmus in the squirrel monkey

Vestibular unitary responses to visual stimulation in the rabbit.