Electrical stimulation of the superior colliculus induces non-topographically organized perturbation of reaching movements in cats.

Besides its well-known contribution to orienting behaviors, the superior colliculus (SC) might also play a role in controlling visually guided reaching movements. This view has been inferred from studies in monkeys showing that some tectal cells located in the deep layers are active prior to reaching movements; it was corroborated by functional imaging studies performed in humans. Likewise, our group has already demonstrated that, in cats, SC electrical stimulation can modify the trajectory of goal-directed forelimb movements without necessarily affecting the gaze position. However, as in monkeys, we could not establish any congruence between the usual retinotopic SC map and direction of evoked forelimb movements, albeit only a small portion of the collicular map was investigated. Therefore, the aim of the current study was to further ascertain the causal contribution of SC to reaching movement by exploring the whole collicular map. Our results confirmed that SC electrical stimulation deflected the trajectory of reaching movements, but this deviation was always directed downward and backward, irrespective of the location of the stimulation site. The lack of a complete map of reach directions in the SC and the absence of congruence between the direction of evoked forelimb movements and the collicular oculomotor map challenge the view that, in the cat, the SC causally contributes to coding forelimb movements. Interestingly, the very short latencies of the effect argue also against the interruption of reaching movements being driven by a disruption of the early visual processing. Our results rather suggest that the SC might contribute to the reach target selection process. Alternatively, SC stimulation might have triggered a postural adjustment anticipating an upcoming orienting reaction, leading to an interruption of the on-going reaching movement.

Influence of stimulus interval on the habituation of vestibulo-ocular reflex and sensation of rotation in humans.

Previous studies in cats revealed that vestibular habituation of the vestibulo-ocular reflex (VOR) only occurs when velocity steps are delivered during the secondary phase nystagmus, suggesting that the presence of anti-compensatory slow phases may trigger the habituation process. We verified this property in humans by comparing vestibular habituation of VOR and sensation of rotation when steps were delivered either immediately after the perception of self-rotation had stopped, which is shortly before the nystagmus reverses direction; or when steps were delivered 60s later, i.e. during the secondary phase. Vestibular habituation of the VOR occurred in both instances. However, the decrease in VOR peak slow phase velocity and time constant was larger when steps were delivered after nystagmus reversal compared to before nystagmus reversal. The duration of the perception of self-rotation habituated equally for both conditions. These results confirm that VOR habituation fully develops only when velocity steps are delivered after the primary phase nystagmus. This finding may be helpful for minimizing the impact of repetitive vestibular stimuli in protocols using crossover design for drug studies, testing recovery in vestibular patients, or training people for different gravitoinertial environments.

Retention of habituation of vestibulo-ocular reflex and sensation of rotation in humans.

In humans, habituation of vestibulo-ocular reflex (VOR) by repeated caloric or rotational stimulation has been well documented. However, less attention has been directed to the effect of habituation on the sensation of self-rotation and little is known about the retention duration of vestibular habituation. To investigate these characteristics, subjects were exposed to ten sessions of angular velocity steps in yaw, with a chair rotating either alternatively in both CW and CCW directions (bidirectional protocol) or always in the same direction (unidirectional protocol), i.e., CW or CCW. The retention of habituation of VOR and sensation of rotation induced by both protocols was studied for a period up to 8 months following the end of the habituation protocols. There was a progressive decline in the VOR peak slow phase velocity and time constant throughout the sessions during both protocols. These parameters then followed an exponential recovery with a time constant of about 1 month. The duration of the sensation of rotation also habituated during repeated angular velocity steps, but it was shorter for both directions of stimulation, including after the unidirectional protocol. Sinusoidal VOR gain was not affected by vestibular habituation to velocity steps, but sinusoidal VOR phase showed an increase in phase lead at 0.02 and 0.04 Hz, which also returned to baseline values within about 1 month. We conclude that vestibular habituation is a long-lasting phenomenon. These results may be helpful for designing and scheduling the protocols for drug studies using crossover design, rehabilitation of balance disorder patients, and for the application of intermittent artificial gravity during space missions.

Subthalamic stimulation improves orienting gaze movements in Parkinson's disease.

OBJECTIVE: To determine the effect of subthalamic stimulation on visually triggered eye and head movements in patients with Parkinson's disease (PD). METHODS: We compared the gain and latency of visually triggered eye and head movements in 12 patients bilaterally implanted into the subthalamic nucleus (STN) for severe PD and six age-matched control subjects. Visually triggered movements of eye (head restrained), and of eye and head (head unrestrained) were recorded in the absence of dopaminergic medication. Bilateral stimulation was turned OFF and then turned ON with voltage and contact used in chronic setting. The latency was determined from the beginning of initial horizontal eye movements relative to the target onset, and the gain was defined as the ratio of the amplitude of the initial movement to the amplitude of the target movement. RESULTS: Without stimulation, the initiation of the head movement was significantly delayed in patients and the gain of head movement was reduced. Our patients also presented significantly prolonged latencies and hypometry of visually triggered saccades in the head-fixed condition and of gaze in head-free condition. Bilateral STN stimulation with therapeutic parameters improved performance of orienting gaze, eye and head movements towards the controls' level CONCLUSIONS: These results demonstrate that visually triggered saccades and orienting eye-head movements are impaired in the advanced stage of PD. In addition, subthalamic stimulation enhances amplitude and shortens latency of these movements. SIGNIFICANCE: These results are likely explained by alteration of the information processed by the superior colliculus (SC), a pivotal visuomotor structure involved in both voluntary and reflexive saccades. Improvement of movements with stimulation of the STN may be related to its positive input either on the STN-Substantia Nigra-SC pathway or on the parietal cortex-SC pathway.

Direct evidence for the contribution of the superior colliculus in the control of visually guided reaching movements in the cat.

The production of visually guided reaching movements relies on a large neural network. Based on indirect experimental evidence, it has been suggested that the superior colliculus, a subcortical centre known for its key role in controlling rapid orienting gaze shifts, also belongs to this network. The aim of the present study was to investigate the role of the cat superior colliculus (SC) in the control of visually guided reaching movements. To address this issue, we studied the effect of SC electrical stimulation on forelimb reaching movements in two cats trained to catch a piece of food. Electrical stimulation delivered just after the movement onset yielded a consistent perturbation of the movement trajectory of the forelimb extremity. This perturbation followed stimulation onset by 56 +/- 11 ms on average, and consisted of a deviation of the spatial path and a deceleration of the movement. The forelimb perturbation was elicited in the absence of concomitant gaze or head displacement in 52% of the stimulation trials. Forelimb perturbations were followed by in-flight adjustments so that reaching movements reliably ended on the target. The present results constitute the first behavioural evidence for a contribution of the cat SC to the control of visually guided forelimb movements.

Vestibular decompensation in labyrinthectomized rats placed in weightlessness during parabolic flight.

The purpose of this study was to determine whether the absence of gravitational cues during weightlessness could alter the posture and static eye deviation of Earth compensated rats with peripheral vestibular lesions. The responses of bilaterally (BL) and unilaterally (UL) labyrinthectomized rats at a compensated stage (40-43 days after lesion) during parabolic flight were compared with those at an acute stage (2-7 h after lesion) on Earth. When free-floating in 0 g, UL animals showed the same postural pattern as during water immersion just after surgery. The most striking observation was a continuous roll body motion at about 4 Hz, and a skewed asymmetric posture. When restrained in 0 g, static eye deviation was also comparable to that observed at an acute stage. A return to a compensated posture and gaze was observed within a few seconds following the end of the weightlessness conditions. BL animals were less affected. These results suggest that vestibular compensation after unilateral lesion can be disrupted momentarily and is a fragile state during which the otolith system in the remaining vestibular apparatus presumably plays a continuous role.

Comparison between habituation of the cat vestibulo-ocular reflex by velocity steps and sinusoidal vestibular stimulation in the dark.

Changes in the horizontal vestibulo-ocular reflex (VOR) in darkness were investigated in naive cats during: (1) repeated sessions of angular velocity steps, (2) one continuous 1-h session of sinusoidal oscillations at 0.01, 0.02, 0.04, or 0.12 Hz, and (3) repeated sessions of 1-h sinusoidal oscillations at 0.02 and 0.04 Hz. Before and after each vestibular training, the VOR response parameters elicited by both velocity steps and sinusoidal oscillations were measured in order to evaluate the transfer of habituation from one stimulus to the other. After training with velocity steps, the amplitude and duration of the VOR to velocity steps decreased by about 67% and 52%, respectively. This vestibular habituation transferred to the VOR response generated by sinusoidal oscillations, since a decrease in VOR gain was observed at 0.02 and 0.04 Hz, and an increase in phase lead was observed at 0.02, 0.04, and 0.08 Hz. After 1 h exposure to sinusoidal oscillations, the VOR gain was only reduced by 21-28%, whereas VOR phase lead decreased. The same changes were observed during subsequent sessions, with no retention of the response decrements from one session to the next. At the end of sinusoidal training, the amplitude of the VOR generated by velocity steps was slightly altered. After sinusoidal training, the weak changes in the VOR gain accompanied by a decrease in the VOR phase lead, and the absence of retention of these effects from one session to the next, suggest these changes are not characteristics of a vestibular habituation. Previous reports of vestibular habituation induced by repeated sinusoidal oscillations may be confounded by the fact that the angular velocity steps used for quantifying the effects may have been responsible for this habituation.