Laurent Goffart

A Neural Mechanism for Microsaccade Generation in the Primate Superior Colliculus

During fixation, the eyes are not still but often exhibit microsaccadic movements. The function of microsaccades is controversial, largely because the neural mechanisms responsible for their generation are unknown. Here, we show that the superior colliculus (SC), a retinotopically organized structure involved in voluntary-saccade target selection, plays a causal role in microsaccade generation. Neurons in the foveal portion of the SC increase their activity before and during microsaccades with sizes of only a few minutes of arc and exhibit selectivity for the direction and amplitude of these movements. Reversible inactivation of these neurons significantly reduces microsaccade rate without otherwise compromising fixation. These results, coupled with computational modeling of SC activity, demonstrate that microsaccades are controlled by the SC and explain the link between microsaccades and visual attention.

Modifications in end positions of arm movements following short-term saccadic adaptation.

We investigated whether short-term saccadic adaptation modifies hand pointing. Subjects were presented with double-step targets, the second target jump occurring during the saccade to the first one and bringing the target back to 66% of the first target eccentricity, in order to reduce the gain of their gaze saccades. Before and after this adaptation phase, they pointed with their hand to single step targets while keeping their gaze straight ahead. The results show that the hand movements terminated at positions that were significantly less eccentric following the adaptation phase, resembling the adaptive modification seen in the gaze movements. These results suggest that the motor systems controlling gaze and hand use common information about target position.

Superior Colliculus Inactivation Causes Stable Offsets in Eye Position during Tracking

The primate superior colliculus (SC) is often viewed as composed of two distinct motor zones with complementary functions: a peripheral region that helps generate saccades to eccentric targets and a central one that maintains fixation by suppressing saccades. Here, we directly tested the alternative interpretation that topography in the SC is not strictly motor, nor does it form two distinct zones, but instead forms a single map of behaviorally relevant goal locations. Primates tracked the invisible midpoint between two moving stimuli, such that the stimuli guiding tracking were peripheral whereas the inferred movement goal was foveal and parafoveal. Temporary inactivation of neurons in the central portion of the topographic map of the SC, representing the invisible goal, caused stable offsets in eye position during tracking that were directed away from the retinotopic position encoded by the inactivated SC site. Critically, these offsets were not accompanied by a systematic inability to generate or suppress saccades, and they were not fully explained by motor deficits in saccades, smooth pursuit, or fixation. In addition, the magnitude of the offset depended on the eccentricity of the inactivated site as well as the degree of spatial uncertainty associated with the behavioral goal. These results indicate that gaze control depends on the balance of activity across a map of goal locations in the SC, and that by silencing some of the neurons in the normally active population representing the behavioral goal, focal inactivation causes a biased estimate of where to look.

Visual fixation as equilibrium: Evidence from superior colliculus inactivation

During visual fixation, the image of an object is maintained within the fovea. Previous studies have shown that such maintenance involves the deep superior colliculus (dSC). However, the mechanisms by which the dSC supports visual fixation remain controversial. According to one view, activity in the rostral dSC maintains gaze direction by preventing neurons in the caudal dSC from issuing saccade commands. An alternative hypothesis proposes that gaze direction is achieved through equilibrium of target position signals originating from the two dSCs. Here, we show in monkeys that artificially reducing activity in the rostral half of one dSC results in a biased estimate of target position during fixation, consistent with the second hypothesis, rather than an inability to maintain gaze fixation as predicted by the first hypothesis. After injection of muscimol at rostral sites in the dSC, fixation became more stable since microsaccade rate was reduced rather than increased. Moreover, the scatter of eye positions was offset relative to preinactivation baselines. The magnitude and the direction of the offsets depended on both the target size and the injected site in the collicular map. Other oculomotor parameters, such as the accuracy of saccades to peripheral targets and the amplitude and velocity of fixational saccades, were largely unaffected. These results suggest that the rostral half of the dSC supports visual fixation through a distributed representation of behaviorally relevant target position signals. The inactivation-induced fixation offset establishes the foveal visual stimulation that is required to restore the balance of activity between the two dSCs.

Fastigial oculomotor region and the control of foveation during fixation.

When primates maintain their gaze directed toward a visual target (visual fixation), their eyes display a combination of miniature fast and slow movements. An involvement of the cerebellum in visual fixation is indicated by the severe gaze instabilities observed in patients suffering from cerebellar lesions. Recent studies in non-human primates have identified a cerebellar structure, the fastigial oculomotor region (FOR), as a major cerebellar output nucleus with projections toward oculomotor regions in the brain stem. Unilateral inactivation of the FOR leads to dysmetric visually guided saccades and to an offset in gaze direction when the animal fixates a visual target. However, the nature of this fixation offset is not fully understood. In the present work, we analyze the inactivation-induced effects on fixation. A novel technique is adopted to describe the generation of saccades when a target is being fixated (fixational saccades). We show that the offset is the result of a combination of impaired saccade accuracy and an altered encoding of the foveal target position. Because they are independent, we propose that these two impairments are mediated by the different projections of the FOR to the brain stem, in particular to the deep superior colliculus and the pontomedullary reticular formation. Our study demonstrates that the oculomotor cerebellum, through the activity in the FOR, regulates both the amplitude of fixational saccades and the position toward which the eyes must be directed, suggesting an involvement in the acquisition of visual information from the fovea.

Saccadic Eye Movements

The sudden appearance of an object in the visual field triggers an orienting shift of the line of sight toward its location. This movement consists of an extremely rapid rotation of the two eyes, the saccade. In this article, instead of describing the path leading from the target-evoked retinal activity to the changes in muscle tension that rotate the eyes, we take the reverse path. Starting from the muscle contractions, we proceed upstream and describe the neural and functional mechanisms involved in generating commands that permit the eyes and, therefore, the fovea to orient toward a sensory event.

Early head movements elicited by visual stimuli or collicular electrical stimulation in the cat

During the course of previous recordings of visually-triggered gaze shifts in the head-unrestrained cat, we occasionally observed small head movements which preceded the initiation of the saccadic eye/head gaze shift toward a visual target. These early head movements (EHMs) were directed toward the target and occurred with a probability varying between animals from 0.4% to 16.4% (mean=5.2%, n=11 animals). The amplitude of EHM ranged from 0.4 degrees to 8.3 degrees (mean=1.9 degrees ), their latency from 66 to 270 ms (median=133 ms) and the delay from EHM onset to gaze shift onset averaged 183+/-108 ms (n=240). Their occurrence did not depend on visual target eccentricity in the studied range (7-35 degrees ), but influenced the metrics and dynamics of the ensuing gaze shifts (gain and velocity reduced). We also found in the two tested cats that low intensity microstimulation of the superior colliculus deeper layers elicited a head movement preceding the gaze shift. Altogether, these results suggest that the presentation of a visual target can elicit a head movement without triggering a saccadic eye/head gaze shift. The visuomotor pathways triggering these early head movements can involve the deep superior colliculus.

Control of saccadic eye movements and combined eye/head gaze shifts by the medio-posterior cerebellum.

The cerebellar areas involved in the control of saccades have recently been identified in the medio-posterior cerebellum (MPC). Unit activity recordings, experimental lesions and electrical microstimulation of this region in cats and monkeys have provided a considerable amount of data and allowed the development of new computational models. In this paper, we review these data and concepts about cerebellar function, discuss their importance and limitations and suggest future directions for research. The anatomical data indicate that the MPC has more than one site of action in the visuo-oculomotor system. In contrast, most models emphasize the role of cerebellar connections with immediate pre-oculomotor circuits in the reticular formation, and only one recent model also incorporates the ascending projections of the MPC to the superior colliculus. A major challenge for future studies, in continuation with this initial attempt, is to determine whether the various cerebellar output pathways correspond to distinct contributions to the control of saccadic eye movements. Also, a series of recent studies in the cat have indicated a more general role of the MPC in the control of orienting movements in space, calling for an increasing effort to the study of the MPC in the production of head-unrestrained saccadic gaze shifts.

On-line compensation of gaze shifts perturbed by micro-stimulation of the superior colliculus in the cat with unrestrained head

Prior studies have led to the gaze feedback hypothesis, which states that quick orienting movements of the visual axis (gaze shifts) are controlled by a feedback system. We have previously provided evidence for this hypothesis by extending the original study of Mays and Sparks (1980) to the cat with unrestrained head (Pélisson et al. 1989). We showed that cats compensated for a stimulation-induced perturbation of initial gaze position by generating, in the dark, an accurate gaze shift towards the remembered location of a flashed target. In the present study, we investigate goal-directed gaze shifts perturbed “in flight” by a brief stimulation of the superior colliculus. The microstimulation parameters were tuned such that significant perturbations were induced without halting the movement. The ambient light was turned off at the onset of the gaze shift, suppressing any visual feedback. We observed that, following stimulation offset, the gaze shift showed temporal and spatial changes in its trajectory to compensate for the transient perturbation. Such compensations, which occurred “on-line” before gaze shift termination, involved both eye and head movements and had dynamic characteristics resembling those of unperturbed saccadic gaze shifts. These on-line compensations maintained gaze accuracy when the stimulation was applied during the early phase of large and medium (about 60 and 40°) movements. These results are compatible with the notion of a gaze feedback loop providing a dynamic gaze error signal.

Saccade Dysmetria during Functional Perturbation of the Caudal Fastigial Nucleus in the Monkey

The caudal fastigial nucleus (cFN) is the output nucleus by which the medioposterior cerebellum influences the brainstem saccade generator. In the monkey, inactivation of one cFN by local injection of muscimol impairs all saccades: ipsiversive saccades become hypermetric, contraversive saccades become hypometric, and saccades aimed at a target located in the upper or lower visual fields are biased horizontally toward the injected side. The pharmacological action of muscimol does not allow deficits that are presaccadic to be distinguished from those occurring during saccade execution. To determine the interval during which altered cFN activity affects saccade accuracy, we applied low‐frequency electrical microstimulation (100 Hz for 100‐300 ms) to the cFN of three monkeys while they were making saccades toward a flashed target. Similar to the effect of muscimol injection in cFN, low‐frequency microstimulation biased all saccades toward the ipsilateral side. When the microstimulation was applied after target flash and before saccade onset, the ipsilateral bias was absent. However, when the stimulation was applied during the ongoing movement, the saccade trajectory was biased toward the stimulated side. The muscimol‐like effect of the microstimulation suggests that the stimulation inhibits cFN activity, possibly by recruiting the inhibitory afferents from the cerebellar vermis (axons of Purkinje cells). Low‐frequency microstimulation had to be applied during the saccade to bias its trajectory. These data suggest that the ipsilateral horizontal bias observed during muscimol inactivation results from an imbalance in the intrasaccadic activity between the two caudal fastigial nuclei.