Single cell signals: an oculomotor perspective

Abstract: We examine the activity of individual neurons in three different brain areas where firing rate, number of spikes (the integral of discharge rate), and the location of the active cell within a motor map are used as coding schemes. The correlations between single cell activity and the parameters of a movement range from extremely tight (motoneurons) to non-existent (superior colliculus). We argue that the relationship between the activity of single cell activity and global aspects of behavior are best described as coarse coding for all three types of neuron. We also present evidence, in some cases in a preliminary and suggestive form, that the distribution of spikes in time, rather than average firing rate, may be important for all three neuron types, including those using a place code. Finally, we describe difficulties encountered in obtaining an estimate of the motor command when more than one oculomotor system is active

Disruption of Saccadic Adaptation with Repetitive Transcranial Magnetic Stimulation of the Posterior Cerebellum in Humans

Saccadic eye movements are driven by motor commands that are continuously modified so that errors created by eye muscle fatigue, injury, or—in humans—wearing spectacles can be corrected. It is possible to rapidly adapt saccades in the laboratory by introducing a discrepancy between the intended and actual saccadic target. Neurophysiological and lesion studies in the non-human primate as well as neuroimaging and patient studies in humans have demonstrated that the oculomotor vermis (lobules VI and VII of the posterior cerebellum) is critical for saccadic adaptation. We studied the effect of transiently disrupting the function of posterior cerebellum with repetitive transcranial magnetic stimulation (rTMS) on the ability of healthy human subjects to adapt saccadic eye movements. rTMS significantly impaired the adaptation of the amplitude of saccades, without modulating saccadic amplitude or variability in baseline conditions. Moreover, increasing the intensity of rTMS produced a larger impairment in the ability to adapt saccadic size. These results provide direct evidence for the role of the posterior cerebellum in man and further evidence that TMS can modulate cerebellar function

Motor expertise modulates the unconscious processing of human body postures

Little is known about the cognitive background of unconscious visuomotor control of complex sports movements. Therefore, we investigated the extent to which novices and skilled high-jump athletes are able to identify visually presented body postures of the high jump unconsciously. We also asked whether or not the manner of processing differs (qualitatively or quantitatively) between these groups as a function of their motor expertise. A priming experiment with not consciously perceivable stimuli was designed to determine whether subliminal priming of movement phases (same vs. different movement phases) or temporal order (i.e. natural vs. reversed movement order) affects target processing. Participants had to decide which phase of the high jump (approach vs. flight phase) a target photograph was taken from. We found a main effect of temporal order for skilled athletes, that is, faster reaction times for prime-target pairs that reflected the natural movement order as opposed to the reversed movement order. This result indicates that temporal-order information pertaining to the domain of expertise plays a critical role in athletes’ perceptual capacities. For novices, data analyses revealed an interaction between temporal order and movement phases. That is, only the reversed movement order of flight-approach pictures increased processing time. Taken together, the results suggest that the structure of cognitive movement representation modulates unconscious processing of movement pictures and points to a functional role of motor representations in visual perception

Sensory Processing of Motor Inaccuracy Depends on Previously Performed Movement and on Subsequent Motor Corrections: A Study of the Saccadic System

When goal-directed movements are inaccurate, two responses are generated by the brain: a fast motor correction toward the target and an adaptive motor recalibration developing progressively across subsequent trials. For the saccadic system, there is a clear dissociation between the fast motor correction (corrective saccade production) and the adaptive motor recalibration (primary saccade modification). Error signals used to trigger corrective saccades and to induce adaptation are based on post-saccadic visual feedback. The goal of this study was to determine if similar or different error signals are involved in saccadic adaptation and in corrective saccade generation. Saccadic accuracy was experimentally altered by systematically displacing the visual target during motor execution. Post-saccadic error signals were studied by manipulating visual information in two ways. First, the duration of the displaced target after primary saccade termination was set at 15, 50, 100 or 800 ms in different adaptation sessions. Second, in some sessions, the displaced target was followed by a visual mask that interfered with visual processing. Because they rely on different mechanisms, the adaptation of reactive saccades and the adaptation of voluntary saccades were both evaluated. We found that saccadic adaptation and corrective saccade production were both affected by the manipulations of post-saccadic visual information, but in different ways. This first finding suggests that different types of error signal processing are involved in the induction of these two motor corrections. Interestingly, voluntary saccades required a longer duration of post-saccadic target presentation to reach the same amount of adaptation as reactive saccades. Finally, the visual mask interfered with the production of corrective saccades only during the voluntary saccades adaptation task. These last observations suggest that post-saccadic perception depends on the previously performed action and that the differences between saccade categories of motor correction and adaptation occur at an early level of visual processing

Fix Your Eyes in the Space You Could Reach: Neurons in the Macaque Medial Parietal Cortex Prefer Gaze Positions in Peripersonal Space

Interacting in the peripersonal space requires coordinated arm and eye movements to visual targets in depth. In primates, the medial posterior parietal cortex (PPC) represents a crucial node in the process of visual-to-motor signal transformations. The medial PPC area V6A is a key region engaged in the control of these processes because it jointly processes visual information, eye position and arm movement related signals. However, to date, there is no evidence in the medial PPC of spatial encoding in three dimensions. Here, using single neuron recordings in behaving macaques, we studied the neural signals related to binocular eye position in a task that required the monkeys to perform saccades and fixate targets at different locations in peripersonal and extrapersonal space. A significant proportion of neurons were modulated by both gaze direction and depth, i.e., by the location of the foveated target in 3D space. The population activity of these neurons displayed a strong preference for peripersonal space in a time interval around the saccade that preceded fixation and during fixation as well. This preference for targets within reaching distance during both target capturing and fixation suggests that binocular eye position signals are implemented functionally in V6A to support its role in reaching and grasping

Impaired peripheral reaching and on-line corrections in patient DF: optic ataxia with visual form agnosia

An influential model of vision suggests the presence of two visual streams within the brain: a dorsal occipito-parietal stream which mediates action and a ventral occipito-temporal stream which mediates perception. One of the cornerstones of this model is DF, a patient with visual form agnosia following bilateral ventral stream lesions. Despite her inability to identify and distinguish visual stimuli, DF can still use visual information to control her hand actions towards these stimuli. These observations have been widely interpreted as demonstrating a double dissociation from optic ataxia, a condition observed after bilateral dorsal stream damage in which patients are unable to act towards objects that they can recognize. In Experiment 1, we investigated how patient DF performed on the classical diagnostic task for optic ataxia, reaching in central and peripheral vision. We replicated recent findings that DF is remarkably inaccurate when reaching to peripheral targets, but not when reaching in free vision. In addition we present new evidence that her peripheral reaching errors follow the optic ataxia pattern increasing with target eccentricity and being biased towards fixation. In Experiments 2 and 3, for the first time we examined DF’s on-line control of reaching using a double-step paradigm in fixation-controlled and free-vision versions of the task. DF was impaired when performing fast on-line corrections on all conditions tested, similarly to optic ataxia patients. Our findings question the long-standing assumption that DF’s dorsal visual stream is functionally intact and that her on-line visuomotor control is spared. In contrast, in addition to visual form agnosia, DF also has visuomotor symptoms of optic ataxia which are most likely explained by bilateral damage to the superior parietal occipital cortex. We thus conclude that patient DF can no longer be considered as an appropriate single-case model for testing the neural basis of perception and action dissociations

Rise and fall of the two visual systems theory

International audienc

Two eyes in action

Do relative binocular disparities guide our movements in depth? In order to find out we asked subjects to move a 'cursor' to a target within a simulated horizontal plane at eye height. They did so by moving a computer mouse. We determined how quickly subjects responded to the target jumping in depth. We found that it took subjects about 200 ms to respond to changes in binocular disparity. Subjects responded just as quickly if the cursor was temporarily only visible to one eye near the time that the target jumped in depth, and less vigorously, though just as quickly, if the cursor jumped rather than the target, so the fastest binocular responses cannot be based directly on the relative retinal disparity between the target and the cursor. Subjects reacted faster to changes in the target's height in the visual field than to changes in binocular disparity, but did not react faster to changes in image size. These results suggest that binocular vision mainly improves people's everyday movements by giving them a better sense of the distances of relevant objects, rather than by relative retinal disparities being used to directly guide the movement. We propose that relative disparities only guide parts of very slow movements that require extreme precision. © Springer-Verlag 2005

Changes in initiation of orienting gaze shifts after muscimol inactivation of the caudal fastigial nucleus in the cat.

1. The production of a goal-directed saccadic gaze shift involves the specification of movement amplitude and direction, and the decision to trigger the movement. Behavioural and neurophysiological data suggest that these two functions involve separate processes which may interact. 2. The medio-posterior cerebellar areas are classically assigned a major contribution to the control of saccade metrics, and previous cerebellar lesion studies have revealed marked dysmetria of visually triggered gaze shifts. In contrast, these studies did not provide evidence for a cerebellar role in saccadic initiation. 3. In the present study, we investigated in the head-unrestrained cat the deficits in both the initiation and the metrics control of saccadic gaze shifts following pharmacological inactivation of the caudal part of the fastigial nucleus (cFN). 4. After cFN inactivation, latencies for contraversive gaze shifts increased to about 137 +/- 28% of normal, and latencies for ipsiversive gaze shifts decreased to about 84 +/- 8% of normal. Similar changes in head movement latency were observed, such that the temporal coupling between eye and head components remained largely unaffected. 5. Contraversive gaze shifts were more hypometric as their latency increased. In contrast, the degree of hypermetria in ipsiversive gaze shifts was unrelated to latency. 6. These results suggest a functional role of the medio-posterior cerebellum in gaze shift initiation and in storing information about the target location and/or the desired gaze shift amplitude

Orienting gaze shifts during muscimol inactivation of caudal fastigial nucleus in the cat. I. Gaze dysmetria.

International audienceThe cerebellar control of orienting behavior toward visual targets was studied in the head-unrestrained cat by analyzing the deficits of saccadic gaze shifts after unilateral injection of muscimol in the caudal part of the fastigial nucleus (cFN). Gaze shifts are rendered strongly inaccurate by muscimol cFN inactivation. The characteristics of gaze dysmetria are specific to the direction of the movement with respect to the inactivated cFN. Gaze shifts directed toward the injected side are hypermetric. Irrespective of their starting position, all these ipsiversive gaze shifts overshoot the target by a constant horizontal error (or bias) to terminate at a "shifted goal" location. In particular, when gaze is directed initially at the future target's location, a response with an amplitude corresponding to the bias moves gaze away from the actual target. Additionally, when gaze is initially in between the target and this shifted goal location, the response again is directed toward the latter. This deficit of ipsiversive gaze shifts is characterized by a consistent increase in the y intercept of the relationship between horizontal gaze amplitude and horizontal retinal error. Slight increases in the slope sometimes are observed as well. Contraversive gaze shifts are markedly hypometric and, in contrast to ipsiversive responses, they do not converge onto a shifted goal but rather underestimate target eccentricity in a proportional way. This is reflected by a decrease in the slope of the relationship between horizontal gaze amplitude and horizontal retinal error, with, for some experiments, a moderate change in the y-intercept value. The same deficits are observed in a different setup, which permits the control of initial gaze position. Correction saccades rarely are observed when visual feedback is eliminated on initiation of the primary orienting response; instead, they occur frequently when the target remains visible. Like the primary contraversive saccades, they are hypometric and the ever-decreasing series of three to five correction saccades reduces the gaze fixation error but often does not completely eliminate it. We measured the position of gaze after the final correction saccade and found that fixation of a visible target is still shifted toward the inactivated cFN by 4.9 +/- 2.4 degrees. This fixation offset is correlated to, but on average 54% smaller than, the hypermetric bias of ipsiversive responses measured in the same experiments. In conclusion, the cFN contributes to the control of saccadic shifts of the visual axis toward a visual target. The hypometria of contraversive gaze shifts suggests a cFN role in adjusting a gain in the translation of retinal signals into gaze motor commands. On the basis of the convergence of ipsiversive gaze shifts onto a shifted goal, the straightness of gaze trajectory during these responses and the production of misdirected or inappropriately initiated responses toward this shifted goal, we propose that the cFN influences the processes that specify the goal of ipsiversive gaze shifts