Saccadic Adaptation Boosts Ongoing Gamma Activity in a Subsequent Visuoattentional Task.

Attention and saccadic adaptation (SA) are critical components of visual perception, the former enhancing sensory processing of selected objects, the latter maintaining the eye movements accuracy toward them. Recent studies propelled the hypothesis of a tight functional coupling between these mechanisms, possibly due to shared neural substrates. Here, we used magnetoencephalography to investigate for the first time the neurophysiological bases of this coupling and of SA per se. We compared visual discrimination performance of 12 healthy subjects before and after SA. Eye movements and magnetic signals were recorded continuously. Analyses focused on gamma band activity (GBA) during the pretarget period of the discrimination and the saccadic tasks. We found that GBA increases after SA. This increase was found in the right hemisphere for both postadaptation saccadic and discrimination tasks. For the latter, GBA also increased in the left hemisphere. We conclude that oculomotor plasticity involves GBA modulation within an extended neural network which persists after SA, suggesting a possible role of gamma oscillations in the coupling between SA and attention.

Studying the neural bases of prism adaptation using fMRI: A technical and design challenge.

Prism adaptation induces rapid recalibration of visuomotor coordination. The neural mechanisms of prism adaptation have come under scrutiny since the observations that the technique can alleviate hemispatial neglect following stroke, and can alter spatial cognition in healthy controls. Relative to non-imaging behavioral studies, fMRI investigations of prism adaptation face several challenges arising from the confined physical environment of the scanner and the supine position of the participants. Any researcher who wishes to administer prism adaptation in an fMRI environment must adjust their procedures enough to enable the experiment to be performed, but not so much that the behavioral task departs too much from true prism adaptation. Furthermore, the specific temporal dynamics of behavioral components of prism adaptation present additional challenges for measuring their neural correlates. We developed a system for measuring the key features of prism adaptation behavior within an fMRI environment. To validate our configuration, we present behavioral (pointing) and head movement data from 11 right-hemisphere lesioned patients and 17 older controls who underwent sham and real prism adaptation in an MRI scanner. Most participants could adapt to prismatic displacement with minimal head movements, and the procedure was well tolerated. We propose recommendations for fMRI studies of prism adaptation based on the design-specific constraints and our results.

A role for the parietal cortex in sensorimotor adaptation of saccades.

Sensorimotor adaptation ensures movement accuracy despite continuously changing environment and body. Adaptation of saccadic eye movements is a classical model of sensorimotor adaptation. Beside the well-established role of the brainstem-cerebellum in the adaptation of reactive saccades (RSs), the cerebral cortex has been suggested to be involved in the adaptation of voluntary saccades (VSs). Here, we provide direct evidence for a causal involvement of the parietal cortex in saccadic adaptation. First, the posterior intraparietal sulcus (pIPS) was identified in each subject using functional magnetic resonance imaging (fMRI). Then, a saccadic adaptation paradigm was used to progressively reduce the amplitude of RSs and VSs, while single-pulse transcranial magnetic stimulation (spTMS) was applied over the right pIPS. The perturbations of pIPS resulted in impairment for the adaptation of VSs, selectively when spTMS was applied 60 ms after saccade onset. In contrast, the adaptation of RSs was facilitated by spTMS applied 90 ms after saccade initiation. The differential effect of spTMS relative to saccade types suggests a direct interference with pIPS activity for the VS adaptation and a remote interference with brainstem-cerebellum activity for the RS adaptation. These results support the hypothesis that the adaptation of VSs and RSs involves different neuronal substrates.

Adaptation of scanning saccades co-occurs in different coordinate systems.

Plastic changes of saccades (i.e., following saccadic adaptation) do not transfer between oppositely directed saccades, except when multiple directions are trained simultaneously, suggesting a saccadic planning in retinotopic coordinates. Interestingly, a recent study in human healthy subjects revealed that after an adaptive increase of rightward-scanning saccades, both leftward and rightward double-step, memory-guided saccades, triggered toward the adapted endpoint, were modified, revealing that target location was coded in spatial coordinates (Zimmermann et al. 2011). However, as the computer screen provided a visual frame, one alternative hypothesis could be a coding in allocentric coordinates. Here, we questioned whether adaptive modifications of saccadic planning occur in multiple coordinate systems. We reproduced the paradigm of Zimmermann et al. (2011) using target light-emitting diodes in the dark, with and without a visual frame, and tested different saccades before and after adaptation. With double-step, memory-guided saccades, we reproduced the transfer of adaptation to leftward saccades with the visual frame but not without, suggesting that the coordinate system used for saccade planning, when the frame is visible, is allocentric rather than spatiotopic. With single-step, memory-guided saccades, adaptation transferred to leftward saccades, both with and without the visual frame, revealing a target localization in a coordinate system that is neither retinotopic nor allocentric. Finally, with single-step, visually guided saccades, the classical, unidirectional pattern of amplitude change was reproduced, revealing retinotopic coordinate coding. These experiments indicate that the same procedure of adaptation modifies saccadic planning in multiple coordinate systems in parallel-each of them revealed by the use of different saccade tasks in postadaptation.

Saccades and eye-head coordination in ataxia with oculomotor apraxia type 2.

Ataxia with oculomotor apraxia type 2 (AOA2) is one of the most frequent autosomal recessive cerebellar ataxias. Oculomotor apraxia refers to horizontal gaze failure due to deficits in voluntary/reactive eye movements. These deficits can manifest as increased latency and/or hypometria of saccades with a staircase pattern and are frequently associated with compensatory head thrust movements. Oculomotor disturbances associated with AOA2 have been poorly studied mainly because the diagnosis of oculomotor apraxia was based on the presence of compensatory head thrusts. The aim of this study was to characterise the nature of horizontal gaze failure in patients with AOA2 and to demonstrate oculomotor apraxia even in the absence of head thrusts. Five patients with AOA2, without head thrusts, were tested in saccadic tasks with the head restrained or free to move and their performance was compared to a group of six healthy participants. The most salient deficit of the patients was saccadic hypometria with a typical staircase pattern. Saccade latency in the patients was longer than controls only for memory-guided saccades. In the head-free condition, head movements were delayed relative to the eye and their amplitude and velocity were strongly reduced compared to controls. Our study emphasises that in AOA2, hypometric saccades with a staircase pattern are a more reliable sign of oculomotor apraxia than head thrust movements. In addition, the variety of eye and head movements' deficits suggests that, although the main neural degeneration in AOA2 affects the cerebellum, this disease affects other structures.

Functional activation of the cerebral cortex related to sensorimotor adaptation of reactive and voluntary saccades.

Potentially dangerous events in the environment evoke automatic ocular responses, called reactive saccades. Adaptation processes, which maintain saccade accuracy against various events (e.g. growth, aging, neuro-muscular lesions), are to date mostly relayed to cerebellar activity. Here we demonstrate that adaptation of reactive saccades also involves cerebral cortical areas. Moreover, we provide the first identification of the neural substrates of adaptation of voluntary saccades, representing the complement to reactive saccades for the active exploration of our environment. An fMRI approach was designed to isolate adaptation from saccade production: an adaptation condition in which the visual target stepped backward 50 ms after saccade termination was compared to a control condition where the same target backstep occurred 500 ms after saccade termination. Subjects were tested for reactive and voluntary saccades in separate sessions. Multi-voxel pattern analyses of fMRI data from previously-defined regions of interests (ROIs) significantly discriminated between adaptation and control conditions for several ROIs. Some of these areas were revealed for adaptation of both saccade categories (cerebellum, frontal cortex), whereas others were specifically related to reactive saccades (temporo-parietal junction, hMT+/V5) or to voluntary saccades (medial and posterior areas of intra-parietal sulcus). These findings critically extend our knowledge on brain motor plasticity by showing that saccadic adaptation relies on a hitherto unknown contribution of the cerebral cortex.

Increases of corticospinal excitability in self-related processing.

Involvement of fronto-parietal structures within the right hemisphere in bodily self recognition has gained convergent support from behavioural, neuropsychological and neuroimaging studies. Increases in corticospinal excitability via transcranial magnetic stimulation (TMS) also testify to right hemisphere self-related processing. However, evidence for self-dependent modulations of motor excitability is limited to the processing of face-related information that, by definition, conveys someone's identity. Here we tested the hypothesis that vision of one's own hand, as compared with vision of somebody else's hand, would also engage specific self-hand processing in the right hemisphere. Healthy participants were submitted to a classic TMS paradigm to assess changes in corticospinal excitability of the right (Experiment 1) and left (Experiment 2) motor cortex, while viewing pictures of a (contralateral) still hand, which could either be their own (Self) or not (Other). As a control for body selectivity, subjects were also presented with pictures of a hand-related, but non-corporeal object, i.e. a mobile phone, which could similarly be their own or not. Results showed a selective right hemisphere increase in corticospinal excitability with self-hand and self-phone stimuli with respect to Other stimuli. Such a Self vs. Other modulation of primary motor cortex appeared at 600 ms and was maintained at 900 ms, but was not present at earlier timings (100 and 300 ms) and was completely absent following stimulation of the left hemisphere. A similar pattern observed for self-hand and self-phone stimuli suggests that owned hands and objects may undergo similar self-processing, possibly via a different cortical network from that responsible for self-face processing.

Impaired Spatial Inhibition Processes for Interhemispheric Anti-saccades following Dorsal Posterior Parietal Lesions.

Anti-saccades are eye movements that require inhibition to stop the automatic saccade to the visual target and to perform instead a saccade in the opposite direction. The inhibitory processes underlying anti-saccades have been primarily associated with frontal cortex areas for their role in executive control. Impaired performance in anti-saccades has also been associated with the parietal cortex, but its role in inhibitory processes remains unclear. Here, we tested the assumption that the dorsal parietal cortex contributes to spatial inhibition processes of contralateral visual target. We measured anti-saccade performance in 2 unilateral optic ataxia patients and 15 age-matched controls. Participants performed 90 degree (across and within visual fields) and 180 degree inversion anti-saccades, as well as pro-saccades. The main result was that our patients took longer to inhibit visually guided saccades when the visual target was presented in the ataxic hemifield and the task required a saccade across hemifields. This was observed through anti-saccades latencies and error rates. These deficits show the crucial role of the dorsal posterior parietal cortex in spatial inhibition of contralateral visual target representations to plan an accurate anti-saccade toward the ipsilesional side.

Two modes of error processing in reaching.

Several processes are devoted to error reduction for the production of purposeful actions. When motor responses deviate from their goal, online corrections can be performed either under voluntary control with additional sub-movements or under fast automatic control with smooth velocity profiles. When errors cannot be corrected online and are repeated over trials, subsequent responses can be improved iteratively through adaptation, a progressive adjustment of motor commands that acts to reduce the magnitude of error. It has been argued that reaching adaptation results essentially from a conflict between actual sensory feedback and expected sensory feedback. Here, we specifically compare two innovative hand-reaching paradigms that provide the subject with undistorted hand sensory feedback. Both paradigms induce motor planning errors unknown to the subjects. Experiment 1 yields a continuous retinal and visuomotor feedback which allows fast and complete automatic online corrections. In experiment 2, all visual feedback is eliminated during movement execution. This prevents online correction and provides information on hand-to-target visual error at movement end only. Despite a reiterated motor planning error and an automatic online correction of the whole error, experiment 1 shows a complete lack of adaptation. In contrast, experiment 2 which yields the same motor planning error exhibits a robust and generalized adaptation, although devoid of limb inter-sensory mismatch. These results demonstrate independence between the induced motor adaptation and automatic online correction, both characterized by the lack of any cognitive interference. Despite these quite different processes acting upon either motor planning or motor control, the general structure of the movement kinematics remains unaltered. A putative visuomotor cerebro-cerebellar network accounting for our results is proposed.

Saccade control and eye-hand coordination in optic ataxia.

The aim of this work was to investigate ocular control in patients with optic ataxia (OA). Following a lesion in the posterior parietal cortex (PPC), these patients exhibit a deficit for fast visuo-motor control of reach-to-grasp movements. Here, we assessed the fast visuo-motor control of saccades as well as spontaneous eye-hand coordination in two bilateral OA patients and five neurologically intact controls in an ecological "look and point" paradigm. To test fast saccadic control, trials with unexpected target-jumps synchronised with saccade onset were randomly intermixed with stationary target trials. Results confirmed that control subjects achieved visual capture (foveation) of the displaced targets with the same timing as stationary targets (fast saccadic control) and began their hand movement systematically at the end of the primary saccade. In contrast, the two bilateral OA patients exhibited a delayed visual capture, especially of displaced targets, resulting from an impairment of fast saccadic control. They also exhibited a peculiar eye-hand coordination pattern, spontaneously delaying their hand movement onset until the execution of a final corrective saccade, which allowed target foveation. To test whether this pathological behaviour results from a delay in updating visual target location, we had subjects perform a second experiment in the same control subjects in which the target-jump was synchronised with saccade offset. With less time for target location updating, the control subjects exhibited the same lack of fast saccadic control as the OA patients. We propose that OA corresponds to an impairment of fast updating of target location, therefore affecting both eye and hand movements.

Reachability judgement in optic ataxia: Effect of peripheral vision on hand and target perception in depth.

The concept of peripersonal space was first proposed by Rizzolatti, Scandolara, Matelli, and Gentilucci (1981), who introduced the term to highlight the close links between somatosensory and visual processing for stimuli close to the body and suggested that this near-body space could in fact be characterized as an action space (Rizzolatti, Fadiga, Fogassi, & Gallese, 1997). Supporting this idea, patients with right hemisphere lesions have been described as impaired in performing actions towards objects and in perceiving their location - but only when the objects were presented within arm's reach (Bartolo, Carlier, Hassaini, Martin, & Coello, 2014; Brain, 1941). Whether the deficit of optic ataxia patients in processing target locations for action has an effect on the representation of peripersonal space has never been explored. The present study highlights optic ataxia patients' specific difficulties in processing hand-to-target distances in a motor task and in a perceptual task requiring identification of what is reachable in the visual environment. The difficulties are especially evident when both the target and the hand are perceived in the visual periphery. Indeed, when patient I.G. was able to fixate the target, her reaching accuracy and her perception of reachable space both largely improved. Furthermore, the difficulties were enhanced when the hand and the target were both in the lower visual field (in a fixed-far condition vs a fixed-near condition). This novel up-down dimension of optic ataxia fits with the larger representation of the lower visual field in the posterior parietal cortex (Pitzalis et al., 2013; Previc, 1990).

Oculomotor plasticity: are mechanisms of adaptation for reactive and voluntary saccades separate?

Saccadic eye movements are permanently controlled and their accuracy maintained by adaptive mechanisms that compensate for physiological or pathological perturbations. In contrast to the adaptation of reactive saccades (RS) which are automatically triggered by the sudden appearance of a single target, little is known about the adaptation of voluntary saccades which allow us to intentionally scan our environment in nearly all our daily activities. In this study, we addressed this issue in human subjects by determining the properties of adaptation of scanning voluntary saccades (SVS) and comparing these features to those of RS. We also tested the reciprocal transfers of adaptation between the two saccade types. Our results revealed that SVS and RS adaptations disclosed similar adaptation fields, time course and recovery levels, with only a slightly lower after-effect for SVS. Moreover, RS and SVS main sequences both remained unaffected after adaptation. Finally and quite unexpectedly, the pattern of adaptation transfers was asymmetrical, with a much stronger transfer from SVS to RS (79%) than in the reverse direction (22%). These data demonstrate that adaptations of RS and SVS share several behavioural properties but at the same time rely on partially distinct processes. Based on these findings, it is proposed that adaptations of RS and SVS may involve a neural network including both a common site and two separate sites specifically recruited for each saccade type.

Influence of initial hand and target position on reach errors in optic ataxic and normal subjects.

Recent neurophysiological studies suggest that reach planning areas in the posterior parietal cortex encode both target and initial hand position in gaze-centered coordinates, which could be used to calculate a desired movement vector. We tested how varying gaze, target position, and initial hand position affected reach errors in two left unilateral optic ataxia patients with right PPC damage and seven neurologically intact controls. Both controls' and patients' reaching errors revealed an influence of target position in gaze-centered coordinates; however, both patients' mean errors were offset toward the left, with greater errors when the target was in their left visual field, consistent with the damage to the right PPC. Control subjects also showed a large quasi-independent shoulder-centered influence of target position. This effect was much less present in patient C.F., who had more medial damage to the PPC. In contrast, for patient O.K., who had more lateral PPC damage, the shoulder-centered effect was larger and interacted with the gaze-centered influence of target position. All subjects' errors also revealed a shoulder-centered influence of the initial hand position, with larger influences on the patients' reaching errors. Both patients also showed an interactive influence of the shoulder-centered and gaze-centered initial hand positions. These results suggest that the target and the hand are compared at more than one level in the visuomotor pathway in multiple reference frames, and these comparisons are then integrated. Depending on the location of the damage within the PPC, these comparisons are disrupted, changing the relative influence of hand and target position in different reference frames on the final reaching movement.

Deployment of spatial attention without moving the eyes is boosted by oculomotor adaptation.

Vertebrates developed sophisticated solutions to select environmental visual information, being capable of moving attention without moving the eyes. A large body of behavioral and neuroimaging studies indicate a tight coupling between eye movements and spatial attention. The nature of this link, however, remains highly debated. Here, we demonstrate that deployment of human covert attention, measured in stationary eye conditions, can be boosted across space by changing the size of ocular saccades to a single position via a specific adaptation paradigm. These findings indicate that spatial attention is more widely affected by oculomotor plasticity than previously thought.

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.

On-line modification of saccadic eye movements by retinal signals.

A saccade is a rapid shift of the position of the eyes (< 100 ms). Saccades are generally considered too quick to be influenced by retinal signals. To address this idea, we displaced the visual target of a rightward horizontal saccade at eye movement onset (when there is suppression of conscious perception). To prevent adaptive and learning effects to occur, jump saccades were always followed by a random series of 10 no-jump saccades. Results indicated that the target jump influenced significantly the amplitude and the peak velocity of the ongoing saccade (opposite effects were found for rightward and leftward jumps). Changes in saccade kinematics occurred as early as 50 ms after the target jump. These results show that retinal information is processed quickly during eye movements, presumably through sub-cortical pathways.

Brain processing of visual information during fast eye movements maintains motor performance.

Movement accuracy depends crucially on the ability to detect errors while actions are being performed. When inaccuracies occur repeatedly, both an immediate motor correction and a progressive adaptation of the motor command can unfold. Of all the movements in the motor repertoire of humans, saccadic eye movements are the fastest. Due to the high speed of saccades, and to the impairment of visual perception during saccades, a phenomenon called "saccadic suppression", it is widely believed that the adaptive mechanisms maintaining saccadic performance depend critically on visual error signals acquired after saccade completion. Here, we demonstrate that, contrary to this widespread view, saccadic adaptation can be based entirely on visual information presented during saccades. Our results show that visual error signals introduced during saccade execution--by shifting a visual target at saccade onset and blanking it at saccade offset--induce the same level of adaptation as error signals, presented for the same duration, but after saccade completion. In addition, they reveal that this processing of intra-saccadic visual information for adaptation depends critically on visual information presented during the deceleration phase, but not the acceleration phase, of the saccade. These findings demonstrate that the human central nervous system can use short intra-saccadic glimpses of visual information for motor adaptation, and they call for a reappraisal of current models of saccadic adaptation.

Iterative fragmentation of cognitive maps in a visual imagery task.

It remains unclear whether spontaneous eye movements during visual imagery reflect the mental generation of a visual image (i.e. the arrangement of the component parts of a mental representation). To address this specificity, we recorded eye movements in an imagery task and in a phonological fluency (non-imagery) task, both consisting in naming French towns from long-term memory. Only in the condition of visual imagery the spontaneous eye positions reflected the geographic position of the towns evoked by the subjects. This demonstrates that eye positions closely reflect the mapping of mental images. Advanced analysis of gaze positions using the bi-dimensional regression model confirmed the spatial correlation of gaze and towns' locations in every single individual in the visual imagery task and in none of the individuals when no imagery accompanied memory retrieval. In addition, the evolution of the bi-dimensional regression's coefficient of determination revealed, in each individual, a process of generating several iterative series of a limited number of towns mapped with the same spatial distortion, despite different individual order of towns' evocation and different individual mappings. Such consistency across subjects revealed by gaze (the mind's eye) gives empirical support to theories postulating that visual imagery, like visual sampling, is an iterative fragmented processing.

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.

Grasping actions remap peripersonal space.

The portion of space that closely surrounds our body parts is termed peripersonal space, and it has been shown to be represented in the brain through multisensory processing systems. Here, we tested whether voluntary actions, such as grasping an object, may remap such multisensory spatial representation. Participants discriminated touches on the hand they used to grasp an object containing task-irrelevant visual distractors. Compared with a static condition, reach-to-grasp movements increased the interference exerted by visual distractors over tactile targets. This remapping of multisensory space was triggered by action onset and further enhanced in real time during the early action execution phase. Additional experiments showed that this phenomenon is hand-centred. These results provide the first evidence of a functional link between voluntary object-oriented actions and multisensory coding of the space around us.