[Cognitive exergames: cognitive-motor synergies in neurorehabilitation]. / Exergames cognitifs: les synergies cognitivo-motrices dans la neuroréhabilitation.

Research on cognitive neurorehabilitation has shown the benefits of both neuropsychological therapy and physical activity on cognitive performance. In this article, we highlight the synergies between these approaches, particularly in the context of "cognitive exergames" that are video games combining cognitive and physical exercise. Even though this area of research is rather novel, the available data suggests cognitive and physical benefits in the elderly, as well as people with brain lesions or neurodegeneration, and point towards the development of multimodal cognitive neurorehabilitation.

La recherche scientifique sur la neuroréhabilitation cognitive a démontré les avantages des prises en charge en neuropsychologie, ainsi que de l'activité physique, sur les performances cognitives. Dans cet article, nous présentons les synergies entre ces deux types d'exercice, notamment dans le contexte des « exergames cognitifs ¼, c'est-à-dire des jeux vidéo combinant tâches cognitives et entraînement physique. Bien qu'il s'agisse d'un domaine de recherche récent, les données indiquent des bénéfices cognitifs et physiques chez les personnes âgées, cérébrolésées ou atteintes de maladies neurodégénératives, et semblent prometteuses pour le développement d'une neuroréhabilitation cognitive multimodale.

Differential Brain Mechanisms of Selection and Maintenance of Information during Working Memory.

Working memory is our ability to select and temporarily hold information as needed for complex cognitive operations. The temporal dynamics of sustained and transient neural activity supporting the selection and holding of memory content is not known. To address this problem, we recorded magnetoencephalography in healthy participants performing a retro-cue working memory task in which the selection rule and the memory content varied independently. Multivariate decoding and source analyses showed that selecting the memory content relies on prefrontal and parieto-occipital persistent oscillatory neural activity. By contrast, the memory content was reactivated in a distributed occipitotemporal posterior network, preceding the working memory decision and in a different format than during the visual encoding. These results identify a neural signature of content selection and characterize differentiated spatiotemporal constraints for subprocesses of working memory.SIGNIFICANCE STATEMENT Our brain selects and maintains information during short time windows in a way that is essential to reasoning and learning. Recent advances in multivariate analysis of brain activity allowed the characterization of brain regions that stores the memory. We applied multivariate analysis to time-resolved brain signals to characterize the spatiotemporal signature underlying these subprocesses. The selection of information relies on sustained oscillatory activity in a network that includes the ventrolateral prefrontal cortex while memory content is transiently replayed in an occipitotemporal network that differs from encoding. Our results characterized differentiated spatiotemporal activity underlying encoding, selection, and maintenance of information during working memory.

State dependency of inhibitory control performance: an electrical neuroimaging study.

Behavioral and brain responses to stimuli not only depend on their physical features but also on the individuals' neurocognitive states before stimuli onsets. While the influence of pre-stimulus fluctuations in brain activity on low-level perceptive processes is well established, the state dependency of high-order executive processes remains unclear. Using a classical inhibitory control Go/NoGo task, we examined whether and how fluctuations in the brain activity during the period preceding the stimuli triggering inhibition influenced inhibitory control performance. Seventeen participants completed the Go/NoGo task while 64-channel electroencephalogram was recorded. We compared the event-related potentials preceding the onset of the NoGo stimuli associated with inhibition failures false alarms (FA) vs. successful inhibition correct rejections (CR) with data-driven statistical analyses of global measures of the topography and strength of the scalp electric field. Distributed electrical source estimations were used to localize the origin of the event-related potentials modulations. We observed differences in the global field power of the event-related potentials (FA > CR) without concomitant topographic modulations over the 40 ms period immediately preceding NoGo stimuli. This result indicates that the same brain networks were engaged in the two conditions, but more strongly before FA than CR. Source estimations revealed that this effect followed from a higher activity before FA than CR within bilateral inferior frontal gyri and the right inferior parietal lobule. These findings suggest that uncontrolled quantitative variations in pre-stimulus activity within attentional and control brain networks influence inhibition performance. The present data thereby demonstrate the state dependency of cognitive processes of up to high-order executive levels.

Age-related changes in post-movement beta synchronization during a selective inhibition task.

Post-movement beta synchronization (PMBS) modulations have been related to sensory reafferences after movement initiation and inhibitory processes after movement interruption. Although these processes have been separately studied in young and old adults, little is known about the age-related changes in PMBS during selective inhibitory control (i.e. stop a part of an action). The present study examines the age-related modulations of PMBS associated with sensory reafferences and inhibitory processes in selective inhibitory control. Young (n = 17) and old (n = 13) participants performed a switching task first engaging bimanual finger tapping then requiring to stop the left while maintaining the right unimanual tapping (i.e. selective inhibition) at an imperative stimulus. Age groups were compared on behavioral (mean, variability and percentage of errors of inter-tap interval during and after the switching) and electrophysiological (time-frequency and source estimations in the 14-30 Hz beta frequency range) data time-locked on the imperative stimulus. Behaviorally, old adults showed larger variability and percentage of errors during the switching but performed as well as young adults after the switching. Electrophysiologically, PMBS significantly increased after the switching in the old compared to the young group within bilateral frontal and parietal areas. Our results show that the effort to maintain selective inhibition involves increased brain activation in old compared to young adults. The larger PMBS within frontal and parietal regions in old adults may reflect an age-related brain compensation enabling to efficiently maintain post-switching inhibition.

Early attentional processes distinguish selective from global motor inhibitory control: an electrical neuroimaging study.

The rapid stopping of specific parts of movements is frequently required in daily life. Yet, whether selective inhibitory control of movements is mediated by a specific neural pathway or by the combination between a global stopping of all ongoing motor activity followed by the re-initiation of task-relevant movements remains unclear. To address this question, we applied time-wise statistical analyses of the topography, global field power and electrical sources of the event-related potentials to the global vs selective inhibition stimuli presented during a Go/NoGo task. Participants (n=18) had to respond as fast as possible with their two hands to Go stimuli and to withhold the response from the two hands (global inhibition condition, GNG) or from only one hand (selective inhibition condition, SNG) when specific NoGo stimuli were presented. Behaviorally, we replicated previous evidence for slower response times in the SNG than in the Go condition. Electrophysiologically, there were two distinct phases of event-related potentials modulations between the GNG and the SNG conditions. At 110-150 ms post-stimulus onset, there was a difference in the strength of the electric field without concomitant topographic modulation, indicating the differential engagement of statistically indistinguishable configurations of neural generators for selective and global inhibitory control. At 150-200 ms, there was topographic modulation, indicating the engagement of distinct brain networks. Source estimations localized these effects within bilateral temporo-parieto-occipital and within parieto-central networks, respectively. Our results suggest that while both types of motor inhibitory control depend on global stopping mechanisms, selective and global inhibition still differ quantitatively at early attention-related processing phases.

Age-related changes in the bimanual advantage and in brain oscillatory activity during tapping movements suggest a decline in processing sensory reafference.

Deficits in the processing of sensory reafferences have been suggested as accounting for age-related decline in motor coordination. Whether sensory reafferences are accurately processed can be assessed based on the bimanual advantage in tapping: because of tapping with an additional hand increases kinesthetic reafferences, bimanual tapping is characterized by a reduced inter-tap interval variability than unimanual tapping. A suppression of the bimanual advantage would thus indicate a deficit in sensory reafference. We tested whether elderly indeed show a reduced bimanual advantage by measuring unimanual (UM) and bimanual (BM) self-paced tapping performance in groups of young (n = 29) and old (n = 27) healthy adults. Electroencephalogram was recorded to assess the underlying patterns of oscillatory activity, a neurophysiological mechanism advanced to support the integration of sensory reafferences. Behaviorally, there was a significant interaction between the factors tapping condition and age group at the level of the inter-tap interval variability, driven by a lower variability in BM than UM tapping in the young, but not in the elderly group. This result indicates that in self-paced tapping, the bimanual advantage is absent in elderly. Electrophysiological results revealed an interaction between tapping condition and age group on low beta band (14-20 Hz) activity. Beta activity varied depending on the tapping condition in the elderly but not in the young group. Source estimations localized this effect within left superior parietal and left occipital areas. We interpret our results in terms of engagement of different mechanisms in the elderly depending on the tapping mode: a 'kinesthetic' mechanism for UM and a 'visual imagery' mechanism for BM tapping movement.

Ultra-fast recovery from right neglect after 'awake surgery' for slow-growing tumor invading the left parietal area.

It is now possible to perform resections of slow-growing tumors in awake patients. Using direct electrical stimulation, real-time functional mapping of the brain can be used to prevent the resection of essential areas near the tumor. Simple clinical observations of patients with a resection of slow-growing tumors have demonstrated substantial recovery within a few days of such 'awake surgery'. The aim of this study was to investigate the kinetics of recovery following the resection of slow-growing tumors invading the left parietal area and to focus mainly on its rapidity. Two patients were assessed by standard line bisection tests and compared with eight healthy individuals. Independently of the pure nature of the symptoms, we report that the patients rapidly and substantially recovered from pronounced right neglect. They were tested 48 hours after the surgery and the recovery was significant for both patients after less than 4 hours. Strikingly, for one patient, recovery was ultra fast and substantial in the first practice session within less than 7 minutes: it occurred without verbal feedback and was substantially retained during the following testing session. Its rapidity suggests a process of unmasking redundant networks. With the slow growth of the lesion, the contralesional hemisphere is probably progressively prepared for rapid unmasking of homologue networks. These results have major clinical implications. For patients with an invading left-side tumor, it is now clear that line bisections are required before, during, and after awake surgery to: plan the surgery, control the quality of the resection, and also optimize the rehabilitation of the patient.

Manual reaction times and brain dynamics after 'awake surgery' of slow-growing tumours invading the parietal area. A case report.

PRIMARY OBJECTIVES: Awake surgeries of slow-growing tumours invading the brain and guided by direct electrical stimulation induce major brain reorganizations accompanied with slight impairments post-operatively. In most cases, these deficits are so slight after a few days that they are often not detectable on classical neuropsychological evaluations. Consequently, this study investigated whether simple visuo-manual reaction time paradigms would sign some level of functional asymmetries between both hemispheres. Importantly, the visual stimulus was located in the saggital plane in order to limit attentional biases and to focus mainly on the inter-hemispheric asymmetry. METHODS AND PROCEDURES: Three patients (aged 41, 59 and 59 years) after resections in parietal regions and a control group (age = 44, SD = 6.9) were compared during simple uni- and bimanual reaction times (RTs). MAIN OUTCOMES AND RESULTS: Longer RTs were observed for the contralesional compared to the ipsilesional hand in the unimanual condition. This asymmetry was reversed for the bimanual condition despite longer RTs. CONCLUSION AND CLINICAL IMPLICATIONS: Reaction time paradigms are useful in these patients to monitor more precisely their functional deficits, especially their level of functional asymmetry, and to understand brain (re)organization following slow-growing lesions.

The field of expertise modulates the time course of neural processes associated with inhibitory control in a sport decision-making task.

Inhibitory control (IC), the ability to suppress inappropriate actions, can be improved by regularly facing complex and dynamic situations requiring flexible behaviors, such as in the context of intensive sport practice. However, researchers have not clearly determined whether and how this improvement in IC transfers to ecological and nonecological computer-based tasks. We explored the spatiotemporal dynamics of changes in the brain activity of three groups of athletes performing sport-nonspecific and sport-specific Go/NoGo tasks with video footages of table tennis situations to address this question. We compared table tennis players (n = 20), basketball players (n = 20) and endurance athletes (n = 17) to identify how years of practicing a sport in an unpredictable versus predictable environment shape the IC brain networks and increase the transfer effects to untrained tasks. Overall, the table tennis group responded faster than the two other groups in both Go/NoGo tasks. The electrical neuroimaging analyses performed in the sport-specific Go/NoGo task revealed that this faster response time was supported by an early engagement of brain structures related to decision-making processes in a time window where inhibition processes typically occur. Our collective findings have relevant applied perspectives, as they highlight the importance of designing more ecological domain-related tasks to effectively capture the complex decision-making processes acquired in real-life situations. Finally, the limited effects from sport practice to laboratory-based tasks found in this study question the utility of cognitive training intervention, whose effects would remain specific to the practice environment.

Alterations in spontaneous electrical brain activity after an extreme mountain ultramarathon.

This study aimed to investigate the impact of an extreme mountain ultramarathon (MUM) on spontaneous electrical brain activity in a group of 16 finishers. By using 4-minute high-density electroencephalographic (EEG) recordings with eyes closed before and after a 330-km race (mean duration: 125 ± 17 h; sleep duration: 7.7 ± 2.9 h), spectral power, source localization and microstate analyses were conducted. After the race, power analyses revealed a centrally localized increase in power in the delta (0.5-3.5 Hz) and theta (4.0-7.5 Hz) frequency bands and a decrease in alpha (8.0-12.0 Hz) power at the parieto-occipital sites. Higher brain activation in the alpha frequency band was observed within the left posterior cingulate cortex, left angular gyrus and visual association areas. Microstate analyses indicated a significant decrease in map C predominance and an increase in the global field power (GFP) for map D at the end of the race. These changes in power patterns and microstate parameters contrast with previously reported findings following short bouts of endurance exercises. We discuss the potential factors that explain lower alpha activity within the parieto-occipital regions and microstate changes after MUMs. In conclusion, high-density EEG resting-state analyses can be recommended to investigate brain adaptations in extreme sporting activities.

Stimulus Reward Value Interacts with Training-induced Plasticity in Inhibitory Control.

Training inhibitory control, the ability to suppress motor or cognitive processes, not only enhances inhibition processes, but also reduces the perceived value and behaviors toward the stimuli associated with the inhibition goals during the practice. While these findings suggest that inhibitory control training interacts with the aversive and reward systems, the underlying spatio-temporal brain mechanisms remain unclear. We used electrical neuroimaging analyses of event-related potentials to examine the plastic brain modulations induced by training healthy participants to inhibit their responses to rewarding (pleasant chocolate) versus aversive food pictures (unpleasant vegetables) with Go/NoGo tasks. Behaviorally, the training resulted in a larger improvement in the aversive than in the rewarding NoGo stimuli condition, suggesting that reward responses impede inhibitory control learning. The electrophysiological results also revealed an interaction between reward responses and inhibitory control plasticity: we observed different effects of practice on the rewarding vs. aversive NoGo stimuli at 200 ms post-stimulus onset, when the conflicts between automatic response tendency and task demands for response inhibition are processed. Electrical source analyses revealed that this effect was driven by an increase in right orbito-cingulate and a decrease in temporo-parietal activity to the rewarding NoGo stimuli and the reverse pattern to the aversive stimuli. Our collective results provide direct neurophysiological evidence for interactions between stimulus reward value and executive control training, and suggest that changes in the assessment of stimuli with repeated motoric inhibition likely follow from associative learning and behavior-stimulus conflicts reduction mechanisms.

Spatiotemporal brain dynamics underlying attentional bias modifications.

Exaggerated attentional biases toward specific elements of the environment contribute to the maintenance of several psychiatric conditions, such as biases to threatening faces in social anxiety. Although recent literature indicates that attentional bias modification may constitute an effective approach for psychiatric remediation, the underlying neurophysiological mechanisms remain unclear. We addressed this question by recording EEG in 24 healthy participants performing a modified dot-probe task in which pairs of neutral cues (colored shapes) were replaced by probe stimuli requiring a discrimination judgment. To induce an attentional bias toward or away from the cues, the probes were systematically presented either at the same or at the opposite position of a specific cue color. This paradigm enabled participants to spontaneously develop biases to initially unbiased, neutral cues, as measured by the response speed to the probe presented after the cues. Behavioral result indicated that the ABM procedure induced approach and avoidance biases. The influence of ABM on inhibitory control was assessed in a separated Go/NoGo task: changes in AB did not influence participants' capacity to inhibit their responses to the cues. Attentional bias modification was associated with a topographic modulation of event-related potentials already 50-84 ms following the onset of the cues. Statistical analyses of distributed electrical source estimations revealed that the development of attentional biases was associated with decreased activity in the left temporo-parieto-occipital junction. These findings suggest that attentional bias modification affects early sensory processing phases related to the extraction of information based on stimulus saliency.

Modulation of inhibitory control by prefrontal anodal tDCS: A crossover double-blind sham-controlled fMRI study.

Prefrontal anodal transcranial direct current stimulation (tDCS) has been proposed as a potential approach to improve inhibitory control performance. The functional consequences of tDCS during inhibition tasks remain, however, largely unresolved. We addressed this question by analyzing functional magnetic resonance imaging (fMRI) recorded while participants completed a Go/NoGo task after right-lateralized prefrontal anodal tDCS with a crossover, sham-controlled, double-blind experimental design. We replicated previous evidence for an absence of offline effect of anodal stimulation on Go/NoGo performance. The fMRI results revealed a larger increase in right ventrolateral prefrontal activity for Go than NoGo trials in the anodal than sham condition. This pattern suggests that tDCS-induced increases in cortical excitability have larger effects on fMRI activity in regions with a lower task-related engagement. This was the case for the right prefrontal cortex in the Go condition in our task because while reactive inhibition was not engaged during execution trials, the unpredictability of the demand for inhibitory control still incited an engagement of proactive inhibition. Exploratory analyses further revealed that right prefrontal stimulation interacted with task-related functional demands in the supplementary motor area and the thalamus. Our collective results emphasize the dependency of offline tDCS functional effects on the task-related engagement of the stimulated areas and suggest that this factor might partly account for the discrepancies in the functional effects of tDCS observed in previous studies.

Enhancing frontal top-down inhibitory control with Go/NoGo training.

Whether and how the capacity to inhibit cognitive and motor processes can be trained and the underlying neuroplastic mechanisms remain unclear. Using electrical neuroimaging methods, we investigated how inhibitory control training regimens can be designed to enhance frontal top-down inhibition processes. We trained participants with a Go/NoGo task in which the stimulus-response mapping rules were systematically varied. This task parameter has indeed be hypothesized to determine the extent to which top-down frontal inhibition processes are involved and thus ultimately reinforced during the training. The effects of training on inhibitory control were assessed by analyzing the event-related potentials (ERPs) measured during the Go/NoGo task with a data-driven time- and electrode-wise 2 × 2 ANOVA with factors Session (beginning; end of the training) and Stimuli (Go; NoGo). To localize the sources of the ERP effects in the brain, the same statistical design was applied to distributed electrical source estimations averaged over the periods of ERP modulations. The training improved inhibitory control performance. Electrophysiologically, we found a significant Session × Stimulus interaction at 300-400 ms post-stimulus onset over centro-occipital electrodes. Statistical parametric mapping on the brain source estimations revealed an interaction within right inferior frontal cortices driven by a decrease in response strength to NoGo but not to Go trials in this region. Our collective results demonstrate that frontal top-down inhibition processes can be enhanced with specifically designed inhibitory control training regimens.

Post-switching beta synchronization reveals concomitant sensory reafferences and active inhibition processes.

It is known that post-movement beta synchronization (PMBS) is involved both in active inhibition and in sensory reafferences processes. The aim of this study was examine the temporal and spatial dynamics of the PMBS involved during multi-limb coordination task. We investigated post-switching beta synchronization (assigned PMBS) using time-frequency and source estimations analyzes. Participants (n=17) initiated an auditory-paced bimanual tapping. After a 1,500 ms preparatory period, an imperative stimulus required to either selectively stop the left while maintaining the right unimanual tapping (Switch condition: SWIT) or to continue the bimanual tapping (Continue condition: CONT). PMBS significantly increased in SWIT compared to CONT with maximal difference within right central region in broad-band 14-30 Hz and within left central region in restricted-band 22-26 Hz. Source estimations localized these effects within right pre-frontal cortex and left parietal cortex, respectively. A negative correlation showed that participants with a low percentage of errors in SWIT had a large PMBS amplitude within right parietal and frontal cortices. This study shows for the first time simultaneous PMBS with distinct functions in different brain regions and frequency ranges. The left parietal PMBS restricted to 22-26 Hz could reflect the sensory reafferences of the right hand tapping disrupted by the switching. In contrast, the right pre-frontal PMBS in a broad-band 14-30 Hz is likely reflecting the active inhibition of the left hand stopped. Finally, correlations between behavioral performance and the magnitude of the PMBS suggest that beta oscillations can be viewed as a marker of successful active inhibition.

EEG alpha activity reflects motor preparation rather than the mode of action selection.

Alpha-band activity (8-13 Hz) is not only suppressed by sensory stimulation and movements, but also modulated by attention, working memory and mental tasks, and could be sensitive to higher motor control functions. The aim of the present study was to examine alpha oscillatory activity during the preparation of simple left or right finger movements, contrasting the external and internal mode of action selection. Three preparation conditions were examined using a precueing paradigm with S1 as the preparatory and S2 as the imperative cue: Full, laterality instructed by S1; Free, laterality freely selected and None, laterality instructed by S2. Time-frequency (TF) analysis was performed in the alpha frequency range during the S1-S2 interval, and alpha motor-related amplitude asymmetries (MRAA) were also calculated. The significant MRAA during the Full and Free conditions indicated effective external and internal motor response preparation. In the absence of specific motor preparation (None), a posterior alpha event-related desynchronization (ERD) dominated, reflecting the main engagement of attentional resources. In Full and Free motor preparation, posterior alpha ERD was accompanied by a midparietal alpha event-related synchronization (ERS), suggesting a concomitant inhibition of task-irrelevant visual activity. In both Full and Free motor preparation, analysis of alpha power according to MRAA amplitude revealed two types of functional activation patterns: (1) a motor alpha pattern, with predominantly midparietal alpha ERS and large MRAA corresponding to lateralized motor activation/visual inhibition and (2) an attentional alpha pattern, with dominating right posterior alpha ERD and small MRAA reflecting visuospatial attention. The present results suggest that alpha oscillatory patterns do not resolve the selection mode of action, but rather distinguish separate functional strategies of motor preparation.