Sylvain Harquel

Neural representations of ethologically relevant hand/mouth synergies in the human precentral gyrus

Significance The motor repertoire of infants is narrow. Yet newborns can accurately bring their hands toward their mouth for self-feeding, thumb-sucking, or perioral exploration, thus showing fine coordinated movement synergies between the hand and mouth. Here, we show that these gestures of high ethological value are selectively encoded in the human brain and represented as integrated primitives within the precentral gyrus, a key region for sensorimotor processing. These findings have major implications for our understanding of the organization and phylogenesis of motor functions in primates. Complex motor responses are often thought to result from the combination of elemental movements represented at different neural sites. However, in monkeys, evidence indicates that some behaviors with critical ethological value, such as self-feeding, are represented as motor primitives in the precentral gyrus (PrG). In humans, such primitives have not yet been described. This could reflect well-known interspecies differences in the organization of sensorimotor regions (including PrG) or the difficulty of identifying complex neural representations in peroperative settings. To settle this alternative, we focused on the neural bases of hand/mouth synergies, a prominent example of human behavior with high ethological value. By recording motor- and somatosensory-evoked potentials in the PrG of patients undergoing brain surgery (2–60 y), we show that two complex nested neural representations can mediate hand/mouth actions within this structure: (i) a motor representation, resembling self-feeding, where electrical stimulation causes the closing hand to approach the opening mouth, and (ii) a motor–sensory representation, likely associated with perioral exploration, where cross-signal integration is accomplished at a cortical site that generates hand/arm actions while receiving mouth sensory inputs. The first finding extends to humans’ previous observations in monkeys. The second provides evidence that complex neural representations also exist for perioral exploration, a finely tuned skill requiring the combination of motor and sensory signals within a common control loop. These representations likely underlie the ability of human children and newborns to accurately produce coordinated hand/mouth movements, in an otherwise general context of motor immaturity.

Neural Dynamics of the Intention to Speak

When we talk we communicate our intentions. Although the origin of intentional action is debated in cognitive neuroscience, the question of how the brain generates the intention in speech remains still open. Using magnetoencephalography, we investigated the cortical dynamics engaged when healthy subjects attended to either their intention to speak or their actual speech. We found that activity in the right and left parietal cortex increased before subjects became aware of intending to speak. Within the time window of parietal activation, we also observed a transient left frontal activity in Brocas area, a crucial region for inner speech. During attention to speech, neural activity was detected in left prefrontal and temporal areas and in the temporoparietal junction. In agreement with previous results, our findings suggest that the parietal cortex plays a multimodal role in monitoring intentional mechanisms in both action and language. The coactivation of parietal regions and Brocas area may constitute the cortical circuit specific for controlling intentional processes during speech.

Brain Processing of Emotional Scenes in Aging: Effect of Arousal and Affective Context

Research on emotion showed an increase, with age, in prevalence of positive information relative to negative ones. This effect is called positivity effect. From the cerebral analysis of the Late Positive Potential (LPP), sensitive to attention, our study investigated to which extent the arousal level of negative scenes is differently processed between young and older adults and, to which extent the arousal level of negative scenes, depending on its value, may contextually modulate the cerebral processing of positive (and neutral) scenes and favor the observation of a positivity effect with age. With this aim, two negative scene groups characterized by two distinct arousal levels (high and low) were displayed into two separate experimental blocks in which were included positive and neutral pictures. The two blocks only differed by their negative pictures across participants, as to create two negative global contexts for the processing of the positive and neutral pictures. The results show that the relative processing of different arousal levels of negative stimuli, reflected by LPP, appears similar between the two age groups. However, a lower activity for negative stimuli is observed with the older group for both tested arousal levels. The processing of positive information seems to be preserved with age and is also not contextually impacted by negative stimuli in both younger and older adults. For neutral stimuli, a significantly reduced activity is observed for older adults in the contextual block of low-arousal negative stimuli. Globally, our study reveals that the positivity effect is mainly due to a modulation, with age, in processing of negative stimuli, regardless of their arousal level. It also suggests that processing of neutral stimuli may be modulated with age, depending on negative context in which they are presented to. These age-related effects could contribute to justify the differences in emotional preference with age.

What saccadic eye movements tell us about TMS-induced neuromodulation of the DLPFC and mood changes: a pilot study in bipolar disorders.

The study assumed that the antisaccade (AS) task is a relevant psychophysical tool to assess (i) short-term neuromodulation of the dorsolateral prefrontal cortex (DLPFC) induced by intermittent theta burst stimulation (iTBS); and (ii) mood change occurring during the course of the treatment. Saccadic inhibition is known to strongly involve the DLPFC, whose neuromodulation with iTBS requires less stimulation time and lower stimulation intensity, as well as results in longer aftereffects than the conventional repetitive transcranial magnetic stimulation (rTMS). Active or sham iTBS was applied every day for 3 weeks over the left DLPFC of 12 drug-resistant bipolar depressed patients. To assess the iTBS-induced short-term neuromodulation, the saccadic task was performed just before (S1) and just after (S2) the iTBS session, the first day of each week. Mood was evaluated through Montgomery and Asberg Depression Rating Scale (MADRS) scores and the difference in scores between the beginning and the end of treatment was correlated with AS performance change between these two periods. As expected, only patients from the active group improved their performance from S1 to S2 and mood improvement was significantly correlated with AS performance improvement. In addition, the AS task also discriminated depressive bipolar patients from healthy control subjects. Therefore, the AS task could be a relevant and useful tool for clinicians to assess if the Transcranial magnetic stimulation (TMS)-induced short-term neuromodulation of the DLPFC occurs as well as a “trait vs. state” objective marker of depressive mood disorder.

Monetary reward suppresses anterior insula activity during social pain

Social pain after exclusion by others activates brain regions also involved in physical pain. Here we evaluated whether monetary reward could compensate for the negative feeling of social pain in the brain. To address this question we used the unique technique of intracranial electroencephalography in subjects with drug resistant epilepsy. Specifically, we recorded theta activity from intracranial electrodes implanted in the insular cortex while subjects experienced conditions of social inclusion and exclusion associated with monetary gain and loss. Our study confirmed that theta rhythm in the insular cortex is the neural signature of social exclusion. We found that while monetary gain suppresses the effect of social pain in the anterior insula, there is no such effect in the posterior insula. These results imply that the anterior insula can use secondary reward signals to compensate for the negative feeling of social pain. Hence, here we propose that the anterior insula plays a pivotal role in integrating contingencies to update social pain feelings. Finally, the possibility to modulate the theta rhythm through the reward system might open new avenues of research for treating pathologies related to social exclusion.

Resting electroencephalographic correlates of the clinical response to repetitive transcranial magnetic stimulation: A preliminary comparison between unipolar and bipolar depression.

BACKGROUND Major depressive disorder (MDD) and bipolar disorder (BP) are two different types of mood disorders, sometimes difficult to distinguish from their depressive symptoms, and for which repetitive transcranial magnetic stimulation (rTMS) of the dorsolateral prefrontal cortex (DLPFC) has been proposed to treat refractory patients. Here we studied whether the electroencephalogram (EEG) at rest could be used to predict the therapeutic response to left DLPFC 10 Hz rTMS, and to which extent BP and MDD patients show similar correlation between the clinical response and the cortical networks at rest. METHODS Eight MDD (6 females) and 10 BP patients (6 females) were included. The rTMS therapy consisted of 10 to 20 neuronavigated sessions, with 2000 pulses continuously applied at 120% motor threshold for each session. RTMS sessions at the beginning, middle and end of the therapy were performed while recording EEG signals. EEG spectral power was partitioned using the common physiological frequency bands and was statistically analysed at the scalp level and after cortical source reconstruction. RESULTS We found significantly higher power in theta and beta bands in BP patients than in MDD patients, mainly localised in the prefrontal cortex. In addition, responders showed higher power in delta and theta bands in parietal regions and weaker frontal alpha power, when compared to non-responders. DISCUSSION These preliminary findings on a small cohort suggest that pre-treatment EEG oscillatory patterns may have some predictive value regarding rTMS therapy, both for MDD and BP disorders.

Single-trial ERP classification of emotional processing

This paper investigates human emotion recognition based on event-related potentials (ERPs) in EEG elicited by picture presentation. Emotion is manipulated through arousal and valence with a calibrated picture dataset. A classification framework is designed for single-trial ERP classification. The most discriminative spatio-temporal features of emotional states were selected and fed to a shrinkage linear discriminant classifier. Various binary classifications were tested according to the emotional valence (positive, negative, neutral) and the arousal level (low, high and no excitation). High classification rate (87%) was obtained for the discrimination between the high-arousal (HA) and low-arousal (LA) negative conditions. Relative good performances were also observed for the (extreme) case “HA negative versus neutral conditions” (66%). Our results suggest that the discrimination of emotional states is better when it is mainly based on an arousal difference between stimuli rather than on a valence difference.

Automatized set-up procedure for transcranial magnetic stimulation protocols

Abstract Transcranial Magnetic Stimulation (TMS) established itself as a powerful technique for probing and treating the human brain. Major technological evolutions, such as neuronavigation and robotized systems, have continuously increased the spatial reliability and reproducibility of TMS, by minimizing the influence of human and experimental factors. However, there is still a lack of efficient set‐up procedure, which prevents the automation of TMS protocols. For example, the set‐up procedure for defining the stimulation intensity specific to each subject is classically done manually by experienced practitioners, by assessing the motor cortical excitability level over the motor hotspot (HS) of a targeted muscle. This is time‐consuming and introduces experimental variability. Therefore, we developed a probabilistic Bayesian model (AutoHS) that automatically identifies the HS position. Using virtual and real experiments, we compared the efficacy of the manual and automated procedures. AutoHS appeared to be more reproducible, faster, and at least as reliable as classical manual procedures. By combining AutoHS with robotized TMS and automated motor threshold estimation methods, our approach constitutes the first fully automated set‐up procedure for TMS protocols. The use of this procedure decreases inter‐experimenter variability while facilitating the handling of TMS protocols used for research and clinical routine. HighlightsAutomatized set‐up procedures would facilitate TMS experiments and increase reproducibility.We developed a Bayesian model aiming at automatically finding the motor hotspot.Implementation of this model in a robotized TMS system allows the automatic search for the motor hotspot.Definition of the motor hotspot is significantly improved in terms of speed and reproducibility.

Evidence of Rapid Modulation by Social Information of Subjective, Physiological, and Neural Responses to Emotional Expressions.

Recent research suggests that conceptual or emotional factors could influence the perceptual processing of stimuli. In this article, we aimed to evaluate the effect of social information (positive, negative, or no information related to the character of the target) on subjective (perceived and felt valence and arousal), physiological (facial mimicry) as well as on neural (P100 and N170) responses to dynamic emotional facial expressions (EFE) that varied from neutral to one of the six basic emotions. Across three studies, the results showed reduced ratings of valence and arousal of EFE associated with incongruent social information (Study 1), increased electromyographical responses (Study 2), and significant modulation of P100 and N170 components (Study 3) when EFE were associated with social (positive and negative) information (vs. no information). These studies revealed that positive or negative social information reduces subjective responses to incongruent EFE and produces a similar neural and physiological boost of the early perceptual processing of EFE irrespective of their congruency. In conclusion, the article suggests that the presence of positive or negative social context modulates early physiological and neural activity preceding subsequent behavior.