Humans can successfully correct deviations of movements without conscious detection of such deviations, suggesting limited awareness of movement details. We ask whether such limited awareness impairs confidence (metacognition). We recorded functional magnetic resonance imaging data while 31 human female and male participants detected cursor deviations during a visuomotor reaching task and rated their confidence retrospectively. We show that participants monitor a summary statistic of the unfolding visual feedback (the peak cursor error) to detect visuomotor deviations and adjust their confidence ratings, even when they report being unaware of a deviation. Crucially, confidence ratings were as metacognitively efficient for aware and unaware deviations. At the neural level, activity in the ventral striatum tracks high confidence, whereas a broad network encodes cursor error but not confidence. These findings challenge the notion of limited conscious action monitoring and uncover how humans monitor their movements as they unfold, even when unaware of ongoing deviations.SIGNIFICANCE STATEMENT We are unaware of the small corrections we apply to our movements as long as our goals are achieved. Here, although we replicate the finding that participants deny perceiving small deviations they correct, we show that their confidence reliably reflects the presence or absence of a deviation. This observation shows they can metacognitively monitor the presence of a deviation, even when they deny perceiving it. We also describe the hemodynamic correlates of confidence ratings. Our study questions the extent to which humans are unaware of the details of their movements; describes a plausible mechanism for metacognition in a visuomotor task, along with its neural correlates; and has important implications for the construction of the sense of self.
Several cortical and sub-cortical regions in the right hemisphere, particularly in parietal and frontal lobe, but also in temporal lobe and thalamus, are part of neural networks critically implicated in spatial and attentional functions. Damage to different sites within these networks can cause hemispatial neglect. The aim of this study was to identify the neural substrates of different spatial processing components that are known to contribute to neglect symptoms. First, three different spatial tasks (visual search, bisection, and visual memory) were tested in 27 patients with focal right brain-damage. Voxel-based lesion–symptom mapping was used to determine the relationships between specific sites of damage and severity of deficits in these three spatial tasks. Secondly, fMRI was used in 26 healthy controls who performed the same tasks. In the healthy group, fMRI results showed a differential activation of regions within the parietal and frontal lobes during bisection and visual search, respectively. In the patients, we confirmed a critical role of right lateral parietal cortex in bisection, but lesions in frontal and temporal lobe were more critical for visual search. These data support the existence of distinct components in spatial attentional processes that might be damaged to different degrees in neglect patients.
Numerous studies have shown that humans can successfully correct deviations to ongoing movements without being aware of them, suggesting limited conscious monitoring of visuomotor performance. Here, we ask whether such limited monitoring impairs the capacity to judiciously place confidence ratings to reflect decision accuracy (metacognitive sensitivity). To this end, we recorded functional magnetic resonance imaging data while thirty-one participants reported visuomotor cursor deviations and rated their confidence retrospectively. We show that participants use a summary statistic of the unfolding visual feedback (the maximum cursor error) to detect deviations but that this information alone is insufficient to explain detection performance. The same summary statistics is used by participants to optimally adjust their confidence ratings, even for unaware deviations. At the neural level, activity in the ventral striatum tracked high confidence, whereas a broad network including the anterior prefrontal cortex encoded cursor error but not confidence, shedding new light on a role of the anterior prefrontal cortex for action monitoring rather than confidence. Together, our results challenge the notion of limited action monitoring and uncover a new mechanism by which humans optimally monitor their movements as they unfold, even when unaware of ongoing deviations.
Immature cognition is susceptible to interference from competing information, and particularly in affectively charged situations. Several studies have reported activation in the anterior cingulate cortex, prefrontal cortex and amygdala associated with emotional conflict processing in adults but literature is lacking regarding children. Moreover, studies in children and adolescents still disagree regarding the functional activation of amygdala related to facial stimuli. In the purpose of investigating both the effect of socio-emotional stimuli and its interaction with interference control, we designed a flanker task associated with an event-related fMRI paradigm in 30 healthy children ages 9-11. In addition to happy, angry and neutral faces, we presented scrambled stimuli to examine a potential effect of faces. Regarding both brain and behavior results, no effect of emotional valence was observed. However, both results evidenced an emotional effect of faces compared with scrambled stimuli. This was expressed by faster RTs associated with increased amygdala activity and activation of the ventral ACC, in congruent trials only. When scrambled were inversely compared to faces, increased activity was observed within the lateral prefrontal cortex. Regarding the amygdala, the results suggest that in late school age children, activity in the amygdala seemed to underlie the socio-emotional effect induced by faces but not the emotional conflict. Studying brain regions involved in emotion regulation is important to further understand neurodevelopmental disorders and psychopathologies, particularly in late childhood and adolescence.
Abstract Background Metacognition refers to the ability to discriminate between one’s own correct and incorrect decisions, thus representing a key function for goal-oriented behavior. The neurobiological underpinnings of metacognition have mainly been studied in perceptual decision-making and memory-related processes; therefore, mechanisms and neural correlates underlying metacognitive processes during visuomotor actions are still poorly characterized and the specific role of confidence remains to be elucidated. This is of particular interest as deficits in goal-directed behavior and insight both are a hallmark of the negative symptoms of schizophrenia. Methods We examined 31 healthy controls who were asked to draw straight reaching trajectories towards a visual target, while measuring their brain activity with functional Magnetic Resonance Imaging (fMRI). Deviations were introduced in 70% of the trajectories seen on the screen. Participants then reported awareness of deviations (first-order), followed by (second-order) confidence in their response. The amount of deviation was titrated to reach a 71% average detection rate using an adaptive staircase procedure. Metacognition was measured using the M-Ratio, which estimates the ratio of first-order information available for confidence computation (Maniscalco & Lau, 2012). Whole brain activity was analyzed via a parametric general linear model (GLM). Results Participants showed good metacognitive abilities at evaluating the correctness of their first-order responses (M-Ratio: 0.98±0.25). Movements were decomposed into two phases based on peaks in the variance of the trajectory deviation and actual joystick position. We found that confidence ratings after deviated trials were explained by a combination of the trajectory deviation in the initial phase (p=0.006; linear mixed model) and the amount of motor correction in the final phase of the movement (p<0.001). At the neural level, as expected, conscious detection of deviation engages strongly the visual cortex, whereas higher visuomotor corrections engage primarily the primary motor cortex. Importantly, we show that high confidence specifically recruits the ventral striatum bilaterally (p<0.05 corrected for multiple comparisons), suggesting a role for confidence in motivating action. Discussion Taken together, these results show for the first time in healthy controls that confidence for visuomotor action strongly engages motivational regions in line with a key role of metacognition in goal directed behavior and accurate insight into self-performed actions. These results in healthy controls are currently being tested in a cohort of schizophrenia patients and our hypothesis is that patients with higher level of apathy will display lower metacognitive confidence and lower ventral striatum activity
Prism adaptation (PA) is one of the few rehabilitation techniques for spatial neglect that directly targets physiological mechanisms underlying space representation, but its efficacy and neural mechanisms remain unresolved. Using PA and fMRI in patients with spatial neglect after an acute right-hemispheric stroke, we previously observed post-PA increases in activity in bilateral parietal, frontal, and occipital cortex during specific visuo-spatial tasks (bisection and visual search). However, given a key role of parietal areas for PA in healthy individuals, we hypothesized that such activation might differ according to the site of brain damage. We studied a group of 10 patients with focal right hemisphere stroke and spatial neglect at baseline and after PA, who were divided in two groups (5 patients with frontal and 5 patients with parietal strokes). We compared their behavioural performance and brain activation patterns during fMRI. At the behavioural level, frontal and parietal patients showed similar neglect signs on visuo-spatial tasks before PA, but frontal patients showed larger benefit from PA. Differences were also observed in cortical activity, with enhanced recruitment of right parietal areas in frontal patients and less consistent patterns in parietal patients. Furthermore, fMRI analysis during PA itself (divided in 5 successive periods) showed differential activations between group in anatomically preserved pathways, including occipital areas and cerebellum, that preceded changes in parietal areas and were specific to frontal patients. These data accord with the hypothesis that intact cerebello-parietal connections may underpin improvement of spatial neglect after PA. Altogether, these results provide important insights on brain networks involved in spatial cognition and may allow an optimal selection of patients benefiting from PA after right hemispheric stroke.
Spatial neglect is one of the main predictors of poor functional recovery after stroke. Many therapeutic interventions have been developed to alleviate this condition, but to date the evidence of their effectiveness is still scarce. OBJECTIVE:The purpose of this study was to test whether combining prism adaptation (PA) and methylphenidate (MP) could enhance the recovery of neglect patients at a functional level. METHODS:RITAPRISM is a multicentre, randomized, double-blind, placebo-controlled study comparing PA plus placebo (control) versus PA plus MP. 24 patients were prospectively enrolled (10 in the placebo group and 14 in the MP group). RESULTS:The main result is a long-term functional improvement (on the functional independence measure (FIM) and on Bergego's scale) induced by MP combined with PA. No serious adverse event occurred. CONCLUSIONS:The long-term benefit on activities of daily living (ADL) obtained in this randomized controlled trial set this intervention apart from previous attempts and supports with a high level of evidence the value of combining PA and MP in order to improve the autonomy of neglect patients. Further studies will be needed to clarify the mechanism of this improvement. Although not specifically assessed at this stage, a part of the improvement in ADL might be related to the collateral effect of MP on mood, executive functions or fatigue, and/or the combined effect of PA and MP on motor intentional bias of neglect patients. CLASSIFICATION OF EVIDENCE:This study provides Class I evidence that adding MP to PA improves the functional outcome of neglect patients. WHO TRIAL REGISTRATION ID:EUCTR2008-000325-20-FR.
Motor conversion disorder (CD) entails genuine disturbances in the subjective experience of patients who maintain they are unable to perform a motor function, despite lack of apparent neurological damage. Abilities by which individuals assess their own capacities during performance in a task are called metacognitive, and distinctive impairment of such abilities is observed in several disorders of self-awareness such as blindsight and anosognosia. In CD, previous research has focused on the recruitment of motor and emotional brain systems, generally linking symptoms to altered limbic-motor interactions; however, metacognitive function has not been studied to our knowledge. Here we tested ten CD patients and ten age-gender matched controls during a visually-guided motor paradigm, previously employed in healthy controls (HC), allowing us to probe for motor awareness and metacognition. Participants had to draw straight trajectories towards a visual target while, unbeknownst to them, deviations were occasionally introduced in the reaching trajectory seen on the screen. Participants then reported both awareness of deviations and confidence in their response. Activity in premotor and cingulate cortex distinguished between conscious and unconscious movement corrections in controls better than patients. Critically, whereas controls engaged the left superior precuneus and middle temporal region during confidence judgments, CD patients recruited bilateral parahippocampal and amygdalo-hippocampal regions instead. These results reveal that distinct brain regions subserve metacognitive monitoring for HC and CD, pointing to different mechanisms and sources of information used to monitor and form confidence judgments of motor performance. While brain systems involved in sensory-motor integration and vision are more engaged in controls, CD patients may preferentially rely on memory and contextual associative processing, possibly accounting for how affect and memories can imbue current motor experience in these patients.
Impairment in mental flexibility may be a key component contributing to cardinal cognitive symptoms among mood disorders patients, particularly thought control disorders. Impaired ability to switch from one thought to another might reflect difficulties in either generating new mental states, inhibiting previous states, or both. However, the neural underpinnings of impaired cognitive flexibility in mood disorders remain largely unresolved. We compared a group of mood disorders patients ( n = 29) and a group of matched healthy subjects ( n = 32) on a novel task‐switching paradigm involving happy and sad faces, that allowed us to separate generation of a new mental set (Switch Cost) and inhibition of the previous set during switching (Inhibition Cost), using fMRI. Behavioral data showed a larger Switch Cost in patients relative to controls, but the average Inhibition Cost did not differ between groups. At the neural level, a main effect of group was found with stronger activation of the subgenual cingulate cortex in patients. The larger Switch Cost in patients was reflected by a stronger recruitment of brain regions involved in attention and executive control, including the left intraparietal sulcus, precuneus, left inferior fontal gyrus, and right anterior cingulate. Critically, activity in the subgenual cingulate cortex was not downregulated by inhibition in patients relative to controls. In conclusion, mood disorder patients have exaggerated Switch Cost relative to controls, and this deficit in cognitive flexibility is associated with increased activation of the fronto‐parietal attention networks, combined with impaired modulation of the subgenual cingulate cortex when inhibition of previous mental states is needed. Hum Brain Mapp 37:1335‐1348, 2016 . © 2016 Wiley Periodicals, Inc.
OBJECTIVES:Thought disorders such as rumination or flight of ideas are frequent in patients with mood disorders, and not systematically linked to mood state. These symptoms point to anomalies in cognitive processes mediating the generation and control of thoughts; for example, associative thinking and inhibition. However, their neural substrates are not known.METHOD:To obtain an ecological measure of neural processes underlying the generation and suppression of spontaneous thoughts, we designed a free word association task during fMRI allowing us to explore verbal associative patterns in patients with mood disorders and matched controls. Participants were presented with emotionally negative, positive or neutral words, and asked to produce two words either related or unrelated to these stimuli.RESULTS:Relative to controls, patients produced a reverse pattern of answer typicality for the related vs unrelated conditions. Controls activated larger semantic and executive control networks, as well as basal ganglia, precuneus and middle frontal gyrus. Unlike controls, patients activated fusiform gyrus, parahippocampal gyrus and medial prefrontal cortex for emotional stimuli.CONCLUSIONS:Mood disorder patients are impaired in automated associative processes, but prone to produce more unique/personal associations through activation of memory and self-related areas.
Le développement de nouveaux outils d’imagerie a permis de confirmer les intuitions des aliénistes du milieu du xixe siècle qui, avant Charcot, avaient introduit le concept de lésion fonctionnelle appliqué aux névroses et notamment à l’hystérie. Le déficit moteur conversif a été plus particulièrement étudié au cours de ces dernières années. Les mécanismes à l’origine de ce déficit apparaissent distincts de ceux mis en jeu chez le sujet sain simulateur et pourraient être expliqués par une activité excessive d’imagerie motrice qui n’est pas mise au repos lors de l’exécution du mouvement. Cette activité excessive pourrait notamment mettre en jeu de façon anormale le cortex préfrontal et le précuneus. Une perturbation des régulations émotionnelles, impliquant le cortex cingulaire antérieur et l’amygdale, pourrait également influencer négativement l’exécution motrice. L’intérêt de ces explorations est illustré à travers l’étude d’un patient qui présente de façon conjointe un déficit sensori-moteur de l’hémicorps gauche, des mouvements dystoniques et un syndrome d’héminégligence sans lésion morphologique. Ce cas montre la nécessité de prendre en compte la singularité de chaque situation comme l’évolution des symptômes dans le temps. La question du passage à l’organicité d’une lésion fonctionnelle est également posée tout comme celle de faire évoluer la rééducation et la prise en charge thérapeutique à la lumière de ces nouvelles données.
•Unlike for perception, metacognition of visuomotor (VM) performance is understudied.•Subjects performed a VM-conflict-detection task then rated confidence in their judgment.•Distinct brain regions for VM performance and metacognition of VM performance.•The right anterior insula and prefrontal areas are implicated in VM metacognition.
Initial research shows that mindfulness training can enhance attention and modulate the affective response. However, links between mindfulness and language processing remain virtually unexplored despite the prominent role of overt and silent negative ruminative speech in depressive and anxiety-related symptomatology. Here, we measured dispositional mindfulness and recorded participants’ event-related brain potential responses to positive and negative target words preceded by words congruent or incongruent with the targets in terms of semantic relatedness and emotional valence. While the low mindfulness group showed similar N400 effect pattern for positive and negative targets, high dispositional mindfulness was associated with larger N400 effect to negative targets. This result suggests that negative meanings are less readily accessible in people with high dispositional mindfulness. Furthermore, high dispositional mindfulness was associated with reduced P600 amplitudes to emotional words, suggesting less post-analysis and attentional effort which possibly relates to a lower inclination to ruminate. Overall, these findings provide initial evidence on associations between modifications in language systems and mindfulness.
Theoretical models of hypnosis have emphasized the importance of attentional processes in accounting for hypnotic phenomena but their exact nature and brain substrates remain unresolved. Individuals vary in their susceptibility to hypnosis, a variability often attributed to differences in attentional functioning such as greater ability to filter irrelevant information and inhibit prepotent responses. However, behavioral studies of attentional performance outside the hypnotic state have provided conflicting results. We used fMRI to investigate the recruitment of attentional networks during a modified flanker task in High and Low hypnotizable participants. The task was performed in a normal (no hypnotized) state. While behavioral performance did not reliably differ between groups, components of the fronto-parietal executive network implicated in monitoring (anterior cingulate cortex; ACC), adjustment (lateral prefrontal cortex; latPFC), and implementation of attentional control (intraparietal sulcus; IPS) were differently activated depending on the hypnotizability of the subjects: the right inferior frontal gyrus (rIFG) was more recruited, whereas IPS and ACC were less recruited by High susceptible individuals compared to Low. Our results demonstrate that susceptibility to hypnosis is associated with particular executive control capabilities allowing efficient attentional focusing, and point to specific neural substrates in right prefrontal cortex.Significance statement: We demonstrated that outside hypnosis, low hypnotizable subjects recruited more parietal cortex and anterior cingulate regions during selective attention conditions suggesting a better detection and implementation of conflict. However, outside hypnosis the right inferior frontal gyrus (rIFG) was more recruited by highly hypnotizable subjects during selective attention conditions suggesting a better control of conflict. Furthermore, in highly hypnotizable subjects this region was more connected to the default mode network suggesting a tight dialogue between internally and externally driven processes that may permit higher flexibility in attention and underlie a greater ability to dissociate. (C) 2015 Elsevier Inc. All rights reserved.
To study emotional reactions to music, it is important to consider the temporal dynamics of both affective responses and underlying brain activity. Here, we investigated emotions induced by music using functional magnetic resonance imaging (fMRI) with a data-driven approach based on intersubject correlations (ISC). This method allowed us to identify moments in the music that produced similar brain activity (i.e. synchrony) among listeners under relatively natural listening conditions. Continuous ratings of subjective pleasantness and arousal elicited by the music were also obtained for the music outside of the scanner. Our results reveal synchronous activations in left amygdala, left insula and right caudate nucleus that were associated with higher arousal, whereas positive valence ratings correlated with decreases in amygdala and caudate activity. Additional analyses showed that synchronous amygdala responses were driven by energy-related features in the music such as root mean square and dissonance, while synchrony in insula was additionally sensitive to acoustic event density. Intersubject synchrony also occurred in the left nucleus accumbens, a region critically implicated in reward processing. Our study demonstrates the feasibility and usefulness of an approach based on ISC to explore the temporal dynamics of music perception and emotion in naturalistic conditions.
Le développement de nouveaux outils d’imagerie a permis de confirmer les intuitions des aliénistes du milieu du xixe siècle qui, avant Charcot, avaient introduit le concept de lésion fonctionnelle appliqué aux névroses et notamment à l’hystérie. Le déficit moteur conversif a été plus particulièrement étudié au cours de ces dernières années. Les mécanismes à l’origine de ce déficit apparaissent distincts de ceux mis en jeu chez le sujet sain simulateur et pourraient être expliqués par une activité excessive d’imagerie motrice qui n’est pas mise au repos lors de l’exécution du mouvement. Cette activité excessive pourrait notamment mettre en jeu de façon anormale le cortex préfrontal et le précuneus. Une perturbation des régulations émotionnelles, impliquant le cortex cingulaire antérieur et l’amygdale, pourrait également influencer négativement l’exécution motrice. L’intérêt de ces explorations est illustré à travers l’étude d’un patient qui présente de façon conjointe un déficit sensori-moteur de l’hémicorps gauche, des mouvements dystoniques et un syndrome d’héminégligence sans lésion morphologique. Ce cas montre la nécessité de prendre en compte la singularité de chaque situation comme l’évolution des symptômes dans le temps. La question du passage à l’organicité d’une lésion fonctionnelle est également posée tout comme celle de faire évoluer la rééducation et la prise en charge thérapeutique à la lumière de ces nouvelles données. Recent progress in functional imagery confirmed the intuition of the 19th century French alienists who introduced, before Charcot, the concept of “functional lesion” applied to hysterical conversion. Neural mechanism underlying conversion paralysis has been more particularly studied in recent years using these new tools. Distinct patterns of brain activation have been elicited in healthy subjects simulating weakness and conversion paralysis. Several brain areas are over-activated in conversion paralysis when compared to healthy subjects: prefrontal cortex, precuneus, anterior cingulate cortex, amygdala. These results, not only confirm that conversion must be distinguished from malingering, they also provide new insights on the neural mechanisms of conversion paralysis. The activation of regions associated to the default mode network such as the precuneus and the ventral prefrontal cortex could reflect an increase in self-monitoring or motor imagery. The involvement of limbic regions like the anterior cingulate cortex and the amygdala suggest disturbed influence of emotional processes over motor execution. In the second part of this study, we report the results of brain structural and functional explorations performed in a case of chronic left conversion paralysis. The abnormal involvement of the precuneus is discussed together with the possible transition from functional to organic lesion in chronic paralysis. Simultaneous presence of sensory impairment and more remarkably left spatial neglect emphasize the singularity of each case and the necessary caution that should be taken for the interpretation of brain images. From a therapeutic point of view, these data could provide some new theoretical basis for rehabilitation and the use of brain stimulation techniques.
The tendency to ruminate, experienced by both healthy individuals and depressed patients, can be quantified by the Ruminative Response Scale (RRS). We hypothesized that brain activity associated with rumination tendency might not only occur at rest but also persist to some degree during a cognitive task. We correlated RRS with whole-brain fMRI data of 20 healthy subjects during rest and during a face categorization task with different levels of cognitive demands (easy or difficult conditions). Our results reveal that the more subjects tend to ruminate, the more they activate the left entorhinal region, both at rest and during the easy task condition, under low attentional demands. Conversely, lower tendency to ruminate correlates with greater activation of visual cortex during rest and activation of insula during the easy task condition. These results indicate a particular neural marker of the tendency to ruminate, corresponding to increased spontaneous activity in memory-related areas, presumably reflecting more internally driven trains of thoughts even during a concomitant task. Conversely, people who are not prone to ruminate show more externally driven activity.
INTRODUCTION:The functional neuroanatomy of the egocentric and allocentric representations of space remains poorly studied with neuroimaging. Here we aim to determine brain structures subserving two different kinds of spatial representations centred on the main axis of either the body or the external scene. METHOD:Sixteen healthy participants evaluated the alignment of a bar relative to the middle of their body (Ego) or relative to another stimulus (Allo) during functional MRI. In a control task (Ctrl), they had to judge the colour of the bar. RESULTS:Correct response rates and response times were similar in the three tasks. fMRI data revealed a predominant role of the right hemisphere in the egocentric task (Ego vs. Allo): selective activity was found in the occipital, superior parietal, and inferior frontal cortices, as well as in the precuneus and supplementary motor area. On the left side, the insula, thalamus, and cerebellum were also activated. Conversely, the allocentric task (Allo vs. Ctrl) showed selective activity centred on the left temporal gyrus. DISCUSSION:This study demonstrates a right hemisphere dominance for representations centred on the longitudinal body axis, but more left-sided activity for scene/object-centred representations of space. These new data shed light on the unique role of several regions involved in spatial perception and help better understand spatial deficits in patients with right hemispheric lesions.
Unilateral spatial neglect involves a failure to report or orient to stimuli in the contralesional (left) space due to right brain damage, with severe handicap in everyday activities and poor rehabilitation outcome. Because behavioral studies suggest that prism adaptation may reduce spatial neglect, we investigated the neural mechanisms underlying prism effects on visuo-spatial processing in neglect patients. We used functional magnetic resonance imaging (fMRI) to examine the effect of (right-deviating) prisms on seven patients with left neglect, by comparing brain activity while they performed three different spatial tasks on the same visual stimuli (bisection, search, and memory), before and after a single prism-adaptation session. Following prism adaptation, fMRI data showed increased activation in bilateral parietal, frontal, and occipital cortex during bisection and visual search, but not during the memory task. These increases were associated with significant behavioral improvement in the same two tasks. Changes in neural activity and behavior were seen only after prism adaptation, but not attributable to mere task repetition. These results show for the first time the neural substrates underlying the therapeutic benefits of prism adaptation, and demonstrate that visuo-motor adaptation induced by prism exposure can restore activation in bilateral brain networks controlling spatial attention and awareness. This bilateral recruitment of fronto-parietal networks may counteract the pathological biases produced by unilateral right hemisphere damage, consistent with recent proposals that neglect may reflect lateralized deficits induced by bilateral hemispheric dysfunction.