Social facilitation and bilingual cognitive advantage: Bridging social psychology and psycholinguistics.

This study examined the role of social context in the expression of the bilingual cognitive advantage in 145 bilingual university students. All participants mastered Arabic as their native language (L1), but half were highly proficient in French (high L2 group), whereas half were less proficient (low L2 group). A color-word Stroop test with incongruent, congruent and neutral stimuli was administered in single language blocks (Arabic or French words) or in a mixed block (Arabic and French words), either under social presence, or alone. Stroop interference was analyzed to assess the cost of resolving conflict in incongruent trials and was compared across groups and experimental conditions. If bilingualism comes with a cognitive advantage, a reduction of interference in high (vs. low) L2 proficient subjects is to be expected. Analysis revealed that interference was significantly reduced in high L2 group, but only under the single language condition. Furthermore, whereas social context and sex had no main effects, analysis revealed a significant 4-factor interaction between L2 proficiency, linguistic context, social context, and sex. Social presence further reduced interference (social facilitation) in high L2 proficient females, but not in males. Overall, the results suggest that mastering a second language comes with cognitive advantages which adapt dynamically to social and linguistic contexts in a sex-dependent manner. We argue that advancing bilingualism research requires more attention to the social environment.

Emotion processing in Parkinson's disease: a blood oxygenation level-dependent functional magnetic resonance imaging study.

Parkinson's disease is a neurodegenerative disorder caused by loss of dopamine neurons in the substantia nigra pars compacta. Tremor, rigidity, and bradykinesia are the major symptoms of the disease. These motor impairments are often accompanied by affective and emotional dysfunctions which have been largely studied over the last decade. The aim of this study was to investigate emotional processing organization in the brain of patients with Parkinson's disease and to explore whether there are differences between recognition of different types of emotions in Parkinson's disease. We examined 18 patients with Parkinson's disease (8 men, 10 women) with no history of neurological or psychiatric comorbidities. All these patients underwent identical brain blood oxygenation level-dependent functional magnetic resonance imaging for emotion evaluation. Blood oxygenation level-dependent functional magnetic resonance imaging results revealed that the occipito-temporal cortices, insula, orbitofrontal cortex, basal ganglia, and parietal cortex which are involved in emotion processing, were activated during the functional control. Additionally, positive emotions activate larger volumes of the same anatomical entities than neutral and negative emotions. Results also revealed that Parkinson's disease associated with emotional disorders are increasingly recognized as disabling as classic motor symptoms. These findings help clinical physicians to recognize the emotional dysfunction of patients with Parkinson's disease.

Role of Anterior Cingulate Cortex in Instrumental Learning: Blockade of Dopamine D1 Receptors Suppresses Overt but Not Covert Learning.

HIGHLIGHTS Blockade of dopamine D1 receptors in ACC suppressed instrumental learning when overt responding was required.Covert learning through observation was not impaired.After treatment with a dopamine antagonist, instrumental learning recovered but not the rat's pretreatment level of effort tolerance.ACC dopamine is not necessary for acquisition of task-relevant cues during learning, but regulates energy expenditure and effort based decision. Dopamine activity in anterior cingulate cortex (ACC) is essential for various aspects of instrumental behavior, including learning and effort based decision making. To dissociate learning from physical effort, we studied both observational (covert) learning, and trial-and-error (overt) learning. If ACC dopamine activity is required for task acquisition, its blockade should impair both overt and covert learning. If dopamine is not required for task acquisition, but solely for regulating the willingness to expend effort for reward, i.e., effort tolerance, blockade should impair overt learning but spare covert learning. Rats learned to push a lever for food rewards either with or without prior observation of an expert conspecific performing the same task. Before daily testing sessions, the rats received bilateral ACC microinfusions of SCH23390, a dopamine D1 receptor antagonist, or saline-control infusions. We found that dopamine blockade suppressed overt responding selectively, leaving covert task acquisition through observational learning intact. In subsequent testing sessions without dopamine blockade, rats recovered their overt-learning capacity but not their pre-treatment level of effort tolerance. These results suggest that ACC dopamine is not required for the acquisition of conditioned behaviors and that apparent learning impairments could instead reflect a reduced level of willingness to expend effort due to cortical dopamine blockade.

Social and asocial prefrontal cortex neurons: a new look at social facilitation and the social brain.

A fundamental aspect of behavior in many animal species is 'social facilitation', the positive effect of the mere presence of conspecifics on performance. To date, the neuronal counterpart of this ubiquitous phenomenon is unknown. We recorded the activity of single neurons from two prefrontal cortex regions, the dorsolateral part and the anterior cingulate cortex in monkeys as they performed a visuomotor task, either in the presence of a conspecific (Presence condition) or alone. Monkeys performed better in the presence condition than alone (social facilitation), and analyses of outcome-related activity of 342 prefrontal neurons revealed that most of them (86%) were sensitive to the performance context. Two populations of neurons were discovered: 'social neurons', preferentially active under social presence and 'asocial neurons', preferentially active under social isolation. The activity of these neurons correlated positively with performance only in their preferred context (social neurons under social presence; asocial neurons under social isolation), thereby providing a potential neuronal mechanism of social facilitation. More generally, the fact that identical tasks recruited either social or asocial neurons depending on the presence or absence of a conspecific also brings a new look at the social brain hypothesis.

Learning by observation in the macaque monkey under high experimental constraints.

While neuroscience research has tremendously advanced our knowledge about the neural mechanisms of individual learning, i.e. through trial-and-error, it is only recently that neuroscientists have begun to study observational learning, and thus little is known about its neural mechanisms. One limitation is that observational learning has been addressed under unconstrained experimental conditions, not compatible with neuronal recordings. This study examined observational learning in macaque monkeys under the constraining conditions of behavioral neurophysiology. Two animals sat in primate chairs facing each other, with their head fixed. A touch screen was placed face up between the chairs at arm's reach, and the monkeys were trained on an abstract visuomotor associative task. In one experiment, the monkeys alternated the roles of "actor" and "observer". The actor learned to associate visual cues with reaching targets, while the observer "watched" freely. Then, the observer was given the same cue-target associations just performed by the actor, or had to learn new, not previously observed ones. The results show that learning performance is better after observation. In experiment 2, one monkey learned from a human actor who performed the task with errors only, or with successes only in separate blocks. The monkey's gain in performance was higher after observation of errors than after successes. The findings suggest that observational learning can occur even under highly constraining conditions, and open the way for investigating the neuronal correlates of social learning using the methods of behavioral neurophysiology.

Neurophysiological correlates of visuo-motor learning through mental and physical practice.

We have previously shown that mental rehearsal can replace up to 75% of physical practice for learning a visuomotor task (Allami, Paulignan, Brovelli, & Boussaoud, (2008). Experimental Brain Research, 184, 105-113). Presumably, mental rehearsal must induce brain changes that facilitate motor learning. We tested this hypothesis by recording scalp electroencephalographic activity (EEG) in two groups of subjects. In one group, subjects executed a reach to grasp task for 240 trials. In the second group, subjects learned the task through a combination of mental rehearsal for the initial 180 trials followed by the execution of 60 trials. Thus, one group physically executed the task for 240 trials, the other only for 60 trials. Amplitudes and latencies of event-related potentials (ERPs) were compared across groups at different stages during learning. We found that ERP activity increases dramatically with training and reaches the same amplitude over the premotor regions in the two groups, despite large differences in physically executed trials. These findings suggest that during mental rehearsal, neuronal changes occur in the motor networks that make physical practice after mental rehearsal more effective in configuring functional networks for skilful behaviour.

Vicarious neural processing of outcomes during observational learning.

Learning what behaviour is appropriate in a specific context by observing the actions of others and their outcomes is a key constituent of human cognition, because it saves time and energy and reduces exposure to potentially dangerous situations. Observational learning of associative rules relies on the ability to map the actions of others onto our own, process outcomes, and combine these sources of information. Here, we combined newly developed experimental tasks and functional magnetic resonance imaging (fMRI) to investigate the neural mechanisms that govern such observational learning. Results show that the neural systems involved in individual trial-and-error learning and in action observation and execution both participate in observational learning. In addition, we identified brain areas that specifically activate for others' incorrect outcomes during learning in the posterior medial frontal cortex (pMFC), the anterior insula and the posterior superior temporal sulcus (pSTS).

Social learning as a way to overcome choice-induced preferences? Insights from humans and rhesus macaques.

Much theoretical attention is currently devoted to social learning. Yet, empirical studies formally comparing its effectiveness relative to individual learning are rare. Here, we focus on free choice, which is at the heart of individual reward-based learning, but absent in social learning. Choosing among two equally valued options is known to create a preference for the selected option in both humans and monkeys. We thus surmised that social learning should be more helpful when choice-induced preferences retard individual learning than when they optimize it. To test this prediction, the same task requiring to find which among two items concealed a reward was applied to rhesus macaques and humans. The initial trial was individual or social, rewarded or unrewarded. Learning was assessed on the second trial. Choice-induced preference strongly affected individual learning. Monkeys and humans performed much more poorly after an initial negative choice than after an initial positive choice. Comparison with social learning verified our prediction. For negative outcome, social learning surpassed or at least equaled individual learning in all subjects. For positive outcome, the predicted superiority of individual learning did occur in a majority of subjects (5/6 monkeys and 6/12 humans). A minority kept learning better socially though, perhaps due to a more dominant/aggressive attitude toward peers. Poor learning from errors due to over-valuation of personal choices is among the decision-making biases shared by humans and animals. The present study suggests that choice-immune social learning may help curbing this potentially harmful tendency. Learning from successes is an easier path. The present data suggest that whether one tends to walk it alone or with a peer's help might depend on the social dynamics within the actor/observer dyad.

Insight in schizophrenia: from conceptualization to neuroscience.

Lack of insight into illness is a prevalent and distinguishing feature of schizophrenia, which has a complex history and has been given a variety of definitions. Currently, insight is measured and treated as a multidimensional phenomenon, because it is believed to result from psychological, neuropsychological and organic factors. Thus, schizophrenia patients may display dramatic disorders including demoralization, depression and a higher risk of suicide, all of which are directly or indirectly related to a lack of insight into their illness, and make the treatment difficult. To improve the treatment of people with schizophrenia, it is thus crucial to advance research on insight into their illness. Insight is studied in a variety of ways. Studies may focus on the relationship between insight and psychopathology, may view behavioral outcomes or look discretely at the cognitive dysfunction versus anatomy level of insight. All have merit but they are dispersed across a wide body of literature and rarely are the findings integrated and synthesized in a meaningful way. The aim of this study was to synthesize findings across the large body of literature dealing with insight, to highlight its multidimensional nature, measurement, neuropsychology and social impact in schizophrenia. The extensive literature on the cognitive consequences of lack of insight and the contribution of neuroimaging techniques to elucidating neurological etiology of insight deficits, is also reviewed.

Advanced Parkinson's disease effect on goal-directed and habitual processes involved in visuomotor associative learning.

The present behavioral study re-addresses the question of habit learning in Parkinson's disease (PD). Patients were early onset, non-demented, dopa-responsive, candidates for surgical treatment, similar to those we found earlier as suffering greater dopamine depletion in the putamen than in the caudate nucleus. The task was the same conditional associative learning task as that used previously in monkeys and healthy humans to unveil the striatum involvement in habit learning. Sixteen patients and 20 age- and education-matched healthy control subjects learned sets of 3 visuo-motor associations between complex patterns and joystick displacements during two testing sessions separated by a few hours. We distinguished errors preceding vs. following the first correct response to compare patients' performance during the earliest phase of learning dominated by goal-directed actions with that observed later on, when responses start to become habitual. The disease significantly retarded both learning phases, especially in patients under 60 years of age. However, only the late phase deficit was disease severity-dependent and persisted on the second testing session. These findings provide the first corroboration in Parkinson patients of two ideas well-established in the animal literature. The first is the idea that associating visual stimuli to motor acts is a form of habit learning that engages the striatum. It is confirmed here by the global impairment in visuo-motor learning induced by PD. The second idea is that goal-directed behaviors are predominantly caudate-dependent whereas habitual responses are primarily putamen-dependent. At the advanced PD stages tested here, dopamine depletion is greater in the putamen than in the caudate nucleus. Accordingly, the late phase of learning corresponding to the emergence of habitual responses was more vulnerable to the disease than the early phase dominated by goal-directed actions.

Multivoxel pattern analysis for FMRI data: a review.

Functional magnetic resonance imaging (fMRI) exploits blood-oxygen-level-dependent (BOLD) contrasts to map neural activity associated with a variety of brain functions including sensory processing, motor control, and cognitive and emotional functions. The general linear model (GLM) approach is used to reveal task-related brain areas by searching for linear correlations between the fMRI time course and a reference model. One of the limitations of the GLM approach is the assumption that the covariance across neighbouring voxels is not informative about the cognitive function under examination. Multivoxel pattern analysis (MVPA) represents a promising technique that is currently exploited to investigate the information contained in distributed patterns of neural activity to infer the functional role of brain areas and networks. MVPA is considered as a supervised classification problem where a classifier attempts to capture the relationships between spatial pattern of fMRI activity and experimental conditions. In this paper , we review MVPA and describe the mathematical basis of the classification algorithms used for decoding fMRI signals, such as support vector machines (SVMs). In addition, we describe the workflow of processing steps required for MVPA such as feature selection, dimensionality reduction, cross-validation, and classifier performance estimation based on receiver operating characteristic (ROC) curves.

Differential roles of caudate nucleus and putamen during instrumental learning.

The dorsal striatum is crucial for the acquisition and consolidation of instrumental behaviour, but the underlying computations and internal dynamics remain elusive. To address this issue, we combined a model of key computations supporting decision-making during instrumental learning with human behavioural and functional magnetic resonance imaging (fMRI) data. The results showed that the associative and sensorimotor dorsal striatum host complementary computations that, we suggest, may differentially support goal-directed and habitual processes. The anterior caudate nucleus integrates information about performance and cognitive control demands, whereas the putamen tracks how likely the conditioning stimuli lead to correct response. Contrary to current models, the putamen is recruited during initial acquisition. As the exploratory phase proceeds, the relative contribution of the caudate nucleus becomes dominant over the putamen. During early consolidation, caudate nucleus and putamen settle to asymptotic values and share control. We then investigated how dorsal striatal computations may affect decision-making. We found that portion of reaction times' variance parallels the combined cost associated with the dorsal striatal computations. Overall, our findings provide a deeper insight into the functional heterogeneity within the dorsal striatum and suggest that the dynamic interplay between caudate nucleus and putamen, rather than their serial recruitment, underlies the acquisition and early consolidation of instrumental behaviours.

Hand modulation of visual, preparatory, and saccadic activity in the monkey frontal eye field.

Behavioral studies have shown that hand position influences saccade characteristics. This study examined the neuronal changes that could underlie this behavioral observation. Single neurons were recorded in the frontal eye field (FEF) of 2 monkeys as they executed a visually guided saccade task, while holding their hand at given locations on a touch screen. The task was performed with the hand either visible or invisible, in order to assess the relative contribution of visual and proprioceptive information on hand position. Among the 224 neurons tested, the visual, saccadic and/or preparatory activity of more than half of them was modulated by hand position, whether the hand was visible or invisible. Comparison of lower (hand's workspace) and upper (out of reach) visual targets showed that hand modulation was predominant in the hand's workspace. Finally, some cells preferred congruency of hand and target in space, others preferred incongruency. Interestingly, hand modulation of saccadic activity correlated with hand position effects on saccade reaction times. We conclude that visual and proprioceptive signals derived from the hand are integrated by FEF neurons. These signals can modulate target selection through attention and allow the oculomotor system to use hand-related somatosensory signals for the initiation of visually guided saccades.

I learned from what you did: Retrieving visuomotor associations learned by observation.

Observational learning allows individuals to acquire knowledge without incurring in the costs and risks of discovering and testing. The neural mechanisms mediating the retrieval of rules learned by observation are currently unknown. To explore this fundamental cognitive ability, we compared the brain responses when retrieving visuomotor associations learned either by observation or by individual learning. To do so, we asked eleven adults to learn two sets of arbitrary visuomotor associations: one set was learned through the observation of an expert actor while the other was learned by trial and error. During fMRI scanning, subjects were requested to retrieve the visuomotor associations previously learned under the two modalities. The conjunction analysis between the two learning conditions revealed a common brain network that included the ventral and dorsal lateral prefrontal cortices, the superior parietal lobe and the pre-SMA. This suggests the existence of a mirror-like system responsible for the storage of rules learned either by trial and error or by observation of others' actions. In addition, the pars triangularis in the right prefrontal cortex (BA45) was found to be selective for rules learned by observation. This suggests a preferential role of this area in the storage of rules learned in a social context.

Hand position affects saccadic reaction times in monkeys and humans.

In daily life, activities requiring the hand and eye to work separately are as frequent as activities requiring tight eye-hand coordination, and we effortlessly switch from one type of activity to the other. Such flexibility is unlikely to be achieved without each effector "knowing" where the other one is at all times, even when it is static. Here, we provide behavioral evidence that the mere position of the static hand affects one eye movement parameter: saccadic reaction time. Two monkeys were trained and 11 humans instructed to perform nondelayed or delayed visually guided saccades to either a right or a left target while holding their hand at a location either near or far from the eye target. From trial to trial, target locations and hand positions varied pseudorandomly. Subjects were tested both when they could and when they could not see their hand. The main findings are 1) the presence of the static hand in the workspace did affect saccade initiation; 2) this interaction persisted when the hand was invisible; 3) it was strongly influenced by the delay duration: hand-target proximity retarded immediate saccades, whereas it could hasten delayed saccades; and 4) this held true both for humans and for each of the two monkeys. We propose that both visual and nonvisual hand position signals are used by the primates' oculomotor system for the planning and execution of saccades, and that this may result in a hand-eye competition for spatial attentional resources that explains the delay-dependent reversal observed.

Understanding the neural computations of arbitrary visuomotor learning through fMRI and associative learning theory.

Associative theory postulates that learning the consequences of our actions in a given context is represented in the brain as stimulus-response-outcome associations that evolve according to prediction-error signals (the discrepancy between the observed and predicted outcome). We tested the theory on brain functional magnetic resonance imaging data acquired from human participants learning arbitrary visuomotor associations. We developed a novel task that systematically manipulated learning and induced highly reproducible performances. This granted the validation of the model-based results and an in-depth analysis of the brain signals in representative single trials. Consistent with the Rescorla-Wagner model, prediction-error signals are computed in the human brain and selectively engage the ventral striatum. In addition, we found evidence of computations not formally predicted by the Rescorla-Wagner model. The dorsal fronto-parietal network, the dorsal striatum, and the ventrolateral prefrontal cortex are activated both on the incorrect and first correct trials and may reflect the processing of relevant visuomotor mappings during the early phases of learning. The left dorsolateral prefrontal cortex is selectively activated on the first correct outcome. The results provide quantitative evidence of the neural computations mediating arbitrary visuomotor learning and suggest new directions for future computational models.

Visuo-motor learning with combination of different rates of motor imagery and physical practice.

Sports psychology suggests that mental rehearsal facilitates physical practice in athletes and clinical rehabilitation attempts to use mental rehearsal to restore motor function in hemiplegic patients. Our aim was to examine whether mental rehearsal is equivalent to physical learning, and to determine the optimal proportions of real execution and rehearsal. Subjects were asked to grasp an object and insert it into an adapted slot. One group (G0) practiced the task only by physical execution (240 trials); three groups imagined performing the task in different rates of trials (25%, G25; 50%, G50; 75%, G75), and physically executed movements for the remaining trials; a fourth, control group imagined a visual rotation task in 75% of the trials and then performed the same motor task as the others groups. Movement time (MT) was compared for the first and last physical trials, together with other key trials, across groups. All groups learned, suggesting that mental rehearsal is equivalent to physical motor learning. More importantly, when subjects rehearsed the task for large numbers of trials (G50 and G75), the MT of the first executed trial was significantly shorter than the first executed trial in the physical group (G0), indicating that mental practice is better than no practice at all. Comparison of the first executed trial in G25, G50 and G75 with the corresponding trials in G0 (61, 121 and 181 trials), showed equivalence between mental and physical practice. At the end of training, the performance was much better with high rates of mental practice (G50/G75) compared to physical practice alone (G0), especially when the task was difficult. These findings confirm that mental rehearsal can be beneficial for motor learning and suggest that imagery might be used to supplement or partly replace physical practice in clinical rehabilitation.

Hand position modulates saccadic activity in the frontal eye field.

Recent neurophysiological studies have begun to uncover the neuronal correlates of eye hand coordination. This study was designed to test whether the frontal eye field (FEF) saccadic activity is modulated by hand position. Single neurons were recorded in two macaque monkeys performing visually guided saccades while holding their hand at given locations on a touchscreen. To determine the relative contributions of hand vision and its proprioception, monkeys executed the task with or without vision of the hand. We found that saccadic activity of more than half of the neuronal sample (54%; n=130) was dependent on hand position relative to the saccade end point. Both visual and proprioceptive signals contributed to this modulation. These data demonstrate that the oculomotor function of the FEF takes into account hand position in space.

Estimating the hidden learning representations.

Successful adaptation relies on the ability to learn the consequence of our actions in different environments. However, understanding the neural bases of this ability still represents one of the great challenges of system neuroscience. In fact, the neuronal plasticity changes occurring during learning cannot be fully controlled experimentally and their evolution is hidden. Our approach is to provide hypotheses about the structure and dynamics of the hidden plasticity changes using behavioral learning theory. In fact, behavioral models of animal learning provide testable predictions about the hidden learning representations by formalizing their relation with the observables of the experiment (stimuli, actions and outcomes). Thus, we can understand whether and how the predicted learning processes are represented at the neural level by estimating their evolution and correlating them with neural data. Here, we present a bayesian model approach to estimate the evolution of the internal learning representations from the observations of the experiment (state estimation), and to identify the set of models' parameters (parameter estimation) and the class of behavioral model (model selection) that are most likely to have generated a given sequence of actions and outcomes. More precisely, we use Sequential Monte Carlo methods for state estimation and the maximum likelihood principle (MLP) for model selection and parameter estimation. We show that the method recovers simulated trajectories of learning sessions on a single-trial basis and provides predictions about the activity of different categories of neurons that should participate in the learning process. By correlating the estimated evolutions of the learning variables, we will be able to test the validity of different models of instrumental learning and possibly identify the neural bases of learning.

Learning by observation in rhesus monkeys.

Habit memory provides us with a vast repertoire of learned rules, including stimulus-reward associations, that ensures fast and adapted decision making in daily life. Because we share this ability with monkeys, lesion and recording studies in rhesus macaques have played a key role in understanding the neural bases of individual trial-and-error habit learning. Humans, however, can learn new rules at a lower cost via observation of conspecifics. The neural properties underlying this more ecological form of habit learning remain unexplored, and it is unclear whether the rhesus macaque can be a useful model in this endeavor. We addressed this issue by testing four monkeys from the same social group in their usual semi-natural habitat using a well-established marker of habit memory, concurrent discrimination learning. Each monkey learned 24 lists of 10 object-reward associations each. For one list out of two, monkeys could observe the testing session of another member of the group prior to being tested with the same list themselves. Learning was faster for these lists than for those learned solely by trial-and-error. Errors to criterion (9/10 correct responses) were reduced by 39%, and faultless performance could be achieved for up to 5 of the 10 pairs. These data demonstrate that rhesus macaques spontaneously observe a conspecific learning new stimulus-reward associations, and substantially benefit from this observation. They ascertain that the neural underpinnings of socially-mediated forms of habit learning can be explored using the powerful tools of monkey research, including neurophysiological recordings.