Esteban Hurtado

Motor-language coupling: direct evidence from early Parkinson’s disease and intracranial cortical recordings

Language and action systems are functionally coupled in the brain as demonstrated by converging evidence using Functional magnetic resonance imaging (fMRI), electroencephalography (EEG), transcranial magnetic stimulation (TMS), and lesion studies. In particular, this coupling has been demonstrated using the action-sentence compatibility effect (ACE) in which motor activity and language interact. The ACE task requires participants to listen to sentences that described actions typically performed with an open hand (e.g., clapping), a closed hand (e.g., hammering), or without any hand action (neutral); and to press a large button with either an open hand position or closed hand position immediately upon comprehending each sentence. The ACE is defined as a longer reaction time (RT) in the action-sentence incompatible conditions than in the compatible conditions. Here we investigated direct motor-language coupling in two novel and uniquely informative ways. First, we measured the behavioural ACE in patients with motor impairment (early Parkinsons disease - EPD), and second, in epileptic patients with direct electrocorticography (ECoG) recordings. In experiment 1, EPD participants with preserved general cognitive repertoire, showed a much diminished ACE relative to non-EPD volunteers. Moreover, a correlation between ACE performance and action-verb processing (kissing and dancing test - KDT) was observed. Direct cortical recordings (ECoG) in motor and language areas (experiment 2) demonstrated simultaneous bidirectional effects: motor preparation affected language processing (N400 at left inferior frontal gyrus and middle/superior temporal gyrus), and language processing affected activity in movement-related areas (motor potential at premotor and M1). Our findings show that the ACE paradigm requires ongoing integration of preserved motor and language coupling (abolished in EPD) and engages motor-temporal cortices in a bidirectional way. In addition, both experiments suggest the presence of a motor-language network which is not restricted to somatotopically defined brain areas. These results open new pathways in the fields of motor diseases, theoretical approaches to language understanding, and models of action-perception coupling.

Applauding with Closed Hands: Neural Signature of Action-Sentence Compatibility Effects

Background Behavioral studies have provided evidence for an action–sentence compatibility effect (ACE) that suggests a coupling of motor mechanisms and action-sentence comprehension. When both processes are concurrent, the action sentence primes the actual movement, and simultaneously, the action affects comprehension. The aim of the present study was to investigate brain markers of bidirectional impact of language comprehension and motor processes. Methodology/Principal Findings Participants listened to sentences describing an action that involved an open hand, a closed hand, or no manual action. Each participant was asked to press a button to indicate his/her understanding of the sentence. Each participant was assigned a hand-shape, either closed or open, which had to be used to activate the button. There were two groups (depending on the assigned hand-shape) and three categories (compatible, incompatible and neutral) defined according to the compatibility between the response and the sentence. ACEs were found in both groups. Brain markers of semantic processing exhibited an N400-like component around the Cz electrode position. This component distinguishes between compatible and incompatible, with a greater negative deflection for incompatible. Motor response elicited a motor potential (MP) and a re-afferent potential (RAP), which are both enhanced in the compatible condition. Conclusions/Significance The present findings provide the first ACE cortical measurements of semantic processing and the motor response. N400-like effects suggest that incompatibility with motor processes interferes in sentence comprehension in a semantic fashion. Modulation of motor potentials (MP and RAP) revealed a multimodal semantic facilitation of the motor response. Both results provide neural evidence of an action-sentence bidirectional relationship. Our results suggest that ACE is not an epiphenomenal post-sentence comprehension process. In contrast, motor-language integration occurring during the verb onset supports a genuine and ongoing brain motor-language interaction.

Cortical deficits of emotional face processing in adults with ADHD: Its relation to social cognition and executive function

Although it has been shown that adults with attention-deficit hyperactivity disorder (ADHD) have impaired social cognition, no previous study has reported the brain correlates of face valence processing. This study looked for behavioral, neuropsychological, and electrophysiological markers of emotion processing for faces (N170) in adult ADHD compared to controls matched by age, gender, educational level, and handedness. We designed an event-related potential (ERP) study based on a dual valence task (DVT), in which faces and words were presented to test the effects of stimulus type (faces, words, or face-word stimuli) and valence (positive versus negative). Individual signatures of cognitive functioning in participants with ADHD and controls were assessed with a comprehensive neuropsychological evaluation, including executive functioning (EF) and theory of mind (ToM). Compared to controls, the adult ADHD group showed deficits in N170 emotion modulation for facial stimuli. These N170 impairments were observed in the absence of any deficit in facial structural processing, suggesting a specific ADHD impairment in early facial emotion modulation. The cortical current density mapping of N170 yielded a main neural source of N170 at posterior section of fusiform gyrus (maximum at left hemisphere for words and right hemisphere for faces and simultaneous stimuli). Neural generators of N170 (fusiform gyrus) were reduced in ADHD. In those patients, N170 emotion processing was associated with performance on an emotional inference ToM task, and N170 from simultaneous stimuli was associated with EF, especially working memory. This is the first report to reveal an adult ADHD-specific impairment in the cortical modulation of emotion for faces and an association between N170 cortical measures and ToM and EF.

Subliminal presentation of other faces (but not own face) primes behavioral and evoked cortical processing of empathy for pain

Current research on empathy for pain emphasizes the overlap in the neural response between the first-hand experience of pain and its perception in others. However, recent studies suggest that the perception of the pain of others may reflect the processing of a threat or negative arousal rather than an automatic pro-social response. It can thus be suggested that pain processing of other-related, but not self-related, information could imply danger rather than empathy, due to the possible threat represented in the expressions of others (especially if associated with pain stimuli). To test this hypothesis, two experiments considering subliminal stimuli were designed. In Experiment 1, neutral and semantic pain expressions previously primed with own or other faces were presented to participants. When other-face priming was used, only the detection of semantic pain expressions was facilitated. In Experiment 2, pictures with pain and neutral scenarios previously used in ERP and fMRI research were used in a categorization task. Those pictures were primed with own or other faces following the same procedure as in Experiment 1 while ERPs were recorded. Early (N1) and late (P3) cortical responses between pain and no-pain were modulated only in the other-face priming condition. These results support the threat value of pain hypothesis and suggest the necessity for the inclusion of own- versus other-related information in future empathy for pain research.

The Neural Basis of Decision-Making and Reward Processing in Adults with Euthymic Bipolar Disorder or Attention-Deficit/Hyperactivity Disorder (ADHD)

Background Attention-deficit/hyperactivity disorder (ADHD) and bipolar disorder (BD) share DSM-IV criteria in adults and cause problems in decision-making. Nevertheless, no previous report has assessed a decision-making task that includes the examination of the neural correlates of reward and gambling in adults with ADHD and those with BD. Methodology/Principal Findings We used the Iowa gambling task (IGT), a task of rational decision-making under risk (RDMUR) and a rapid-decision gambling task (RDGT) which elicits behavioral measures as well as event-related potentials (ERPs: fERN and P3) in connection to the motivational impact of events. We did not observe between-group differences for decision-making under risk or ambiguity (RDMUR and IGT); however, there were significant differences for the ERP-assessed RDGT. Compared to controls, the ADHD group showed a pattern of impaired learning by feedback (fERN) and insensitivity to reward magnitude (P3). This ERP pattern (fERN and P3) was associated with impulsivity, hyperactivity, executive function and working memory. Compared to controls, the BD group showed fERN- and P3-enhanced responses to reward magnitude regardless of valence. This ERP pattern (fERN and P3) was associated with mood and inhibitory control. Consistent with the ERP findings, an analysis of source location revealed reduced responses of the cingulate cortex to the valence and magnitude of rewards in patients with ADHD and BD. Conclusions/Significance Our data suggest that neurophysiological (ERPs) paradigms such as the RDGT are well suited to assess subclinical decision-making processes in patients with ADHD and BD as well as for linking the cingulate cortex with action monitoring systems.

Contextual blending of ingroup/outgroup face stimuli and word valence: LPP modulation and convergence of measures

BackgroundSeveral event related potential (ERP) studies have investigated the time course of different aspects of evaluative processing in social bias research. Various reports suggest that the late positive potential (LPP) is modulated by basic evaluative processes, and some reports suggest that in-/outgroup relative position affects ERP responses. In order to study possible LPP blending between facial race processing and semantic valence (positive or negative words), we recorded ERPs while indigenous and non-indigenous participants who were matched by age and gender performed an implicit association test (IAT). The task involved categorizing faces (ingroup and outgroup) and words (positive and negative). Since our paradigm implies an evaluative task with positive and negative valence association, a frontal distribution of LPPs similar to that found in previous reports was expected. At the same time, we predicted that LPP valence lateralization would be modulated not only by positive/negative associations but also by particular combinations of valence, face stimuli and participant relative position.ResultsResults showed that, during an IAT, indigenous participants with greater behavioral ingroup bias displayed a frontal LPP that was modulated in terms of complex contextual associations involving ethnic group and valence. The LPP was lateralized to the right for negative valence stimuli and to the left for positive valence stimuli. This valence lateralization was influenced by the combination of valence and membership type relevant to compatibility with prejudice toward a minority. Behavioral data from the IAT and an explicit attitudes questionnaire were used to clarify this finding and showed that ingroup bias plays an important role. Both ingroup favoritism and indigenous/non-indigenous differences were consistently present in the data.ConclusionOur results suggest that frontal LPP is elicited by contextual blending of evaluative judgments of in-/outgroup information and positive vs. negative valence association and confirm recent research relating in-/outgroup ERP modulation and frontal LPP. LPP modulation may cohere with implicit measures of attitudes. The convergence of measures that were observed supports the idea that racial and valence evaluations are strongly influenced by context. This result adds to a growing set of evidence concerning contextual sensitivity of different measures of prejudice.

Early Neural Markers of Implicit Attitudes: N170 Modulated by Intergroup and Evaluative Contexts in IAT.

The Implicit Association Test (IAT) is the most popular measure to evaluate implicit attitudes. Nevertheless, its neural correlates are not yet fully understood. We examined event related potentials (ERPs) in response to face- and word processing while indigenous and non-indigenous participants performed an IAT displaying faces (ingroup and outgroup members) and words (positive and negative valence) as targets of category judgments. The N170 component was modulated by valence of words and by ingroup/outgroup face categorization. Contextual effects (face–words implicitly associated in the task) had an influence on the N170 amplitude modulation. On the one hand, in face categorization, right N170 showed differences according to the association between social categories of faces and affective valence of words. On the other, in word categorization, left N170 presented a similar modulation when the task implied a negative-valence associated with ingroup faces. Only indigenous participants showed a significant IAT effect and N170 differences. Our results demonstrate an early ERP blending of stimuli processing with both intergroup and evaluative contexts, suggesting an integration of contextual information related to intergroup attitudes during the early stages of word and face processing. To our knowledge, this is the first report of early ERPs during an ethnicity IAT, opening a new branch of exchange between social neuroscience and social psychology of attitudes.

The face and its emotion: Right N170 deficits in structural processing and early emotional discrimination in schizophrenic patients and relatives

Previous studies have reported facial emotion recognition impairments in schizophrenic patients, as well as abnormalities in the N170 component of the event-related potential. Current research on schizophrenia highlights the importance of complexly-inherited brain-based deficits. In order to examine the N170 markers of face structural and emotional processing, DSM-IV diagnosed schizophrenia probands (n=13), unaffected first-degree relatives from multiplex families (n=13), and control subjects (n=13) matched by age, gender and educational level, performed a categorization task which involved words and faces with positive and negative valence. The N170 component, while present in relatives and control subjects, was reduced in patients, not only for faces, but also for face-word differences, suggesting a deficit in structural processing of stimuli. Control subjects showed N170 modulation according to the valence of facial stimuli. However, this discrimination effect was found to be reduced both in patients and relatives. This is the first report showing N170 valence deficits in relatives. Our results suggest a generalized deficit affecting the structural encoding of faces in patients, as well as the emotion discrimination both in patients and relatives. Finally, these findings lend support to the notion that cortical markers of facial discrimination can be validly considered as vulnerability markers.

Context-sensitive social cognition is impaired in schizophrenic patients and their healthy relatives

Social cognition performance has been extensively studied within the schizophrenic population since Frith (1992) proposed amodel relatingmentalizing deficits and symptoms of the disorder. Moreover, recent research has suggested that social cognition is also impaired in unaffected relatives. Their deficits seem to be more pronounced when highly sophisticated tests are used (Janssen et al., 2003). Fifteen clinically-stable medicated schizophrenic patients from multiplex families, fourteen healthy first-degree relatives, and eighteen controls were examined. Groups were similar in age, education, and sex distribution. Initial selection criteria for all patients were: (1) diagnosis of paranoid schizophrenia according to DSM-IV-TR criteria (APA, 2000) and confirmed with Schedules of Clinical Assessment in Neuropsychiatry (SCAN) applied to both the patients and their relatives; and (2) the presence of one or more relativeswith the diagnosis of schizophrenia (no greater than third-degree relative), evidenced by the Family Interview for Genetic Studies (FIGS). Healthy relatives had to be first-degree relatives. SCANwas applied to relatives in order to rule out any psychiatric conditions in this group. All participants were between 20 and 55 years old. Participants completed written informed consent and were paid for their participation in the study. Participants completed the Ravens Coloured Progressive Matrices, Trail Making Test, Reading theMind in the Eyes, and Faux Pas Test. Additionally, Positive and Negative Syndrome Scale (PANSS) and Calgary Depression Scale for Schizophrenia were applied to patients to characterize symptomatology and mood. Detailed information about participants, results and discussion is presented as Supplementary data. Main results (Table 1) were:

Gesture influences the processing of figurative language in non-native speakers: ERP evidence.

Gestures should play a role in second language comprehension, given their importance in conveying contextual information. In this study, the N400 and the LPC were evaluated in a task involving the observation of videos showing utterances accompanied by gestures. Students studying advanced (G-High participants) and basic German (G-Low participants) as a second language were investigated. The utterance-gesture congruence and metaphoric meaning of content were manipulated during the task. As in previous ERP reports with native speakers, metaphorical expressions were sensitive to gestures. In G-Low participants, no modulation in the 300-500 ms window was observed, and only a modest effect was observed for the 500-700 ms window. More subtle differences of verbal expression were not processed in this group. Consistent with previous reports of the same paradigm with native speakers, the N400 from G-High group discriminated both congruent and incongruent gestures as well as literal and metaphorical sentences. Our results suggest that semantic processing is robust in the learning of a second language, although the amplitude modulation and latency of ERPs might depend on the speakers proficiency level.