Agustín Ibáñez

Contextual social cognition and the behavioral variant of frontotemporal dementia

The significance of social situations is commonly context-embedded. Although the role of context has been extensively studied in basic sensory processing or simple stimulus-response settings, its relevance for social cognition is unknown. We propose the social context network model (SCNM), a fronto-insular-temporal network responsible for processing social contextual effects. The SCNM may 1) update the context and use it to make predictions, 2) coordinate internal and external milieus, and 3) consolidate context-target associative learning. We suggest the behavioral variant of frontotemporal dementia (bvFTD) as a specific disorder in which the reported deficits in social cognition (e.g., facial recognition, empathy, decision-making, figurative language, theory of mind) can be described as context impairments due to deficits in the SCNM. Disruption of orbitofrontal-amygdala circuit, as well as the frontal, temporal, and insular atrophy in bVFTD, suggests a relationship between context-sensitive social cognition and SCNM. In considering context as an intrinsic part of social cognition, we highlight the need for a situated cognition approach in social cognition research as opposed to an abstract, universal, and decontextualized approach. The assessment of context-dependent social cognition paradigms, the SCNM, and their possible application to neuropsychiatric disorders may provide new insight into bvFTD and other related frontal disorders.

Decision-making cognition in neurodegenerative diseases

A large proportion of human social neuroscience research has focused on the issue of decision-making. Impaired decision-making is a symptomatic feature of a number of neurodegenerative diseases, but the nature of these decision-making deficits depends on the particular disease. Thus, examining the qualitative differences in decision-making impairments associated with different neurodegenerative diseases could provide valuable information regarding the underlying neural basis of decision-making. Nevertheless, few comparative reports of decision-making across patient groups exist. In this Review, we examine the neuroanatomical substrates of decision-making in relation to the neuropathological changes that occur in Alzheimer disease, frontotemporal dementia, Parkinson disease and Huntington disease. We then examine the main findings from studies of decision-making in these neurodegenerative diseases. Finally, we suggest a number of recommendations that future studies could adopt to aid our understanding of decision-making cognition.

Clinical effects of insular damage in humans.

Multiple disturbances following lesions of the insula are reviewed in the present article, including those related to autonomic function; gustatory, olfactory, auditory, somatosensory, and multimodal perception, as well as body awareness; the emotion of disgust; mood and willed action, addiction behavior, and language. Given the multiple and varied nature of the impairments revealed by lesion studies, we suggest that the insula, as a multimodal area, has a major role as a convergence zone implicated in the coordination between internal and external information through emotional subjective awareness. Methodological issues are discussed with attention paid to lesion etiology, and lesions involving adjacent areas to the insular cortex.

Expectation and Attention in Hierarchical Auditory Prediction

Hierarchical predictive coding suggests that attention in humans emerges from increased precision in probabilistic inference, whereas expectation biases attention in favor of contextually anticipated stimuli. We test these notions within auditory perception by independently manipulating top-down expectation and attentional precision alongside bottom-up stimulus predictability. Our findings support an integrative interpretation of commonly observed electrophysiological signatures of neurodynamics, namely mismatch negativity (MMN), P300, and contingent negative variation (CNV), as manifestations along successive levels of predictive complexity. Early first-level processing indexed by the MMN was sensitive to stimulus predictability: here, attentional precision enhanced early responses, but explicit top-down expectation diminished it. This pattern was in contrast to later, second-level processing indexed by the P300: although sensitive to the degree of predictability, responses at this level were contingent on attentional engagement and in fact sharpened by top-down expectation. At the highest level, the drift of the CNV was a fine-grained marker of top-down expectation itself. Source reconstruction of high-density EEG, supported by intracranial recordings, implicated temporal and frontal regions differentially active at early and late levels. The cortical generators of the CNV suggested that it might be involved in facilitating the consolidation of context-salient stimuli into conscious perception. These results provide convergent empirical support to promising recent accounts of attention and expectation in predictive coding.

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.

Structural neuroimaging of social cognition in progressive non-fluent aphasia and behavioral variant of frontotemporal dementia

Social cognition impairments are pervasive in the frontotemporal dementias (FTD). These deficits would be triggered by (a) basic emotion and face recognition processes as well as by (b) higher level social cognition (e.g., theory of mind, ToM). Both emotional processing and social cognition impairments have been previously reported in the behavioral variant of FTD (bvFTD) and also in other versions of FTDs, including primary progressive aphasia. However, no neuroanatomic comparison between different FTD variants has been performed. We report selective behavioral impairments of face recognition, emotion recognition, and ToM in patients with bvFTD and progressive non-fluent aphasia (PNFA) when compared to controls. Voxel-based morphometry (VBM) shows a classical impairment of mainly orbitofrontal (OFC), anterior cingulate (ACC), insula and lateral temporal cortices in patients. Comparative analysis of regional gray matter related to social cognition deficits (VBM) reveals a differential pattern of fronto-insulo-temporal atrophy in bvFTD and an insulo-temporal involvement in PNFA group. Results suggest that in spite of similar social cognition impairments reported in bvFTD and PNFA, the former represents an inherent ToM affectation whereas in the PNFA these deficits could be related to more basic processes of face and emotion recognition. These results are interpreted in the frame of the fronto-insulo-temporal social context network model (SCNM).

Action-verb processing in Parkinson’s disease: new pathways for motor–language coupling

Recent studies suggest that action-verb processing is particularly affected in early stage Parkinson’s disease (PD), highlighting the potential role of subcortical areas in language processing and in the semantic integration of actions. However, this disorder-related language impairment is frequently unrecognized by clinicians and often remains untreated. Early detection of action-language processing deficits could be critical for diagnosing and developing treatment strategies for PD. In this article, we review how action-verb processing is affected in PD and propose a model in which multiple and parallel frontotemporal circuits between the cortex and the basal ganglia provide the anatomic substrate for supporting action-language processing. We hypothesize that contextual coupling of action-language networks are partially dependent on cortical–subcortical integration, and not only on somatotopic motor cortical organization or in a mirror neuron system. This hypothesis is supported by both experimental and clinical evidence. Then, we identify further research steps that would help to determine the reliability of action-language impairments as an early marker of PD. Finally, theoretical implications for clinical assessment and for models of action-language interaction (action–perception cycle theories, mirror system models of language, and embodied cognition approaches to language) are discussed.

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.

Contextual social cognition impairments in schizophrenia and bipolar disorder.

Background The ability to integrate contextual information with social cues to generate social meaning is a key aspect of social cognition. It is widely accepted that patients with schizophrenia and bipolar disorders have deficits in social cognition; however, previous studies on these disorders did not use tasks that replicate everyday situations. Methodology/Principal Findings This study evaluates the performance of patients with schizophrenia and bipolar disorders on social cognition tasks (emotional processing, empathy, and social norms knowledge) that incorporate different levels of contextual dependence and involvement of real-life scenarios. Furthermore, we explored the association between social cognition measures, clinical symptoms and executive functions. Using a logistic regression analysis, we explored whether the involvement of more basic skills in emotional processing predicted performance on empathy tasks. The results showed that both patient groups exhibited deficits in social cognition tasks with greater context sensitivity and involvement of real-life scenarios. These deficits were more severe in schizophrenic than in bipolar patients. Patients did not differ from controls in tasks involving explicit knowledge. Moreover, schizophrenic patients’ depression levels were negatively correlated with performance on empathy tasks. Conclusions/Significance Overall performance on emotion recognition predicted performance on intentionality attribution during the more ambiguous situations of the empathy task. These results suggest that social cognition deficits could be related to a general impairment in the capacity to implicitly integrate contextual cues. Important implications for the assessment and treatment of individuals with schizophrenia and bipolar disorders, as well as for neurocognitive models of these pathologies are discussed.