Blas Couto

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).

Insular networks for emotional processing and social cognition: Comparison of two case reports with either cortical or subcortical involvement

INTRODUCTION The processing of the emotion of disgust is attributed to the insular cortex (IC), which is also responsible for social emotions and higher-cognitive functions. We distinguish the role of the IC from its connections in regard to these functions through the assessment of emotions and social cognition in a double case report. These subjects were very rare cases that included a focal IC lesion and a subcortical focal stroke affecting the connections of the IC with frontotemporal areas. MATERIALS & METHODS Both patients and a sample of 10 matched controls underwent neuropsychological and affective screening questionnaires, a battery of multimodal basic emotion recognition tests, an emotional inference disambiguation task using social contextual clues, an empathy task and a theory of mind task. RESULTS The insular lesion (IL) patient showed no impairments in emotion recognition and social emotions and presented with a pattern of delayed reaction times (RTs) in a subset of both groups of tasks. The subcortical lesion (SL) patient was impaired in multimodal aversive emotion recognition, including disgust, and exhibited delayed RTs and a heterogeneous pattern of impairments in subtasks of empathy and in the contextual inference of emotions. CONCLUSIONS Our results suggest that IC related networks, and not the IC itself, are related to negative emotional processing and social emotions. We discuss these results with respect to theoretical approaches of insular involvement in emotional and social processing and propose that IC connectivity with frontotemporal and subcortical regions might be relevant for contextual emotional processing and social cognition.

Comparing Moral Judgments of Patients With Frontotemporal Dementia and Frontal Stroke

IMPORTANCE Several clinical reports have stated that patients with prefrontal lesions or patients with the behavioral variant of frontotemporal dementia share social cognition impairments. Moral reasoning is impaired in both conditions but there have been few investigations that directly compare this domain in the 2 groups. OBSERVATIONS This work compared the moral judgments of these patient groups using a task designed to disentangle the contributions of intentions and outcomes in moral judgment. For both disorders, patients judged scenarios where the protagonists believed that they would cause harm but did not as being more permissible than the control group. Moreover, patients with frontotemporal dementia judged harmful outcomes in the absence of harmful intentions as less permissible than the control participants. There were no differences between the 2 conditions. CONCLUSIONS AND RELEVANCE Both disorders involved impairments in integrating intention and outcome information for moral judgment. This study was the first, to our knowledge, to directly compare a social cognition domain in 2 frontal pathologies with different etiology. Our results highlighted the importance of comparing patients with vascular lesions and patients with neurodegenerative diseases.

How do you feel when you can't feel your body? Interoception, functional connectivity and emotional processing in depersonalization-derealization disorder.

Depersonalization-Derealization Disorder (DD) typically manifests as a disruption of body self-awareness. Interoception −defined as the cognitive processing of body signals− has been extensively considered as a key processing for body self-awareness. In consequence, the purpose of this study was to investigate whether there are systematic differences in interoception between a patient with DD and controls that might explain the disembodiment symptoms suffered in this disease. To assess interoception, we utilized a heartbeat detection task and measures of functional connectivity derived from fMRI networks in interoceptive/exteroceptivo/mind-wandering states. Additionally, we evaluated empathic abilities to test the association between interoception and emotional experience. The results showed patients impaired performance in the heartbeat detection task when compared to controls. Furthermore, regarding functional connectivity, we found a lower global brain connectivity of the patient relative to controls only in the interoceptive state. He also presented a particular pattern of impairments in affective empathy. To our knowledge, this is the first experimental research that assesses the relationship between interoception and DD combining behavioral and neurobiological measures. Our results suggest that altered neural mechanisms and cognitive processes regarding body signaling might be engaged in DD phenomenology. Moreover, our study contributes experimental data to the comprehension of brain-body interactions and the emergence of self-awareness and emotional feelings.

Auditory Feedback Differentially Modulates Behavioral and Neural Markers of Objective and Subjective Performance When Tapping to Your Heartbeat

Interoception, the perception of our body internal signals, plays a key role in maintaining homeostasis and guiding our behavior. Sometimes, we become aware of our body signals and use them in planning and strategic thinking. Here, we show behavioral and neural dissociations between learning to follow ones own heartbeat and metacognitive awareness of ones performance, in a heartbeat-tapping task performed before and after auditory feedback. The electroencephalography amplitude of the heartbeat-evoked potential in interoceptive learners, that is, participants whose accuracy of tapping to their heartbeat improved after auditory feedback, was higher compared with non-learners. However, an increase in gamma phase synchrony (30–45 Hz) after the heartbeat auditory feedback was present only in those participants showing agreement between objective interoceptive performance and metacognitive awareness. Source localization in a group of participants and direct cortical recordings in a single patient identified a network hub for interoceptive learning in the insular cortex. In summary, interoceptive learning may be mediated by the right insular response to the heartbeat, whereas metacognitive awareness of learning may be mediated by widespread cortical synchronization patterns.

Beyond Extrastriate Body Area (EBA) and Fusiform Body Area (FBA): Context Integration in the Meaning of Actions

Our ability to identify and interpret the actions and intentions of other people in a meaningful way is the bedrock of social cognition. Visual perception of human body is a critical component of this complex task as long as it provides cues which enable the observer to make the required inferences to accurately extract the meaning of daily action events. During the last decade, neuroimaging studies have identified two brain regions of the extrastriate visual cortex that are highly sensitive to the perception of human bodies and body parts. These regions are the extrastriate body area (EBA), located at the posterior inferior temporal sulcus/middle temporal gyrus (Downing et al., 2001) and the fusiform body area (FBA) found ventrally in the fusiform gyrus (Peelen and Downing, 2005; Schwarzlose et al., 2005). Evidence derived from fMRI studies has shown that both areas become significantly activated in response to body/body parts stimuli visually presented in different formats like photos, line drawings, stick figures, and silhouettes compared to control stimuli like faces/face parts, tools/tool parts, and scenes (Downing et al., 2001; Peelen and Downing, 2005; Schwarzlose et al., 2005; Spiridon et al., 2006; Weiner and Grill-Spector, 2010). Recently, it has been suggested that EBA and FBA can be functionally dissociated, with a more selective activation for local body parts in EBA relative to more holistic images of the human body in FBA (Taylor et al., 2007). Based on these findings, many authors have claimed that EBA/FBA should be directly involved in complex functions such as perceiving goal-directed actions and other higher-level related processes (Costantini et al., 2005; Saxe et al., 2006; Moro et al., 2008; Marsh et al., 2010; Kuhn et al., 2011). However, as suggested by Downing and Peelen (2011), it might be more accurate to interpret the activity of these regions in terms of populations of neurons that selectively encode and make explicit low-level visual features of human bodies like body shape and posture. According to this hypothesis, the comprehension of meaningful actions could be supported by a more distributed neural network where visual information extracted by EBA/FBA is integrated with the contextual information processed in other parts of the brain. Although this hypothesis seems to be more plausible, the authors do not give further information on how this integration might be accomplished or, more specifically, about which other cortical areas would be actively engaged in this network. In order to address this issue, we propose a functional neuroanatomic model for the contextual processing of goal-directed actions where the general perceptual processing provided by EBA/FBA is integrated in a larger fronto-insular–temporal network. When we witness a simple event, our brain integrates the information about people, objects, and the interactions among them into a coherent meaningful representation. For instance, object recognition is thought to be instantiated by cognitive structures that integrate information about the identity of the objects that tend to co-occur in a given context with previously learned information about their possible relationships (Bar, 2004). These structures can be thought of as a set of expectations about what is more probable to see or not to see in a given context, enabling us to make predictions and accurately disambiguate incoming information. We proposed that in a fronto-insular–temporal “social context network” (SCN), several frontal areas update and associate ongoing contextual information in relation to episodic memory and target-context associations (Sigala et al., 2008; Bar, 2009; Burgess et al., 2009). The temporal regions [e.g., the parahippocampal cortex (PHC), hippocampus, and amygdala] may index the value learning of target-context associations (Langston and Wood, 2010). Finally, the insular cortex would coordinate internal and external milieus in an inner motivational state (Singer et al., 2009; Ibanez et al., 2010a). See Figure ​Figure11. Figure 1 Lateral view of the left hemisphere showing the proposed fronto-insular–temporal network (light-blue, violet, and green regions of interest, respectively). In this context network, prefrontal areas (PFC) such as frontopolar and dorsolateral prefrontal ... This contextual dimension of action understanding is also supported by ERP studies on the N400-like component, an ongoing negativity elicited when a meaningful action is incongruent (unexpected) with a previous context. N400 seems to be a specific context integration component (Bar, 2004). For example, videos and pictures of everyday-life actions, co-speech gestures, and semantic processing of current motor events (Sitnikova et al., 2003; Aravena et al., 2010; Ibanez et al., 2010b, 2011; Proverbio et al., 2010) have shown that, as the action-related stimulus becomes more expected/congruent with the context in which it is embedded, the N400 amplitude is reduced compared to incongruent/unexpected conditions. These findings suggest that when the previous context builds up meaning, processing of upcoming stimulus that fit with that context is facilitated. Evidence derived from lesion studies, MEG, and intracranial recordings includes the left superior/middle temporal gyrus, the anterior-medial temporal lobe, the PHC and fusiform gyrus as well as frontopolar, orbital, and dorsolateral prefrontal regions as the possible sources of this N400 effect (Halgren et al., 2002; Van Petten and Luka, 2006). Finally, as well as frontal and temporal regions, the insular cortex plays a crucial role in the proposed network. This region has been recently implicated in the contextual integration of interoceptive information (conscious representation about ones body physiological state and motivational drives) with external stimuli (sensory current environment) into a global feeling state (Craig, 2002; Ibanez et al., 2010a). Moreover, anterior insular cortex has also shown to be recruited during motivational decision-making in uncertain contexts, suggesting that this area also mediates risk behavior when the available information is not sufficient to predict an outcome (Singer et al., 2009). Overall, the SCN provides an empirically testable set of hypotheses regarding contextual update, contextual prediction, and target-context association in action meaning paradigms. For instance, we expect to observe the engagement of the SCN during action meaning processing. This prediction is partially confirmed since frontal, temporal, or insular activations have been previously observed together with EBA and FBA during action paradigms (Kable and Chatterjee, 2006; Lamm et al., 2007; Lamm and Decety, 2008; Hodzic et al., 2009a,b; Cross et al., 2010; Kret et al., 2011). Additionally, a more straight empirical testing would be provided by direct contextual manipulation of action-related stimuli. The use of frames, background information or multimodal designs (as used in other domains of contextual studies, e.g., Bar, 2004) adapted to action meaning tasks would provide simple experimental shortcuts. An ideal experimental approach would comprise a battery of tasks that vary the degree of context for action/non-action stimuli, in order to test the relative engagement of the SCN in EBA/FBA activation during action and non-action processing. We expect that, while manipulating the contextual information (e.g., by increasing its influence), stronger activation in frontal, temporal, and insular regions rather than in EBA/FBA would be observed. Furthermore, if the contextual information being processed crucially requires the extraction of specific information regarding body/body parts (e.g., imagine a task where body posture is important for disentangle the emotional state of a person), we expect that activity in EBA/FBA will be enhanced as much as in the other regions of the SCN. In brief, we suggest that action meaning is beyond EBA and FBA through the integration of contextual information processed by a distributed fronto-insular–temporal network. Moreover, action meaning is not an amodal, invariant, immutable representation in a brain area, but instead a polymodal, context-sensitive, constructive, and distributed process. Similar to context integration during visual object recognition (Bar, 2004), information of body appearance and posture in EBA/FBA should be integrated within a SCN in order to process action meaning. We propose a multimodal system of action meaning in which expectations (frontal areas) of external information (including body processing in EBA/FBA), interacts with their semantic association (temporal regions) and the current internal motivational states (insula) in order to get a specific significance of an event. Thus, a context–facilitation large-scale distributed neural network may process and influence the EBA/FBA activity in a top-down manner.

Preliminary evidence about the effects of meditation on interoceptive sensitivity and social cognition

BackgroundInteroception refers to the conscious perception of body signals. Mindfulness is a meditation practice that encourages individuals to focus on their internal experiences such as bodily sensations, thoughts, and emotions. In this study, we selected a behavioral measure of interoceptive sensitivity (heartbeat detection task, HBD) to compare the effect of meditation practice on interoceptive sensitivity among long term practitioners (LTP), short term meditators (STM, subjects that completed a Mindfulness-Based Stress Reduction (MBSR) program) and controls (non-meditators). All participants were examined with a battery of different tasks including mood state, executive function and social cognition tests (emotion recognition, empathy and theory of mind).FindingsCompared to controls, both meditators’ groups showed lower levels of anxiety and depression, but no improvement in executive function or social cognition performance was observed (except for lower scores compared to controls only in the personal distress dimension of empathy). More importantly, meditators’ performance did not differ from that of nonmeditators regarding cardiac interoceptive sensitivity.ConclusionResults suggest no influence of meditation practice in cardiac interoception and in most related social cognition measures. These negative results could be partially due to the fact that awareness of heartbeat sensations is not emphasized during mindfulness/vipassana meditation and may not be the best index of the awareness supported by the practice of meditation.

Brain network organization and social executive performance in frontotemporal dementia

OBJECTIVES Behavioral variant frontotemporal dementia (bvFTD) is characterized by early atrophy in the frontotemporoinsular regions. These regions overlap with networks that are engaged in social cognition-executive functions, two hallmarks deficits of bvFTD. We examine (i) whether Network Centrality (a graph theory metric that measures how important a node is in a brain network) in the frontotemporoinsular network is disrupted in bvFTD, and (ii) the level of involvement of this network in social-executive performance. METHODS Patients with probable bvFTD, healthy controls, and frontoinsular stroke patients underwent functional MRI resting-state recordings and completed social-executive behavioral measures. RESULTS Relative to the controls and the stroke group, the bvFTD patients presented decreased Network Centrality. In addition, this measure was associated with social cognition and executive functions. To test the specificity of these results for the Network Centrality of the frontotemporoinsular network, we assessed the main areas from six resting-state networks. No group differences or behavioral associations were found in these networks. Finally, Network Centrality and behavior distinguished bvFTD patients from the other groups with a high classification rate. CONCLUSIONS bvFTD selectively affects Network Centrality in the frontotemporoinsular network, which is associated with high-level social and executive profile.

The roles of interoceptive sensitivity and metacognitive interoception in panic

BackgroundInteroception refers to the ability to sense body signals. Two interoceptive dimensions have been recently proposed: (a) interoceptive sensitivity (IS) –objective accuracy in detecting internal bodily sensations (e.g., heartbeat, breathing)–; and (b) metacognitive interoception (MI) –explicit beliefs and worries about one’s own interoceptive sensitivity and internal sensations. Current models of panic assume a possible influence of interoception on the development of panic attacks. Hypervigilance to body symptoms is one of the most characteristic manifestations of panic disorders. Some explanations propose that patients have abnormal IS, whereas other accounts suggest that misinterpretations or catastrophic beliefs play a pivotal role in the development of their psychopathology. Our goal was to evaluate these theoretical proposals by examining whether patients differed from controls in IS, MI, or both. Twenty-one anxiety disorders patients with panic attacks and 13 healthy controls completed a behavioral measure of IS motor heartbeat detection (HBD) and two questionnaires measuring MI.FindingsPatients did not differ from controls in IS. However, significant differences were found in MI measures. Patients presented increased worries in their beliefs about somatic sensations compared to controls. These results reflect a discrepancy between direct body sensing (IS) and reflexive thoughts about body states (MI).ConclusionOur findings support the idea that hypervigilance to body symptoms is not necessarily a bottom-up dispositional tendency (where patients are hypersensitive about bodily signals), but rather a metacognitive process related to threatening beliefs about body/somatic sensations.

Convergence of interoception, emotion, and social cognition: A twofold fMRI meta-analysis and lesion approach

Guided by indirect evidence, recent approaches propose a tripartite crosstalk among interoceptive signaling, emotional regulation, and low-level social cognition. Here we examined the neurocognitive convergence of such domains. First, we performed three meta-analyses of functional magnetic resonance imaging studies to identify which areas are consistently coactivated by these three systems. Multi-level Kernel Density Analysis (MKDA) revealed major overlaps in the right anterior insular and frontotemporal regions (viz., the orbitofrontal and inferior frontal gyri, the amygdala, and mid temporal lobe/subcortical structures). Second, we explored such domains in patients with fronto-insulo-temporal damage. Relative to controls, the patients showed behavioral impairments of interoception, emotional processing, and social cognition, with preservation of other cognitive functions. Convergent results from both studies offer direct support for a model of insular-frontotemporal regions integrating interoception, emotion, and social cognition.