Amygdala lesions do not compromise the cortical network for false-belief reasoning.
ABSTRACT: The amygdala plays an integral role in human social cognition and behavior, with clear links to emotion recognition, trust judgments, anthropomorphization, and psychiatric disorders ranging from social phobia to autism. A central feature of human social cognition is a theory-of-mind (ToM) that enables the representation other people's mental states as distinct from one's own. Numerous neuroimaging studies of the best studied use of ToM--false-belief reasoning--suggest that it relies on a specific cortical network; moreover, the amygdala is structurally and functionally connected with many components of this cortical network. It remains unknown whether the cortical implementation of any form of ToM depends on amygdala function. Here we investigated this question directly by conducting functional MRI on two patients with rare bilateral amygdala lesions while they performed a neuroimaging protocol standardized for measuring cortical activity associated with false-belief reasoning. We compared patient responses with those of two healthy comparison groups that included 480 adults. Based on both univariate and multivariate comparisons, neither patient showed any evidence of atypical cortical activity or any evidence of atypical behavioral performance; moreover, this pattern of typical cortical and behavioral response was replicated for both patients in a follow-up session. These findings argue that the amygdala is not necessary for the cortical implementation of ToM in adulthood and suggest a reevaluation of the role of the amygdala and its cortical interactions in human social cognition.
Project description:Theory of mind (ToM), the capacity to reason about others' mental states, is central to healthy social development. Neural mechanisms supporting ToM may contribute to individual differences in children's social cognitive behavior. Employing a false belief functional magnetic resonance imaging paradigm, we identified patterns of neural activity and connectivity elicited by ToM reasoning in school-age children (N = 32, ages 9-13). Next, we tested relations between these neural ToM correlates and children's everyday social cognition. Several key nodes of the neural ToM network showed greater activity when reasoning about false beliefs (ToM condition) vs non-mentalistic false content (control condition), including the bilateral temporoparietal junction (RTPJ and LTPJ), precuneus (PC) and right superior temporal sulcus. In addition, children demonstrated task-modulated changes in connectivity among these regions to support ToM relative to the control condition. ToM-related activity in the PC was negatively associated with variation in multiple aspects of children's social cognitive behavior. Together, these findings elucidate how nodes of the ToM network act and interact to support false belief reasoning in school-age children and suggest that neural ToM mechanisms are linked to variation in everyday social cognition.
Project description:The focus of studies on second-order false belief reasoning generally was on investigating the roles of executive functions and language with correlational studies. Different from those studies, we focus on the question how 5-year-olds select and revise reasoning strategies in second-order false belief tasks by constructing two computational cognitive models of this process: an instance-based learning model and a reinforcement learning model. Unlike the reinforcement learning model, the instance-based learning model predicted that children who fail second-order false belief tasks would give answers based on first-order theory of mind (ToM) reasoning as opposed to zero-order reasoning. This prediction was confirmed with an empirical study that we conducted with 72 5- to 6-year-old children. The results showed that 17% of the answers were correct and 83% of the answers were wrong. In line with our prediction, 65% of the wrong answers were based on a first-order ToM strategy, while only 29% of them were based on a zero-order strategy (the remaining 6% of subjects did not provide any answer). Based on our instance-based learning model, we propose that when children get feedback "Wrong," they explicitly revise their strategy to a higher level instead of implicitly selecting one of the available ToM strategies. Moreover, we predict that children's failures are due to lack of experience and that with exposure to second-order false belief reasoning, children can revise their wrong first-order reasoning strategy to a correct second-order reasoning strategy.
Project description:Impaired Theory of Mind (ToM) has been repeatedly reported as a feature of psychotic disorders. ToM is crucial in social interactions and for the development of social behavior. It has been suggested that reasoning about the belief of others, requires inhibition of the self-perspective. We investigated the neural correlates of self-inhibition in nineteen low psychosis prone (PP) and eighteen high PP subjects presenting with subclinical features. High PP subjects have a more than tenfold increased risk of developing a schizophrenia-spectrum disorder. Brain activation was measured with functional Magnetic Resonance Imaging during a ToM task differentiating between self-perspective inhibition and belief reasoning. Furthermore, to test underlying inhibitory mechanisms, we included a stop-signal task. We predicted worse behavioral performance for high compared to low PP subjects on both tasks. Moreover, based on previous neuroimaging results, different activation patterns were expected in the inferior frontal gyrus (IFG) in high versus low PP subjects in self-perspective inhibition and simple response inhibition. Results showed increased activation in left IFG during self-perspective inhibition, but not during simple response inhibition, for high PP subjects as compared to low PP subjects. High and low PP subjects showed equal behavioral performance. The results suggest that at a neural level, high PP subjects need more resources for inhibiting the self-perspective, but not for simple motor response inhibition, to equal the performance of low PP subjects. This may reflect a compensatory mechanism, which may no longer be available for patients with schizophrenia-spectrum disorders resulting in ToM impairments.
Project description:Human social interaction crucially relies on the ability to infer what other people think. Referred to as Theory of Mind (ToM), this ability has long been argued to emerge around 4 y of age when children start passing traditional verbal ToM tasks. This developmental dogma has recently been questioned by nonverbal ToM tasks passed by infants younger than 2 y of age. How do young children solve these tests, and what is their relation to the later-developing verbal ToM reasoning? Are there two different systems for nonverbal and verbal ToM, and when is the developmental onset of mature adult ToM? To address these questions, we related markers of cortical brain structure (i.e., cortical thickness and surface area) of 3- and 4-y-old children to their performance in novel nonverbal and traditional verbal TM tasks. We showed that verbal ToM reasoning was supported by cortical surface area and thickness of the precuneus and temporoparietal junction, classically involved in ToM in adults. Nonverbal ToM reasoning, in contrast, was supported by the cortical structure of a distinct and independent neural network including the supramarginal gyrus also involved in emotional and visual perspective taking, action observation, and social attention or encoding biases. This neural dissociation suggests two systems for reasoning about others' minds-mature verbal ToM that emerges around 4 y of age, whereas nonverbal ToM tasks rely on different earlier-developing possibly social-cognitive processes.
Project description:Human adults recruit distinct networks of brain regions to think about the bodies and minds of others. This study characterizes the development of these networks, and tests for relationships between neural development and behavioral changes in reasoning about others' minds ('theory of mind', ToM). A large sample of children (n?=?122, 3-12 years), and adults (n?=?33), watched a short movie while undergoing fMRI. The movie highlights the characters' bodily sensations (often pain) and mental states (beliefs, desires, emotions), and is a feasible experiment for young children. Here we report three main findings: (1) ToM and pain networks are functionally distinct by age 3 years, (2) functional specialization increases throughout childhood, and (3) functional maturity of each network is related to increasingly anti-correlated responses between the networks. Furthermore, the most studied milestone in ToM development, passing explicit false-belief tasks, does not correspond to discontinuities in the development of the social brain.
Project description:Theory of mind (ToM) is the ability to attribute mental states to oneself and others, and to understand that others have beliefs that are different from one's own. Although functional neuroimaging techniques have been widely used to establish the neural correlates implicated in ToM, the specific mechanisms are still not clear. We make our efforts to integrate and adopt existing biological findings of ToM, bridging the gap through computational modeling, to build a brain-inspired computational model for ToM. We propose a Brain-inspired Model of Theory of Mind (Brain-ToM model), and the model is applied to a humanoid robot to challenge the false belief tasks, two classical tasks designed to understand the mechanisms of ToM from Cognitive Psychology. With this model, the robot can learn to understand object permanence and visual access from self-experience, then uses these learned experience to reason about other's belief. We computationally validated that the self-experience, maturation of correlate brain areas (e.g., calculation capability) and their connections (e.g., inhibitory control) are essential for ToM, and they have shown their influences on the performance of the participant robot in false-belief task. The theoretic modeling and experimental validations indicate that the model is biologically plausible, and computationally feasible as a foundation for robot theory of mind.
Project description:Current measures of social cognition have shown inconsistent findings regarding the effects of healthy aging. Moreover, no tests are currently available that allow clinicians and researchers to examine cognitive and affective theory of mind (ToM) and understanding of social norms within the same test. To address these limitations, we present the Edinburgh Social Cognition Test (ESCoT) which assesses cognitive and affective ToM and inter- and intrapersonal understanding of social norms. We examined the effects of age, measures of intelligence and the Broader Autism Phenotype (BAP) on the ESCoT and established tests of social cognition. Additionally, we investigated the convergent validity of the ESCoT based on traditional social cognition measures. The ESCoT was administered alongside Reading the Mind in Films (RMF), Reading the Mind in Eyes (RME), Judgement of Preference and Social Norm Questionnaire to 91 participants (30 aged 18-35 years, 30 aged 45-60 years and 31 aged 65-85 years). Poorer performance on the cognitive and affective ToM ESCoT subtests were predicted by increasing age. The affective ToM ESCoT subtest and RMF were predicted by gender, where being female predicted better performance. Unlike the ESCoT, better performance on the RMF was predicted by higher verbal comprehension and perceptual reasoning abilities, while better performance on the RME was predicted by higher verbal comprehension scores. Lower scores on inter-and intrapersonal understanding of social norms were both predicted by the presence of more autism-like traits while poorer interpersonal understanding of social norms performance was predicted by increasing age. These findings show that the ESCoT is a useful measure of social cognition and, unlike established tests of social cognition, performance is not predicted by measures of verbal comprehension and perceptual reasoning. This is particularly valuable to obtain an accurate assessment of the influence of age on our social cognitive abilities.
Project description:Inner speech has been implicated in important aspects of normal and atypical cognition, including the development of auditory hallucinations. Studies to date have focused on covert speech elicited by simple word or sentence repetition, while ignoring richer and arguably more psychologically significant varieties of inner speech. This study compared neural activation for inner speech involving conversations ('dialogic inner speech') with single-speaker scenarios ('monologic inner speech'). Inner speech-related activation differences were then compared with activations relating to Theory-of-Mind (ToM) reasoning and visual perspective-taking in a conjunction design. Generation of dialogic (compared with monologic) scenarios was associated with a widespread bilateral network including left and right superior temporal gyri, precuneus, posterior cingulate and left inferior and medial frontal gyri. Activation associated with dialogic scenarios and ToM reasoning overlapped in areas of right posterior temporal cortex previously linked to mental state representation. Implications for understanding verbal cognition in typical and atypical populations are discussed.
Project description:High-functioning autism (ASD) is characterized by real-life difficulties in social interaction; however, these individuals often succeed on laboratory tests that require an understanding of another person's beliefs and intentions. This paradox suggests a theory of mind (ToM) deficit in adults with ASD that has yet to be demonstrated in an experimental task eliciting ToM judgments. We tested whether ASD adults would show atypical moral judgments when they need to consider both the intentions (based on ToM) and outcomes of a person's actions. In experiment 1, ASD and neurotypical (NT) participants performed a ToM task designed to test false belief understanding. In experiment 2, the same ASD participants and a new group of NT participants judged the moral permissibility of actions, in a 2 (intention: neutral/negative) × 2 (outcome: neutral/negative) design. Though there was no difference between groups on the false belief task, there was a selective difference in the moral judgment task for judgments of accidental harms, but not neutral acts, attempted harms, or intentional harms. Unlike the NT group, which judged accidental harms less morally wrong than attempted harms, the ASD group did not reliably judge accidental and attempted harms as morally different. In judging accidental harms, ASD participants appeared to show an underreliance on information about a person's innocent intention and, as a direct result, an overreliance on the action's negative outcome. These findings reveal impairments in integrating mental state information (e.g., beliefs, intentions) for moral judgment.
Project description:The human capacity to reason about others' minds includes making causal inferences about intentions, beliefs, values, and goals. Previous fMRI research has suggested that a network of brain regions, including bilateral temporo-parietal junction (TPJ), superior temporal sulcus (STS), and medial prefrontal-cortex (MPFC), are reliably recruited for mental state reasoning. Here, in two fMRI experiments, we investigate the representational content of these regions. Building on existing computational and neural evidence, we hypothesized that social brain regions contain at least two functionally and spatially distinct components: one that represents information related to others' motivations and values, and another that represents information about others' beliefs and knowledge. Using multi-voxel pattern analysis, we find evidence that motivational versus epistemic features are independently represented by theory of mind (ToM) regions: RTPJ contains information about the justification of the belief, bilateral TPJ represents the modality of the source of knowledge, and VMPFC represents the valence of the resulting emotion. These representations are found only in regions implicated in social cognition and predict behavioral responses at the level of single items. We argue that cortical regions implicated in mental state inference contain complementary, but distinct, representations of epistemic and motivational features of others' beliefs, and that, mirroring the processes observed in sensory systems, social stimuli are represented in distinct and distributed formats across the human brain.