Anterior insular cortex and emotional awareness Gu, Xiaosi; Hof, Patrick R.; Friston, Karl J. ...
Journal of comparative neurology,
15 October 2013, Letnik:
521, Številka:
15
Journal Article
Recent brain imaging studies have shown that the neural substrates underlying the ability to infer and share the feeling of pain of other individuals overlap with the pain matrix that mediates the ...process of one's own pain. While there has been evidence that the neural activity mediating pain experience is influenced by top–down attention, it remains unclear whether the neural substrates of empathy for pain are modulated by top–down controlled mechanisms. The current work investigated whether the neural correlates of empathic processes of pain are altered by task demand and prior knowledge of stimulus reality. Subjects were scanned using functional magnetic resonance imaging (fMRI) while watching pictures or cartoons of hands that were in painful or neutral situations. Subjects were asked either to evaluate pain intensity supposedly felt by the model or to count the number of hands in the stimulus displays. Relative to counting neutral stimuli, rating pain intensity of painful pictures and cartoons induced increased activation in ACC/paracingulate and the right middle frontal gyrus. Rating pain intensity also activated the inferior frontal cortex bilaterally and the right insula/putamen for pictures but activated the left parietal cortex, the postcentral gyrus, and the occipito-temporal cortex for cartoons. However, the neural activities related to pain rating were eliminated when subjects counted the number of hands in the painful stimuli. In addition, the ACC activity associated with empathy for pain was stronger for the pictures than for the cartoons. Our findings indicate that the involvement of the neural substrates underlying pain-related empathy is constrained by top–down attention and contextual reality of stimuli.
Autism spectrum disorder (ASD) is characterized by hallmark impairments in social functioning. Nevertheless, nonsocial cognition, including hippocampus-dependent spatial reasoning and episodic ...memory, is also commonly impaired in ASD. ASD symptoms typically emerge between 12 and 24 months of age, a time window associated with critical developmental events in the hippocampus. Despite this temporal overlap and evidence of hippocampal structural abnormalities in ASD individuals, relatively few human studies have focused on hippocampal function in ASD. Herein, we review the existing evidence for the involvement of the hippocampus in ASD and highlight the hippocampus as a promising area of interest for future research in ASD.
Social interaction, spatial reasoning, and memory are supported by the hippocampus and impaired in autism spectrum disorder (ASD), but these functions remain understudied in neuroimaging research in ASD.There is evidence of altered hippocampal structure and function in ASD.Hippocampal maturation and ASD symptom-onset display coinciding developmental timelines.Impaired hippocampal-mediated cognitive mechanisms and policies such as cognitive mapping, affordance perception, and model-based planning may contribute to ASD phenotypes.Future neuroimaging research should explore hippocampal functioning in ASD, particularly as a potential neural basis for impairments in social interaction in ASD.
Accumulating evidence indicates that the anterior insular cortex (AIC) mediates interoceptive attention which refers to attention towards physiological signals arising from the body. However, the ...necessity of the AIC in this process has not been demonstrated. Using a novel task that directs attention toward breathing rhythm, we assessed the involvement of the AIC in interoceptive attention in healthy participants using functional magnetic resonance imaging and examined the necessity of the AIC in interoceptive attention in patients with AIC lesions. Results showed that interoceptive attention was associated with increased AIC activation, as well as enhanced coupling between the AIC and somatosensory areas along with reduced coupling between the AIC and visual sensory areas. In addition, AIC activation was predictive of individual differences in interoceptive accuracy. Importantly, AIC lesion patients showed disrupted interoceptive discrimination accuracy and sensitivity. These results provide compelling evidence that the AIC plays a critical role in interoceptive attention.
Understanding how humans represent others' pain is critical for understanding pro-social behavior. 'Shared experience' theories propose common brain representations for somatic and vicarious pain, ...but other evidence suggests that specialized circuits are required to experience others' suffering. Combining functional neuroimaging with multivariate pattern analyses, we identified dissociable patterns that predicted somatic (high versus low: 100%) and vicarious (high versus low: 100%) pain intensity in out-of-sample individuals. Critically, each pattern was at chance in predicting the other experience, demonstrating separate modifiability of both patterns. Somatotopy (upper versus lower limb: 93% accuracy for both conditions) was also distinct, located in somatosensory versus mentalizing-related circuits for somatic and vicarious pain, respectively. Two additional studies demonstrated the generalizability of the somatic pain pattern (which was originally developed on thermal pain) to mechanical and electrical pain, and also demonstrated the replicability of the somatic/vicarious dissociation. These findings suggest possible mechanisms underlying limitations in feeling others' pain, and present new, more specific, brain targets for studying pain empathy.
•We investigated belief updating in two tasks, with and without explicit feedback.•Model-based fMRI revealed similar confidence-encoding networks across tasks.•The anterior hippocampus led the ...confidence-encoding network, w/o feedbacks.•The medial PFC and amygdala led a confidence-encoding network, with feedbacks.
Classic decision theories typically assume the presence of explicit value-based outcomes after action selections to update beliefs about action-outcome contingencies. However, ecological environments are often opaque, and it remains unclear whether the neural dynamics underlying belief updating vary under conditions characterized by the presence or absence of such explicit value-based information, after each choice selection. We investigated this question in healthy humans (n = 28) using Bayesian inference and two multi-option fMRI tasks: a multi-armed bandit task, and a probabilistic perceptual task, respectively with and without explicit value-based feedback after choice selections. Model-based fMRI analysis revealed a network encoding belief updating which did not change depending on the task. More precisely, we found a confidence-building network that included anterior hippocampus, amygdala, and medial prefrontal cortex (mPFC), which became more active as beliefs about action-outcome probabilities were confirmed by newly acquired information. Despite these consistent responses across tasks, dynamic causal modeling estimated that the network dynamics changed depending on the presence or absence of trial-by-trial value-based outcomes. In the task deprived of immediate feedback, the hippocampus increased its influence towards both amygdala and mPFC, in association with increased strength in the confidence signal. However, the opposite causal relations were found (i.e., from both mPFC and amygdala towards the hippocampus), in presence of immediate outcomes. This finding revealed an asymmetric relationship between decision confidence computations, which were based on similar computational models across tasks, and neural implementation, which varied depending on the availability of outcomes after choice selections.
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Several decision-making vulnerabilities have been identified as underlying causes for addictive behaviours, or the repeated execution of stereotyped actions despite their adverse consequences. These ...vulnerabilities are mostly associated with brain alterations caused by the consumption of substances of abuse. However, addiction can also happen in the absence of a pharmacological component, such as seen in pathological gambling and videogaming. We use a new reinforcement learning model to highlight a previously neglected vulnerability that we suggest interacts with those already identified, whilst playing a prominent role in non-pharmacological forms of addiction. Specifically, we show that a dual-learning system (i.e. combining model-based and model-free) can be vulnerable to highly rewarding, but suboptimal actions, that are followed by a complex ramification of stochastic adverse effects. This phenomenon is caused by the overload of the capabilities of an agent, as time and cognitive resources required for exploration, deliberation, situation recognition, and habit formation, all increase as a function of the depth and richness of detail of an environment. Furthermore, the cognitive overload can be aggravated due to alterations (e.g. caused by stress) in the bounded rationality, i.e. the limited amount of resources available for the model-based component, in turn increasing the agent’s chances to develop or maintain addictive behaviours. Our study demonstrates that, independent of drug consumption, addictive behaviours can arise in the interaction between the environmental complexity and the biologically finite resources available to explore and represent it.
Empathy refers to the ability to perceive and share another person's affective state. Much neuroimaging evidence suggests that observing others' suffering and pain elicits activations of the anterior ...insular and the anterior cingulate cortices associated with subjective empathetic responses in the observer. However, these observations do not provide causal evidence for the respective roles of anterior insular and anterior cingulate cortices in empathetic pain. Therefore, whether these regions are 'necessary' for empathetic pain remains unknown. Herein, we examined the perception of others' pain in patients with anterior insular cortex or anterior cingulate cortex lesions whose locations matched with the anterior insular cortex or anterior cingulate cortex clusters identified by a meta-analysis on neuroimaging studies of empathetic pain perception. Patients with focal anterior insular cortex lesions displayed decreased discrimination accuracy and prolonged reaction time when processing others' pain explicitly and lacked a typical interference effect of empathetic pain on the performance of a pain-irrelevant task. In contrast, these deficits were not observed in patients with anterior cingulate cortex lesions. These findings reveal that only discrete anterior insular cortex lesions, but not anterior cingulate cortex lesions, result in deficits in explicit and implicit pain perception, supporting a critical role of anterior insular cortex in empathetic pain processing. Our findings have implications for a wide range of neuropsychiatric illnesses characterized by prominent deficits in higher-level social functioning.
Both cognitive and affective processes require mental resources. However, it remains unclear whether these 2 processes work in parallel or in an integrated fashion. In this functional magnetic ...resonance imaging study, we investigated their interaction using an empathy-for-pain paradigm, with simultaneous manipulation of cognitive demand of the tasks and emotional valence of the stimuli. Eighteen healthy adult participants viewed photographs showing other people's hands and feet in painful or nonpainful situations while performing tasks of low (body part judgment) and high (laterality judgment) cognitive demand. Behavioral data showed increased reaction times and error rates for painful compared with nonpainful stimuli under laterality judgment relative to body part judgment, indicating an interaction between cognitive demand and stimulus valence. Imaging analyses showed activity in bilateral anterior insula (AI) and primary somatosensory cortex (SI), but not posterior insula, for main effects of cognitive demand and stimulus valence. Importantly, cognitive demand and stimulus valence showed a significant interaction in AI, SI, and regions of the frontoparietal network. These results suggest that cognitive and emotional processes at least partially share common brain networks and that AI might serve as a key node in a brain network subserving cognition-emotion integration.
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