Influential theories of human emotion argue that subjective feeling states involve representation of bodily responses elicited by emotional events. Within this framework, individual differences in intensity of emotional experience reflect variation in sensitivity to internal bodily responses. We measured regional brain activity by functional magnetic resonance imaging (fMRI) during an interoceptive task wherein subjects judged the timing of their own heartbeats. We observed enhanced activity in insula, somatomotor and cingulate cortices. In right anterior insular/opercular cortex, neural activity predicted subjects' accuracy in the heartbeat detection task. Furthermore, local gray matter volume in the same region correlated with both interoceptive accuracy and subjective ratings of visceral awareness. Indices of negative emotional experience correlated with interoceptive accuracy across subjects. These findings indicate that right anterior insula supports a representation of visceral responses accessible to awareness, providing a substrate for subjective feeling states.
Interoception refers to the sensing of internal bodily changes. Interoception interacts with cognition and emotion, making measurement of individual differences in interoceptive ability broadly relevant to neuropsychology. However, inconsistency in how interoception is defined and quantified led to a three-dimensional model. Here, we provide empirical support for dissociation between dimensions of: (1) interoceptive accuracy (performance on objective behavioural tests of heartbeat detection), (2) interoceptive sensibility (self-evaluated assessment of subjective interoception, gauged using interviews/questionnaires) and (3) interoceptive awareness (metacognitive awareness of interoceptive accuracy, e.g. confidence-accuracy correspondence). In a normative sample (N=80), all three dimensions were distinct and dissociable. Interoceptive accuracy was only partly predicted by interoceptive awareness and interoceptive sensibility. Significant correspondence between dimensions emerged only within the sub-group of individuals with greatest interoceptive accuracy. These findings set the context for defining how the relative balance of accuracy, sensibility and awareness dimensions explain cognitive, emotional and clinical associations of interoceptive ability.
Temporal difference learning has been proposed as a model for Pavlovian conditioning, in which an animal learns to predict delivery of reward following presentation of a conditioned stimulus (CS). A key component of this model is a prediction error signal, which, before learning, responds at the time of presentation of reward but, after learning, shifts its response to the time of onset of the CS. In order to test for regions manifesting this signal profile, subjects were scanned using event-related fMRI while undergoing appetitive conditioning with a pleasant taste reward. Regression analyses revealed that responses in ventral striatum and orbitofrontal cortex were significantly correlated with this error signal, suggesting that, during appetitive conditioning, computations described by temporal difference learning are expressed in the human brain.
Influential theoretical models propose a central role for afferent information from the body in the expression of emotional feeling states. Feedback representations of changing states of bodily arousal influence learning and facilitate concurrent and prospective decision-making. Functional neuroimaging studies have increased understanding of brain mechanisms that generate changes in autonomic arousal during behavior and those which respond to internal feedback signals to influence subjective feeling states. In particular, anterior cingulate cortex is implicated in generating autonomic changes, while insula and orbitofrontal cortices may be specialized in mapping visceral responses. Independently, ventromedial prefrontal cortex is recognized to support processes of internal (self-) reference that predominate in states of rest and disengagement and which putatively serve as a benchmark for dynamic interactions with the environment. Lesion data further highlight the integrated role of these cortical regions in autonomic and motivational control. In computational models of control, forward (efference copies) and inverse models are proposed to enable prediction and correction of action and, by extension, the interpretation of the behavior of others. It is hypothesized that the neural substrate for these processes during motivational and affective behavior lies within the interactions of anterior cingulate, insula, and orbitofrontal cortices. Generation of visceral autonomic correlates of control reinforce experiential engagement in simulatory models and underpin concepts such as somatic markers to bridge the dualistic divide.
Human anterior cingulate function has been explained primarily within a cognitive framework. We used functional MRI experiments with simultaneous electrocardiography to examine regional brain activity associated with autonomic cardiovascular control during performance of cognitive and motor tasks. Using indices of heart rate variability, and high- and low-frequency power in the cardiac rhythm, we observed activity in the dorsal anterior cingulate cortex (ACC) related to sympathetic modulation of heart rate that was dissociable from cognitive and motor-related activity. The findings predict that during effortful cognitive and motor behaviour the dorsal ACC supports the generation of associated autonomic states of cardiovascular arousal. We subsequently tested this prediction by studying three patients with focal damage involving the ACC while they performed effortful cognitive and motor tests. Each showed abnormalities in autonomic cardiovascular responses with blunted autonomic arousal to mental stress when compared with 147 normal subjects tested in identical fashion. Thus, converging neuroimaging and clinical findings suggest that ACC function mediates context-driven modulation of bodily arousal states.
We describe a theoretical model of the neurocognitive mechanisms underlying conscious presence and its disturbances. The model is based on interoceptive prediction error and is informed by predictive models of agency, general models of hierarchical predictive coding and dopaminergic signaling in cortex, the role of the anterior insular cortex (AIC) in interoception and emotion, and cognitive neuroscience evidence from studies of virtual reality and of psychiatric disorders of presence, specifically depersonalization/derealization disorder. The model associates presence with successful suppression by top-down predictions of informative interoceptive signals evoked by autonomic control signals and, indirectly, by visceral responses to afferent sensory signals. The model connects presence to agency by allowing that predicted interoceptive signals will depend on whether afferent sensory signals are determined, by a parallel predictive-coding mechanism, to be self-generated or externally caused. Anatomically, we identify the AIC as the likely locus of key neural comparator mechanisms. Our model integrates a broad range of previously disparate evidence, makes predictions for conjoint manipulations of agency and presence, offers a new view of emotion as interoceptive inference, and represents a step toward a mechanistic account of a fundamental phenomenological property of consciousness.
Mental processes and their neural substrates are intimately linked to the homeostatic control of internal bodily state. There are a set of distinct interoceptive pathways that directly and indirectly influence brain functions. The anatomical organization of these pathways and the psychological/behavioral expressions of their influence appear along discrete, evolutionarily conserved dimensions that are tractable to a mechanistic understanding. Here, we review the role of these pathways as sources of biases to perception, cognition, emotion, and behavior and arguably the dynamic basis to the concept of self.
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