Computational models of reward processing suggest that foregone or fictive outcomes serve as important information sources for learning and augment those generated by experienced rewards (e.g. reward prediction errors). An outstanding question is how these learning signals interact with top-down cognitive influences, such as cognitive reappraisal strategies. Using a sequential investment task and functional magnetic resonance imaging, we show that the reappraisal strategy selectively attenuates the influence of fictive, but not reward prediction error signals on investment behavior; such behavioral effect is accompanied by changes in neural activity and connectivity in the anterior insular cortex, a brain region thought to integrate subjective feelings with high-order cognition. Furthermore, individuals differ in the extent to which their behaviors are driven by fictive errors versus reward prediction errors, and the reappraisal strategy interacts with such individual differences; a finding also accompanied by distinct underlying neural mechanisms. These findings suggest that the variable interaction of cognitive strategies with two important classes of computational learning signals (fictive, reward prediction error) represent one contributing substrate for the variable capacity of individuals to control their behavior based on foregone rewards. These findings also expose important possibilities for understanding the lack of control in addiction based on possibly foregone rewarding outcomes.
Decision-making; reward prediction errors; fictive learning; emotion regulation; reappraisal; insula; fMRI
Social norms and their enforcement are fundamental to human societies. The ability to detect deviations from norms and to adapt to norms in a changing environment is therefore important to individuals' normal social functioning. Previous neuroimaging studies have highlighted the involvement of the insular and ventromedial prefrontal (vmPFC) cortices in representing norms. However, the necessity and dissociability of their involvement remain unclear. Using model-based computational modeling and neuropsychological lesion approaches, we examined the contributions of the insula and vmPFC to norm adaptation in seven human patients with focal insula lesions and six patients with focal vmPFC lesions, in comparison with forty neurologically intact controls and six brain-damaged controls. There were three computational signals of interest as participants played a fairness game (ultimatum game): sensitivity to the fairness of offers, sensitivity to deviations from expected norms, and the speed at which people adapt to norms. Significant group differences were assessed using bootstrapping methods. Patients with insula lesions displayed abnormally low adaptation speed to norms, yet detected norm violations with greater sensitivity than controls. Patients with vmPFC lesions did not have such abnormalities, but displayed reduced sensitivity to fairness and were more likely to accept the most unfair offers. These findings provide compelling computational and lesion evidence supporting the necessary, yet dissociable roles of the insula and vmPFC in norm adaptation in humans: the insula is critical for learning to adapt when reality deviates from norm expectations, and that the vmPFC is important for valuation of fairness during social exchange.
brain lesion; computational modeling; decision-making; insular cortex; social norms; ventromedial prefrontal cortex
Autism spectrum disorders are associated with social and emotional deficits, the aetiology of which are not well understood. A growing consensus is that the autonomic nervous system serves a key role in emotional processes, by providing physiological signals essential to subjective states. We hypothesized that altered autonomic processing is related to the socio-emotional deficits in autism spectrum disorders. Here, we investigated the relationship between non-specific skin conductance response, an objective index of sympathetic neural activity, and brain fluctuations during rest in high-functioning adults with autism spectrum disorder relative to neurotypical controls. Compared with control participants, individuals with autism spectrum disorder showed less skin conductance responses overall. They also showed weaker correlations between skin conductance responses and frontal brain regions, including the anterior cingulate and anterior insular cortices. Additionally, skin conductance responses were found to have less contribution to default mode network connectivity in individuals with autism spectrum disorders relative to controls. These results suggest that autonomic processing is altered in autism spectrum disorders, which may be related to the abnormal socio-emotional behaviours that characterize this condition.
autism; autonomic nervous system; emotion; skin conductance; resting state
Political ideologies summarize dimensions of life that define how a person organizes their public and private behavior, including their attitudes associated with sex, family, education, and personal autonomy [1, 2]. Despite the abstract nature of such sensibilities, fundamental features of political ideology have been found to be deeply connected to basic biological mechanisms [3–7] that may serve to defend against environmental challenges like contamination and physical threat [8–12]. These results invite the provocative claim that neural responses to nonpolitical stimuli (like contaminated food or physical threats) should be highly predictive of abstract political opinions (like attitudes toward gun control and abortion) . We applied a machine-learning method to fMRI data to test the hypotheses that brain responses to emotionally evocative images predict individual scores on a standard political ideology assay. Disgusting images, especially those related to animal-reminder disgust (e.g., mutilated body), generate neural responses that are highly predictive of political orientation even though these neural predictors do not agree with participants’ conscious rating of the stimuli. Images from other affective categories do not support such predictions. Remarkably, brain responses to a single disgusting stimulus were sufficient to make accurate predictions about an individual subject’s political ideology. These results provide strong support for the idea that fundamental neural processing differences that emerge under the challenge of emotionally evocative stimuli may serve to structure political beliefs in ways formerly unappreciated.
•Literature suggests negativity bias might underlie variations in political views•fMRI responses to disgusting images accurately predict political orientation•Self-reports about affective images are not predictive of their political views•Single-stimulus data can reliably classify conservatives from liberals
Ahn et al. show that fMRI responses to disgusting images accurately predict political orientation. The effect is strong enough to elicit good classification of conservatives from liberals from single-stimulus data, suggesting that emotional processes play a much larger role in structuring our abstract political beliefs than we currently believe.
This paper reviews the foundation for a role of the human anterior insular cortex (AIC) in emotional awareness, defined as the conscious experience of emotions. We first introduce the neuroanatomical features of AIC and existing findings on emotional awareness. Using empathy, the awareness and understanding of other people’s emotional states, as a test case, we then present evidence to demonstrate: 1) AIC and anterior cingulate cortex (ACC) are commonly coactivated as revealed by a meta-analysis, 2) AIC is functionally dissociable from ACC, 3) AIC integrates stimulus-driven and top-down information, and 4) AIC is necessary for emotional awareness. We propose a model in which AIC serves two major functions: integrating bottom-up interoceptive signals with top-down predictions to generate a current awareness state and providing descending predictions to visceral systems that provide a point of reference for autonomic reflexes. We argue that AIC is critical and necessary for emotional awareness.
anterior insular cortex; emotional awareness; empathy; fMRI; meta-analysis; top-down; bottom-up; predictive coding
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.
cognition; emotion; empathy; fMRI; insula
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.
anterior cingulate cortex; anterior insular cortex; empathy; meta-analysis; necessity
Children with conduct problems (CP) persistently violate others’ rights and represent a considerable societal cost . These children also display atypical empathic responses to others’ distress , which may partly account for their violent and antisocial behavior. Callous traits index lack of empathy in these children and confer risk for adult psychopathy . Investigating neural responses to others’ pain is an ecologically valid method to probe empathic processing , but studies in children with CP have been inconclusive [5, 6]. Using functional magnetic resonance imaging (fMRI), we measured neural responses to pictures of others in pain (versus no pain) in a large sample of children with CP and matched controls. Relative to controls, children with CP showed reduced blood oxygen level-dependent responses to others’ pain in bilateral anterior insula (AI), anterior cingulate cortex (ACC), and inferior frontal gyrus, regions associated with empathy for pain in previous studies [7, 8]. In the CP group, callous traits were negatively associated with responses to others’ pain in AI and ACC. We conclude that children with CP have atypical neural responses to others’ pain. The negative association between callous traits and AI/ACC response could reflect an early neurobiological marker indexing risk for empathic deficits seen in adult psychopathy.
•Children with conduct problems showed reduced neural responses to others’ pain•Reductions in anterior insula, anterior cingulate cortex, and inferior frontal gyrus•Callous traits associated with the magnitude of reduction•Findings may reflect early neurobiological risk for adult psychopathy
Although possible sources and functions of the resting state networks (RSN) of the brain have been proposed, most evidence relies on circular logic and reverse inference. We propose that autonomic arousal provides an objective index of psychophysiological states during rest that may also function as a driving source of the activity and connectivity of RSN. Recording blood oxygenation level-dependent (BOLD) signal using functional magnetic resonance imaging and skin conductance simultaneously during rest in human subjects, we found that the spontaneous fluctuations of BOLD signals in key nodes of RSN are associated with changes in non-specific skin conductance response, a sensitive psychophysiological index of autonomic arousal. Our findings provide evidence of an important role for the autonomic nervous system to the spontaneous activity of the brain during ‘rest’.
resting-state functional connectivity MRI; autonomic arousal; skin conductance response; interoception; consciousness
Although amnestic mild cognitive impairment (aMCI; often considered a prodromal phase of Alzheimer’s disease, AD) is most recognized by its implications for decline in memory function, research suggests that deficits in attention are present early in aMCI and may be predictive of progression to AD. The present study used functional magnetic resonance imaging to examine differences in the brain during the attention network test between 8 individuals with aMCI and 8 neurologically healthy, demographically matched controls. While there were no significant behavioral differences between groups for the alerting and orienting functions, patients with aMCI showed more activity in neural regions typically associated with the networks subserving these functions (e.g., temporoparietal junction and posterior parietal regions, respectively). More importantly, there were both behavioral (i.e., greater conflict effect) and corresponding neural deficits in executive control (e.g., less activation in the prefrontal and anterior cingulate cortices). Although based on a small number of patients, our findings suggest that deficits of attention, especially the executive control of attention, may significantly contribute to the behavioral and cognitive deficits of aMCI.
Attentional dysfunction is among the most consistent observations of autism spectrum disorders (ASD). However, the neural nature of this deficit in ASD is still unclear. In this study, we aimed to identify the neurobehavioral correlates of attentional dysfunction in ASD. We used the Attention Network Test-Revised and functional magnetic resonance imaging to examine alerting, orienting, and executive control functions, as well as the neural substrates underlying these attentional functions in unmedicated, high-functioning adults with ASD (n = 12) and matched healthy controls (HC, n = 12). Compared with HC, individuals with ASD showed increased error rates in alerting and executive control, accompanied by lower activity in the mid-frontal gyrus and the caudate nucleus for alerting, and by the absence of significant functional activation in the anterior cingulate cortex (ACC) for executive control. In addition, greater behavioral deficiency in executive control in ASD was correlated with less functional activation of the ACC. These findings of behavioral and neural abnormalities in alerting and executive control of attention in ASD may suggest core attentional deficits, which require further investigation.
Alerting; anterior cingulate cortex; attentional networks; autism; executive control
The anterior cingulate cortex (ACC) and frontoinsular cortex (FI) have been implicated in processing information across a variety of domains, including those related to attention and emotion. However, their role in rapid information processing, for example, as required for timely processing of salient stimuli, is not well understood. Here, we designed an emotional face priming paradigm and employed functional magnetic resonance imaging to elucidate their role in these mechanisms. Target faces with either neutral or fearful emotion were briefly primed by either neutral or fearful faces, or by blank ovals. Activation in the pregenual ACC and the FI, together with other regions, such as the amygdala, were preferentially activated in response to fearful face priming, suggesting that these regions are involved in the rapid processing of salient facial emotional information.
anterior cingulate cortex; emotion; fMRI; frontoinsular cortex; priming
Our recent work showed that self-trait judgment is associated with increased activity in the ventral medial prefrontal cortex (VMPFC) in non-religious Chinese, but in the dorsal medial prefrontal cortex (DMPFC) in Chinese Christians. The current work further investigated neural substrates of self-referential processing in Chinese Buddhists. Using functional magnetic resonance imaging, we scanned 14 Chinese Buddhists, while they conducted trait judgments of the self, Zhu Rongji (the former Chinese premier), Sakyamuni (the Buddhist leader) and Jesus (the Christian leader). We found that, relative to Zhu Rongji judgment, self-judgment in Buddhist participants failed to generate increased activation in the VMPFC but induced increased activations in the DMPFC/rostral anterior cingulate cortex, midcingulate and the left frontal/insular cortex. Self-judgment was also associated with decreased functional connectivity between the DMPFC and posterior parietal cortex compared with Zhu Rongji judgment. The results suggest that Buddhist doctrine of No-self results in weakened neural coding of stimulus self-relatedness in the VMPFC, but enhanced evaluative processes of self-referential stimuli in the DMPFC. Moreover, self-referential processing in Buddhists is characterized by monitoring the conflict between the doctrine of No-self and self-focus thinking during self-trait judgment.
self; Buddhist; fMRI; medial prefrontal cortex; midcingulate
The frontoinsular cortex (FI) and the anterior cingulate cortex (ACC) are known to be involved in empathy for others’ pain. However, the functional roles of FI and ACC in empathetic responses have not yet been clearly dissociated in previous studies. In this study, participants viewed color photographs depicting human body parts (hands or feet) in painful or non-painful situations and performed either pain judgment (painful/non-painful) or laterality judgment (left/right) of the body parts. We found that activation of FI, rather than ACC, showed significant increase for painful compared to non-painful images, regardless of the task requirement. These findings suggest a clear functional dissociation between FI and ACC in which FI is more domain-specific than ACC in processing of empathy for pain.
empathy; fMRI; insula; anterior cingulate cortex; pain; Emotion
One current conceptualization of attention subdivides it into functions of alerting, orienting, and executive control. Alerting describes the function of tonically maintaining the alert state and phasically responding to a warning signal. Automatic and voluntary orienting are involved in the selection of information among multiple sensory inputs. Executive control describes a set of more complex operations that includes monitoring and resolving conflicts in order to control thoughts or behaviors. Converging evidence supports this theory of attention by showing that each function appears to be subserved by anatomically distinct networks in the brain and differentially innervated by various neuromodulatory systems. Although much research has been dedicated to understanding the functional separation of these networks in both healthy and disease states, the interaction and integration among these networks still remain unclear. In this study, we aimed to characterize possible behavioral interaction and integration in healthy adult volunteers using a revised attentional network test (ANT-R) with cue-target interval and cue validity manipulations. We found that whereas alerting improves overall response speed, it exerts negative influence on executive control under certain conditions. A valid orienting cue enhances but an invalid cue diminishes the ability of executive control to overcome conflict. The results support the hypothesis of functional integration and interaction of these brain networks.
attention; attentional networks; alerting; orienting; executive control
Alexithymia is a personality trait characterized by deficiency in understanding, processing, or describing emotions. Recent studies have revealed that alexithymia is associated with less activation of the anterior cingulate cortex, a brain region shown to play a role in cognitive and emotional processing. However, few studies have directly investigated the cognitive domain in relation to alexithymia to examine whether alexithymic trait is related to less efficient voluntary control.
Methodology/ Principal Findings
We examined the relationship between alexithymic trait and voluntary control in a group of healthy volunteers. We used the 20-item Toronto Alexithymia Scale (TAS-20) to measure alexithymic trait. Additionally, we examined state and trait voluntary control using the revised Attention Network Test (ANT-R) and the Adult Temperament Questionnaire (ATQ), respectively. Alexithymic trait was positively correlated with the overall reaction time of the ANT-R, and negatively correlated with the Effortful Control factor of the ATQ.
Our results suggest that alexithymic trait is associated with less efficient voluntary control.
Computational models of reward processing suggest that foregone or fictive outcomes serve as important information sources for learning and augment those generated by experienced rewards (e.g. reward prediction errors). An outstanding question is how these learning signals interact with top-down cognitive influences, such as cognitive reappraisal strategies. Using a sequential investment task and functional magnetic resonance imaging, we show that the reappraisal strategy selectively attenuates the influence of fictive, but not reward prediction error signals on investment behavior; such behavioral effect is accompanied by changes in neural activity and connectivity in the anterior insular cortex, a brain region thought to integrate subjective feelings with high-order cognition. Furthermore, individuals differ in the extent to which their behaviors are driven by fictive errors versus reward prediction errors, and the reappraisal strategy interacts with such individual differences; a finding also accompanied by distinct underlying neural mechanisms. These findings suggest that the variable interaction of cognitive strategies with two important classes of computational learning signals (fictive, reward prediction error) represent one contributing substrate for the variable capacity of individuals to control their behavior based on foregone rewards. These findings also expose important possibilities for understanding the lack of control in addiction based on possibly foregone rewarding outcomes. Hum Brain Mapp 35:3738–3749, 2014.
decision-making; reward prediction errors; fictive learning; emotion regulation; reappraisal; insula; fMRI