Xiaosi Gu

Attention and reality constraints on the neural processes of empathy for pain

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 ones 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.

Anterior Insular Cortex and Emotional Awareness

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 peoples 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. J. Comp. Neurol. 521:3371‐3388, 2013.

Testing the behavioral interaction and integration of attentional networks

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 include detecting 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 attention 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.

Neural consequences of religious belief on self-referential processing

Abstract Christianity strongly encourages its believers to surrender to God and to judge the self from Gods perspective. We used functional MRI to assess whether this religious belief is associated with neural correlates of self-referential processing distinct from that of non-religious people. Non-religious and Christian participants were scanned while performing tasks of personal-trait judgments regarding the self or public persons. We found that, while self-judgment was linked to better memory of traits related to the self than to others, self-referential processing induced increased activity in the ventral medial prefrontal cortex (MPFC) for non-religious participants but in the dorsal MPFC for Christian participants. In addition, the dorsal MPFC activity was positively correlated with the rating scores of the importance of Jesus’ judgment in subjective evaluation of a persons personality. Because the ventral and dorsal MPFC are respectively engaged in representation of stimulus self-relevance and evaluation of self-referential stimuli, our findings suggest that Christian beliefs result in weakened neural coding of stimulus self-relatedness but enhanced neural activity underlying evaluative processes applied to self-referential stimuli.

Cognition–Emotion Integration in the Anterior Insular Cortex

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 peoples 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.

Spontaneous Brain Activity Relates to Autonomic Arousal

Although possible sources and functions of the resting-state networks (RSNs) 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 RSNs. 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 RSNs are associated with changes in nonspecific 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.”

Somatic and vicarious pain are represented by dissociable multivariate brain patterns

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. DOI: http://dx.doi.org/10.7554/eLife.15166.001

Neural substrates of self-referential processing in Chinese Buddhists.

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.

Involvement of the anterior cingulate and frontoinsular cortices in rapid processing of salient facial emotional information

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. 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.

Neural substrates underlying evaluation of pain in actions depicted in words

Previous research has shown that evaluation of pain shown in pictures is mediated by a cortical circuit consisting of the primary and secondary somatosensory cortex (SI and SII), the anterior cingulate cortex (ACC), and the insula. SI and SII subserve the sensory-discriminative component of pain processing whereas ACC and the insula mediate the affective-motivational aspect of pain processing. The current work investigated the neural correlates of evaluation of pain depicted in words. Subjects were scanned using functional magnetic resonance imaging (fMRI) while reading words or phrases depicting painful or neutral actions. Subjects were asked to rate pain intensity of the painful actions depicted in words or counting the number of Chinese characters in the words. Relative to the counting task, rating pain intensity induced activations in SII, the insula, the right middle frontal gyrus, the left superior temporal sulcus and the left middle occipital gyrus. Our results suggest that both the sensory-discriminative and affective-motivational components of the pain matrix are engaged in the processing of pain depicted in words.