Voluntary control of anterior insula and its functional connections is feedback-independent and increases pain empathy

Yao, Shuxia; Becker, Benjamin; Geng, Yayuan; Zhao, Zhiying; Xu, Xiaoling; Zhao, Weihua; Ren, Peng; Kendrick, Keith M.

doi:10.1016/j.neuroimage.2016.02.035

Cited by 73 publications

(100 citation statements)

References 72 publications

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“…These findings are in line with previous studies evaluating transfer and maintenance effects of rt-fMRI NF-assisted control over regional brain activity [31, 75], and additionally suggest that successful neuromodulatory control on the pathway level can last beyond the duration of the initial training and thus transfer to contexts outside of the MRI environment. However, despite maintenance of the neural training success, attenuation of anxiety levels following the training of the target pathway as observed on day 1 was not maintained over the follow-up period [for similar results, see 31]. …”

Section: Discussionsupporting

confidence: 91%

“…Two-way repeated-measures ANOVA with the factors training (EXP vs. SHC) and time (run 1 + run 2 vs. run 3 + run 4) and connectivity strengths of the target pathway as dependent variable [31, 52] revealed a significant training × time interaction effect ( F 1, 21 = 4.47, p = 0.047). Post hoc comparisons demonstrated that connectivity in the target pathway increased over the course of the EXP training (run 3 + run 4 > run 1 + run 2, t 22 = 2.81, p = 0.010, Cohen’s d = 0.79, paired t test, two-tailed).…”

Section: Resultsmentioning

confidence: 99%

“…22) by means of repeated-measure ANOVAs (analysis of variance) and Bonferroni-corrected post hoc tests. In line with previous studies evaluating the functional and clinical relevance of rt-fMRI NFTs [31, 52] training success was assessed by comparing changes in connectivity strengths between the early stages of learning (first 2 runs) and later stages of the training during which successful control has been implemented (run 3 + run 4 > run 1 + run 2). Training-induced changes in subjective anxiety levels as assessed by the VAS administered before and after each training session served as the primary behavioral outcome.…”

Section: Methodsmentioning

confidence: 99%

“…Within this context, the emergence of real-time functional magnetic resonance imaging neurofeedback (rt-fMRI NF) training (NFT) approaches that allow subjects to gain volitional control over regional brain activity have been considered as a putatively promising strategy [28-30]. Importantly, previous studies have confirmed this potential of rt-fMRI NF by demonstrating that training success in terms of control over regional activity can be maintained beyond the training session [31-34], and that training-induced neural activity changes can modulate emotional experience in healthy subjects [31] and patients with major depression [32-35]. …”

Section: Introductionmentioning

confidence: 99%

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Real-Time Functional Connectivity-Informed Neurofeedback of Amygdala-Frontal Pathways Reduces Anxiety

Zhao

Yao

et al. 2019

Psychother Psychosom

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Background: Deficient emotion regulation and exaggerated anxiety represent a major transdiagnostic psychopathological marker. On the neural level these deficits have been closely linked to impaired, yet treatment-sensitive, prefrontal regulatory control over the amygdala. Gaining direct control over these pathways could therefore provide an innovative and promising intervention to regulate exaggerated anxiety. To this end the current proof-of-concept study evaluated the feasibility, functional relevance and maintenance of a novel connectivity-informed real-time fMRI neurofeedback training. Methods: In a randomized crossover sham-controlled design, 26 healthy subjects with high anxiety underwent real-time fMRI-guided neurofeedback training to enhance connectivity between the ventrolateral prefrontal cortex (vlPFC) and the amygdala (target pathway) during threat exposure. Maintenance of regulatory control was assessed after 3 days and in the absence of feedback. Training-induced changes in functional connectivity of the target pathway and anxiety ratings served as primary outcomes. Results: Training of the target, yet not the sham control, pathway significantly increased amygdala-vlPFC connectivity and decreased levels of anxiety. Stronger connectivity increases were significantly associated with higher anxiety reduction on the group level. At the follow-up, volitional control over the target pathway was maintained in the absence of feedback. Conclusions: The present results demonstrate for the first time that successful self-regulation of amygdala-prefrontal top-down regulatory circuits may represent a novel intervention to control anxiety. As such, the present findings underscore both the critical contribution of amygdala-prefrontal circuits to emotion regulation and the therapeutic potential of connectivity-informed real-time neurofeedback.

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Section: Discussionsupporting

confidence: 91%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Real-Time Functional Connectivity-Informed Neurofeedback of Amygdala-Frontal Pathways Reduces Anxiety

Zhao

Yao

et al. 2019

Psychother Psychosom

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“…The present study should be considered a convenient example towards the realization of this strategy, and it is in line with concurrent efforts and suggestions forwarded by globally operating initiatives such as TINNET (http://tinnet.tinnitusresearch.net/). We were not surprised to notice a relationship between distress and insular morphology as this sub-sylvian area can be conceived as an interface between the auditory system [70,71] and the emotional brain circuitry [72] in the human brain. Along the same lines, Leaver and coworkers [34] observed a positive relationship between tinnitus distress and CT in the left anterior insula.…”

Section: Discussionmentioning

confidence: 97%

Differential tinnitus-related neuroplastic alterations of cortical thickness and surface area

et al. 2016

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Structural neuroimaging techniques have been used to identify cortical and subcortical regions constituting the neuroarchitecture of tinnitus. One recent investigation used voxel-based morphometry (VBM) to analyze a sample of tinnitus patients (TI, n=257) [1]. A negative relationship between individual distress and cortical volume (CV) in bilateral auditory regions was observed. However, CV has meanwhile been identified as a neuroanatomical measurement that confounds genetically distinct neuroanatomical traits, namely cortical thickness (CT) and cortical surface area (CSA). We performed a re-analysis of the identical sample using the automated FreeSurfer surface-based morphometry (SBM) approach [2]. First, we replicated the negative correlation between tinnitus distress and bilateral supratemporal gray matter volume. Second, we observed a negative correlation for CSA in the left peri-auditory cortex and anterior insula. Furthermore, we noted a positive correlation between tinnitus duration and CT in the left peri-auditory cortex as well as a negative correlation in the subcallosal anterior cingulate, a region collated to the serotonergic circuit and germane to inhibitory functions. In short, the results elucidate differential neuroanatomical alterations of CSA and CT for the two independent tinnitus-related psychological traits distress and duration. Beyond this, the study provides further evidence for the distinction and specific susceptibility of CSA and CT within the context of neuroplasticity of the human brain. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. A negative relationship between individual distress and cortical volume (CV) in bilateral auditory regions was observed. However, CV has meanwhile been identified as a neuroanatomical measurement that confounds genetically distinct neuroanatomical traits, namely cortical thickness (CT) and cortical surface area (CSA). We performed a re-analysis of the identical sample using the automated FreeSurfer surface-based morphometry (SBM) approach [2]. First, we replicated the negative correlation between tinnitus distress and bilateral supratemporal gray matter volume. Second, we observed a negative correlation for CSA in the left peri-auditory cortex and anterior insula. Furthermore, we noted a positive correlation between tinnitus duration and CT in the left peri-auditory cortex as well as a negative correlation in the subcallosal anterior cingulate, a region collated to the serotonergic circuit and germane to inhibitory functions. In short, the results elucidate differential neuroanatomical alterations of CSA and CT for the two independent...

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Linking brain structure and activation in anterior insula cortex to explain the trait empathy for pain

Zhang

et al. 2019

Human Brain Mapping

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The ability to perceive, understand, and react to the feelings of others' pain is referred to as empathy for pain which is composed of two components, affectiveperceptual empathy and cognitive-evaluative empathy. Recent reviews on the neural mechanisms of empathetic pain showed the anterior insula (AI) cortex as a core circuit for empathy. However, little is known about the modulation of brain anatomy and empathic responses by trait measures of empathy (trait empathy). Thus, we investigated whether individual variation in the personality trait of empathy is associated with individual variation in the structure of specific brain regions using voxelbased morphometry (VBM). We further investigated the relationship between the trait empathy and the activity of the same regions using state measures of empathy for pain in a trial-by-trial fashion in the given situation. VBM analysis indicated a small but significant negative relationship between trait empathy and gray matter volume in the bilateral AI. Functional MRI study further demonstrated that experimentally induced activity of the bilateral AI during state empathy for pain was also correlated with trait empathy. An asymmetry exists between the right and left AI between the affective and cognitive empathy. The right AI was found to be involved in the affective-perceptual form of empathy and the left AI was active in cognitiveevaluative forms of empathy. The interindividual differences in trait empathy may be reflected both in the state empathy and more stable brain structure difference. K E Y W O R D Santerior insula cortex, empathy for pain, gray matter volume, trait empathy

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Voluntary control of anterior insula and its functional connections is feedback-independent and increases pain empathy

Cited by 73 publications

References 72 publications

Real-Time Functional Connectivity-Informed Neurofeedback of Amygdala-Frontal Pathways Reduces Anxiety

Real-Time Functional Connectivity-Informed Neurofeedback of Amygdala-Frontal Pathways Reduces Anxiety

Differential tinnitus-related neuroplastic alterations of cortical thickness and surface area

Linking brain structure and activation in anterior insula cortex to explain the trait empathy for pain

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