Using real-time fMRI to learn voluntary regulation of the anterior insula in the presence of threat-related stimuli.

Previous studies have shown that healthy participants learn to control local brain activity with operant training by using real-time functional magnetic resonance imaging (rt-fMRI). Very little data exist, however, on the dynamics of interaction between critical brain regions during rt-fMRI-based training. Here, we examined self-regulation of stimulus-elicited insula activation and performed a psychophysiological interaction (PPI) analysis of real-time self-regulation data. During voluntary up-regulation of the left anterior insula in the presence of threat-related pictures, differential activations were observed in the ventrolateral prefrontal cortex, the frontal operculum, the middle cingulate cortex and the right insula. Down-regulation in comparison to no-regulation revealed additional activations in right superior temporal cortex, right inferior parietal cortex and right middle frontal cortex. There was a significant learning effect over sessions during up-regulation, documented by a significant improvement of anterior insula control over time. Connectivity analysis revealed that successful up-regulation of the activity in left anterior insula while viewing aversive pictures was directly modulated by dorsomedial and ventrolateral prefrontal cortex. Down-regulation of activity was more difficult to achieve and no learning effect was observed. More extensive training might be necessary for successful down-regulation. These findings illustrate the functional interactions between different brain areas during regulation of anterior insula activity in the presence of threat-related stimuli.

[1]  H. Critchley,et al.  Neural systems supporting interoceptive awareness , 2004, Nature Neuroscience.

[2]  M. Erb,et al.  Brain activity underlying emotional valence and arousal: A response‐related fMRI study , 2004, Human brain mapping.

[3]  Michael Erb,et al.  Physiological self-regulation of regional brain activity using real-time functional magnetic resonance imaging (fMRI): methodology and exemplary data , 2003, NeuroImage.

[4]  J. Gross,et al.  The cognitive control of emotion , 2005, Trends in Cognitive Sciences.

[5]  Rainer Goebel,et al.  Neurofeedback: A promising tool for the self-regulation of emotion networks , 2010, NeuroImage.

[6]  Wolfgang Grodd,et al.  Regulation of anterior insular cortex activity using real-time fMRI , 2007, NeuroImage.

[7]  Niels Birbaumer,et al.  LEARNED CONTROL OF INSULAR ACTIVITY USING fMRI BRAIN COMPUTER INTERFACE IN SCHIZOPHRENIA , 2008, Schizophrenia Research.

[8]  Sven Haller,et al.  Real-time fMRI feedback training may improve chronic tinnitus , 2010, European Radiology.

[9]  Andrew L. Alexander,et al.  Contextual Modulation of Amygdala Responsivity to Surprised Faces , 2004, Journal of Cognitive Neuroscience.

[10]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[11]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[12]  Hugo D. Critchley,et al.  Volitional Control of Autonomic Arousal: A Functional Magnetic Resonance Study , 2002, NeuroImage.

[13]  J. Gross,et al.  The Neural Bases of Emotion Regulation: Reappraisal and Suppression of Negative Emotion , 2008, Biological Psychiatry.

[14]  S. Thompson-Schill,et al.  Modulation of Amygdalar Activity by the Conscious Regulation of Negative Emotion , 2002, Journal of Cognitive Neuroscience.

[15]  M. Beauregard,et al.  Neural Correlates of Conscious Self-Regulation of Emotion , 2001, The Journal of Neuroscience.

[16]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[17]  Frank Schneider,et al.  Real-time fMRI of temporolimbic regions detects amygdala activation during single-trial self-induced sadness , 2003, NeuroImage.

[18]  Kevin Murphy,et al.  Individual differences in the functional neuroanatomy of inhibitory control , 2006, Brain Research.

[19]  K. Luan Phan,et al.  Subjective rating of emotionally salient stimuli modulates neural activity , 2003, NeuroImage.

[20]  A. Young,et al.  Neuropsychology of fear and loathing , 2001 .

[21]  Gary H Glover,et al.  Modulation of subgenual anterior cingulate cortex activity with real‐time neurofeedback , 2011, Human brain mapping.

[22]  Heather L. Urry,et al.  Amygdala and Ventromedial Prefrontal Cortex Are Inversely Coupled during Regulation of Negative Affect and Predict the Diurnal Pattern of Cortisol Secretion among Older Adults , 2006, The Journal of Neuroscience.

[23]  A. Craig,et al.  Pain mechanisms: labeled lines versus convergence in central processing. , 2003, Annual review of neuroscience.

[24]  R. Davidson,et al.  Dysfunction in the neural circuitry of emotion regulation--a possible prelude to violence. , 2000, Science.

[25]  John D E Gabrieli,et al.  Control over brain activation and pain learned by using real-time functional MRI. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Tatia M.C. Lee,et al.  Neural correlates of regulation of positive and negative emotions: An fMRI study , 2009, Neuroscience Letters.

[27]  Niels Birbaumer,et al.  Real-time support vector classification and feedback of multiple emotional brain states , 2011, NeuroImage.

[28]  B. Mensour,et al.  Neural circuitry underlying voluntary suppression of sadness , 2003, Biological Psychiatry.

[29]  Niels Birbaumer,et al.  Volitional Control of Anterior Insula Activity Modulates the Response to Aversive Stimuli. A Real-Time Functional Magnetic Resonance Imaging Study , 2010, Biological Psychiatry.

[30]  D. Weinberger,et al.  Neocortical modulation of the amygdala response to fearful stimuli , 2003, Biological Psychiatry.

[31]  Tilo Kircher,et al.  Acquired self‐control of insula cortex modulates emotion recognition and brain network connectivity in schizophrenia , 2013, Human brain mapping.

[32]  Keith M. Shafritz,et al.  The interaction of emotional and cognitive neural systems in emotionally guided response inhibition , 2006, NeuroImage.

[33]  J. Duncan,et al.  Prefrontal cortical function and anxiety: controlling attention to threat-related stimuli , 2004, Nature Neuroscience.

[34]  Niels Birbaumer,et al.  Hemodynamic brain-computer interfaces for communication and rehabilitation , 2009, Neural Networks.

[35]  S. Clare,et al.  Imaging how attention modulates pain in humans using functional MRI. , 2002, Brain : a journal of neurology.

[36]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[37]  J. Gabrieli,et al.  Rethinking Feelings: An fMRI Study of the Cognitive Regulation of Emotion , 2002, Journal of Cognitive Neuroscience.

[38]  N. Birbaumer,et al.  fMRI Brain-Computer Interfaces , 2008, IEEE Signal Processing Magazine.

[39]  E. Kandel,et al.  Resolving Emotional Conflict: A Role for the Rostral Anterior Cingulate Cortex in Modulating Activity in the Amygdala , 2006, Neuron.

[40]  R. Lane,et al.  Neuroanatomical correlates of happiness, sadness, and disgust. , 1997, The American journal of psychiatry.

[41]  Jennifer S. Beer,et al.  Prefrontal involvement in the regulation of emotion: convergence of rat and human studies , 2006, Current Opinion in Neurobiology.

[42]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[43]  George Bush,et al.  The emotional counting stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division , 1998, Biological Psychiatry.

[44]  Kevin N. Ochsner,et al.  For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion , 2004, NeuroImage.

[45]  R. Veit,et al.  Regulation of emotional responses elicited by threat‐related stimuli , 2007, Human brain mapping.

[46]  Jieun Kim,et al.  Investigating the neural basis for fMRI-based functional connectivity in a blocked design: application to interregional correlations and psycho-physiological interactions. , 2008, Magnetic resonance imaging.

[47]  O. Pollatos,et al.  Neural systems connecting interoceptive awareness and feelings , 2007, Human brain mapping.

[48]  Hugo D Critchley,et al.  Imitating expressions: emotion-specific neural substrates in facial mimicry. , 2006, Social cognitive and affective neuroscience.

[49]  Heidi Johansen-Berg,et al.  Faculty of 1000 evaluation for Acquired control of ventral premotor cortex activity by feedback training: an exploratory real-time FMRI and TMS study. , 2012 .

[50]  Karl J. Friston,et al.  Dynamic causal modeling , 2010, Scholarpedia.

[51]  Niels Birbaumer,et al.  Acquired Control of Ventral Premotor Cortex Activity by Feedback Training , 2012, Neurorehabilitation and neural repair.

[52]  J. D Steele,et al.  Segregation of cognitive and emotional function in the prefrontal cortex: a stereotactic meta-analysis , 2004, NeuroImage.

[53]  Hugo D. Critchley,et al.  Modulation of Emotional Appraisal by False Physiological Feedback during fMRI , 2007, PloS one.

[54]  Ravi S. Menon,et al.  Imaging Attentional Modulation of Pain in the Periaqueductal Gray in Humans , 2002, The Journal of Neuroscience.

[55]  K. Phan,et al.  Neural substrates for voluntary suppression of negative affect: A functional magnetic resonance imaging study , 2005, Biological Psychiatry.

[56]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[57]  J. Mazziotta,et al.  Modulating emotional responses: effects of a neocortical network on the limbic system , 2000, Neuroreport.

[58]  R. Kalisch The functional neuroanatomy of reappraisal: Time matters , 2009, Neuroscience & Biobehavioral Reviews.

[59]  D. Perrett,et al.  A differential neural response in the human amygdala to fearful and happy facial expressions , 1996, Nature.

[60]  R. Deichmann,et al.  Real-time functional magnetic resonance imaging: methods and applications. , 2007, Magnetic resonance imaging.

[61]  Jin Fan,et al.  Neural correlates of using distancing to regulate emotional responses to social situations , 2010, Neuropsychologia.

[62]  Niels Birbaumer,et al.  Detection of Cerebral Reorganization Induced by Real-Time fMRI Feedback Training of Insula Activation , 2011, Neurorehabilitation and neural repair.