Self-regulation of the anterior insula: Reinforcement learning using real-time fMRI neurofeedback

The anterior insula (AI) plays a key role in affective processing, and insular dysfunction has been noted in several clinical conditions. Real-time functional MRI neurofeedback (rtfMRI-NF) provides a means of helping people learn to self-regulate activation in this brain region. Using the Blood Oxygenated Level Dependant (BOLD) signal from the right AI (RAI) as neurofeedback, we trained participants to increase RAI activation. In contrast, another group of participants was shown 'control' feedback from another brain area. Pre- and post-training affective probes were shown, with subjective ratings and skin conductance response (SCR) measured. We also investigated a reward-related reinforcement learning model of rtfMRI-NF. In contrast to the controls, we hypothesised a positive linear increase in RAI activation in participants shown feedback from this region, alongside increases in valence ratings and SCR to affective probes. Hypothesis-driven analyses showed a significant interaction between the RAI/control neurofeedback groups and the effect of self-regulation. Whole-brain analyses revealed a significant linear increase in RAI activation across four training runs in the group who received feedback from RAI. Increased activation was also observed in the caudate body and thalamus, likely representing feedback-related learning. No positive linear trend was observed in the RAI in the group receiving control feedback, suggesting that these data are not a general effect of cognitive strategy or control feedback. The control group did, however, show diffuse activation across the putamen, caudate and posterior insula which may indicate the representation of false feedback. No significant training-related behavioural differences were observed for valence ratings, or SCR. In addition, correlational analyses based on a reinforcement learning model showed that the dorsal anterior cingulate cortex underpinned learning in both groups. In summary, these data demonstrate that it is possible to regulate the RAI using rtfMRI-NF within one scanning session, and that such reward-related learning is mediated by the dorsal anterior cingulate.

[1]  Daniel S. Margulies,et al.  Mapping the functional connectivity of anterior cingulate cortex , 2007, NeuroImage.

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

[3]  Hans-Jochen Heinze,et al.  Differential parametric modulation of self‐relatedness and emotions in different brain regions , 2009, Human brain mapping.

[4]  Wolfgang Grodd,et al.  Principles of a brain-computer interface (BCI) based on real-time functional magnetic resonance imaging (fMRI) , 2004, IEEE Transactions on Biomedical Engineering.

[5]  Sven Haller,et al.  Real-time fMRI neurofeedback: Progress and challenges , 2013, NeuroImage.

[6]  J. Spillane Journal Of Neurology , 2005 .

[7]  Kevin A. Johnson,et al.  Volitional reduction of anterior cingulate cortex activity produces decreased cue craving in smoking cessation: a preliminary real‐time fMRI study , 2013, Addiction biology.

[8]  Stefan Schmidt,et al.  Measuring mindfulness—the Freiburg Mindfulness Inventory (FMI) , 2006 .

[9]  J. O'Doherty,et al.  Model‐Based fMRI and Its Application to Reward Learning and Decision Making , 2007, Annals of the New York Academy of Sciences.

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

[11]  W. K. Simmons,et al.  Self-Regulation of Amygdala Activation Using Real-Time fMRI Neurofeedback , 2011, PloS one.

[12]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[13]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[14]  A. Beck,et al.  An inventory for measuring clinical anxiety: psychometric properties. , 1988, Journal of consulting and clinical psychology.

[15]  N. Andreasen,et al.  Insular cortex abnormalities in schizophrenia: a structural magnetic resonance imaging study of first-episode patients , 2000, Schizophrenia Research.

[16]  G. Berríos,et al.  The Cambridge Depersonalization Scale: a new instrument for the measurement of depersonalization. , 2000, Psychiatry research.

[17]  M. Dawson,et al.  The electrodermal system , 2007 .

[18]  A. Schulze-Bonhage,et al.  Functional organization of the human anterior insular cortex , 2009, Neuroscience Letters.

[19]  D. F. Marks,et al.  Visual imagery differences in the recall of pictures. , 1973, British journal of psychology.

[20]  Hillary C. M. Nelson The National Adult Reading Test , 1982 .

[21]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[22]  Luca Passamonti,et al.  Brain structure abnormalities in early-onset and adolescent-onset conduct disorder. , 2011, The American journal of psychiatry.

[23]  Richard S. Sutton,et al.  Reinforcement Learning: An Introduction , 1998, IEEE Trans. Neural Networks.

[24]  Kevin Murphy,et al.  Learning from Errors: Error-Related Neural Activity Predicts Improvements in Future Inhibitory Control Performance , 2009, The Journal of Neuroscience.

[25]  Nikolaus Weiskopf,et al.  Real-time fMRI and its application to neurofeedback , 2012, NeuroImage.

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

[27]  M. Delgado,et al.  Motivation-dependent responses in the human caudate nucleus. , 2004, Cerebral cortex.

[28]  J. Russell,et al.  The neurophysiological bases of emotion: An fMRI study of the affective circumplex using emotion‐denoting words , 2009, Human brain mapping.

[29]  M. Yașargil,et al.  Topographic anatomy of the insular region. , 1999, Journal of neurosurgery.

[30]  Irene Liu,et al.  Improved modulation of rostrolateral prefrontal cortex using real-time fMRI training and meta-cognitive awareness , 2011, NeuroImage.

[31]  Jamil Zaki,et al.  Overlapping activity in anterior insula during interoception and emotional experience , 2012, NeuroImage.

[32]  M. Bradley,et al.  Measuring emotion: the Self-Assessment Manikin and the Semantic Differential. , 1994, Journal of behavior therapy and experimental psychiatry.

[33]  Niels Birbaumer,et al.  Using real-time fMRI to learn voluntary regulation of the anterior insula in the presence of threat-related stimuli. , 2012, Social cognitive and affective neuroscience.

[34]  Geraint Rees,et al.  Improving Visual Perception through Neurofeedback , 2012, The Journal of Neuroscience.

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

[36]  J. Cacioppo,et al.  Handbook Of Psychophysiology , 2019 .

[37]  Stephan G. Boehm,et al.  Upregulation of emotion areas through neurofeedback with a focus on positive mood , 2011, Cognitive, affective & behavioral neuroscience.

[38]  R. DeCharms Applications of real-time fMRI , 2008, Nature Reviews Neuroscience.

[39]  Margot J. Taylor,et al.  Lateralization of affective processing in the insula , 2013, NeuroImage.

[40]  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.

[41]  R. Veit,et al.  Self‐regulation of regional cortical activity using real‐time fMRI: The right inferior frontal gyrus and linguistic processing , 2009, Human brain mapping.

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

[43]  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.

[44]  W. K. Simmons,et al.  Keeping the body in mind: Insula functional organization and functional connectivity integrate interoceptive, exteroceptive, and emotional awareness , 2013, Human brain mapping.

[45]  A. Beck,et al.  Psychometric properties of the Beck Depression Inventory: Twenty-five years of evaluation , 1988 .

[46]  John Suckling,et al.  Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain , 1999, IEEE Transactions on Medical Imaging.

[47]  A. Dale,et al.  Dorsal anterior cingulate cortex: A role in reward-based decision making , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[48]  Irene Liu,et al.  Improved modulation of merostrolateral prefrontal cortex using real-time fMRI training and metacognitive awareness , 2022 .

[49]  N. Daw,et al.  Reinforcement Learning Signals in the Human Striatum Distinguish Learners from Nonlearners during Reward-Based Decision Making , 2007, The Journal of Neuroscience.

[50]  Clay B. Holroyd,et al.  Motivation of extended behaviors by anterior cingulate cortex , 2012, Trends in Cognitive Sciences.

[51]  N. Farb,et al.  Attending to the present: mindfulness meditation reveals distinct neural modes of self-reference. , 2007, Social cognitive and affective neuroscience.

[52]  John Suckling,et al.  Depersonalization disorder: thinking without feeling , 2001, Psychiatry Research: Neuroimaging.

[53]  Clay B. Holroyd,et al.  Dorsal anterior cingulate cortex shows fMRI response to internal and external error signals , 2004, Nature Neuroscience.

[54]  G. Berríos,et al.  The Cambridge Depersonalisation Scale: a new instrument for the measurement of depersonalisation , 2000, Psychiatry Research.

[55]  P. Lang International affective picture system (IAPS) : affective ratings of pictures and instruction manual , 2005 .

[56]  H Garavan,et al.  Artifactual fMRI group and condition differences driven by performance confounds , 2004, NeuroImage.

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

[58]  John Suckling,et al.  A computational morphometric MRI study of schizophrenia: effects of hallucinations. , 2002, Cerebral cortex.

[59]  T A Carpenter,et al.  Colored noise and computational inference in neurophysiological (fMRI) time series analysis: Resampling methods in time and wavelet domains , 2001, Human brain mapping.

[60]  J C Mazziotta,et al.  Automated labeling of the human brain: A preliminary report on the development and evaluation of a forward‐transform method , 1997, Human brain mapping.

[61]  Kevin A. Johnson,et al.  Intermittent “Real‐time” fMRI Feedback Is Superior to Continuous Presentation for a Motor Imagery Task: A Pilot Study , 2012, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[62]  S C Williams,et al.  Generic brain activation mapping in functional magnetic resonance imaging: a nonparametric approach. , 1997, Magnetic resonance imaging.

[63]  P. E. Morris,et al.  Water proton T1 measurements in brain tissue at 7, 3, and 1.5T using IR-EPI, IR-TSE, and MPRAGE: results and optimization , 2008, Magnetic Resonance Materials in Physics, Biology and Medicine.

[64]  H. Critchley,et al.  A common role of insula in feelings, empathy and uncertainty , 2009, Trends in Cognitive Sciences.

[65]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

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

[67]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[68]  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.

[69]  R. C. Oldfield THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[70]  Jean-Baptiste Poline,et al.  Analysis of a large fMRI cohort: Statistical and methodological issues for group analyses , 2007, NeuroImage.