Shared states: using MVPA to test neural overlap between self-focused emotion imagery and other-focused emotion understanding

Abstract The present study tested whether the neural patterns that support imagining ‘performing an action’, ‘feeling a bodily sensation’ or ‘being in a situation’ are directly involved in understanding other people’s actions, bodily sensations and situations. Subjects imagined the content of short sentences describing emotional actions, interoceptive sensations and situations (self-focused task), and processed scenes and focused on how the target person was expressing an emotion, what this person was feeling, and why this person was feeling an emotion (other-focused task). Using a linear support vector machine classifier on brain-wide multi-voxel patterns, we accurately decoded each individual class in the self-focused task. When generalizing the classifier from the self-focused task to the other-focused task, we also accurately decoded whether subjects focused on the emotional actions, interoceptive sensations and situations of others. These results show that the neural patterns that underlie self-imagined experience are involved in understanding the experience of other people. This supports the theoretical assumption that the basic components of emotion experience and understanding share resources in the brain.

[1]  Reginald B. Adams,et al.  If it bleeds, it leads: separating threat from mere negativity. , 2015, Social cognitive and affective neuroscience.

[2]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[3]  J. Gallant,et al.  Identifying natural images from human brain activity , 2008, Nature.

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

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

[6]  Kristen A. Lindquist,et al.  The brain basis of emotion: A meta-analytic review , 2012, Behavioral and Brain Sciences.

[7]  J. Haynes A Primer on Pattern-Based Approaches to fMRI: Principles, Pitfalls, and Perspectives , 2015, Neuron.

[8]  Claus Lamm,et al.  Placebo analgesia and its opioidergic regulation suggest that empathy for pain is grounded in self pain , 2015, Proceedings of the National Academy of Sciences.

[9]  William W. Graves,et al.  Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. , 2009, Cerebral cortex.

[10]  Carolyn Parkinson,et al.  A Common Cortical Metric for Spatial, Temporal, and Social Distance , 2014, The Journal of Neuroscience.

[11]  C. Keysers,et al.  Evidence for mirror systems in emotions , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[12]  W. K. Simmons,et al.  Interoceptive predictions in the brain , 2015, Nature Reviews Neuroscience.

[13]  J. Mazziotta,et al.  Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Andres Hoyos Idrobo,et al.  Assessing and tuning brain decoders: Cross-validation, caveats, and guidelines , 2016, NeuroImage.

[15]  Tobias Brosch,et al.  Implicit Race Bias Decreases the Similarity of Neural Representations of Black and White Faces , 2013, Psychological science.

[16]  L. Fadiga,et al.  Active perception: sensorimotor circuits as a cortical basis for language , 2010, Nature Reviews Neuroscience.

[17]  Lawrence W Barsalou,et al.  Simulation, situated conceptualization, and prediction , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[18]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[19]  Christine D. Wilson-Mendenhall,et al.  Concepts in context: Processing mental state concepts with internal or external focus involves different neural systems , 2015, Social neuroscience.

[20]  H. Critchley,et al.  Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response , 2010, Brain Structure and Function.

[21]  Tania Singer,et al.  The past, present and future of social neuroscience: A European perspective , 2012, NeuroImage.

[22]  Christian Keysers,et al.  The impact of certain methodological choices on multivariate analysis of fMRI data with support vector machines , 2011, NeuroImage.

[23]  Aixia Guo,et al.  Gene Selection for Cancer Classification using Support Vector Machines , 2014 .

[24]  Dimitri Van De Ville,et al.  Decoding of Emotional Information in Voice-Sensitive Cortices , 2009, Current Biology.

[25]  Matthew D. Lieberman,et al.  The Busy Social Brain , 2013, Psychological science.

[26]  R. N. Spreng,et al.  The default network and self‐generated thought: component processes, dynamic control, and clinical relevance , 2014, Annals of the New York Academy of Sciences.

[27]  Jamil Zaki,et al.  The Anatomy of Suffering: Understanding the Relationship between Nociceptive and Empathic Pain , 2016, Trends in Cognitive Sciences.

[28]  M. Iacoboni,et al.  The self and social cognition: the role of cortical midline structures and mirror neurons , 2007, Trends in Cognitive Sciences.

[29]  Nikolaus Kriegeskorte,et al.  Comparison of multivariate classifiers and response normalizations for pattern-information fMRI , 2010, NeuroImage.

[30]  Christian Keysers,et al.  Dissociating the ability and propensity for empathy , 2014, Trends in Cognitive Sciences.

[31]  S. Gilbert,et al.  Evaluative vs. trait representation in intergroup social judgments: Distinct roles of anterior temporal lobe and prefrontal cortex , 2012, Neuropsychologia.

[32]  J. Crocker,et al.  From painkiller to empathy killer: acetaminophen (paracetamol) reduces empathy for pain. , 2016, Social cognitive and affective neuroscience.

[33]  Lisa Feldman Barrett,et al.  States of mind: Emotions, body feelings, and thoughts share distributed neural networks , 2012, NeuroImage.

[34]  Leo Breiman,et al.  Bagging Predictors , 1996, Machine Learning.

[35]  Jason P. Mitchell,et al.  Two Mechanisms for Simulating Other Minds , 2011 .

[36]  Ajay B. Satpute,et al.  Large-scale brain networks in affective and social neuroscience: towards an integrative functional architecture of the brain , 2013, Current Opinion in Neurobiology.

[37]  J. Decety Dissecting the Neural Mechanisms Mediating Empathy , 2011 .

[38]  Heather C. Lench,et al.  Discrete emotions predict changes in cognition, judgment, experience, behavior, and physiology: a meta-analysis of experimental emotion elicitations. , 2011, Psychological bulletin.

[39]  Lisa Feldman Barrett,et al.  Grounding emotion in situated conceptualization , 2011, Neuropsychologia.

[40]  Suzanne Oosterwijk,et al.  Embodiment in the Construction of Emotion Experience and Emotion Understanding , 2014 .

[41]  Frank Van Overwalle,et al.  Understanding others' actions and goals by mirror and mentalizing systems: A meta-analysis , 2009, NeuroImage.

[42]  Patrik Vuilleumier,et al.  Cross-modal representations of first-hand and vicarious pain, disgust and fairness in insular and cingulate cortex , 2016, Nature Communications.

[43]  K. Ochsner,et al.  The neuroscience of empathy: progress, pitfalls and promise , 2012, Nature Neuroscience.

[44]  Kevin N. Ochsner,et al.  A Meta-analysis of Functional Neuroimaging Studies of Self- and Other Judgments Reveals a Spatial Gradient for Mentalizing in Medial Prefrontal Cortex , 2012, Journal of Cognitive Neuroscience.

[45]  Jin Fan,et al.  Somatic and vicarious pain are represented by dissociable multivariate brain patterns , 2016, eLife.

[46]  Gaël Varoquaux,et al.  Scikit-learn: Machine Learning in Python , 2011, J. Mach. Learn. Res..

[47]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[48]  R. Nathan Spreng,et al.  The Common Neural Basis of Autobiographical Memory, Prospection, Navigation, Theory of Mind, and the Default Mode: A Quantitative Meta-analysis , 2009, Journal of Cognitive Neuroscience.

[49]  M. Peelen,et al.  Supramodal Representations of Perceived Emotions in the Human Brain , 2010, The Journal of Neuroscience.

[50]  Mark W. Woolrich,et al.  FSL , 2012, NeuroImage.

[51]  Michael L. Anderson Précis of After Phrenology: Neural Reuse and the Interactive Brain , 2014, Behavioral and Brain Sciences.

[52]  Lisa Feldman Barrett,et al.  Emotions are real. , 2012, Emotion.

[53]  Matthew D. Lieberman,et al.  An integrative model of the neural systems supporting the comprehension of observed emotional behavior , 2012, NeuroImage.

[54]  김정란 The Real , 2020, The Palm at the End of the Mind.

[55]  Claus Lamm,et al.  Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain , 2011, NeuroImage.

[56]  Marco Tamietto,et al.  Standing up for the body. Recent progress in uncovering the networks involved in the perception of bodies and bodily expressions , 2010, Neuroscience & Biobehavioral Reviews.

[57]  G. Rizzolatti,et al.  A unifying view of the basis of social cognition , 2004, Trends in Cognitive Sciences.

[58]  Daniel S. Margulies,et al.  Prioritizing spatial accuracy in high-resolution fMRI data using multivariate feature weight mapping , 2014, Front. Neurosci..

[59]  Qingyang Li,et al.  Emotional perception: Meta-analyses of face and natural scene processing , 2011, NeuroImage.

[60]  P. Ruby,et al.  What is self-specific? Theoretical investigation and critical review of neuroimaging results. , 2009, Psychological review.

[61]  C. Lamm,et al.  The role of shared neural activations, mirror neurons, and morality in empathy – A critical comment , 2015, Neuroscience Research.