Association between interoception and empathy: evidence from heartbeat-evoked brain potential.

Physiological bodily states play an important role in affective experiences. This study investigated whether the neural processing of internal body state (interoception) is associated with empathy, the understanding of the affective states of others. We used the 'heartbeat-evoked potential' (HEP), a surface electroencephalography (EEG) pattern, as a neural index of interoceptive processing. The HEP is contingent on the most prominent peak (R-wave) of the electrocardiogram (ECG) and is thought to reflect cortical processing of cardiac afferent input. Twenty-one healthy adults performed empathy and control tasks while EEG and ECG were recorded, where they made judgments based on either the affective or physical aspects of images of human eyes. HEP, ECG and heart rate in each task block were calculated and compared. Results showed that cardiac activity was not significantly different between tasks. In contrast, HEP showed a significant task difference, exhibited as an increased negativity during the empathy task over frontocentral sites at a latency of approximately 250-430 ms. Furthermore, a self-reported measure of empathy was associated with mean HEP amplitude during the period of task-related differentiation. These results suggest that afferent feedback from visceral activity may contribute to inferences about the affective state of others.

[1]  S. Wiens Interoception in emotional experience , 2005, Current opinion in neurology.

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

[3]  K. Yau,et al.  Interoception: the sense of the physiological condition of the body , 2003, Current Opinion in Neurobiology.

[4]  P. Montoya,et al.  Heartbeat evoked potentials (HEP): topography and influence of cardiac awareness and focus of attention. , 1993, Electroencephalography and clinical neurophysiology.

[5]  J. O'Doherty,et al.  Empathic neural responses are modulated by the perceived fairness of others , 2006, Nature.

[6]  B. Vogt Pain and emotion interactions in subregions of the cingulate gyrus , 2005, Nature Reviews Neuroscience.

[7]  R. Schandry,et al.  The heartbeat-evoked brain potential in patients suffering from diabetic neuropathy and in healthy control persons , 2001, Clinical Neurophysiology.

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

[9]  Hongmei Yan,et al.  Effect of heartbeat perception on heartbeat evoked potential waves , 2007, Neuroscience bulletin.

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

[11]  R. Weitkunat,et al.  Enhancement of heartbeat-related brain potentials through cardiac awareness training. , 1990, The International journal of neuroscience.

[12]  J. Cacioppo,et al.  Multilevel integrative analyses of human behavior: social neuroscience and the complementing nature of social and biological approaches. , 2000, Psychological bulletin.

[13]  Karl J. Friston,et al.  Neuroanatomical correlates of externally and internally generated human emotion. , 1997, The American journal of psychiatry.

[14]  J. Driver,et al.  Modulation of visual processing by attention and emotion: windows on causal interactions between human brain regions , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[15]  J. Furedy,et al.  Effects of psychological and physiological challenges on heart rate, T-wave amplitude, and pulse-transit time. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[16]  J. Decety,et al.  Neural correlates of feeling sympathy , 2003, Neuropsychologia.

[17]  S. Preston,et al.  Empathy: Its ultimate and proximate bases. , 2001, The Behavioral and brain sciences.

[18]  G. Rizzolatti,et al.  Both of Us Disgusted in My Insula The Common Neural Basis of Seeing and Feeling Disgust , 2003, Neuron.

[19]  R. Lane Neural substrates of implicit and explicit emotional processes: a unifying framework for psychosomatic medicine. , 2008, Psychosomatic medicine.

[20]  D. Auer,et al.  Brain structures mediating cardiovascular arousal and interoceptive awareness , 2007, Brain Research.

[21]  Olga Pollatos,et al.  Interoceptive awareness mediates the relationship between anxiety and the intensity of unpleasant feelings. , 2007, Journal of anxiety disorders.

[22]  Christian Keysers,et al.  Empathy for positive and negative emotions in the gustatory cortex , 2007, NeuroImage.

[23]  M. Carrasco,et al.  PSYCHOLOGICAL SCIENCE Research Article Emotion Facilitates Perception and Potentiates the Perceptual Benefits of Attention , 2022 .

[24]  S. Stewart,et al.  Heartbeat awareness and heart rate reactivity in anxiety sensitivity: a further investigation. , 2001, Journal of anxiety disorders.

[25]  Matthew D. Lieberman,et al.  Social cognitive neuroscience: a review of core processes. , 2007, Annual review of psychology.

[26]  Meyer Solomon,et al.  THE MECHANISM OF THE EMOTIONS1 , 1927 .

[27]  E. Katkin,et al.  Individual differences in cortical evoked potentials as a function of heartbeat detection ability. , 1991, The International journal of neuroscience.

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

[29]  J. Decety,et al.  The functional architecture of human empathy. , 2004, Behavioral and cognitive neuroscience reviews.

[30]  H. Critchley,et al.  Neuroanatomical basis for first- and second-order representations of bodily states , 2001, Nature Neuroscience.

[31]  O. Cameron,et al.  Interoception: The Inside Story—A Model for Psychosomatic Processes , 2001, Psychosomatic medicine.

[32]  Satoshi Minoshima,et al.  Regional Brain Activation Due to Pharmacologically Induced Adrenergic Interoceptive Stimulation in Humans , 2002, Psychosomatic medicine.

[33]  Olga Pollatos,et al.  Differential effects of anxiety and depression on interoceptive accuracy , 2009, Depression and anxiety.

[34]  J. E. Rose,et al.  Autonomic Nervous System Activity Distinguishes Among Emotions , 2009 .

[35]  J. Slangen,et al.  The electrocardiogram during emotional and physical stress. , 1985, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[36]  J. Decety,et al.  Human Empathy Through the Lens of Social Neuroscience , 2006, TheScientificWorldJournal.

[37]  M. Iacoboni Imitation, empathy, and mirror neurons. , 2009, Annual review of psychology.

[38]  G Dirlich,et al.  Topography and morphology of heart action-related EEG potentials. , 1998, Electroencephalography and clinical neurophysiology.

[39]  J. O'Doherty,et al.  Empathy for Pain Involves the Affective but not Sensory Components of Pain , 2004, Science.

[40]  O. Pollatos,et al.  Interoceptive sensitivity and emotion processing: an EEG study. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[41]  Jessica A. Sommerville,et al.  Shared representations between self and other: a social cognitive neuroscience view , 2003, Trends in Cognitive Sciences.

[42]  K. Demyttenaere,et al.  Central nervous system involvement in functional gastrointestinal disorders. , 2004, Best practice & research. Clinical gastroenterology.

[43]  A. Damasio The Feeling of What Happens: Body and Emotion in the Making of Consciousness , 1999 .

[44]  O. Pollatos,et al.  Accuracy of heartbeat perception is reflected in the amplitude of the heartbeat-evoked brain potential. , 2004, Psychophysiology.

[45]  A. Damasio Descarte's error : emotion, reason, and the human brain , 1994 .

[46]  S. Baron-Cohen,et al.  Another advanced test of theory of mind: evidence from very high functioning adults with autism or asperger syndrome. , 1997, Journal of child psychology and psychiatry, and allied disciplines.

[47]  M. Iacoboni Understanding Others: Imitation, Language, Empathy , 2002 .

[48]  Matthew D. Lieberman,et al.  Pains and Pleasures of Social Life , 2009, Science.

[49]  L. Fogassi,et al.  A Touching Sight SII/PV Activation during the Observation and Experience of Touch , 2004, Neuron.

[50]  Andrew N. Meltzoff,et al.  How do we perceive the pain of others? A window into the neural processes involved in empathy , 2005, NeuroImage.

[51]  A. Damasio,et al.  Subcortical and cortical brain activity during the feeling of self-generated emotions , 2000, Nature Neuroscience.

[52]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[53]  A. Damasio,et al.  The neural substrates of cognitive empathy , 2007, Social neuroscience.

[54]  E. Bullmore,et al.  Social intelligence in the normal and autistic brain: an fMRI study , 1999, The European journal of neuroscience.

[55]  G. Ginsburg,et al.  T-wave amplitude: relationships to phasic RSA and heart period changes. , 1998, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[56]  O. Pollatos,et al.  Brain structures involved in interoceptive awareness and cardioafferent signal processing: A dipole source localization study , 2005, Human brain mapping.

[57]  P. Montoya,et al.  Event-related brain potentials and the processing of cardiac activity , 1996, Biological Psychology.

[58]  T. Singer,et al.  The Social Neuroscience of Empathy , 2009, Annals of the New York Academy of Sciences.

[59]  Greg J Siegle,et al.  Common and distinct brain networks underlying explicit emotional evaluation: a meta-analytic study. , 2012, Social cognitive and affective neuroscience.

[60]  L. Parsons,et al.  Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. , 1999, The American journal of psychiatry.

[61]  M. Cabanac What is emotion? , 2002, Behavioural Processes.

[62]  W. James,et al.  What Is an Emotion , 1977 .

[63]  R. Schandry,et al.  Heartbeat detection and the experience of emotions , 2009 .

[64]  R. Zatorre,et al.  Intensely pleasurable responses to music correlate with activity in brain regions implicated in reward and emotion , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[65]  C. Neil Macrae,et al.  The Link between Social Cognition and Self-referential Thought in the Medial Prefrontal Cortex , 2005, Journal of Cognitive Neuroscience.

[66]  R. Weitkunat,et al.  From the heart to the brain: a study of heartbeat contingent scalp potentials. , 1986, The International journal of neuroscience.

[67]  Vittorio Gallese,et al.  Mirrors of the mind. , 2006, Scientific American.

[68]  Mark H. Davis Measuring individual differences in empathy: Evidence for a multidimensional approach. , 1983 .

[69]  Benjamin Rand,et al.  The Classical Psychologists. , 1912 .