1,040
Views
7
CrossRef citations to date
0
Altmetric
Original Articles

Childhood emotional invalidation and right hemispheric mu suppression during a pain empathy task: An EEG study

ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 236-250 | Received 25 Jul 2017, Published online: 04 Mar 2018

References

  • Avenanti, A., Bueti, D., Galati, G., & Aglioti, S. M. (2005). Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain. Nature Neuroscience, 8(7), 955–960.
  • Baron-Cohen, S., Knickmeyer, R., & Belmonte, M. K. (2005). Sex differences in the brain: Implications for explaining autism. Science, 310, 819–823.
  • Baron-Cohen, S., & Wheelsright, S. (2004). The empathy quotient: An investigation of adults with asperger syndrome or high functioning autism, and normal sex differences. Journal of Autism and Developmental Disorders, 34, 163–175.
  • Binder, E., Dovern, A., Hesse, M. D., Ebke, M., Karbe, H., Saliger, J., ... Weiss, P.H. (2017). Lesion evidence for a human mirror neuron system. Cortex, 90, 125–137.
  • Carr, L., Iacoboni, M., Dubeau, M. C., Mazziotta, J. C., & Lenzi, G. L. (2003). Neural mechanisms of empathy in humans: A relay from neural systems forimitation to limbic areas. Proceedings of the National Academy of Science, 100, 5497–5502.
  • Caspers, S., Zilles, K., Laird, A. R., & Eickhoff, S. B. (2010). ALE meta-analysis of action observation and imitation in the human brain. NeuroImage, 50(3), 1148–1167.
  • Cattaneo, L., & Rizzolatti, G. (2009). The mirror neuron system. Archives of Neurology, 66(5), 557–560.
  • Cheng, Y., Chen, C., & Decety, J. (2014). An EEG/ERP investigation of the development of empathy in early and middle childhood. Developmental Cognitive Neuroscience, 10, 160–169.
  • Cheng, Y., Lee, P. L., Yang, C. Y., Lin, C. P., Hung, D., & Decety, J. (2008). Gender differences in the mu rhythm of the human mirror-neuron system. PLoS One, 3(5), e2113.
  • Cheng, Y., Yang, C.-Y., Lin, C.-P., Lee, P.-L., & Decety, J. (2008). The perception of pain in others suppresses somatosensory oscillations: A magnetoencephalography study. NeuroImage, 40(4), 1833–1840. doi:10.1016/j.neuroimage.2008.01.064
  • Crowell, S. E., Beauchaine, T. P., & Linehan, M. M. (2009). A biosocial developmental model of borderline personality: Elaborating and extending Linehan’s theory. Psychological Bulletin, 135(3), 495–510.
  • Datko, M., Pineda, J. A., & Muller, R. A. (2017). Positive effects of neurofeedback on autism symptoms correlate with brain activation during imitation and observation. The European Journal of Neuroscience. doi:10.1111/ejn.13551
  • de Waal, F. B. M. (2012). The antiquity of empathy. Science, 336, 874–876.
  • Decety, J., & Jackson, P. L. (2004). The functional architecture of human empathy. Behavioral and Cognitive Neuroscience Reviews, 3, 71–100.
  • Decety, J., Lewis, K. L., & Cowell, J. M. (2015). Specific electrophysiological components disentangle affective sharing and empathic concern in psychopathy. Journal of Neurophysiology, 114(1), 493–504.
  • Decety, J., Meidenbauer, K. L., & Cowell, J. M. (2017). The development of cognitive empathy and concern in preschool children: A behavioral neuroscience investigation. Developmental Science, e12570. doi:10.1111/desc.12570
  • di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., & Rizzolatti, G. (1992). Understanding motor events: A neurophysiological study. Experimental Brain Research, 91(1), 176–180.
  • Eisenberg, N., Cumberland, A., & Spinrad, T. L. (1998). Parental socialization of emotion. Psychological Inquiry, 9(4), 241–273.
  • Eisenberg, N., Fabes, R. A., & Murphy, B. C. (1996). Parents’ reactions to children’s negative emotions: Relations to children’s social competence and comforting behavior. Child Development, 67(5), 2227–2247.
  • Eisenberg, N., & Miller, P. A. (1987). The relation of empathy to prosocial and related behaviors. Psychological Bulletin, 101(1), 91–119.
  • Faul, F., Erdfelder, E., Lang, A. G., & Buchner, A. (2007). G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods, 39(2), 175–191.
  • Fecteau, S., Pascual-Leone, A., & Théoret, H. (2008). Psychopathy and the mirror neuron system: Preliminary findings from a non-psychiatric sample. Psychiatry Research, 160(2), 137–144.
  • Fox, N. A., Bakermans-Kranenburg, M. J., Yoo, K. H., Bowman, L. C., Cannon, E. N., Vanderwert, R. E., et al. (2016). Assessing human mirror activity with EEG mu rhythm: A meta-analysis. Psychological Bulletin, 142(3), 291–11291–313.
  • Frenkel-Toledo, S., Bentin, S., Perry, A., Liebermann, D. G., & Soroker, N. (2014). Mirror-neuron system recruitment by action observation: Effects of focal brain damage on mu suppression. NeuroImage, 87, 127–137.
  • Frenkel-Toledo, S., Liebermann, D. G., Bentin, S., & Soroker, N. (2016). Dysfunction of the human mirror neuron system in ideomotor apraxia: Evidence from mu suppression. Journal of Cognitive Neuroscience, 28(6), 775–791.
  • Gallese, V., Eagle, M. N., & Migone, P. (2007). Intentional attunement: Mirror neurons and the neural underpinnings of interpersonal relations. Journal of the American Psychoanalytic Association, 55(1), 131–176.
  • Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996). Action recognition in the premotor cortex. Brain, 119(2), 593–609.
  • Gastaut, H. J., & Bert, J. (1954). EEG changes during cinematographic presentation; moving picture activation of the EEG. Electroencephalography and Clinical Neurophysiology, 6(3), 433–444.
  • Gazzola, V., & Keysers, C. (2009). The observation and execution of actions share motor and somatosensory voxels in all tested subjects: Single-subject analyses of unsmoothed fMRI data. Cerebral Cortex, 19(6), 1239–1255.
  • Giummarra, M. J., Poudel, G., Niu, P. A., Nicholls, M. E. R., Fielding, J., Verdejo-Garcia, A., & Labuschagne, I. (2018). Emotion processing in persons who respond vicariously towards others in pain: Disinhibited left-lateralized neural activity for threatening expressions. Laterality, 23(2), 184–208.
  • Gottman, J. M., Katz, L. F., & Hooven, C. (1996). Parental meta-emotion philosophy and the emotional life of families: Theoretical models and preliminary data. Journal of Family Psychology, 10(3), 243–268.
  • Haslam, M., Mountford, V., Meyer, C., & Waller, G. (2008). Invalidating childhood environments in anorexia and bulimia nervosa. Eating Behaviors, 9(3), 313–318.
  • Herr, N. R., Jones, A. C., Cohn, D. M., & Weber, D. M. (2015). The impact of validation and invalidation on aggression in individuals with emotion regulation difficulties. Personality Disorders, 6(4), 310–314.
  • Heyes, C. (2010). Where do mirror neurons come from? Neuroscience & Biobehavioral Reviews, 34(4), 575–583.
  • Hickok, G. (2009). Eight problems for the mirror neuron theory of action understanding in monkeys and humans. Journal of Cognitive Neuroscience, 21(7), 1229–1243.
  • Hobson, H. M., & Bishop, D. V. M. (2017). The interpretation of mu suppression as an index of mirror neuron activity: Past, present and future. Royal Society Open Science, 4(3), 160662.
  • Hoenen, M., Lubke, K. T., & Pause, B. M. (2015). Somatosensory mu activity reflects imagined pain intensity of others. Psychophysiology, 52(12), 1551–1558.
  • Hoenen, M., Lubke, K. T., & Pause, B. M. (2017). Sensitivity of the human mirror neuron system for abstract traces of actions: An EEG-study. Biological Psychology, 124, 57–64.
  • Hudson, J. L., Comer, J. S., & Kendall, P. C. (2008). Parental responses to positive and negative emotions in anxious and nonanxious children. Journal of Clinical Child and Adolescent Psychology, 53, 37(2), 303–313.
  • Iacoboni, M., Molnar-Szakacs, I., Gallese, V., Buccino, G., Mazziotta, J. C., & Rizzolatti, G. (2005). Grasping the intentions of others with one’s own mirror neuron system. PLoS Biology, 3(3), e79.
  • Jackson, P. L., Brunet, E., Meltzoff, A. N., & Decety, J. (2006). Empathy examined through the neural mechanisms involved in imagining how I feel versus how you feel pain. Neuropsychologia, 44(5), 752–761.
  • Jackson, P. L., Meltzoff, A. N., & Decety, J. (2005). How do we perceive the pain of others? A window into the neural processes involved in empathy. NeuroImage, 24(3), 771–779.
  • Kaplan, J. T., & Iacoboni, M. (2006). Getting a grip on other minds: Mirror neurons, intention understanding, and cognitive empathy. Social Neuroscience, 1(3–4), 175–183.
  • Katz, L. F., Maliken, A. C., & Stettler, N. M. (2012). Parental meta-emotion philosophy: A review of research and theoretical framework. Child Development Perspectives, 6(4), 417–422.
  • Katz, L. F., Shortt, J. W., Allen, N. B., Davis, B., Hunter, E., Leve, C., & Sheeber, L. (2014). Parental emotion socialization in clinically depressed adolescents: Enhancing and dampening positive affect. Journal of Abnormal Child Psychology, 42(2), 205–215.
  • Keysers, C., & Gazzola, V. (2009). Expanding the mirror: Vicarious activity for actions, emotions, and sensations. Current Opinion in Neurobiology, 19(6), 666–671.
  • Klem, G. H., Lüders, H. O., & Jasper, H. H. (1999). The ten-twenty electrode system of the International Federation. Electroencephalography Clinical Neurophysiology, 52, 3–6.
  • Leigh, R., Oishi, K., Hsu, J., Lindquist, M., Gottesman, R. F., Jarso, S., et al. (2013). Acute lesions that impair affective empathy. Brain, 136(Pt 8), 2539–2549.
  • Leslie, K. R., Johnson-Frey, S. H., & Grafton, S. T. (2004). Functional imaging of face and hand imitation: Towards a motor theory of empathy. NeuroImage, 21(2), 601–607.
  • Levy, J., Goldstein, A., & Feldman, R. (2017). Perception of social synchrony induces mother-child gamma coupling in the social brain. Social Cognitive and Affective Neuroscience, 12, 1036–1046.
  • Linehan, M. (1998). Cognitive-behavioral treatment of borderline personality disorder. New York: Guilford Press.
  • Luck, S. J. (2014). An introduction to the event-related potential technique. Cambridge, MA: MIT Press.
  • Messina, A., Beadle, J. N., & Paradiso, S. (2014). Towards a classification of alexithymia: Primary, secondary and organic. Journal of Psychopathology, 20(1), 38–49.
  • Mier, D., Haddad, L., Diers, K., Dressing, H., Meyer-Lindenberg, A., & Kirsch, P. (2014). Reduced embodied simulation in psychopathy. The World Journal of Biological Psychiatry, 15(6), 479–487.
  • Molenberghs, P., Hayward, L., Mattingley, J. B., & Cunnington, R. (2012). Activation patterns during action observation are modulated by context in mirror system areas. NeuroImage, 59(1), 608–615.
  • Moore, A., Gorodnitsky, I., & Pineda, J. (2012). EEG mu component responses to viewing emotional faces. Behavioural Brain Research, 226(1), 309–316.
  • Morris, A. S., Silk, J. S., Steinberg, L., Myers, S. S., & Robinson, L. R. (2007). The role of the family context in the development of emotion regulation. Social Development, 16(2), 361–388.
  • Mountford, V., Corstorphine, E., Tomlinson, S., & Waller, G. (2007). Development of a measure to assess invalidating childhood environments in the eating disorders. Eating Behaviors, 8(1), 48–58.
  • Muthukumaraswamy, S. D., & Johnson, B. W. (2004). Primary motor cortex activation during action observation revealed by wavelet analysis of the EEG. Clinical Neurophysiology, 115(8), 1760–1766.
  • Oberman, L. M., Hubbard, E. M., McCleery, J. P., Altschuler, E. L., Ramachandran, V. S., & Pineda, J. A. (2005). EEG evidence for mirror neuron dysfunction in autism spectrum disorders. Brain Research. Cognitive Brain Research, 24(2), 190–198.
  • Oberman, L. M., McCleery, J. P., Hubbard, E. M., Bernier, R., Wiersema, J. R., Raymaekers, R., & Pineda, J. A. (2013). Developmental changes in mu suppression to observed and executed actions in autism spectrum disorders. Social Cognitive and Affective Neuroscience, 8(3), 300–304.
  • Oberman, L. M., Pineda, J. A., & Ramachandran, V. S. (2007). The human mirror neuron system: A link between action observation and social skills. Social Cognitive and Affective Neuroscience, 2(1), 62–66.
  • Oberman, L. M., & Ramachandran, V. S. (2008). Preliminary evidence for deficits in multisensory integration in autism spectrum disorders: The mirror neuron hypothesis. Social Neuroscience, 3(3–4), 348–355.
  • Oberman, L. M., Ramachandran, V. S., & Pineda, J. A. (2008). Modulation of mu suppression in children with autism spectrum disorders in response to familiar or unfamiliar stimuli: The mirror neuron hypothesis. Neuropsychologia, 46(5), 1558–1565.
  • Oishi, K., Faria, A. V., Hsu, J., Tippett, D., Mori, S., & Hillis, A. E. (2015). Critical role of the right uncinate fasciculus in emotional empathy. Annals of Neurology, 77(1), 68–74.
  • Perry, A., Bentin, S., Bartal, I. B.-A., Lamm, C., & Decety, J. (2010). “Feeling” the pain of those who are different from us: Modulation of EEG in the mu/alpha range. Cognitive, Affective, & Behavioral Neuroscience, 10(4), 493–504.
  • Pfurtscheller, G., Neuper, C., Andrew, C., & Edlinger, G. (1997). Foot and hand area mu rhythms. International Journal of Psychophysiology: Official Journal of the International Organization of Psychophysiology, 26(1–3), 121–135.
  • Pineda, J. A. (2008). Sensorimotor cortex as a critical component of an “extended” mirror neuron system: Does it solve the development, correspondence, and control problems in mirroring? Behavioral and Brain Functions, 4(1), 47.
  • Preston, S. D., & DeWaal, F. B. M. (2002). Empathy: Its ultimate and proximate bases. Behavioral and Brain Sciences, 25, 1–20-discussion 20–71.
  • Rizzolatti, G., Camarda, R., Fogassi, L., Gentilucci, M., Luppino, G., & Matelli, M. (1988). Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Experimental Brain Research, 71(3), 491–507.
  • Rizzolatti, G., & Craighero, L. (2004). The mirror-neuron system. Annual Review of Neuroscience, 27(1), 169–192.
  • Rizzolatti, G., Fabbri-Destro, M., & Cattaneo, L. (2009). Mirror neurons and their clinical relevance. Nature Clinical Practice Neurology, 5(1), 24–34.
  • Rizzolatti, G., & Fadiga, L. (1998). Grasping objects and grasping action meanings: The dual role of monkey rostroventral premotor cortex (area F5). Novartis Foundation Symposium, 218, 81–95; discussion 95–103.
  • Rizzolatti, G., Fadiga, L., Gallese, V., & Fogassi, L. (1996). Premotor cortex and the recognition of motor actions. Brain Research. Cognitive Brain Research, 3(2), 131–141.
  • Rizzolatti, G., Fogassi, L., & Gallese, V. (2001). Neurophysiological mechanisms underlying the understanding and imitation of action. Nature Reviews Neuroscience, 2(9), 661-70. doi:10.1038/35090060
  • Rizzolatti, G., & Sinigaglia, C. (2010). The functional role of the parieto-frontal mirror circuit: Interpretations and misinterpretations. Nature Reviews Neuroscience, 11(4), 264–274.
  • Robertson, C. D., Kimbrel, N. A., & Nelson-Gray, R. O. (2013). The Invalidating Childhood Environment Scale (ICES): Psychometric properties and relationship to borderline personality symptomatology. Journal of Personality Disorders, 27(3), 402–410.
  • Rueckert, L., & Naybar, N. (2008). Gender differences in empathy: The role of the right hemisphere. Brain and Cognition, 67(2), 162–167.
  • Selby, E. A., Braithwaite, S. R., Joiner, T. E., & Fincham, F. D. (2008). Features of borderline personality disorder, perceived childhood emotional invalidation, and dysfunction within current romantic relationships. Journal of Family Psychology, 22(6), 885–893.
  • Shamay-Tsoory, S. G., Tomer, R., Berger, B. D., & Aharon-Peretz, J. (2003). Characterization of empathy deficits following prefrontal brain damage: The role of the right ventromedial prefrontal cortex. Journal of Cognitive Neuroscience, 15(3), 324–337.
  • Snyder, J., Stoolmiller, M., & Wilson, M. (2003). Child anger regulation, parental responses to children’s anger displays, and early child antisocial behavior. Social Development, 12, 335–360.
  • Spunt, R. P., & Lieberman, M. D. (2012). Dissociating modality-specific and supramodal neural systems for action understanding. Journal of Neuroscience, 32, 3575–3583.
  • Stanley, D., & Adolphs, R. (2013). Toward a neural basis for social behavior. Neuron, 80, 816–826.
  • Sturrock, B., & Mellor, D. (2013). Perceived emotional invalidation and borderline personality disorder features: A test of theory. Personality and Mental Health, 8(2), 128–142.
  • Taylor, S. J., Barker, L. A., Heavey, L., & McHale, S. (2015). The longitudinal development of social and executive functions in late adolescence and early adulthood. Frontiers in Behavioral Neuroscience, 9(252), 1–12.
  • Taylor, Z. E., Eisenberg, N., Spinrad, T. L., Eggum, N. D., & Sulik, M. J. (2013). The relations of ego-resiliency and emotion socialization to the development of empathy and prosocial behavior across early childhood. Emotion, 13(5), 822–831.
  • Theoret, H., & Pascual-Leone, A. (2002). Language acquisition: Do as you hear. Current Biology: CB, 12(21), R736–7.
  • Virji-Babul, N., Moiseev, A., Cheung, T., Weeks, D., Cheyne, D., & Ribary, U. (2008). Changes in mu rhythm during action observation and execution in adults with Down syndrome: Implications for action representation. Neuroscience Letters, 436(2), 177–180.
  • Waller, G., Corstorphine, E., & Mountford, V. (2007). The role of emotional abuse in the eating disorders: Implications for treatment. Eating Disorders, 15(4), 317–331.
  • Yang, C. Y., Decety, J., Lee, S., Chen, C., & Cheng, Y. (2009). Gender differences in the mu rhythm during empathy for pain: An electroencephalographic study. Brain Research, 1251, 176–184.
  • Yang, J., & Hofmann, J. (2016). Action observation and imitation in autism spectrum disorders: An ALE meta-analysis of fMRI studies. Brain Imaging and Behavior, 10(4), 960–969.
  • Yeh, Z.-T., & Tsai, C. F. (2014). Impairment on theory of mind and empathy in patients with stroke. Psychiatry and Clinical Neurosciences, 68(8), 612–620.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.