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Brain Structure and Function

, Volume 224, Issue 2, pp 937–947 | Cite as

Sex differences in somatomotor representations of others’ pain: a permutation-based analysis

  • Leonardo Christov-MooreEmail author
  • Marco Iacoboni
Original Article

Abstract

Sex differences in empathy for pain have been repeatedly observed. However, it is unclear whether this is due to sex differences in “bottom-up” somatomotor representations of others’ pain (self-other resonance) or to “top-down” prefrontal control of such responses. Here, we provide data from 70 subjects suggesting that sex differences in empathy for pain lie primarily in pre-reflective, bottom-up resonance mechanisms. Subjects viewed a right hand pierced by a needle during fMRI. They also filled out a self-report measure of trait empathy, the Interpersonal Reactivity Index. A permutation-based analysis (FSL’s Randomise) found that females showed greater signal in a cluster in primary somatomotor cortex that includes the motor hand area. No significant differences were observed in other task-implicated areas. An examination of condition-specific parameter estimates found that this difference was due to reduced signal in this cluster in males. No significant differences in resting connectivity or within-task (generalized psychophysiological interaction analysis or gPPI) dynamic connectivity of this region with prefrontal areas were observed. While female subjects scored higher on affective subscales of the IRI, there were no sex differences in Perspective-Taking, the primary index of cognitive, top-down empathy processes. These findings suggest that localized internal somatomotor representations of others’ pain, a functional index of bottom-up resonance processes, are stronger in female subjects.

Keywords

Sex Pain Empathy Functional magnetic resonance imaging Cognitive neuroscience 

Notes

Funding

This work was supported by the National Institute of Mental Health under grant R21 MH097178 to M. I., and by the National Science Foundation under a Graduate Fellowship Grant DGE-1144087 to L.C.M. For generous support, the authors also wish to thank the Brain Mapping Medical Research Organization, Brain Mapping Support Foundation, Pierson-Lovelace Foundation, The Ahmanson Foundation, William M. and Linda R. Dietel Philanthropic Fund at the Northern Piedmont Community Foundation, Tamkin Foundation, Jennifer Jones-Simon Foundation, Capital Group Companies Charitable Foundation, Robson Family and Northstar Fund.

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to declare.

Ethical standards

All recruitment and experimental procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee, and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

429_2018_1814_MOESM1_ESM.docx (98 kb)
Supplementary material 1 (DOCX 98 KB)

References

  1. Avenanti A, Bueti D, Galati G, Aglioti SM (2005) Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain. Nat Neurosci 8:955–960CrossRefGoogle Scholar
  2. Avenanti A, Minio-Paluello I, Bufalari I, Aglioti SM (2009) The pain of a model in the personality of an onlooker: Influence of state-reactivity and personality traits on embodied empathy for pain. NeuroImage 44(1):275–283.  https://doi.org/10.1016/j.neuroimage.2008.08.001 CrossRefGoogle Scholar
  3. Aziz-Zadeh L, Iacoboni M, Zaidel E, Wilson S, Mazziotta J (2004) Left hemisphere motor facilitation in response to manual action sounds. Eur J Neurosci 19(9):2609–2612CrossRefGoogle Scholar
  4. Banks S, Eddy K, Angstadt M, Nathan P, Phan K (2007) Amyg- dala–frontal connectivity during emotion regulation. Soc Cogn Affect Neurosci 2:303–312CrossRefGoogle Scholar
  5. Brighina F, De Tommaso M, Giglia F, Scalia S, Cosentino G, Puma A et al (2011) Modulation of pain perception by transcranial magnetic stimulation of left prefrontal cortex. J Headache Pain 12(2):185–191.  https://doi.org/10.1007/s10194-011-0322-8 CrossRefGoogle Scholar
  6. Bufalari I, Aprile T, Avenanti A, Di Russo F, Aglioti SM (2007) Empathy for pain and touch in the human somatosensory cortex. Cereb Cortex 17:2553–2561CrossRefGoogle Scholar
  7. Cheng Y, Lee PL, Yang CY, Lin CP, Hung D, Decety J (2008) Gender differences in the mu rhythm of the human mirror-neuron system. PLoS One 3(5):1–7.  https://doi.org/10.1371/journal.pone.0002113 CrossRefGoogle Scholar
  8. Cheng Y, Chen C, Lin CP, Chou KH, Decety J (2010) Love hurts: an fmri study. NeuroImage 51(2):923–929.  https://doi.org/10.1016/j.neuroimage.2010.02.047 CrossRefGoogle Scholar
  9. Cho SS, Strafella AP (2009) rTMS of the left dorsolateral prefrontal cortex modulates dopamine release in the ipsilateral anterior cingulate cortex and orbitofrontal cortex. PloS One 4:e6725CrossRefGoogle Scholar
  10. Christov-Moore L, Iacoboni M (2016a) Self-other resonance, its control and prosocial inclinations: brain-behavior relationships. Hum Brain Mapp 37(4):1544–1558.  https://doi.org/10.1002/hbm.23119 CrossRefGoogle Scholar
  11. Christov-Moore L, Simpson EA, Coude G, Grigaityte K, Iacoboni M, Ferrari PF (2014) Empathy: gender effects in brain and behavior. Neurosci Biobehav R 46(P4):604–627.  https://doi.org/10.1016/j.neubiorev.2014.09.001 CrossRefGoogle Scholar
  12. Christov-Moore L, Sugiyama T, Grigaityte K, Iacoboni M (2016b) Increasing generosity by disrupting prefrontal cortex. Soc Neurosci 919(June):1–8Google Scholar
  13. Christov-moore L, Conway P, Iacoboni M (2017) Deontological dilemma response tendencies and sensorimotor representations of harm to others. Front Integr Neurosci 11(December):1–9Google Scholar
  14. Cross KA, Torrisi S, Reynolds Losin EA, Iacoboni M (2013) Controlling automatic imitative tendencies: interactions between mirror neuron and cognitive control systems. Neuroimage 83(310):493–504CrossRefGoogle Scholar
  15. Dapretto M, Davies MS, Pfeifer JH, Scott AA, Sigman M, Bookheimer SY, Iacoboni M (2005) Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders. Nat Neurosci 9(1):28–30.  https://doi.org/10.1038/nn1611 CrossRefGoogle Scholar
  16. Davis MH (1983) Measuring individual differences in empathy: evidence for a multidimensional approach. J Pers Soc Psy 44(1):113–126.  https://doi.org/10.1037/0022-3514.44.1.113 CrossRefGoogle Scholar
  17. Davis MH, Franzoi SL (1991) Stability and change in adolescent self-consciousness and empathy. J Res Pers 25(1):70–87CrossRefGoogle Scholar
  18. Decety J, Lamm C (2007) The role of the right temporoparietal junction in social interaction: How low-level computational processes contribute to meta-cognition. Neuroscientist 13:580–593CrossRefGoogle Scholar
  19. De Renzi E, Cavalleri F, Facchini S (1996) Imitation and utilisation behaviour. J Neurol 61:396–400Google Scholar
  20. Eisenberg N, Lennon R (1993) Sex differences in empathy and related capacities. Psychol Bull 94(1):100–131.  https://doi.org/10.1037/0033-2909.94.1.100 CrossRefGoogle Scholar
  21. Eklund A, Nichols TE, Knutsson H (2016) Cluster failure: why fMRI inferences for spatial extent have inflated false-positive rates. Proc Natl Acad Sci USA 113(28):7900–7905.  https://doi.org/10.1073/pnas.1602413113 CrossRefGoogle Scholar
  22. Fadiga L, Fogassi L, Pavesi G, Rizzolatti G (1995) Motor facilitation during action observation: a magnetic stimulation study. J Neurophys 73:2608–2611CrossRefGoogle Scholar
  23. Friesdorf R, Conway P, Gawronski B (2015) Gender differences in responses to moral dilemmas: a process dissociation analysis. Pers Soc Psychol Rev 42:696–713.  https://doi.org/10.1177/0146167215575731 Google Scholar
  24. Gangitano M, Mottaghy F, Pascual-Leone A (2001) Phase-specific modulation of cortical motor output during movement observation. NeuroReport 12:1489–1492CrossRefGoogle Scholar
  25. Groen Y, Wijers AA, Tucha O, Althaus M (2013) Are there sex differences in ERPs related to processing empathy-evoking pictures? Neuropsychologia 51(1):142–155.  https://doi.org/10.1016/j.neuropsychologia.2012.11.012 CrossRefGoogle Scholar
  26. Gu X, Han S (2007) Attention and reality constraints on the neural processes of empathy for pain. NeuroImage 36(1):256–267.  https://doi.org/10.1016/j.neuroimage2007.02.025 CrossRefGoogle Scholar
  27. Guo X, Zheng L, Zhang W, Zhu L, Jianqi L, Wang Q, Dienes Z, Yang Z (2012) Empathic neural responses to others’ pain depend on monetary reward. Soc Cogn Affect Neurosci 7(5):535–541.  https://doi.org/10.1093/scan/nsr034 CrossRefGoogle Scholar
  28. Häfner H (2003) Gender differences in schizophrenia. Psychoneuroendocrinology 28(Suppl 2):17–54.  https://doi.org/10.1016/S0306-4530(02)00125-7 CrossRefGoogle Scholar
  29. Halladay AK, Bishop S, Constantino JN, Daniels AM, Koenig K, Palmer K et al (2015) Sex and gender differences in autism spectrum disorder: summarizing evidence gaps and identifying emerging areas of priority. Mol Autism 6:36.  https://doi.org/10.1186/s13229-015-0019-y CrossRefGoogle Scholar
  30. Hein G, Singer T (2008) I feel how you feel but not always: the empathic brain and its modulation. Curr Opin Neurobiol 18:153–158CrossRefGoogle Scholar
  31. Hein G, Silani G, Preuschoff K, Batson CD, Singer T (2010) Neural responses to ingroup and outgroup members’ suffering predict individual differences in costly helping. Neuron 68(1):149–160.  https://doi.org/10.1016/j.neuron.2010.09.003 CrossRefGoogle Scholar
  32. Iacoboni M (2009) Imitation, empathy, and mirror neurons. Annu Rev Psychol 60(0066–4308, 0066–4308):653–670.  https://doi.org/10.1146/annurev.psych.60.110707.163604 Google Scholar
  33. Ingersoll B, Schreibman L (2006) Teaching reciprocal imitation skills to young children with autism using a naturalistic behavioral approach: effects on language, pretend play, and joint attention. J Autism Dev Disord 36(4):487–505.  https://doi.org/10.1007/s10803-006-0089-y CrossRefGoogle Scholar
  34. Lamm C, Nusbaum HC, Meltzoff AN, Decety J (2007) What are you feeling? Using functional magnetic resonance imaging to assess the modulation of sensory and affective responses during empathy for pain. PLoS One 2:e1292CrossRefGoogle Scholar
  35. Lamm C, Decety J, Singer T (2011) NeuroImage Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain. NeuroImage 54(3):2492–2502.  https://doi.org/10.1016/j.neuroimage.2010.10.014 CrossRefGoogle Scholar
  36. Lhermitte F (1983) “Utilization behaviour” and its relation to lesions of the frontal lobes. Brain 106:237–255CrossRefGoogle Scholar
  37. Loggia ML, Mogil JS, Bushnell MC (2008) Empathy hurts: Compassion for another increases both sensory and affective components of pain perception. Pain 136:168–176CrossRefGoogle Scholar
  38. McCarthy MM, Arnold AP, Ball GF, Blaustein JD, De Vries GJ (2012) Sex differences in the brain: the not so inconvenient truth. J Neurosci 32(7):2241–2247CrossRefGoogle Scholar
  39. Mclaren DG, Ries ML, Xu G, Johnson SC (2012) NeuroImage A generalized form of context-dependent psychophysiological interactions (gPPI): a comparison to standard approaches. NeuroImage 61(4):1277–1286.  https://doi.org/10.1016/j.neuroimage.2012.03.068 CrossRefGoogle Scholar
  40. Mesch DJ, Brown MS, Moore ZI, Hayat AD (2011) gender differences in charitable giving. Int J Nonprofit Vol Sect Mark 21(July):3–12.  https://doi.org/10.1002/nvsm Google Scholar
  41. Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Ann Rev Neurosci 24:167–202CrossRefGoogle Scholar
  42. Morelli SA, Rameson LT, Lieberman MD (2014) The neural components of empathy: predicting daily prosocial behavior. Soc Cog Affect Neurosci 9:3947.  https://doi.org/10.1093/scan/nss088 Google Scholar
  43. Muthukumaraswamy SD, Johnson BW (2004) Changes in rolandic mu rhythm during observation of a precision grip. Psychophysiology 41(1):152–156.  https://doi.org/10.1046/j.1469-8986.2003.00129.x CrossRefGoogle Scholar
  44. Nicholls TL, Petrila J (2005) Gender and psychopathy: an overview of important issues and introduction to the special issue. Behav Sci Law 23(6):729–741.  https://doi.org/10.1002/bsl.677 CrossRefGoogle Scholar
  45. Pfeifer JH, Iacoboni M, Mazziotta JC, Dapretto M (2008) Mirroring others’ emotions relates to empathy and interpersonal competence in children. NeuroImage 39(4):2076–2085.  https://doi.org/10.1016/j.neuroimage.2007.10.032 CrossRefGoogle Scholar
  46. Singer T, Seymour B, O’Doherty J, Kaube H, Dolan RJ, Frith C (2004) Empathy for pain involves the affective but not sensory components of pain. Science 303(5661):1157–1162.  https://doi.org/10.1126/science.1093535 CrossRefGoogle Scholar
  47. Singer T, Seymour B, O’Doherty JP, Stephan KE, Dolan RJ, Frith CD (2006) Empathic neural responses are modulated by the perceived fairness of others. Nature 439(7075):466–469.  https://doi.org/10.1038/nature04271 CrossRefGoogle Scholar
  48. Sonnby-Borgström M (2002) Automatic mimicry reactions as related to differences in emotional empathy. Scand J Psychol 43(5):433–443.  https://doi.org/10.1111/1467-9450.00312 CrossRefGoogle Scholar
  49. Spengler S, von Cramon DY, Brass M (2009) Control of shared representations relies on key processes involved in mental state attribution. Hum Brain Mapp 30:3704–3718CrossRefGoogle Scholar
  50. Spengler S, Von Cramon DY, Brass M (2010) Resisting motor mimicry: Control of imitation involves processes central to social cognition in patients with frontal and temporo-parietal lesions. Soc Neurosci 5:401–416CrossRefGoogle Scholar
  51. Tassy S, Ouillier O, Duclos Y, Coulon O, Mancini J, Deruelle C, Attarian S, Felician O, Wicker B (2012) Disrupting the right prefrontal cortex alters moral judgement. Soc Cogn Affect Neurosci 7:282–288CrossRefGoogle Scholar
  52. Volman I, Katinka Louise von Borries, A, Hendrik Bulten B, Verkes J, Toni RI, Roelofs K (2016) Testosterone modulates altered prefrontal control of emotional actions in psychopathic offenders. Eneuro 3(February):1–12.  https://doi.org/10.1523/ENEURO.0107-15.2016 Google Scholar
  53. Winecoff A, Clithero JA, Carter RM, Bergman SR, Wang L, Huettel SA (2013) Ventromedial prefrontal cortex encodes emotional value. J Neurosci 33:11032–11039CrossRefGoogle Scholar
  54. Winkler AM, Ridgway GR, Webster MA, Smith SM, Nichols TE (2014) Permutation inference for the general linear model. Neuroimage 92:381–397CrossRefGoogle Scholar
  55. Yang CY, Decety J, Lee S, Chen C, Cheng Y (2009) Gender differences in the mu rhythm during empathy for pain: an electroencephalographic study. Brain Res 1251:176–184.  https://doi.org/10.1016/j.brainres.2008.11.062 CrossRefGoogle Scholar
  56. Zaki J, Ochsner KN (2012) The neuroscience of empathy: progress, pitfalls and promise, Nat Neurosci.  https://doi.org/10.1038/nn.3085 Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Ahmanson-Lovelace Brain Mapping CenterBrain Research Institute, UCLALos AngelesUSA
  2. 2.The Jane and Terry Semel Institute for Neuroscience and Human BehaviorDavid Geffen School of Medicine at UCLALos AngelesUSA

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