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The effects of repetitive transcranial magnetic stimulation on empathy: a systematic review and meta-analysis

Published online by Cambridge University Press:  22 August 2017

C.-C. Yang
Affiliation:
Division of Psychiatry and Applied Psychology, School of Medicine, University of Nottingham, UK
N. Khalifa
Affiliation:
Division of Psychiatry and Applied Psychology, School of Medicine, University of Nottingham, UK
B. Völlm*
Affiliation:
Division of Psychiatry and Applied Psychology, School of Medicine, University of Nottingham, UK
*
*Address for correspondence: Professor B. Völlm, Institute of Mental Health, Innovation Park, Triumph Road, Nottingham, NG7 2TU, UK. (Email: birgit.vollm@nottingham.ac.uk)

Abstract

Empathy is a multi-dimensional concept with affective and cognitive components, the latter often referred to as Theory of Mind (ToM). Impaired empathy is prevalent in people with neuropsychiatric disorders, such as personality disorder, psychopathy, and schizophrenia, highlighting the need to develop therapeutic interventions to address this. Repetitive transcranial magnetic stimulation (rTMS), a non-invasive therapeutic technique that has been effective in treating various neuropsychiatric conditions, can be potentially used to modulate empathy. To our knowledge, no systematic reviews or meta-analyses in this field have been conducted. The aim of the current study was to review the literature on the use of rTMS to modulate empathy in adults. Seven electronic databases (AMED, Cochrane library, EMBASE, Medline, Pubmed, PsycInfo, and Web of Science) were searched using appropriate search terms. Twenty-two studies were identified, all bar one study involved interventions in healthy rather than clinical populations, and 18 of them, providing results for 24 trials, were included in the meta-analyses. Results showed an overall small, but statistically significant, effect in favour of active rTMS in healthy individuals. Differential effects across cognitive and affective ToM were evident. Subgroup analyses for cognitive ToM revealed significant effect sizes on excitatory rTMS, offline paradigms, and non-randomised design trials. Subgroup analyses for affective ToM revealed significant effect sizes on excitatory rTMS, offline paradigms, and non-randomised design trials. Meta-regression revealed no significant sources of heterogeneity. In conclusion, rTMS may have discernible effects on different components of empathy. Further research is required to examine the effects of rTMS on empathy in clinical and non-clinical populations, using appropriate empathy tasks and rTMS protocols.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2017 

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References

Balconi, M, Bortolotti, A (2012). Detection of the facial expression of emotion and self-report measures in empathic situations are influenced by sensorimotor circuit inhibition by low-frequency rTMS. Brain Stimulation 5, 330336.CrossRefGoogle ScholarPubMed
Balconi, M, Bortolotti, A (2013). Emotional face recognition, empathic trait (BEES), and cortical contribution in response to positive and negative cues. The effect of rTMS on dorsal medial prefrontal cortex. Cognitive Neurodynamics 7, 1321.Google Scholar
Balconi, M, Bortolotti, A, Gonzaga, L (2011). Emotional face recognition, EMG response, and medial prefrontal activity in empathic behaviour. Neuroscience Research 71, 251259.CrossRefGoogle ScholarPubMed
Balconi, M, Canavesio, Y (2013). High-frequency rTMS improves facial mimicry and detection responses in an empathic emotional task. Neuroscience 236, 1220.CrossRefGoogle Scholar
Balconi, M, Canavesio, Y (2016). Empathy, approach attitude, and rTMS on left DLPFC affect emotional face recognition and facial feedback (EMG). Journal of Psychophysiology 30, 1728.CrossRefGoogle Scholar
Balconi, M, Crivelli, D, Bortolotti, A (2010). Detection of facial expression of emotion and self-report measures in empathic situations are influenced by ACC inhibition: rTMS evidences. Neuropsychological Trends 8, 9599.Google Scholar
Baron-Cohen, S (1989). The autistic child's theory of mind: a case of specific developmental delay. Journal of Child Psychology and Psychiatry and Allied Disciplines 30, 285297.CrossRefGoogle ScholarPubMed
Baron-Cohen, S, Leslie, AM, Frith, U (1985). Does the autistic-child have a theory of mind. Cognition 21, 3746.CrossRefGoogle ScholarPubMed
Baron-Cohen, S, Wheelwright, S, Hill, J, Raste, Y, Plumb, I (2001). The “Reading the Mind in the Eyes’ test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. Journal of Child Psychology and Psychiatry and Allied Disciplines 42, 241251.Google Scholar
Begg, CB, Mazumdar, M (1994). Operating characteristics of a rank correlation test for publication bias. Biometrics 50, 10881101.Google Scholar
Behan, B, Stone, A, Garavan, H (2015). Right prefrontal and ventral striatum interactions underlying impulsive choice and impulsive responding. Human Brain Mapping 36, 187198.CrossRefGoogle ScholarPubMed
Blair, J, Mitchell, DR, Blair, K (2005). The Psychopath: Emotion and the Brain. Blackwell Pub.: Malden, MA, USA.Google Scholar
Blair, RJ (2005). Responding to the emotions of others: dissociating forms of empathy through the study of typical and psychiatric populations. Consciousness and Cognition 14, 698718.Google Scholar
Bolognini, N, Rossetti, A, Convento, S, Vallar, G (2013). Understanding others' feelings: the role of the right primary somatosensory cortex in encoding the affective valence of others' touch. Journal of Neuroscience 33, 42014205.Google Scholar
Borenstein, M, Hedges, LV, Higgins, JPT, Rothstein, HR (2009). Meta-Regression. In Introduction to Meta-Analysis (ed. Borenstein, M, Hedges, LV, Higgins, JPT, Rothstein, HR), pp. 187203. John Wiley & Sons: Chichester, UK.Google Scholar
Bragado-Jimenez, MD, Taylor, PJ (2012). Empathy, schizophrenia and violence: a systematic review. Schizophrenia Research 141, 8390.CrossRefGoogle ScholarPubMed
Carrington, SJ, Bailey, AJ (2009). Are there theory of mind regions in the brain? A review of the neuroimaging literature. Human Brain Mapping 30, 23132335.Google Scholar
Chou, YH, Hickey, PT, Sundman, M, Song, AW, Chen, NK (2015). Effects of repetitive transcranial magnetic stimulation on motor symptoms in Parkinson disease: a systematic review and meta-analysis. JAMA Neurology 72, 432440.Google Scholar
Costa, A, Torriero, S, Oliveri, M, Caltagirone, C (2008). Prefrontal and temporo-parietal involvement in taking others’ perspective: TMS evidence. Behavioural Neurology 19, 7174.Google Scholar
Dal Monte, O, Schintu, S, Pardini, M, Berti, A, Wassermann, EM, Grafman, J, Krueger, F (2014). The left inferior frontal gyrus is crucial for reading the mind in the eyes: brain lesion evidence. Cortex 58, 917.Google Scholar
Day, A, Casey, S, Gerace, A (2010). Interventions to improve empathy awareness in sexual and violent offenders: conceptual, empirical, and clinical issues. Aggression and Violent Behavior 15, 201208.Google Scholar
Denny, BT, Kober, H, Wager, TD, Ochsner, KN (2012). A meta-analysis of functional neuroimaging studies of self- and other judgments reveals a spatial gradient for mentalizing in medial prefrontal cortex. Journal of Cognitive Neuroscience 24, 17421752.CrossRefGoogle ScholarPubMed
Dolan, M, Fullam, R (2004). Theory of mind and mentalizing ability in antisocial personality disorders with and without psychopathy. Psychological Medicine 34, 10931102.Google Scholar
Dvash, J, Shamay-Tsoory, SG (2014). Theory of mind and empathy as multidimensional constructs neurological foundations. Topics in Language Disorders 34, 282295.Google Scholar
Egger, M, Smith, GD (1995). Misleading meta-analysis. British Medical Journal 310, 752754.Google Scholar
Egger, M, Smith, GD, Schneider, M, Minder, C (1997). Bias in meta-analysis detected by a simple, graphical test. British Medical Journal 315, 629634.Google Scholar
Eisenegger, C, Treyer, V, Fehr, E, Knoch, D (2008). Time-course of ‘off-line’ prefrontal rTMS effects – a PET study. Neuroimage 42, 379384.CrossRefGoogle ScholarPubMed
Ekman, P, Friesen, W (1976). Pictures of Facial Affect. Consulting Psychologists Press: Palo Alto, CA, USA.Google Scholar
Enticott, PG, Fitzgibbon, BM, Kennedy, HA, Arnold, SL, Elliot, D, Peachey, A, Zangen, A, Fitzgerald, PB (2014). A double-blind, randomized trial of deep repetitive transcranial magnetic stimulation (rTMS) for autism spectrum disorder. Brain Stimulation 7, 206211.Google Scholar
Frith, CD, Frith, U (1999). Interacting minds – a biological basis. Science 286, 16921695.Google Scholar
Gallese, V (2003). The roots of empathy: the shared manifold hypothesis and the neural basis of intersubjectivity. Psychopathology 36, 171180.Google Scholar
Gentili, C, Cristea, IA, Ricciardi, E, Costescu, C, David, D, Pietrini, P (2015). Neurobiological correlates of the attitude toward human empathy. Rivista Internazionale Di Filosofia E Psicologia 6, 7087.Google Scholar
Giardina, A, Caltagirone, C, Oliveri, M (2011). Temporo-parietal junction is involved in attribution of hostile intentionality in social interactions: an rTMS study. Neuroscience Letters 495, 150154.Google Scholar
Glannon, W (2014). Intervening in the psychopath's brain. Theoretical Medicine and Bioethics 35, 4357.Google Scholar
Glenn, AL, Raine, A (2008). The neurobiology of psychopathy. Psychiatric Clinics of North America 31, 463475.Google Scholar
Gonzalez-Liencres, C, Shamay-Tsoory, SG, Brune, M (2013). Towards a neuroscience of empathy: ontogeny, phylogeny, brain mechanisms, context and psychopathology. Neuroscience and Biobehavioral Reviews 37, 15371548.Google Scholar
Hetu, S, Taschereau-Dumouchel, V, Jackson, PL (2012). Stimulating the brain to study social interactions and empathy. Brain Stimulation 5, 95102.CrossRefGoogle ScholarPubMed
Higgins, JP, Thompson, SG (2002). Quantifying heterogeneity in a meta-analysis. Statistics in Medicine 21, 15391558.Google Scholar
Higgins, JP, Thompson, SG, Deeks, JJ, Altman, DG (2003). Measuring inconsistency in meta-analyses. British Medical Journal 327, 557560.CrossRefGoogle ScholarPubMed
Hoekert, M, Vingerhoets, G, Aleman, A (2010). Results of a pilot study on the involvement of bilateral inferior frontal gyri in emotional prosody perception: an rTMS study. BMC Neuroscience 11, 93.CrossRefGoogle ScholarPubMed
Hogan, R (1969). Development of an empathy scale. Journal of Consulting and Clinical Psychology 33, 307316.CrossRefGoogle ScholarPubMed
Hsu, WY, Ku, Y, Zanto, TP, Gazzaley, A (2015). Effects of noninvasive brain stimulation on cognitive function in healthy aging and Alzheimer's disease: a systematic review and meta-analysis. Neurobiol Aging 36, 23482359.Google Scholar
Huang, YZ, Edwards, MJ, Rounis, E, Bhatia, KP, Rothwell, JC (2005). Theta burst stimulation of the human motor cortex. Neuron 45, 201206.Google Scholar
Jolliffe, D, Farrington, DP (2004). Empathy and offending: a systematic review and meta-analysis. Aggression and Violent Behavior 9, 441476.Google Scholar
Kalbe, E, Schlegel, M, Sack, AT, Nowak, DA, Dafotakis, M, Bangard, C, Brand, M, Shamay-Tsoory, S, Onur, OA, Kessler, J (2010). Dissociating cognitive from affective theory of mind: a TMS study. Cortex 46, 769780.Google Scholar
Keuken, MC, Hardie, A, Dorn, BT, Dev, S, Paulus, MP, Jonas, KJ, Van den Wildenberg, WPM, Pineda, JA (2011). The role of the left inferior frontal gyrus in social perception: an rTMS study. Brain Research 1383, 196205.Google Scholar
Krall, SC, Volz, LJ, Oberwelland, E, Grefkes, C, Fink, GR, Konrad, K (2016). The right temporoparietal junction in attention and social interaction: a transcranial magnetic stimulation study. Human Brain Mapping 37, 796807.CrossRefGoogle ScholarPubMed
Krause, L, Enticott, PG, Zangen, A, Fitzgerald, PB (2012). The role of medial prefrontal cortex in theory of mind: a deep rTMS study. Behavioural Brain Research 228, 8790.Google Scholar
Laisney, M, Bon, L, Guiziou, C, Daluzeau, N, Eustache, F, Desgranges, B (2013). Cognitive and affective theory of mind in mild to moderate Alzheimer's disease. Journal of Neuropsychology 7, 107120.Google Scholar
Lev-Ran, S, Shamay-Tsoory, S, Zangen, A, Levkovitz, Y (2012). Transcranial magnetic stimulation of the ventromedial prefrontal cortex impairs theory of mind learning. European Psychiatry 27, 285289.Google Scholar
Li, YH, Chiu, MJ, Yeh, ZT, Liou, HH, Cheng, TW, Hua, MS (2013). Theory of mind in patients with temporal lobe epilepsy. Journal of the International Neuropsychological Society 19, 594600.Google Scholar
Luber, B, Lisanby, SH (2014). Enhancement of human cognitive performance using transcranial magnetic stimulation (TMS). Neuroimage 85, 961970.Google Scholar
Mehrabian, A (2000). Beyond IQ: broad-based measurement of individual success potential or ‘emotional intelligence’. Genetic Social and General Psychology Monographs 126, 133239.Google Scholar
Michael, J, Sandberg, K, Skewes, J, Wolf, T, Blicher, J, Overgaard, M, Frith, CD (2014). Continuous theta-burst stimulation demonstrates a causal role of premotor homunculus in action understanding. Psychological Science 25, 963972.Google Scholar
Moher, D, Shamseer, L, Clarke, M, Ghersi, D, Liberati, A, Petticrew, M, Shekelle, P, Stewart, LA, PRISMA-P Group (2015). Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Systematic Reviews 4, 1.Google Scholar
National Collaborating Centre for Methods and Tools (2008). Quality Assessment Tool for Quantitative Studies Method. McMaster University: Hamilton, ON.Google Scholar
Pascual-Leone, A, Walsh, V, Rothwell, J (2000). Transcranial magnetic stimulation in cognitive neuroscience – virtual lesion, chronometry, and functional connectivity. Current Opinion in Neurobiology 10, 232237.Google Scholar
Pobric, G, Hamilton, AFdC (2006). Action understanding requires the left inferior frontal cortex. Current Biology 16, 524529.Google Scholar
Poletti, M, Enrici, I, Adenzato, M (2012). Cognitive and affective theory of mind in neurodegenerative diseases: neuropsychological, neuroanatomical and neurochemical levels. Neuroscience and Biobehavioral Reviews 36, 21472164.CrossRefGoogle ScholarPubMed
Reidy, DE, Kearns, MC, DeGue, S (2013). Reducing psychopathic violence: a review of the treatment literature. Aggression and Violent Behavior 18, 527538.Google Scholar
Reniers, RLEP, Corcoran, R, Drake, R, Shryane, NM, Völlm, BA (2011). The QCAE: a questionnaire of cognitive and affective empathy. Journal of Personality Assessment 93, 8495.Google Scholar
Reniers, RLEP, Völlm, BA, Elliott, R, Corcoran, R (2014). Empathy, ToM, and self-other differentiation: an fMRI study of internal states. Social Neuroscience 9, 5062.Google Scholar
Robertson, EM, Theoret, H, Pascual-Leone, A (2003). Studies in cognition: the problems solved and created by transcranial magnetic stimulation. Journal of Cognitive Neuroscience 15, 948960.Google Scholar
Rossi, S, Hallett, M, Rossini, PM, Pascual-Leone, A, Safety of TMS Consensus Group (2009). Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clinical Neurophysiology 120, 20082039.CrossRefGoogle ScholarPubMed
Sandrini, M, Umilta, C, Rusconi, E (2011). The use of transcranial magnetic stimulation in cognitive neuroscience: a new synthesis of methodological issues. Neuroscience and Biobehavioral Reviews 35, 516536.CrossRefGoogle ScholarPubMed
Schreiter, S, Pijnenborg, GHM, Aan Het Rot, M (2013). Empathy in adults with clinical or subclinical depressive symptoms. Journal of Affective Disorders 150, 116.Google Scholar
Schuwerk, T, Langguth, B, Sommer, M (2014a). Modulating functional and dysfunctional mentalizing by transcranial magnetic stimulation. Frontiers in Psychology 5, 1309. http://dx.doi.org/10.3389/fpsyg.2014.01309.Google Scholar
Schuwerk, T, Schecklmann, M, Langguth, B, Dohnel, K, Sodian, B, Sommer, M (2014b). Inhibiting the posterior medial prefrontal cortex by rTMS decreases the discrepancy between self and other in Theory of Mind reasoning. Behavioural Brain Research 274, 312318.Google Scholar
Sebastian, CL, Fontaine, NMG, Bird, G, Blakemore, SJ, De Brito, SA, McCrory, EJP, Viding, E (2012). Neural processing associated with cognitive and affective Theory of Mind in adolescents and adults. Social Cognitive and Affective Neuroscience 7, 5363.CrossRefGoogle ScholarPubMed
Serafini, G, Pompili, M, Belvederi Murri, M, Respino, M, Ghio, L, Girardi, P, Fitzgerald, PB, Amore, M (2015). The effects of repetitive transcranial magnetic stimulation on cognitive performance in treatment-resistant depression. A systematic review. Neuropsychobiology 71, 125139.Google Scholar
Shamay-Tsoory, SG, Aharon-Peretz, J (2007). Dissociable prefrontal networks for cognitive and affective theory of mind: a lesion study. Neuropsychologia 45, 30543067.CrossRefGoogle ScholarPubMed
Shamay-Tsoory, SG, Aharon-Peretz, J, Perry, D (2009). Two systems for empathy: a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain 132, 617627.Google Scholar
Shamseer, L, Moher, D, Clarke, M, Ghersi, D, Liberati, A, Petticrew, M, Shekelle, P, Stewart, LA, PRISMA-P Group (2015). Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. British Medical Journal 349, g7647.Google Scholar
Shimoni, HN, Weizman, A, Yoran, RH, Raviv, A (2012). Theory of mind, severity of autistic symptoms and parental correlates in children and adolescents with Asperger syndrome. Psychiatry Research 197, 8589.CrossRefGoogle Scholar
Silani, G, Lamm, C, Ruff, CC, Singer, T (2013). Right supramarginal gyrus is crucial to overcome emotional egocentricity bias in social judgments. Journal of Neuroscience 33, 1546615476.CrossRefGoogle ScholarPubMed
StataCorp (2013). Stata Statistical Software: Release 13. StataCorp LP: College Station, TX, USA.Google Scholar
Stone, VE, Baron-Cohen, S, Knight, RT (1998). Frontal lobe contributions to theory of mind. Journal of Cognitive Neuroscience 10, 640656.Google Scholar
Uddin, LQ, Molnar-Szakacs, I, Zaidel, E, Iacoboni, M (2006). rTMS to the right inferior parietal lobule disrupts self-other discrimination. Social Cognitive and Affective Neuroscience 1, 6571.Google Scholar
Völlm, BA, Taylor, ANW, Richardson, P, Corcoran, R, Stirling, J, McKie, S, Deakin, JFW, Elliott, R (2006). Neuronal correlates of theory of mind and empathy: a functional magnetic resonance imaging study in a nonverbal task. Neuroimage 29, 9098.Google Scholar
Wassermann, EM, Zimmermann, T (2012). Transcranial magnetic brain stimulation: therapeutic promises and scientific gaps. Pharmacology & Therapeutics 133, 98107.Google Scholar
Young, L, Camprodon, JA, Hauser, M, Pascual-Leone, A, Saxe, R (2010). Disruption of the right temporoparietal junction with transcranial magnetic stimulation reduces the role of beliefs in moral judgments. Proceedings of the National Academy of Sciences of the United States of America 107, 67536758.Google Scholar
Yu, RL, Wu, RM, Chiu, MJ, Tai, CH, Lin, CH, Hua, MS (2012). Advanced Theory of Mind in patients at early stage of Parkinson's disease. Parkinsonism & Related Disorders 18, 2124.Google Scholar
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