Skip to main content
×
Home

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

  • C.-C. Yang (a1), N. Khalifa (a1) and B. Völlm (a1)
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.

Copyright
Corresponding author
*Address for correspondence: Professor B. Völlm, Institute of Mental Health, Innovation Park, Triumph Road, Nottingham, NG7 2TU, UK. (Email: birgit.vollm@nottingham.ac.uk)
References
Hide All
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.
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.
Balconi M, Bortolotti A, Gonzaga L (2011). Emotional face recognition, EMG response, and medial prefrontal activity in empathic behaviour. Neuroscience Research 71, 251259.
Balconi M, Canavesio Y (2013). High-frequency rTMS improves facial mimicry and detection responses in an empathic emotional task. Neuroscience 236, 1220.
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.
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.
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.
Baron-Cohen S, Leslie AM, Frith U (1985). Does the autistic-child have a theory of mind. Cognition 21, 3746.
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.
Begg CB, Mazumdar M (1994). Operating characteristics of a rank correlation test for publication bias. Biometrics 50, 10881101.
Behan B, Stone A, Garavan H (2015). Right prefrontal and ventral striatum interactions underlying impulsive choice and impulsive responding. Human Brain Mapping 36, 187198.
Blair J, Mitchell DR, Blair K (2005). The Psychopath: Emotion and the Brain. Blackwell Pub.: Malden, MA, USA.
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.
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.
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.
Bragado-Jimenez MD, Taylor PJ (2012). Empathy, schizophrenia and violence: a systematic review. Schizophrenia Research 141, 8390.
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.
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.
Costa A, Torriero S, Oliveri M, Caltagirone C (2008). Prefrontal and temporo-parietal involvement in taking others’ perspective: TMS evidence. Behavioural Neurology 19, 7174.
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.
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.
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.
Dolan M, Fullam R (2004). Theory of mind and mentalizing ability in antisocial personality disorders with and without psychopathy. Psychological Medicine 34, 10931102.
Dvash J, Shamay-Tsoory SG (2014). Theory of mind and empathy as multidimensional constructs neurological foundations. Topics in Language Disorders 34, 282295.
Egger M, Smith GD (1995). Misleading meta-analysis. British Medical Journal 310, 752754.
Egger M, Smith GD, Schneider M, Minder C (1997). Bias in meta-analysis detected by a simple, graphical test. British Medical Journal 315, 629634.
Eisenegger C, Treyer V, Fehr E, Knoch D (2008). Time-course of ‘off-line’ prefrontal rTMS effects – a PET study. Neuroimage 42, 379384.
Ekman P, Friesen W (1976). Pictures of Facial Affect. Consulting Psychologists Press: Palo Alto, CA, USA.
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.
Frith CD, Frith U (1999). Interacting minds – a biological basis. Science 286, 16921695.
Gallese V (2003). The roots of empathy: the shared manifold hypothesis and the neural basis of intersubjectivity. Psychopathology 36, 171180.
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.
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.
Glannon W (2014). Intervening in the psychopath's brain. Theoretical Medicine and Bioethics 35, 4357.
Glenn AL, Raine A (2008). The neurobiology of psychopathy. Psychiatric Clinics of North America 31, 463475.
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.
Hetu S, Taschereau-Dumouchel V, Jackson PL (2012). Stimulating the brain to study social interactions and empathy. Brain Stimulation 5, 95102.
Higgins JP, Thompson SG (2002). Quantifying heterogeneity in a meta-analysis. Statistics in Medicine 21, 15391558.
Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003). Measuring inconsistency in meta-analyses. British Medical Journal 327, 557560.
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.
Hogan R (1969). Development of an empathy scale. Journal of Consulting and Clinical Psychology 33, 307316.
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.
Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC (2005). Theta burst stimulation of the human motor cortex. Neuron 45, 201206.
Jolliffe D, Farrington DP (2004). Empathy and offending: a systematic review and meta-analysis. Aggression and Violent Behavior 9, 441476.
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.
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.
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.
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.
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.
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.
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.
Luber B, Lisanby SH (2014). Enhancement of human cognitive performance using transcranial magnetic stimulation (TMS). Neuroimage 85, 961970.
Mehrabian A (2000). Beyond IQ: broad-based measurement of individual success potential or ‘emotional intelligence’. Genetic Social and General Psychology Monographs 126, 133239.
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.
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.
National Collaborating Centre for Methods and Tools (2008). Quality Assessment Tool for Quantitative Studies Method. McMaster University: Hamilton, ON.
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.
Pobric G, Hamilton AFdC (2006). Action understanding requires the left inferior frontal cortex. Current Biology 16, 524529.
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.
Reidy DE, Kearns MC, DeGue S (2013). Reducing psychopathic violence: a review of the treatment literature. Aggression and Violent Behavior 18, 527538.
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.
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.
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.
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.
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.
Schreiter S, Pijnenborg GHM, Aan Het Rot M (2013). Empathy in adults with clinical or subclinical depressive symptoms. Journal of Affective Disorders 150, 116.
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.
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.
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.
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.
Shamay-Tsoory SG, Aharon-Peretz J (2007). Dissociable prefrontal networks for cognitive and affective theory of mind: a lesion study. Neuropsychologia 45, 30543067.
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.
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.
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.
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.
StataCorp (2013). Stata Statistical Software: Release 13. StataCorp LP: College Station, TX, USA.
Stone VE, Baron-Cohen S, Knight RT (1998). Frontal lobe contributions to theory of mind. Journal of Cognitive Neuroscience 10, 640656.
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.
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.
Wassermann EM, Zimmermann T (2012). Transcranial magnetic brain stimulation: therapeutic promises and scientific gaps. Pharmacology & Therapeutics 133, 98107.
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.
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.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Psychological Medicine
  • ISSN: 0033-2917
  • EISSN: 1469-8978
  • URL: /core/journals/psychological-medicine
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Type Description Title
WORD
Supplementary Materials

Yang et al supplementary material
Yang et al supplementary material 1

 Word (76 KB)
76 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 9
Total number of PDF views: 57 *
Loading metrics...

Abstract views

Total abstract views: 407 *
Loading metrics...

* Views captured on Cambridge Core between 22nd August 2017 - 11th December 2017. This data will be updated every 24 hours.