Anterior insula GABA levels correlate with emotional aspects of empathy: A proton magnetic resonance spectroscopy study

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Wang, Qianfeng ^a   Zhang, Zhuwei ^a   Dong, Fang ^a   Chen, Luguang ^a   Zheng, Li ^a   Guo, Xiuyan ^a   Li, Jianqi ^a  

^a EAST CHINA NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID;

ADULT; ANTERIOR CINGULATE; ANTERIOR INSULA; ARTICLE; EMOTION; EMPATHY; FEMALE; HUMAN; INTERPERSONAL REACTIVITY INDEX; LEFT HEMISPHERE; MALE; NORMAL HUMAN; PROTON NUCLEAR MAGNETIC RESONANCE; QUESTIONNAIRE; BRAIN CORTEX; CINGULATE GYRUS; HUMAN RELATION; METABOLISM; PHYSIOLOGY; PROCEDURES; YOUNG ADULT;

ADULT; CEREBRAL CORTEX; EMOTIONS; EMPATHY; FEMALE; GAMMA-AMINOBUTYRIC ACID; GYRUS CINGULI; HUMANS; INTERPERSONAL RELATIONS; MALE; PROTON MAGNETIC RESONANCE SPECTROSCOPY; SURVEYS AND QUESTIONNAIRES; YOUNG ADULT;

EID: 84913584712     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0113845     Document Type: Article

References (51)

1. Guo XY, Zheng L, Zhang W, Zhu L, Li JQ, et al. (2012) Empathic neural responses to others' pain depend on monetary reward. Social Cognitive and Affective Neuroscience 7: 535-541.
2. Bora E, Gokcen S, Veznedaroglu B (2008) Empathic abilities in people with schizophrenia. Psychiatry Research 160: 23-29.
3. Lombardo MV, Barnes JL, Wheelwright SJ, Baron-Cohen S (2007) Self-referential cognition and empathy in autism. PLoS One 2: e883.
4. Montag C, Heinz A, Kunz D, Gallinat J (2007) Self-reported empathic abilities in schizophrenia. Schizophrenia Research 92: 85-89.
5. Rogers K, Dziobek I, Hassenstab J, Wolf OT, Convit A (2007) Who cares? Revisiting empathy in Asperger syndrome. Journal of Autism and Developmental Disorders 37: 709-715.
6. Cheng YW, Lin CP, Liu HL, Hsu YY, Lim KE, et al. (2007) Expertise modulates the perception of pain in others. Current Biology 17: 1708-1713.
7. Danziger N, Faillenot I, Peyron R (2009) Can we share a pain we never felt? Neural correlates of empathy in patients with congenital insensitivity to pain. Neuron 61: 203-212.
8. Decety J, Echols S, Correll J (2010) The Blame Game: The effect of responsibility and social stigma on empathy for pain. Journal of Cognitive Neuroscience 22: 985-997.
9. Jackson PL, Brunet E, Meltzoff AN, Decety J (2006) Empathy examined through the neural mechanisms involved in imagining how I feel versus how you feel pain. Neuropsychologia 44: 752-761.
10. Morrison I, Downing PE (2007) Organization of felt and seen pain responses in anterior cingulate cortex. NeuroImage 37: 642-651.
11. Morrison I, Lloyd D, di Pellegrino G, Roberts N (2004) Vicarious responses to pain in anterior cingulate cortex: is empathy a multisensory issue? Cognitive, Affective, & Behavioral Neuroscience 4: 270-278.
12. Singer T, Seymour B, O'Doherty J, Kaube H, Dolan RJ, et al. (2004) Empathy for pain involves the affective but not sensory components of pain. Science 303: 1157-1162.
13. Lanctot KL, Herrmann N, Mazzotta P, Khan LR, Ingber N (2004) GABAergic function in Alzheimer's disease: evidence for dysfunction and potential as a therapeutic target for the treatment of behavioural and psychological symptoms of dementia. The Canadian Journal of Psychiatry 49: 439-453.
14. Marsman A, van den Heuvel MP, Klomp DW, Kahn RS, Luijten PR, et al. (2013) Glutamate in schizophrenia: a focused review and meta-analysis of 1H-MRS studies. Schizophrenia Bull 39: 120-129.
15. Martin WR (2007) MR spectroscopy in neurodegenerative disease. Molecular Imaging and Biology 9: 196-203.
16. O'Gorman RL, Michels L, Edden RA, Murdoch JB, Martin E (2011) In vivo detection of GABA and glutamate with MEGA-PRESS: reproducibility and gender effects. Journal of Magnetic Resonance Imaging 33: 1262-1267.
17. Montag C, Schubert F, Heinz A, Gallinat J (2008) Prefrontal Cortex Glutamate Correlates with Mental Perspective-Taking. PLoS One 3: e3890.
18. Coghlan S, Hordera J, Inkster B, Mendeza MA, Murphya DG, et al. (2012) GABA system dysfunction in autism and related disorders: From synapse to symptoms. Neuroscience and Biobehavioral Reviews 36: 2044-2055.
19. Rosso IM, Weiner MR, Crowley DJ, Silveri MM, Rauch SL, et al. (2014) Insula and anterior cingulate GABA levels in posttraumatic stress disorder: preliminary findings using magnetic resonance spectroscopy. Depress Anxiety 31: 115-123.
20. Ham BJ, Sung Y, Kim N, Kim JK, Kim DJ, et al. (2007) Decreased GABA levels in anterior cingulate and basal ganglia in medicated subjects with panic disorder: a proton magnetic resonance spectroscopy (1H-MRS) study. Progress in Neuro-Psychopharmacology & Biological Psychiatry 31: 403-411.
21. Long Z, Medlock C, Dzemidzic M, Shin YW, Goddard AW, et al. (2013) Decreased GABA levels in anterior cingulate cortex/medial prefrontal cortex in panic disorder. Progress in Neuro-Psychopharmacology & Biological Psychiatry 44: 131-135.
22. Davis MH (1980) A multidimensional approach to individual differences in empathy. JSAS Catalog of Selected Documents in Psychology 10: 85.
23. Mescher M, Merkle H, Kirsch J, Garwood M, Gruetter R (1998) Simultaneous in vivo spectral editing and water suppression. NMR in Biomedicine 11: 266-272.
24. Mullins PG, McGonigle DJ, O'Gorman RL, Puts NA, Vidyasagar R, et al. (2014) Current practice in the use of MEGA-PRESS spectroscopy for the detection of GABA. NeuroImage 86: 43-52.
25. Near J, Ho YCL, Sandberg K, Kumaragamage C, Blicher JU (2014) Long-term reproducibility of GABA magnetic resonance spectroscopy. NeuroImage 99: 191-196.
26. Naressi A, Couturier C, Castang I, de Beer R, Graveron-Demilly D (2001) Java-based graphical user interface for MRUI, a software package for quantitation of in vivo/medical magnetic resonance spectroscopy signals. Computers in Biology and Medicine 31: 269-286.
27. Donahue MJ, Near J, Blicher JU, Jezzard P (2010) Baseline GABA concentration and fMRI response. NeuroImage 53: 392-398.
28. Near J, Edden R, Evans CJ, Paquin R, Harris A, Jezzard P (2014) Frequency and phase drift correction of magnetic resonance spectroscopy data by spectral registration in the time domain. Magn Reson Med 00: 00-00.
29. Near J, Simpson R, Cowen P, Jezzard P (2011) Efficient-aminobutyric acid editing at 3T without macromolecule contamination: MEGA-SPECIAL. NMR Biomed 24: 1277-1285.
30. Vanhamme L, Sundin T, Hecke PV, Huffel SV (2001) MR spectroscopy quantitation: a review of time-domain methods. NMR in Biomedicine 14: 233-246.
31. Sandberg K, Blicher JU, Dong MY, Rees G, Near J, et al. (2014) Occipital GABA correlates with cognitive failures in daily life. NeuroImage 87: 55-60.
32. Davis MH (1983) Measuring individual-differences in empathy - evidence for a multidimensional approach. Journal of Personality and Social Psychology 44: 113-126.
33. Fujiwara H, Shimizu M, Hirao K, Hirao K, Miyata J, et al. (2008) Female specific anterior cingulate abnormality and its association with empathic disability in schizophrenia. Progress in Neuro-Psychopharmacology & Biological Psychiatry 32: 1728-1734.
34. Kleppner SR, Tobin AJ (2001) GABA signalling: therapeutic targets for epilepsy, Parkinson's disease and Huntington's disease. Expert Opinion on Therapeutic Targets 5: 219-239.
35. Sanacora G, Mason GF, Rothman DL, Rothman DL, Behar KL, et al. (1999) Reduced cortical gamma-aminobutyric acid levels in depressed patients determined by proton magnetic resonance spectroscopy. Archives of General Psychiatry 56: 1043-1047.
36. Decety J, Jackson PL (2004) The functional architecture of human empathy. Behavioral and Cognitive Neuroscience Reviews 3: 71-100.
37. Lee SJ, Kang DH, Kim CW, Gu BM, Park JY, et al. (2010) Multi-level comparison of empathy in schizophrenia: an fMRI study of a cartoon task. Psychiatry Reseach 181: 121-129.
38. Preis MA, Schmidt-Samoa C, Dechent P, Kroener-Herwig B (2013) The effects of prior pain experience on neural correlates of empathy for pain: An fMRI study. Pain 154: 411-418.
39. Jackson PL, Meltzoff AN, Decety J (2005) How do we perceive the pain of others? A window into the neural processes involved in empathy. NeuroImage 24: 771-779.
40. Citron FM, Gray MA, Critchley HD, Weekes BS, Ferstl EC (2014) Emotional valence and arousal affect reading in an interactive way: Neuroimaging evidence for an approach-withdrawal framework. Neuropsychologia 56: 79-89.
41. Mutschler I, Wieckhorst B, Kowalevski S, Derix J, Wentlandt J, et al. (2009) Functional organization of the human anterior insular cortex. Neurosci Lett 457: 66-70.
42. Zhu L, Zheng L, Chen M, Guo X, Li J, et al. (2013) The neural correlates of incidental self-processing induced by handwritten negative words. EXP BRAIN RES 228: 1-8.
43. Wiebking C, Duncan NW, Tiret B, Hayes DJ, Marjanska M, et al. (2014) GABA in the insula - a predictor of the neural response to interoceptive awareness. NeuroImage 86: 10-18.
44. Fan Y, Duncan NW, de Greck M, Northoff G (2011) Is there a core neural network in empathy? An fMRI based quantitative meta-analysis. Neurosci Biobehav Rev 35: 903-911.
45. Ernst J, Böker H, Hättenschwiler J, Schüpbach D, Northoff G, et al. (2014) The association of interoceptive awareness and alexithymia with neurotransmitter concentrations in insula and anterior cingulate. Soc Cogn Affect Neurosci 9: 857-63.
46. Gu X, Gao Z, Wang X, Liu X, Knight RT, Hof PR, Fan J (2012) Anterior insular cortex is necessary for empathetic pain perception. Brain 135: 2726-2735.
47. Mutschler I, Wieckhorst B, Kowalevski S, Derix J, Wentlandt J, et al. (2009) Functional organization of the human anterior insular cortex. Neurosci Lett 457: 66-70.
48. Michalska KJ, Kinzler KD, Decety J (2013) Age-related sex differences in explicit measures of empathy do not predict brain responses across childhood and adolescence. Developmental Cognitive Neuroscience 3: 22-32.
49. Kaplan JT, Iacoboni M (2006) Getting a grip on other minds: mirror neurons, intention understanding, and cognitive empathy. Social Neuroscience 1: 175-183.
50. Gazzola V, Aziz-Zadeh L, Keysers C (2006) Empathy and the somatotopic auditory mirror system in humans. Current Biology 16: 1824-1829.
51. Near J, Simpson R, Cowen P, Jezzard P (2011) Efficient-aminobutyric acid editing at 3T without macromolecule contamination: MEGA-SPECIAL. NMR Biomed 24: 1277-1285.