The association of interoceptive awareness and alexithymia with neurotransmitter concentrations in insula and anterior cingulate

Social Cognitive and Affective Neuroscience

Volumn 9, Issue 6, 2013, Pages 857-863

  Ernst, Jutta ^a   Böker, Heinz ^a   Hättenschwiler, Joe ^b   Schüpbach, Daniel ^a   Northoff, Georg ^c   Seifritz, Erich ^a   Grimm, Simone ^a,d,e  

^a UNIVERSITY HOSPITAL OF PSYCHIATRY   (Switzerland)

^b Center for Anxiety and Depression   (Switzerland)

^c UNIVERSITY OF OTTAWA   (Canada)

^d CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^e FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Alexithymia; Interoceptive awareness; Neurotransmitter; Proton magnetic resonance spectroscopy

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID;

ADULT; BRAIN CORTEX; CINGULATE GYRUS; EMOTIONAL DISORDER; FEMALE; HUMAN; MALE; METABOLISM; PERSONALITY; PHYSIOLOGY; PROTON NUCLEAR MAGNETIC RESONANCE; QUESTIONNAIRE; SELF EVALUATION;

ADULT; AFFECTIVE SYMPTOMS; CEREBRAL CORTEX; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; GYRUS CINGULI; HUMANS; MALE; PERSONALITY; PROTON MAGNETIC RESONANCE SPECTROSCOPY; QUESTIONNAIRES; SELF-ASSESSMENT;

EID: 84902299637     PISSN: 17495016     EISSN: 17495024     Source Type: Journal    
DOI: 10.1093/scan/nst058     Document Type: Article

References (105)

1. Abler, B., Hofer, C., Walter, H., et al. (2010). Habitual emotion regulation strategies and depressive symptoms in healthy subjects predict fMRI brain activation patterns related to major depression. Psychiatry Research, 183, 105-13.
2. Bach, M., Bach, D., de Zwaan, M., Serim, M., Böhmer, F. (1996). Validierung der deutschen Version der 20-Item Toronto-Alexithymie-Skala bei Normalpersonen und psychiatrischen Patienten. Psychotherapie, Psychosomatik, medizinische Psychologie, 46, 23-8.
3. Bagby, R.M., Parker, J.D., Taylor, G.J. (1994a). The twenty-item Toronto Alexithymia Scale-I. Item selection and cross-validation of the factor structure. Journal of Psychosomatic Research, 38, 23-32.
4. Bagby, R.M., Taylor, G.J., Parker, J.D. (1994b). The twenty-item Toronto Alexithymia Scale-II. Convergent, discriminant, and concurrent validity. Journal of Psychosomatic Research, 38, 33-40.
5. Batra, N.A., Seres-Mailo, J., Hanstock, C., et al. (2008). Proton magnetic resonance spectroscopy measurement of brain glutamate levels in premenstrual dysphoric disorder. Biological Psychiatry, 63, 1178-84.
6. Beauregard, M., Lévesque, J., Bourgouin, P. (2001). Neural correlates of conscious self-regulation of emotion. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 21(18), RC165.
7. Bechara, A., Tranel, D., Damasio, H., Damasio, A.R. (1996). Failure to respond autonomically to anticipated future outcomes following damage to prefrontal cortex. Cerebral Cortex, 6, 215-25.
8. Berthoz, S., Artiges, E., van de Moortele, P.F., et al. (2002). Effect of impaired recognition and expression of emotions on frontocingulate cortices: an fMRI study of men with alexithymia. The American Journal of Psychiatry, 159, 961-7.
9. Bird, G., Silani, G., Brindley, R., White, S., Frith, U., Singer, T. (2010). Empathic brain responses in insula are modulated by levels of alexithymia but not autism. Brain, 133, 1515-25.
10. Borsci, G., Boccardi, M., Rossi, R., et al. (2009). Alexithymia in healthy women: a brain morphology study. Journal of Affective Disorders, 114(1-3), 208-15.
11. Brühl, A.B., Viebke, M.-C., Baumgartner, T., Kaffenberger, T., Herwig, U. (2011). Neural correlates of personality dimensions and affective measures during the anticipation of emotional stimuli. Brain Imaging and Behavior, 5, 86-96.
12. Bush, G., Luu, P., Posner, M.I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Science, 4(6), 215-22.
13. Cameron, O.G. (2001). Interoception: the inside story-a model for psychosomatic processes. Psychosomatic Medicine, 63, 697-710.
14. Canli, T. (2004). Functional brain mapping of extraversion and neuroticism: learning from individual differences in emotion processing. Journal of Personality, 72, 1105-32.
15. Canli, T., Amin, Z. (2002). Neuroimaging of emotion and personality: scientific evidence and ethical considerations. Brain and Cognition, 50, 414-31.
16. Canli, T., Zhao, Z., Desmond, J.E., Kang, E., Gross, J., Gabrieli, J.D. (2001). An fMRI study of personality influences on brain reactivity to emotional stimuli. Behavioral Neuroscience, 115, 33-42.
17. Conrad, R., Wegener, I., Imbierowicz, K., Liedtke, R., Geiser, F. (2009). Alexithymia, temperament and character as predictors of psychopathology in patients with major depression. Psychiatry Research, 165, 137-44.
18. Craig, A.D. (2003). Interoception: the sense of the physiological condition of the body. Current Opinion in Neurobiology, 13, 500-5.
19. Craig, A.D.B. (2009). How do you feel-now? The anterior insula and human awareness. Nature Reviews. Neuroscience, 10, 59-70.
20. Critchley, H.D., Wiens, S., Rotshtein, P., Ohman, A., Dolan, R.J. (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience, 7, 189-95.
21. Deckersbach, T., Miller, K.K., Klibanski, A., et al. (2006). Regional cerebral brain metabolism correlates of neuroticism and extraversion. Depression and Anxiety, 23, 133-38.
22. Dunn, B.D., Stefanovitch, I., Evans, D., Oliver, C., Hawkins, A., Dalgleish, T. (2010). Can you feel the beat? Interoceptive awareness is an interactive function of anxiety-and depression-specific symptom dimensions. Behaviour Research and Therapy, 48, 1133-38.
23. Fairclough, S.H., Goodwin, L. (2007). The effect of psychological stress and relaxation on interoceptive accuracy: implications for symptom perception. Journal of Psychosomatic Research, 62, 289-95.
24. Franz, M., Popp, K., Schaefer, R., et al. (2008). Alexithymia in the German general population. Social Psychiatry and Psychiatric Epidemiology, 43, 54-62.
25. Frewen, P.A., Dozois, D.J.A., Neufeld, R.W.J., Lanius, R.A. (2008). Meta-analysis of alexithymia in posttraumatic stress disorder. Journal of Traumatic Stress, 21, 243-46.
26. Goto, N., Yoshimura, R., Moriya, J., et al. (2010). Critical examination of a correlation between brain gamma-aminobutyric acid (GABA) concentrations and a personality trait of extroversion in healthy volunteers as measured by a 3 Tesla proton magnetic resonance spectroscopy study. Psychiatry Research, 182, 53-7.
27. Grimm, S., Boesiger, P., Beck, J., et al. (2009). Altered negative BOLD responses in the default-mode network during emotion processing in depressed subjects. Neuropsychopharmacology, 34, 932-843.
28. Grimm, S., Ernst, J., Boesiger, P., et al. (2011a). Reduced negative BOLD responses in the default-mode network and increased self-focus in depression. The World Journal of Biological Psychiatry, 12, 627-37.
29. Grimm, S., Schubert, F., Jaedke, M., Gallinat, J., Bajbouj, M. (2011b). Prefrontal cortex glutamate and extraversion. Social Cognitive and Affective Neuroscience, 7, 811-18.
30. Grimm, S., Schubert, F., Jaedke, M., Gallinat, J., Bajbouj, M. (2012b). Prefrontal cortex glutamate and extraversion. Social Cognitive and Affective Neuroscience, 7, 811-8.
31. Grimm, S., Luborzewski, A., Schubert, F., et al. (2012a). Region-specific glutamate changes in patients with unipolar depression. Journal of Psychiatric Research, 46, 1059-65.
32. Gündel, H., López-Sala, A., Ceballos-Baumann, A.O., et al. (2004). Alexithymia correlates with the size of the right anterior cingulate. Psychosomatic Medicine, 66, 132-40.
33. Gussew, A., Rzanny, R., Erdtel, M., et al. (2010). Time-resolved functional 1H MR spectroscopic detection of glutamate concentration changes in the brain during acute heat pain stimulation. NeuroImage, 49, 1895-902.
34. Guttman, H., Laporte, L. (2002). Alexithymia, empathy, and psychological symptoms in a family context. Comprehensive Psychiatry, 43, 448-55.
35. Gutzeit, A., Meier, D., Meier, M.L., et al. (2011). Insula-specific responses induced by dental pain. A proton magnetic resonance spectroscopy study. European Radiology, 21, 807-15.
36. Harris, R.E., Sundgren, P.C., Pang, Y., et al. (2008). Dynamic levels of glutamate within the insula are associated with improvements in multiple pain domains in fibromyalgia. Arthritis and Rheumatism, 58, 903-7.
37. Harrison, B.J., Pujol, J., Ortiz, H., Fornito, A., Pantelis, C., Yücel, M. (2008). Modulation of brain resting-state networks by sad mood induction. PLoS One, 3(3), e1794.
38. Hashimoto, T., Matsubara, T., Lewis, D.A. (2010). Schizophrenia and cortical GABA neurotransmission. Psychiatria et Neurologia Japonica, 112, 439-52.
39. Heinzel, A., Minnerop, M., Schäfer, R., Müller, H.W., Franz, M., Hautzel, H. (2012). Alexithymia in healthy young men: a voxel-based morphometric study. Journal of Affective Disorders, 136(3), 1252-6.
40. Heinzel, A., Schäfer, R., Müller, H.W., et al. (2010). Increased activation of the supragenual anterior cingulate cortex during visual emotional processing in male subjects with high degrees of alexithymia: an event-related fMRI study. Psychotherapy and Psychosomatics, 79, 363-70.
41. Helmes, E., McNeill, P.D., Holden, R.R., Jackson, C. (2008). The construct of alexithymia: associations with defense mechanisms. Journal of Clinical Psychology, 64, 318-31.
42. Horn, D.I., Yu, C., Steiner, J., et al. (2010). Glutamatergic and resting-state functional connectivity correlates of severity in major depression-the role of pregenual anterior cingulate cortex and anterior insula. Frontiers in Systems Neuroscience, 4, 33.
43. Johnson, D.L., Wiebe, J.S., Gold, S.M., et al. (1999). Cerebral blood flow and personality: a positron emission tomography study. The American Journal of Psychiatry, 156, 252-57.
44. Karlsson, H., Näätänen, P., Stenman, H. (2008). Cortical activation in alexithymia as a response to emotional stimuli. The British Journal of Psychiatry, 192, 32-38.
45. Kim, S.H., Hamann, S. (2007). Neural correlates of positive and negative emotion regulation. Journal of Cognitive Neuroscience, 19, 776-98.
46. Kim, H.J., Kim, J.E., Cho, G., et al. (2009). Associations between anterior cingulate cortex glutamate and gamma-aminobutyric acid concentrations and the harm avoidance temperament. Neuroscience Letters, 464, 103-7.
47. Kober, H., Barrett, L.F., Joseph, J., Bliss-Moreau, E., Lindquist, K., Wager, T.D. (2008). Functional grouping and cortical-subcortical interactions in emotion: a meta-analysis of neuroimaging studies. NeuroImage, 42, 998-1031.
48. Kotov, R., Gamez, W., Schmidt, F., Watson, D. (2010). Linking " big" personality traits to anxiety, depressive, and substance use disorders: a meta-analysis. Psychological Bulletin, 136, 768-821.
49. Kumari, V., Ffytche, D.H., Williams, S.C.R., Gray, J.A. (2004). Personality predicts brain responses to cognitive demands. The Journal of Neuroscience, 24, 10636-41.
50. Kupers, R., Danielsen, E.R., Kehlet, H., Christensen, R., Thomsen, C. (2009). Painful tonic heat stimulation induces GABA accumulation in the prefrontal cortex in man. Pain, 142, 89-93.
51. Lane, R.D., Ahern, G.L., Schwartz, G.E., Kaszniak, A.W. (1997). Is alexithymia the emotional equivalent of blindsight? Biological Psychiatry, 42, 834-44.
52. Lane, R.D., Reiman, E.M., Axelrod, B., Yun, L.S., Holmes, A., Schwartz, G.E. (1998). Neural correlates of levels of emotional awareness. Evidence of an interaction between emotion and attention in the anterior cingulate cortex. Journal of Cognitive Neuroscience, 10, 525-35.
53. Larisch, R., Klimke, A., Vosberg, H., Löffler, S., Gaebel, W., Müller-Gärtner, H.W. (1997). In vivo evidence for the involvement of dopamine-D2 receptors in striatum and anterior cingulate gyrus in major depression. NeuroImage, 5, 251-60.
54. Leweke, F., Leichsenring, F., Kruse, J., Hermes, S. (2012). Is alexithymia associated with specific mental disorders? Psychopathology, 45, 22-8.
55. Leweke, F., Stark, R., Milch, W., et al. (2004). Neuronale Aktivitätsmuster auf affektinduktive Reize bei Alexithymie. Psychotherapie, Psychosomatik, medizinische Psychologie, 54, 437-44.
56. Liemburg, E.J., Swart, M., Bruggeman, R., et al. (2012). Altered resting state connectivity of the default mode network in alexithymia. Social Cognitive and Affective Neuroscience, 7, 660-6.
57. Linden, W., Wen, F., Paulhus, D.L. (1995). Measuring alexithymia: reliability, validity, and prevalence. Advances in Personality Assessment, 10, 51-95.
58. Luminet, O. (2010). Commentary on the paper " Is alexithymia a risk factor for major depression, personality disorder, or alcohol use disorders? A prospective populationbased study" . Journal of Psychosomatic Research, 68, 275-77.
59. Mathew, S.J., Manji, H.K., Charney, D.S. (2008). Novel drugs and therapeutic targets for severe mood disorders. Neuropsychopharmacology, 33, 2080-92.
60. Mayberg, H.S. (2003). Modulating dysfunctional limbic-cortical circuits in depression: towards development of brain-based algorithms for diagnosis and optimised treatment. British Medical Bulletin, 65, 193-207.
61. McKiernan, K.A., D'Angelo, B.R., Kaufman, J.N., Binder, J.R. (2006). Interrupting the " stream of consciousness" : an fMRI investigation. NeuroImage, 29, 1185-91.
62. Medford, N., Critchley, H.D. (2010). Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response. Brain Structure & Function, 214, 535-49.
63. Menon, V., Uddin, L.Q. (2010). Saliency, switching, attention and control: a network model of insula function. Brain Structure & Function, 214, 655-67.
64. Mériau, K., Wartenburger, I., Kazzer, P., et al. (2006). A neural network reflecting individual differences in cognitive processing of emotions during perceptual decision making. NeuroImage, 33, 1016-27.
65. Moisset, X., Bouhassira, D., Denis, D., Dominique, G., Benoit, C., Sabaté, J.-M. (2010). Anatomical connections between brain areas activated during rectal distension in healthy volunteers: a visceral pain network. European Journal of Pain, 14, 142-48.
66. Montag, C., Weber, B., Jentgens, E., Elger, C., Reuter, M. (2010). An epistasis effect of functional variants on the BDNF and DRD2 genes modulates gray matter volume of the anterior cingulate cortex in healthy humans. Neuropsychologia, 48(4), 1016-21.
67. Montag, C., Schubert, F., Heinz, A., Gallinat, J. (2008). Prefrontal cortex glutamate correlates with mental perspective-taking. PloS One, 3(12), e3890.
68. Moriguchi, Y., Decety, J., Ohnishi, T., et al. (2007). Empathy and judging other's pain: an fMRI study of alexithymia. Cerebral Cortex, 17, 2223-34.
69. Nieuwenhuys, R., Voogd, J., van Huijzen, C. (2008). The Human Central Nervous System, 4th edn. Heidelberg, Germany: Springer.
70. Northoff, G., Heinzel, A., de Greck, M., Bermpohl, F., Dobrowolny, H., Panksepp, J. (2006). Self-referential processing in our brain-a meta-analysis of imaging studies on the self. NeuroImage, 31, 440-57.
71. Northoff, G., Walter, M., Schulte, R.F., et al. (2007). GABA concentrations in the human anterior cingulate cortex predict negative BOLD responses in fMRI. Nature Neuroscience, 10, 1515-7.
72. Ochsner, K.N., Bunge, S.A., Gross, J.J., Gabrieli, J.D.E. (2002). Rethinking feelings: an FMRI study of the cognitive regulation of emotion. Journal of Cognitive Neuroscience, 14, 1215-29.
73. Oldfield, R.C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9, 97-113.
74. Paulus,M.P., Stein,M.B. (2006). An insular view of anxiety. Biological Psychiatry, 60, 383-87.
75. Phan, K.L., Fitzgerald, D.A., Nathan, P.J., Moore, G.J., Uhde, T.W., Tancer, M.E. (2005). Neural substrates for voluntary suppression of negative affect: a functional magnetic resonance imaging study. Biological Psychiatry, 57, 210-19.
76. Phillips, M.L., Drevets, W.C., Rauch, S.L., Lane, R. (2003). Neurobiology of emotion perception II: Implications for major psychiatric disorders. Biological Psychiatry, 54, 515-28.
77. Picardi, A., Toni, A., Caroppo, E. (2005). Stability of alexithymia and its relationships with the 'big five' factors, temperament, character, and attachment style. Psychotherapy and Psychosomatics, 74, 371-8.
78. Pollatos, O., Gramann, K., Schandry, R. (2007). Neural systems connecting interoceptive awareness and feelings. Human Brain Mapping, 28, 9-18.
79. Pollatos, O., Kirsch, W., Schandry, R. (2005). On the relationship between interoceptive awareness, emotional experience, and brain processes. Cognitive Brain Research, 25, 948-62.
80. Porges, S.W. (1993). Body Perception Questionnaire. (German version). Laboratory of Developmental Assessment, University of Maryland.
81. Reker, M., Ohrmann, P., Rauch, A.V., et al. (2010). Individual differences in alexithymia and brain response to masked emotion faces. Cortex, 46, 658-67.
82. Salminen, J.K., Saarijärvi, S., Aärelä, E., Toikka, T., Kauhanen, J. (1999). Prevalence of alexithymia and its association with sociodemographic variables in the general population of Finland. Journal of Psychosomatic Research, 46, 75-82.
83. Sanacora, G., Zarate, C.A., Krystal, J.H., Manji, H.K. (2008). Targeting the glutamatergic system to develop novel, improved therapeutics for mood disorders. Nature Reviews. Drug Discovery, 7, 426-37.
84. Scheidegger, M., Walter, M., Lehmann, M., et al. (2012). Ketamine decreases resting state functional network connectivity in healthy subjects: implications for antidepressant drug action. PLoS One, 7(9), e44799.
85. Schulte, R.F., Boesiger, P. (2006). ProFit: two-dimensional prior-knowledge fitting of J-resolved spectra. NMR in Biomedicine, 19, 255-63.
86. Silani, G., Bird, G., Brindley, R., Singer, T., Frith, C., Frith, U. (2008). Levels of emotional awareness and autism: an fMRI study. Social Neuroscience, 3, 97-112.
87. Simmons, W.K., Avery, J.A., Barcalow, J.C., Bodurka, J., Drevets, W.C., Bellgowan, P. (2012). Keeping the body in mind: insula functional organization and functional connectivity integrate interoceptive, exteroceptive, and emotional awareness. Human Brain Mapping, ebup ahead of print.
88. Simon, J.J., Walther, S., Fiebach, C.J., et al. (2010). Neural reward processing is modulated by approach-and avoidance-related personality traits. NeuroImage, 49, 1868-74.
89. Smith, S.A., Levante, T.O., Meier, B.H., Ernst, R.R. (1994). Computer simulations in magnetic resonance: an object-oriented programming approach. Journal of Magnetic Resonance, Series A, 106, 75-105.
90. Stein, M.B., Simmons, A.N., Feinstein, J.S., Paulus, M.P. (2007). Increased amygdala and insula activation during emotion processing in anxiety-prone subjects. The American Journal of Psychiatry, 164, 318-27.
91. Swart, M., Kortekaas, R., Aleman, A. (2009). Dealing with feelings: characterization of trait alexithymia on emotion regulation strategies and cognitive-emotional processing. PloS One, 4(6), e5751.
92. Taylor, G.J. (2000). Recent developments in alexithymia theory and research. Canadian Journal of Psychiatry, 45, 134-42.
93. Taylor, K.S., Seminowicz, D.A., Davis, K.D. (2009). Two systems of resting state connectivity between the insula and cingulate cortex. Human Brain Mapping, 30, 2731-45.
94. Terasawa, Y., Fukushima, H., Umeda, S. (2011). How does interoceptive awareness interact with the subjective experience of emotion? An fMRI Study. Human Brain Mapping, 34, 598-612.
95. Urry, H.L., van Reekum, C.M., Johnstone, T., Davidson, R.J. (2009). Individual differences in some (but not all) medial prefrontal regions reflect cognitive demand while regulating unpleasant emotion. NeuroImage, 47, 852-63.
96. Vaidya, J.G., Paradiso, S., Andreasen, N.C., Johnson, D.L., Boles Ponto, L.L., Hichwa, R.D. (2007). Correlation between extraversion and regional cerebral blood flow in response to olfactory stimuli. The American Journal of Psychiatry, 164, 339-41.
97. Wager, T.D., Davidson, M.L., Hughes, B.L., Lindquist, M.A., Ochsner, K.N. (2008). Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron, 59, 1037-50.
98. Walter, M., Henning, A., Grimm, S., et al. (2009). The relationship between aberrant neuronal activation in the pregenual anterior cingulate, altered glutamatergic metabolism, and anhedonia in major depression. Archives of General Psychiatry, 66, 478-86.
99. Walter, N.T., Montag, C., Markett, S.A., Reuter, M. (2011). Interaction effect of functional variants of the BDNF and DRD2/ANKK1 gene is associated with alexithymia in healthy human subjects. Psychosomatic Medicine, 73(1), 23-8.
100. Watson, D., Clark, L.A. (1997). Measurement and mismeasurement of mood: recurrent and emergent issues. Journal of Personality Assessment, 68, 267-96.
101. Werner, N.S., Jung, K., Duschek, S., Schandry, R. (2009). Enhanced cardiac perception is associated with benefits in decision-making. Psychophysiology, 46, 1123-29.
102. Wiebking, C., Bauer, A., de Greck, M., Duncan, N.W., Tempelmann, C., Northoff, G. (2010). Abnormal body perception and neural activity in the insula in depression: an fMRI study of the depressed " material me" . The World Journal of Biological Psychiatry, 11, 538-49.
103. Wiebking, C., de Greck, M., Duncan, N.W., Heinzel, A., Tempelmann, C., Northoff, G. (2011). Are emotions associated with activity during rest or interoception? An exploratory fMRI study in healthy subjects. Neuroscience Letters, 491, 87-92.
104. Wiens, S., Palmer, S.N. (2001). Quadratic trend analysis and heartbeat detection. Biological Psychology, 58, 159-75.
105. Wise, T.N., Mann, L.S., Shay, L. (1992). Alexithymia and the five-factor model of personality. Comprehensive Psychiatry, 33, 147-51.