Altered insula activation during pain anticipation in individuals recovered from anorexia nervosa: Evidence of interoceptive dysregulation

International Journal of Eating Disorders

Volumn 46, Issue 1, 2013, Pages 23-33

  Strigo, Irina A ^a,b,c,d   Matthews, Scott C ^a,b,c   Simmons, Alan N ^a,b,c   Oberndorfer, Tyson ^a   Klabunde, Megan ^e   Reinhardt, Lindsay E ^b   Kaye, Walter H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^c VA Center of Excellence for Stress and Mental Health (CESAMH)   (United States)

^d UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^e STANFORD UNIVERSITY   (United States)

Author keywords

alexithymia; anorexia; anticipation; dorsolateral prefrontal; eating disorders; fmri; homeostasis; insula; interoception; pain

Indexed keywords

ADULT; ANOREXIA NERVOSA; ARTICLE; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INSULA; MALNUTRITION; NEUROIMAGING; NOCICEPTION; PAIN ASSESSMENT; PREFRONTAL CORTEX; PRIORITY JOURNAL;

ADOLESCENT; ADULT; ANOREXIA NERVOSA; BRAIN MAPPING; CEREBRAL CORTEX; FEMALE; FUNCTIONAL NEUROIMAGING; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; PAIN; PAIN PERCEPTION; QUESTIONNAIRES;

EID: 84871280566     PISSN: 02763478     EISSN: 1098108X     Source Type: Journal    
DOI: 10.1002/eat.22045     Document Type: Article

References (77)

1. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, 4th ed, text revision (DSM-IV-TR). Washington, DC: American Psychiatric Association, 2000.
2. Klein DA, Walsh BT,. Eating disorders. Int Rev Psychiatry 2003; 15: 205-216.
3. Herzog DB,. Eating disorders. New threats to health. Psychosomatics 1992; 33: 10-15.
4. McKenzie JM, Joyce PR,. Hospitalization for anorexia nervosa. Int J Eat Disord 1992; 11: 235-241.
5. Sullivan PF,. Mortality in anorexia nervosa. Am J Psychiatry 1995; 152: 1073-1074.
6. Keel PK, Dorer DJ, Eddy KT, Franko D, Charatan DL, Herzog DB,. Predictors of mortality in eating disorders. Arch Gen Psychiatry 2003; 60: 179-183.
7. NICE. Eating Disorders-Core Interventions in the Treatment and Management of anorexia Nervosa, Bulimia Nervosa and related Eating Disorders. 2004. Available at:http://www.nice. org.uk/CG009. Accessed on 13 July 2012.
8. Attia E, Schroeder L,. Pharmacologic treatment of anorexia nervosa: Where do we go from here? Int J Eat Disord 2005; 37 (Suppl): S60-S63; discussion S87-S99.
9. Bulik CM, Berkman ND, Brownley KA, Sedway JA, Lohr KN,. Anorexia nervosa treatment: A systematic review of randomized controlled trials. Int J Eat Disord 2007; 40: 310-320.
10. Jimerson DC, Wolfe BE, Brotman AW, Metzger ED,. Medications in the treatment of eating disorders. Psychiatr Clin North Am 1996; 19: 739-754.
11. Van den Eynde F, Treasure J,. Neuroimaging in eating disorders and obesity: Implications for research. Child Adolesc Psychiatr Clin N Am 2009; 18: 95-115.
12. Kaye WH, Fudge JL, Paulus M,. New insights into symptoms and neurocircuit function of anorexia nervosa. Nat Rev Neurosci 2009; 10: 573-584.
13. Pollatos O, Kurz A-L, Albrecht J, Schreder T, Kleemann AM, Schöpf V, et al. Reduced perception of bodily signals in anorexia nervosa. Eat Behav 2008; 9: 381-388.
14. Nunn K, Frampton I, Fuglset TS, Torzsok-Sonnevend M, Lask B,. Anorexia nervosa and the insula. Med Hypotheses 2011; 76: 353-357.
15. Craig AD,. How do you feel? Interoception: The sense of the physiological condition of the body. Nat Rev Neurosci 2002; 3: 655-666.
16. Craig AD,. Interoception and emotion: A neuroanatomical perspective. In, Lewis M, Haviland-Jones JM, Barrett LF, editors. Handbook of Emotions, 3rd ed. New York: Guilford Publications, 2008. pp. 272-288.
17. Mayer EA, Naliboff BD, Craig AD,. Neuroimaging of the brain-gut axis: From basic understanding to treatment of functional GI disorders. Gastroenterology 2006; 131: 1925-1942.
18. Craig AD,. A new view of pain as a homeostatic emotion. Trends Neurosci 2003; 26: 303-307.
19. Heilbrun AB Jr, Flodin A,. Food cues and perceptual distortion of the female body: Implications for food avoidance in the early dynamics of anorexia nervosa. J Clin Psychol 1989; 45: 843-851.
20. Wagner A, Aizenstein H, Mazurkewicz L, Fudge J, Frank GK, Putnam K, et al. Altered insula response to taste stimuli in individuals recovered from restricting-type anorexia nervosa. Neuropsychopharmacology 2008; 33: 513-523.
21. Yoshikatsu N, Toshikiyo K,. Perception of hunger to insulin-induced hypoglycemia in anorexia nervosa. Int J Eat Disord 2001; 29: 354-357.
22. Santel S, Baving L, Krauel K, Munte TF, Rotte M,. Hunger and satiety in anorexia nervosa: fMRI during cognitive processing of food pictures. Brain Res 2006; 1114: 138-148.
23. Lautenbacher S, Pauls AM, Strian F, Pirke KM, Krieg JC,. Pain perception in patients with eating disorders. Psychosom Med 1990; 52: 673-682.
24. de Zwaan M, Biener D, Bach M, Wiesnagrotzki S, Stacher G,. Pain sensitivity, alexithymia, and depression in patients with eating disorders: Are they related? J Psychosom Res 1996; 41: 65-70.
25. Bar K-JMD, Boettger SMD, Wagner GPD, Wilsdorf C, Gerhard UJMD, Boettger MKMD, et al. Changes of pain perception, autonomic function, and endocrine parameters during treatment of anorectic adolescents. J Am Acad Child Adolesc Psychiatry 2006; 45: 1068-1076.
26. Papezova H, Yamamotova A, Uher R,. Elevated pain threshold in eating disorders: Physiological and psychological factors. J Psychiatr Res 2005; 39: 431-438.
27. Raymond NC, Faris PL, Thuras PD, Eiken B, Howard LA, Hofbauer RD, et al. Elevated pain threshold in anorexia nervosa subjects. Biol Psychiatry 1999; 45: 1389-1392.
28. Pauls AM, Lautenbacher S, Strian F, Pirke KM, Krieg JC,. Assessment of somatosensory indicators of polyneuropathy in patients with eating disorders. Eur Arch Psychiatry Clin Neurosci 1991; 241: 8-12.
29. Herbert BM, Herbert C, Pollatos O,. On the relationship between interoceptive awareness and alexithymia: Is interoceptive awareness related to emotional awareness? J Pers 2011; 79: 1149-1175.
30. Henrik K, Markus S, Suzanne F, Harald CT, Joern von W,. Alexithymia and facial emotion recognition in patients with eating disorders. Int J Eat Disord 2006; 39: 245-251.
31. Bagby RM, Taylor GJ, Parker JD,. The twenty-item Toronto Alexithymia Scale-II. Convergent, discriminant, and concurrent validity. J Psychosom Res 1994; 38: 33-40.
32. Bagby RM, Parker JD, Taylor GJ,. The twenty-item Toronto Alexithymia Scale-I. Item selection and cross-validation of the factor structure. J Psychosom Res 1994; 38: 23-32.
33. Tracey I, Mantyh PW,. The cerebral signature for pain perception and its modulation. Neuron 2007; 55: 377-391.
34. Ploner M, Lee MC, Wiech K, Bingel U, Tracey I,. Prestimulus functional connectivity determines pain perception in humans. Proc Natl Acad Sci USA 2010; 107: 355.
35. Strigo IA, Simmons AN, Matthews SC, Craig AD, Paulus MP,. Association of major depressive disorder with altered functional brain response during anticipation and processing of heat pain. Arch Gen Psychiatry 2008; 65: 1275-1284.
36. Simmons A, Strigo I, Matthews SC, Paulus MP, Stein MB,. Anticipation of aversive visual stimuli is associated with increased insula activation in anxiety-prone subjects. Biol Psychiatry 2006; 60: 402-409.
37. Simmons AN, Paulus MP, Thorp SR, Matthews SC, Norman SB, Stein MB,. Functional activation and neural networks in women with posttraumatic stress disorder related to intimate partner violence. Biol Psychiatry 2008; 64: 681-690.
38. Lautenbacher S, Pauls AM, Strian F, Pirke KM, Krieg JC,. Pain sensitivity in anorexia nervosa and bulimia nervosa. Biol Psychiatry 1991; 29: 1073-1078.
39. Wagner A, Aizenstein H, Venkatraman VK, Fudge J, May JC, Mazurkewicz L, et al. Altered reward processing in women recovered from anorexia nervosa. Am J Psychiatry 2007; 164: 1842-1849.
40. Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ,. Neural systems supporting interoceptive awareness. Nat Neurosci 2004; 7: 189-195.
41. Craig AD,. How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci 2009; 10: 59-70.
42. Oberndorfer TA, Kaye WH, Simmons AN, Strigo IA, Matthews SC,. Demand-specific alteration of medial prefrontal cortex response during an inhibition task in recovered anorexic women. Int J Eat Disord 2011; 44: 1-8.
43. Wagner A, Aizenstein H, Venkatraman VK, Bischoff-Grethe A, Fudge J, May JC, et al. Altered striatal response to reward in bulimia nervosa after recovery. Int J Eat Disord 2009;.
44. First MB, Spitzer RL, Gibbon M, Williams JBW,. Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition (SCID-I/P). New York: Biometrics Research, New York State Psychiatric Institute, 2002.
45. Kooiman CG, Spinhoven P, Trijsburg RW,. The assessment of alexithymia: A critical review of the literature and a psychometric study of the Toronto Alexithymia Scale-20. J Psychosom Res 2002; 53: 1083-1090.
46. Lumley MA, Smith JA, Longo DJ,. The relationship of alexithymia to pain severity and impairment among patients with chronic myofascial pain: Comparisons with self-efficacy, catastrophizing, and depression. J Psychosom Res 2002; 53: 823-830.
47. Lumley MA, Radcliffe AM, Macklem DJ, Mosley-Williams A, Leisen JCC, Huffman JL, et al. Alexithymia and pain in three chronic pain samples: Comparing Caucasians and African Americans. Pain Med 2005; 6: 251-261.
48. Spielberger CD,. Manual for the State-Trait Anxiety Inventory (Form Y). Consulting Psychologists Press, 1983.
49. Beck AT, Steer RA, Ball R, Ranieri W,. Comparison of Beck Depression Inventories-IA and -II in psychiatric outpatients. J Pers Assess 1996; 67: 588-597.
50. Seminowicz DA, Davis KD,. A re-examination of pain-cognition interactions: Implications for neuroimaging. Pain 2007; 130: 8-13.
51. Christenfeld N,. Memory for pain and the delayed effects of distraction. Health Psychol 1997; 16: 327-330.
52. Ogawa S, Lee TM, Kay AR, Tank DW,. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA 1990; 87: 9868-9872.
53. Cox RW,. AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Comput Biomed Res 1996; 29: 162-173.
54. Talairach J, Tournoux P,. Co-planar Stereotaxic Atlas of the Human Brain. New York: Thieme, 1988
55. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC,. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): Use of a cluster-size threshold. Magn Reson Med 1995; 33: 636-647.
56. Katz J, Martin AL, Page MG, Calleri V,. Alexithymia and fear of pain independently predict heat pain intensity ratings among undergraduate university students. Pain Res Manag 2009; 14: 299-305.
57. Wagner A, Greer P, Bailer UF, Frank GK, Henry SE, Putnam K, et al. Normal brain tissue volumes after long-term recovery in anorexia and bulimia nervosa. Biol Psychiatry 2006; 59: 291-293.
58. Ploghaus A, Tracey I, Gati JS, Clare S, Menon RS, Matthews PM, et al. Dissociating pain from its anticipation in the human brain. Science 1999; 284: 1979-1981.
59. Shin LM, Liberzon I,. The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 2010; 35: 169-191.
60. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, et al. Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 2007; 27: 2349-2356.
61. Strigo IA, Simmons AN, Matthews SC, Grimes EM, Allard CB, Reinhardt LE, et al. Neural correlates of altered pain response in women with posttraumatic stress disorder from intimate partner violence. Biol Psychiatry 2010; 68: 442-450.
62. Moeller-Bertram T, Keltner J, Strigo IA,. Pain and post traumatic stress disorder-Review of clinical and experimental evidence. Neuropharmacology I 2012; 62: 586-597.
63. Craig AD, Chen K, Bandy D, Reiman EM,. Thermosensory activation of insular cortex. Nat Neurosci 2000; 3: 184-190.
64. Craig AD,. Pain mechanisms: Labeled lines versus convergence in central processing. Annu Rev Neurosci 2003; 26: 1-30.
65. Merwin RM, Zucker NL, Lacy JL, Elliott CA,. Interoceptive awareness in eating disorders: Distinguishing lack of clarity from non-acceptance of internal experience. Cogn Emot 2010; 24: 892.
66. Bird G, Silani G, Brindley R, White S, Frith U, Singer T,. Empathic brain responses in insula are modulated by levels of alexithymia but not autism. Brain 2010; 133: 1515-1525.
67. Silani G, Bird G, Brindley R, Singer T, Frith C, Frith U,. Levels of emotional awareness and autism: An fMRI study. Soc Neurosci 2008; 3: 97-112.
68. Kano M, Hamaguchi T, Itoh M, Yanai K, Fukudo S,. Correlation between alexithymia and hypersensitivity to visceral stimulation in human. Pain 2007; 132: 252-263.
69. Ochsner KN, Gross JJ,. The cognitive control of emotion. Trends Cogn Sci 2005; 9: 242-249.
70. Lorenz J, Minoshima S, Casey KL,. Keeping pain out of mind: The role of the dorsolateral prefrontal cortex in pain modulation. Brain 2003; 126: 1079-1091.
71. Wager TD, Rilling JK, Smith EE, Sokolik A, Casey KL, Davidson RJ, et al. Placebo-induced changes in FMRI in the anticipation and experience of pain. Science 2004; 303: 1162-1167.
72. Zastrow A, Kaiser S, Stippich C, Walther S, Herzog W, Tchanturia K, et al. Neural correlates of impaired cognitive-behavioral flexibility in anorexia nervosa. Am J Psychiatry 2009; 166: 608-616.
73. Uher R, Brammer MJ, Murphy T, Campbell IC, Ng VW, Williams SC, et al. Recovery and chronicity in anorexia nervosa: Brain activity associated with differential outcomes. Biol Psychiatry 2003; 54: 934-942.
74. Srinivasagam NM, Kaye WH, Plotnicov KH, Greeno C, Weltzin TE, Rao R,. Persistent perfectionism, symmetry, and exactness after long-term recovery from anorexia nervosa. Am J Psychiatry 1995; 152: 1630-1634.
75. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van EDC, Raichle ME,. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 2005; 102: 9673-9678.
76. Yamamotova A, Papezova H, Uher R,. Modulation of thermal pain perception by stress and sweet taste in women with bulimia nervosa. Neuro Endocrinol Lett 2009; 30: 237-244.
77. Krieg JR-C, Roscher S, Strian F, Pirke K-M, Lautenbacher S,. Pain sensitivity in recovered anorexics, restrained and unrestrained eaters. J Psychosom Res 1993; 37: 595-601.