Altered neural processing of emotional faces in remitted Cushing's disease

Psychoneuroendocrinology

Volumn 59, Issue , 2015, Pages 134-146

  Bas Hoogendam, Janna Marie ^a,b   Andela, Cornelie D ^a,b   van der Werff, Steven J A ^a,b   Pannekoek, J Nienke ^a,c   van Steenbergen, Henk ^a   Meijer, Onno C ^a,b   van Buchem, Mark A ^a,b   Rombouts, Serge A R B ^a,b   van der Mast, Roos C ^b   Biermasz, Nienke R ^a,b   van der Wee, Nic J A ^a,b   Pereira, Alberto M ^a,b  

^a LEIDEN UNIVERSITY   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Amygdala; Cushing's syndrome; Emotional processing; Functional magnetic resonance imaging; Hypercortisolism; Medial prefrontal cortex

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ARTICLE; BRAIN FUNCTION; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; CUSHING DISEASE; DISEASE SEVERITY; EXPLORATORY RESEARCH; FACIAL EXPRESSION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; IMAGE ANALYSIS; MALE; MEDIAL ORBITOFRONTAL CORTEX; MEDIAL PREFRONTAL CORTEX; MORBIDITY; NERVE CELL NETWORK; NEUROANATOMY; PATTERN RECOGNITION; POSTERIOR CINGULATE; PRIORITY JOURNAL; PSYCHOPHYSIOLOGY; REMISSION; TASK PERFORMANCE; VENTROMEDIAL PREFRONTAL CORTEX; ADOLESCENT; AMYGDALA; BRAIN MAPPING; CASE CONTROL STUDY; EMOTION; FACIAL RECOGNITION; MIDDLE AGED; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX; PROCEDURES; PSYCHOLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; AMYGDALA; BRAIN MAPPING; CASE-CONTROL STUDIES; CROSS-SECTIONAL STUDIES; EMOTIONS; FACIAL EXPRESSION; FACIAL RECOGNITION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEURAL PATHWAYS; PITUITARY ACTH HYPERSECRETION; PREFRONTAL CORTEX; YOUNG ADULT;

EID: 84937436519     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2015.05.001     Document Type: Article

References (52)

1. Andela C.D., van der Werff S.J.A., Pannekoek J.N., van den Berg S.M., Meijer O.C., van Buchem M.A., Rombouts S.A.R.B., van der Mast R.C., Romijn J.A., Tiemensma J., Biermasz N.R., van der Wee N.J.A., Pereira A.M. Smaller grey matter volumes in the anterior cingulate cortex and greater cerebellar volumes in patients with long-term remission of Cushing's disease: a case-control study. Eur. J. Endocrinol. 2013, 169:811-819.
2. Andela C.D., Van Haalen F., Ragnarsson O., Papakokkinou E., Johannsson G., Santos A., Webb S., Biermasz N.R., van der Wee N.J.A., Pereira A.M. Mechanisms in endocrinology: Cushing's syndrome causes irreversible effects on the human brain: a systematic review of structural and functional MRI studies. Eur. J. Endocrinol. 2015, (Epub ahead of print).
3. Beck A.T., Steer R.A., Carbin M.G. Psychometric properties of the Beck Depression Inventory: twenty-five years of evaluation. Clin. Psychol. Rev. 1988, 8:77-100.
4. Bluhm R.L., Williamson P.C., Osuch E.A., Frewen P.A., Stevens T.K., Boksman K., Neufeld R.W.J., Théberge J., Lanius R.A. Alterations in default network connectivity in posttraumatic stress disorder related to early-life trauma. J. Psychiatry Neurosci. 2009, 34:187-194.
5. Bourdeau I., Bard C., Noël B., Leclerc I., Cordeau M.-P., Bélair M., Lesage J., Lafontaine L., Lacroix A. Loss of brain volume in endogenous Cushing's syndrome and its reversibility after correction of hypercortisolism. J. Clin. Endocrinol. Metab. 2002, 87:1949-1954.
6. Broadbent D.E., Cooper P.F., FitzGerald P., Parkes K.R. The Cognitive Failures Questionnaire (CFQ) and its correlates. Br. J. Clin. Psychol. 1982, 21:1-16.
7. Chatterjee A., Anderson K.E., Moskowitz C.B., Hauser W.A., Marder K.S. A comparison of self-report and caregiver assessment of depression, apathy, and irritability in Huntington's disease. J. Neuropsychiatry Clin. Neurosci. 2005, 17:378-383.
8. De Kloet E.R., Joëls M., Holsboer F. Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 2005, 6:463-475.
9. Demenescu L.R., Renken R., Kortekaas R., van Tol M.-J., Marsman J.B.C., van Buchem M.A., van der Wee N.J.A., Veltman D.J., den Boer J.A., Aleman A. Neural correlates of perception of emotional facial expressions in out-patients with mild-to-moderate depression and anxiety. A multicenter fMRI study. Psychol. Med. 2011, 41:2253-2264.
10. Etkin A., Wager T.D. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am. J. Psychiatry 2007, 164:1476-1488.
11. Friston K.J., Buechel C., Fink G.R., Morris J., Rolls E., Dolan R.J. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 1997, 6:218-229.
12. Hook J.N., Giordani B., Schteingart D.E., Guire K., Giles J., Ryan K., Gebarski S.S., Langenecker S.A., Starkman M.N. Patterns of cognitive change over time and relationship to age following successful treatment of Cushing's disease. J. Int. Neuropsychol. Soc. 2007, 13:21-29.
13. Jenkinson M., Beckmann C.F., Behrens T.E.J., Woolrich M.W., Smith S.M. FSL. Neuroimage 2012, 62:782-790.
14. Khalsa S., Mayhew S.D., Chechlacz M., Bagary M., Bagshaw A.P. The structural and functional connectivity of the posterior cingulate cortex: comparison between deterministic and probabilistic tractography for the investigation of structure-function relationships. Neuroimage 2013, 102:118-127.
15. Killgore W.D.S., Britton J.C., Schwab Z.J., Price L.M., Weiner M.R., Gold A.L., Rosso I.M., Simon N.M., Pollack M.H., Rauch S.L. Cortico-limbic responses to masked affective faces across PTSD, panic disorder, and specific phobia. Depress. Anxiety 2014, 31:150-159.
16. Kim M.J., Loucks R.A., Palmer A.L., Brown A.C., Solomon K.M., Marchante A.N., Whalen P.J. The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety. Behav. Brain Res. 2011, 223:403-410.
17. Klumpp H., Post D., Angstadt M., Fitzgerald D.A., Phan K.L. Anterior cingulate cortex and insula response during indirect and direct processing of emotional faces in generalized social anxiety disorder. Biol. Mood Anxiety Disord. 2013, 3:7.
18. Langenecker S.A., Weisenbach S.L., Giordani B., Briceño E.M., Guidotti Breting L.M., Schallmo M.-P., Leon H.M., Noll D.C., Zubieta J.-K., Schteingart D.E., Starkman M.N. Impact of chronic hypercortisolemia on affective processing. Neuropharmacology 2012, 62:217-225.
19. Leech R., Sharp D.J. The role of the posterior cingulate cortex in cognition and disease. Brain 2014, 137:12-32.
20. Lundqvist, D., Flykt, A., Öhman, A., 1998. The Karolinska Directed Emotional Faces Department.
21. Maheu F.S., Mazzone L., Merke D.P., Keil M.F., Stratakis C.A., Pine D.S., Ernst M. Altered amygdala and hippocampus function in adolescents with hypercortisolemia: a functional magnetic resonance imaging study of Cushing syndrome. Dev. Psychopathol. 2008, 20:1177-1189.
22. Marks I., Mathews A. Brief standard self-rating for phobic patients. Behav. Res. Ther. 1979, 17:263-267.
23. Montgomery S.A., Asberg M. A new depression scale designed to be sensitive to change. Br. J. Psychiatry 1979, 134:382-389.
24. Newell-Price J., Bertagna X., Grossman A.B., Nieman L.K. Cushing's syndrome. Lancet 2006, 367:1605-1617.
25. Palm M.E., Elliott R., McKie S., Deakin J.F.W., Anderson I.M. Attenuated responses to emotional expressions in women with generalized anxiety disorder. Psychol. Med. 2011, 41:1009-1018.
26. Ragnarsson O., Berglund P., Eder D.N., Johannsson G. Long-term cognitive impairments and attentional deficits in patients with Cushing's disease and cortisol-producing adrenal adenoma in remission. J. Clin. Endocrinol. Metab. 2012, 97:E1640-E1648.
27. Ragnarsson O., Glad C.A.M., Berglund P., Bergthorsdottir R., Eder D.N., Johannsson G. Common genetic variants in the glucocorticoid receptor and the 11β-hydroxysteroid dehydrogenase type 1 genes influence long-term cognitive impairments in patients with Cushing's syndrome in remission. J. Clin. Endocrinol. Metab. 2014, 99:E1803-E1807.
28. Resmini E. Persistent comorbidities in Cushing's syndrome after endocrine cure. Adv. Endocrinol. 2014, 2014:1-15.
29. Resmini E., Santos A., Gómez-Anson B., López-Mourelo O., Pires P., Vives-Gilabert Y., Crespo I., Portella M.J., de Juan-Delago M., Webb S.M. Hippocampal dysfunction in cured Cushing's syndrome patients, detected by (1) H-MR-spectroscopy. Clin. Endocrinol. (Oxf.) 2013, 79:700-707.
30. Resmini E., Santos A., Gómez-Anson B., Vives Y., Pires P., Crespo I., Portella M.J., de Juan-Delago M., Barahona M.-J., Webb S.M. Verbal and visual memory performance and hippocampal volumes, measured by 3-Tesla magnetic resonance imaging, in patients with Cushing's syndrome. J. Clin. Endocrinol. Metab. 2012, 97:663-671.
31. Rush A.J., Gullion C.M., Basco M.R., Jarrett R.B., Trivedi M.H. The Inventory of Depressive Symptomatology (IDS): psychometric properties. Psychol. Med. 1996, 26:477-486.
32. Schoorl M., Putman P., Van Der Werff S., Van Der Does A.J.W. Attentional bias and attentional control in Posttraumatic Stress Disorder. J. Anxiety Disord. 2014, 28:203-210.
33. Shin L., Wright C. A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. Arch. Gen. Psychiatry 2005, 62:273-281.
34. Shin L.M., Liberzon I. The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 2010, 35:169-191.
35. Shin L.M., Wright C.I., Cannistraro P.A., Wedig M.M., McMullin K., Martis B., Macklin M.L., Lasko N.B., Cavanagh S.R., Krangel T.S., Orr S.P., Pitman R.K., Whalen P.J., Rauch S.L. A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. Arch. Gen. Psychiatry 2005, 62:273-281.
36. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E.J., Johansen-Berg H., Bannister P.R., De Luca M., Drobnjak I., Flitney D.E., Niazy R.K., Saunders J., Vickers J., Zhang Y., De Stefano N., Brady J.M., Matthews P.M. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004, 23(Suppl. 1):S208-S219.
37. Sonino N., Boscaro M., Fallo F., Fava G.A. A clinical index for rating severity in Cushing's syndrome. Psychother. Psychosom. 2000, 69:216-220.
38. Starkman M.N., Gebarski S.S., Berent S., Schteingart D.E. Hippocampal formation volume, memory dysfunction, and cortisol levels in patients with Cushing's syndrome. Biol. Psychiatry 1992, 32:756-765.
39. Starkman M.N., Giordani B., Gebarski S.S., Berent S., Schork M.A., Schteingart D.E. Decrease in cortisol reverses human hippocampal atrophy following treatment of Cushing's disease. Biol. Psychiatry 1999, 46:1595-1602.
40. Starkstein S.E. Syndromic validity of apathy in Alzheimer's disease. Am. J. Psychiatry 2001, 158:872-877.
41. Stein M.B., Goldin P.R., Sareen J., Zorrilla L.T.E., Brown G.G. Increased amygdala activation to angry and contemptuous faces in generalized social phobia. Arch. Gen. Psychiatry 2002, 59:1027-1034.
42. Sylvester C.M., Corbetta M., Raichle M.E., Rodebaugh T.L., Schlaggar B.L., Sheline Y.I., Zorumski C.F., Lenze E.J. Functional network dysfunction in anxiety and anxiety disorders. Trends Neurosci. 2012, 35:527-535.
43. Tiemensma J., Biermasz N.R., Middelkoop H.A.M., van der Mast R.C., Romijn J.A., Pereira A.M. Increased prevalence of psychopathology and maladaptive personality traits after long-term cure of Cushing's disease. J. Clin. Endocrinol. Metab. 2010, 95:E129-E141.
44. Tiemensma J., Kokshoorn N.E., Biermasz N.R., Keijser B.-J.S.A., Wassenaar M.J.E., Middelkoop H.A.M., Pereira A.M., Romijn J.A. Subtle cognitive impairments in patients with long-term cure of Cushing's disease. J. Clin. Endocrinol. Metab. 2010, 95:2699-2714.
45. Van Aken M.O., Pereira A.M., Biermasz N.R., van Thiel S.W., Hoftijzer H.C., Smit J.W.A., Roelfsema F., Lamberts S.W.J., Romijn J.A. Quality of life in patients after long-term biochemical cure of Cushing's disease. J. Clin. Endocrinol. Metab. 2005, 90:3279-3286.
46. Van den Heuvel M., Mandl R., Luigjes J., Hulshoff Pol H. Microstructural organization of the cingulum tract and the level of default mode functional connectivity. J. Neurosci. 2008, 28:10844-10851.
47. Van der Werff S.J., Pannekoek J.N., Andela C.D., Meijer O.C., van Buchem M.A., Rombouts S.A., van der Mast R.C., Biermasz N.R., Pereira A.M., van der Wee N.J. Resting-state functional connectivity in patients with long-term remission of Cushing's disease. Neuropsychopharmacology 2015, (Epub ahead of print).
48. Van der Werff S.J.A., Andela C.D., Nienke Pannekoek J., Meijer O.C., van Buchem M.A., Rombouts S.A.R.B., van der Mast R.C., Biermasz N.R., Pereira A.M., van der Wee N.J.A. Widespread reductions of white matter integrity in patients with long-term remission of Cushing's disease. NeuroImage. Clin. 2014, 4:659-667.
49. Van Harmelen A.-L., van Tol M.-J., Dalgleish T., van der Wee N.J.A., Veltman D.J., Aleman A., Spinhoven P., Penninx B.W.J.H., Elzinga B.M. Hypoactive medial prefrontal cortex functioning in adults reporting childhood emotional maltreatment. Soc. Cogn. Affect. Neurosci. 2014, 9(December (12)):2026-2033.
50. Van Harmelen A.-L., van Tol M.-J., Demenescu L.R., van der Wee N.J.A., Veltman D.J., Aleman A., van Buchem M.A., Spinhoven P., Penninx B.W.J.H., Elzinga B.M. Enhanced amygdala reactivity to emotional faces in adults reporting childhood emotional maltreatment. Soc. Cogn. Affect. Neurosci. 2013, 8:362-369.
51. Wolfensberger S.P.A., Veltman D.J., Hoogendijk W.J.G., Boomsma D.I., de Geus E.J.C. Amygdala responses to emotional faces in twins discordant or concordant for the risk for anxiety and depression. Neuroimage 2008, 41:544-552.
52. Worsley K.J. Statistical analysis of activation images. Functional MRI: An Introduction to Methods 2001, Oxford University Press. P. Jezzard, P.M. Matthews, S.M. Smith (Eds.).