The impact of mineralocorticoid receptor ISO/VAL genotype (rs5522) and stress on reward learning

Genes, Brain and Behavior

Volumn 9, Issue 6, 2010, Pages 658-667

  Bogdan, R ^a   Perlis, R H ^b,c   Fagerness, J ^b   Pizzagalli, D A ^a  

^a HARVARD UNIVERSITY   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Anhedonia; cortisol; depression; endophenotype; gene; glucocorticoid; HPA; mineralocorticoid; reward; stress

Indexed keywords

MINERALOCORTICOID RECEPTOR;

ADULT; ALLELE; ANHEDONIA; ARTICLE; DEPRESSION; FEMALE; GENETIC LINKAGE; GENOTYPE; HUMAN; LEARNING; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; REINFORCEMENT; REWARD; STRESS; TASK PERFORMANCE;

ADOLESCENT; ADULT; FEMALE; GENOTYPE; HUMANS; LEARNING; MALE; MOTIVATION; MUTATION, MISSENSE; RECEPTORS, MINERALOCORTICOID; REINFORCEMENT SCHEDULE; REWARD; STRESS, PSYCHOLOGICAL;

EID: 77955167878     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/j.1601-183X.2010.00600.x     Document Type: Article

References (54)

1. Anisman, H. Matheson, K. (2005) Stress, depression, and anhedonia: caveats concerning animal models. Neurosci Biobehav Rev 29, 525 546.
2. Arai, K., Nakagomi, Y., Iketani, M., Shimura, Y., Amemiya, S., Ohyama, K. Shibasaki, T. (2003) Functional polymorphisms in the mineralocorticoid receptor and amirolide-sensitive sodium channel genes in a patient with sporadic pseudohypoaldosteronism. Hum Genet 112, 91 97.
3. Arvat, E., Maccagno, B., Giordano, R., Pellegrino, M., Broglio, F., Gianotti, L., Maccario, M., Camanni, F. Ghigo, E. (2001) Mineralocorticoid receptor blockade by canrenoate increases both spontaneous and stimulated adrenal function in humans. J Clin Endocrinol Metab 86, 3176 3181.
4. Beck, A.T., Steer, R.A. Brown, G.K. (1996) Beck Depression Inventory Manual, 2nd edn. The Psychological Corporation, San Antonio, TX, USA.
5. Berenbaum, H. Connelly, J. (1993) The effect of stress on hedonic capacity. J Abnorm Psychol 102, 474 481.
6. Berridge, K.C. Kringelbach, M.L. (2008) Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology 199, 457 480.
7. Blascovich, J., Mendes, W.B., Tomaka, J., Salomon, K. Seery, M. (2003) The robust nature of the biopsychosocial model challenge and threat: a reply to Wright and Kirby. Pers Soc Psychol Rev 7, 234 243.
8. Bogdan, R. Pizzagalli, D.A. (2006) Acute stress reduces hedonic capacity: implications for depression. Biol Psychiatry 60, 1147 1154.
9. Bogdan, R. Pizzagalli, D.A. (2009) The heritability of hedonic capacity and perceived stress: a twin study evaluation of candidate depressive phenotypes. Psychol Med 39, 211 218.
10. Bogdan, R., Perlis, R.H., Fagerness, J. Pizzagalli, D.A. (2008) A CRHR1 single nucleotide polymorphism interacts with stress to impact hedonic capacity: implications for depression. Poster presented at the Twenty-second Annual Meeting of the Society for Research in Psychopathology, Pittsburgh, PA, USA.
11. Breier, A., Albus, M., Pickar, D., Zahn, T.P., Wolkowitz, O.M. Paul, S.M. (1987) Controllable and uncontrollable stress in humans: alterations in mood and neuroendocrine and psychophysiological function. Am J Psychiatry 144, 1419 1425.
12. Brown, G.W. Harris, T.O. (1978). Social Origins of Depression. A Study of Psychiatric Disorder in Women. Free Press, New York.
13. Chapman, L.J. Chapman, J.P. (1987) The measurement of handedness. Brain Cogn 6, 175 183.
14. Cohen, S., Kamarck, T. Mermelstein, R. (1983) A global measure of perceived stress. J Health Soc Behav 24, 385 396.
15. DeRijk, R.H., Wüst, S., Meijer, O.C., Zennaro, M.C., Federenko, I.S., Hellhammer, D.H., Giacchetti, G., Vreugdenhil, E., Zitman, F.G. de Kloet, E.R. (2006) A common polymorphism in the mineralocorticoid receptor modulates stress responsiveness. J Clin Endocrinol Metab 91, 5083 5089.
16. DeRijk, R.H., van Leeuwen, N., Klok, M.D. Zitman, F.G. (2008) Corticosteroid receptor-gene variants: modulators of the stress-response and implications for mental health. Eur J Pharmacol 585, 492 501.
17. Dickerson, S.S. Kemeny, M.E. (2004) Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol Bull 130, 355 391.
18. Diekhof, E.K., Falkai, P. Gruber, O. (2008) Functional neuroimaging of reward processing and decision-making: a review of aberrant motivational and affective processing in addiction and mood disorders. Brain Res Rev 59, 164 184.
19. Dillon, D.G., Holmes, A.J., Birk, J.L., Brooks, N., Lyons-Ruth, K. Pizzagalli D.A. (2009) Childhood adversity is associated with left basal ganglia dysfunction during reward anticipation in adulthood. Biol Psychiatry 66, 206 213.
20. First, M.B., Spitzer, R.L., Gibbon, M. Williams, J.B.W. (2002) Structured Clinical Interview for DSM-IV Axis I Disorders. Biometrics Research, New York, State Psychiatric Institute, USA.
21. Forbes, E.E., Brown, S.M., Kimak, M., Ferrell, R.E., Manuck, S.B. Hariri, A.R. (2009) Genetic variation in components of dopamine neurotransmission impacts ventral striatal reactivity associated with impulsivity. Mol Psychiatry 14, 60 70.
22. Freedman, M.L., Reich, D., Penney, K.L., McDonald, G.J., Mignault, A.A., Patterson, N., Gabriel, S.B., Topol, E.J., Smoller, J.W., Pato, C.N., Pato, M.T., Petryshen, T.L., Kolonel, L.N., Lander, E.S., Sklar, P., Henderson, B., Hirschhorn, J.N. Altshuler, D. (2004) Assessing the impact of population stratification on genetic association studies. Nat Genetics 36, 388 393.
23. Hasler, G., Drevets, W.C., Manji, H.K. Charney, D.S. (2004) Discovering endophenotypes for major depression. Neuropsychopharmacology 9, 1765 1781.
24. Hautus, M.J. (1995) Corrections for extreme proportions and their biasing effects of estimated values of d'. Res Methods Instum Comput 27, 46 51.
25. Joëls, M., Karst, H., DeRijk, R. de Kloet, E.R. (2008) The coming out of the brain mineralocorticoid receptor. Trends Neurosci 31, 1 7.
26. Kendler, K.S., Thornton, L.M. Gardner, C.O. (2000) Stressful life events and previous episodes in the etiology of major depression in women: an evaluation of the "kindling" hypothesis. Am J Psychiatry 157, 1243 1251.
27. de Kloet, E.R., DeRijk, R.H. Meijer, O.C. (2007) Therapy insight: is there an imbalanced response of mineralocorticoid and glucocorticoid receptors in depression?. Nat Clin Pract Endocrinol Metab 3, 168 179.
28. Kuningas, M., de Rijk, R.H., Westendorp, R.G., Jolles, J., Slagboom, P.E. van Heemst, D. (2007) Mental performance in old age dependent on cortisol and genetic variance in the mineralocorticoid and glucocorticoid receptors. Neuropsychopharmacology 32, 1295 1301.
29. Macmillan, N.A. Creelman, C.D. (2005) Detection Theory: A User's Guide, 2nd edn. Lawrence Erlbaum, Mahwah, New Jersey, USA.
30. Mehta, M.A., Gore-Langton, E., Golembo, N., Colvert, E., Williams, S.C. Sonuga-Barke, E. (2009). Hyporesponsive reward anticipation in the basal ganglia following severe institutional deprivation early in life. J Cogn Neurosci, in press.
31. Mitra, R., Ferguson, D. Sapolsky, R.M. (2009) Mineralocorticoid receptor overexpression in basolateral amygdala reduces corticosterone secretion and anxiety. Biol Psychiatry 66, 686 690.
32. rd Annual Meeting of the Society for Research in Psychopathology, Minneapolis, MN, USA.
33. Nolen-Hoeksema, S., Larson, J. Grayson, C. (1999) Explaining the gender difference in depressive symptoms. J Pers Soc Psychol 77, 1061 1072.
34. Pace, T.W. Spencer, R.L. (2005) Disruption of mineralocorticoid receptor function increases corticosterone responding to a mild, but not moderate, psychological stressor. Am J Physiol Endocrinol Metab 288, E1082 E1088.
35. Peciña, S., Schulkin, J. Berridge, K.C. (2006) Nucleus accumbens corticotropin-releasing factor increases cue-triggered motivation for sucrose reward: paradoxical positive incentive effects in stress?. BMC Biol 4, 8
36. Pizzagalli, D.A., Jahn, A.L. O'Shea, J.P. (2005) Toward an objective characterization of an anhedonic phenotype: a signal-detection approach. Biol Psychiatry 57, 319 327.
37. Pizzagalli, D.A., Bogdan, R., Ratner, K.G. Jahn, A.L. (2007) Increased perceived stress is associated with blunted hedonic capacity: potential implications for depression research. Beh Res Ther 45, 2742 2753.
38. Pizzagalli, D.A., Iosifescu, D., Hallett, L.A., Ratner, K.G. Fava, M. (2009) Reduced hedonic capacity in major depressive disorder: evidence from a probabilistic reward task. J Psychiatr Res 43, 76 87.
39. Post, R.M. (1992) Transduction of psychosocial stress into the neurobiology of recurrent affective disorder. Am J Psychiatry 149, 999 1010.
40. Pruessner, J.C., Champagne, F., Meaney, M.J. Dagher, A. (2004) Dopamine release in response to a psychological stress in humans and its relationship to early life maternal care: a positron emission tomography study using [11C]raclopride. J Neurosci 24, 2825 2831.
41. Reich, D.E. Goldstein, D.B. (2001) Detecting association in a case-control study while correcting for population stratification. Genet Epidemiol 20, 4 16.
42. Rozeboom, A.M., Akil, H. Seasholtz, A.F. (2007) Mineralocorticoid receptor overexpression in forebrain decreases anxiety-like behavior and alters the stress response in mice. Proc Natl Acad Sci U S A 104, 4688 4693.
43. Santesso, D.L., Dillon, D.G., Birk, J.L., Holmes, A.J., Goetz, E., Bogdan, R. Pizzagalli, D.A. (2008) Individual differences in reinforcement learning: behavioral, electrophysiological, and neuroimaging correlates. Neuroimage 42, 807 816.
44. Sapolsky, R.M. (2003) Stress and plasticity in the limbic system. Neurochem Res 28, 1735 1742.
45. Spielberger, C.D., Gorsuch, R.L. Lushere, R.E. (1970) Manual of the State-Trait Anxiety Inventory. Consulting Psychologists Press, Palo Alto, CA, USA.
46. Sterlemann, V., Ganea, K., Liebl, C., Harbich, D., Alam, S., Holsboer, F., Müller, M.B. Schmidt, M.V. (2008) Long-term behavioral and neuroendocrine alterations following chronic social stress in mice: implications for stress-related disorders. Horm Behav 53, 386 394.
47. Tripp, G. Alsop, B. (1999) Sensitivity to reward frequency in boys with attention deficit hyperactivity disorder. J Clin Child Psychol 28, 366 375.
48. Wanat, M.J., Hopf, F.W., Stuber, G.D., Phillips, P.E. Bonci, A. (2008) Corticotropin-releasing factor increases mouse ventral tegmental area dopamine neuron firing through a protein kinase C-dependent enhancement of Ih. J Physiol 586, 2157 2170.
49. Wang, S.S., Kamphuis, W., Huitinga, I., Zhou, J.N. Swaab, D.F. (2008) Gene expression analysis in the human hypothalamus in depression by laser microdissection and real-time PCR: the presence of multiple receptor imbalances. Mol Psychiatry 13, 786 799.
50. Watson, D., Clark, L.A. Tellegen, A. (1988) Development and validation of brief measures of positive and negative affect: the PANAS scales. J Pers Soc Psychol 54, 1063 1070.
51. Watson, D., Weber, K., Assenheimer, J.S., Clark, L.A., Strauss, M.E. McCormick, R.A. (1995) Testing a tripartite model: I. Evaluating the convergent and discriminant validity of anxiety and depression symptom scales. J Abnorm Psychol 104, 3 14.
52. Wellhoener, P., Born, J., Fehm, H.L. Dodt, C. (2004) Elevated resting and exercise-induced cortisol levels after mineralocorticoid receptor blockade with canrenoate in healthy humans. J Clin Endocrinol Metab 89, 5048 5052.
53. Young, E. Korszun, A. (2010) Sex, trauma, stress hormones and depression. Mol Psychiatry 15, 23 28.
54. Young, E.A., Lopez, J.F., Murphy-Weinberg, V., Watson, S.J. Akil, H. (2003) Mineralocorticoid receptor function in major depression. Arch Gen Psychiatry 60, 24 28. This work was supported by NIH R01 (MH68376) and R21 (MH078979) grants to D.A.P. and a Sackler Scholarship and NIMH NRSA predoctoral training grant (R90; DA023427-01) to R.B. The authors would like to thank Jeffrey Birk, Sara Dainese, Brian Galloway, Elena Goetz, Allison Jahn, Yuliya Nikolova, Miles Nugent, James O'Shea, Kyle Ratner, Sara Rubinstein, Ritchie Siburian, Sunny Dutra and Yan Emily Yuan for study assistance. Dr D.A.P. has received consulting fees from ANT North America Inc. (Advanced Neuro Technology) and AstraZeneca, and honoraria from AstraZeneca. Dr R.H.P. has received speakers or consulting fees/honoraria from AstraZeneca, BMS, Eli Lilly & Co., GSK, Pfizer, Concordant Rater Systems and Proteus Biomedical. Dr R.H.P. is a major stockholder in Concordant Rater Systems, LLC. R.B. and J.F. report no competing interests.