CREB1 genotype modulates adaptive reward-based decisions in humans

Cerebral Cortex

Volumn 26, Issue 7, 2016, Pages 2970-2981

  Wolf, Claudia ^a,b   Mohr, Holger ^a,c   Diekhof, Esther K ^a,d   Vieker, Henning ^a,e   Goya Maldonado, Roberto ^a   Trost, Sarah ^a   Krämer, Bernd ^a   Keil, Maria ^a   Binder, Elisabeth B ^f   Gruber, Oliver ^a  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b NATIONAL INSTITUTE ON AGING   (United States)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^d UNIVERSITY OF HAMBURG   (Germany)

^e UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^f MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

CREB1; Decision making; Fmri; Genetics; Reward

Indexed keywords

ADAPTIVE BEHAVIOR; ADULT; AMYGDALA; ARTICLE; BOLD SIGNAL; BRAIN CORTEX; BRAIN FUNCTION; CINGULATE GYRUS; CONTROLLED STUDY; CREB1 GENE; DECISION MAKING; EMOTION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; GENE; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; INSULA; MEMORY; NORMAL HUMAN; PRECUNEUS; PRIORITY JOURNAL; REWARD; STATISTICAL ANALYSIS; YOUNG ADULT; BLOOD; BRAIN; BRAIN CIRCULATION; BRAIN MAPPING; COPING BEHAVIOR; DIAGNOSTIC IMAGING; EXECUTIVE FUNCTION; FEMALE; GENETICS; GENOTYPING TECHNIQUE; MALE; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; SINGLE NUCLEOTIDE POLYMORPHISM;

CREB1 PROTEIN, HUMAN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; OXYGEN;

ADAPTATION, PSYCHOLOGICAL; ADULT; BRAIN; BRAIN MAPPING; CEREBROVASCULAR CIRCULATION; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DECISION MAKING; EXECUTIVE FUNCTION; FEMALE; GENOTYPE; GENOTYPING TECHNIQUES; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEUROPSYCHOLOGICAL TESTS; OXYGEN; POLYMORPHISM, SINGLE NUCLEOTIDE; REWARD; YOUNG ADULT;

EID: 84981215133     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhv104     Document Type: Article

References (51)

1. Barrot M, Olivier JD, Perrotti LI, DiLeone RJ, Berton O, Eisch AJ, Impey S, Storm DR, Neve RL, Yin JC, et al. 2002. CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc Natl Acad Sci USA. 99:11435-11440.
2. Bermudez-Rattoni F. 2004. Molecular mechanisms of taste-recognition memory. Nat Rev Neurosci. 5:209-217.
3. Bitner RS, Bunnelle WH, Anderson DJ, Briggs CA, Buccafusco J, Curzon P, Decker MW, Frost JM, Gronlien JH, Gubbins E, et al. 2007. Broad-spectrum efficacy across cognitive domains by alpha7 nicotinic acetylcholine receptor agonism correlates with activation of ERK1/2 and CREB phosphorylation pathways. J Neurosci. 27:10578-10587.
4. Brett M, Anton JL, Valbregue R, Poline JB. 8th International Conference on Functional Mapping of the Human Brain, June 2-6, Sendai, Japan. Available on CD-ROM in NeuroImage. 16. 2002. Region of interest analysis using an SPM toolbox [abstract].
5. Chawla S, Bading H. 2001. CREB/CBP and SRE-interacting transcriptional regulators are fast on-off switches: duration of calcium transients specifies the magnitude of transcriptional responses. J Neurochem. 79:849-858.
6. David JT, Cervantes MC, Trosky KA, Salinas JA, Delville Y. 2004. A neural network underlying individual differences in emotion and aggression in male golden hamsters. Neuroscience. 126:567-578.
7. Diekhof EK, Gruber O. 2010. When desire collides with reason: functional interactions between anteroventral prefrontal cortex and nucleus accumbens underlie the human ability to resist impulsive desires. J Neurosci. 30:1488-1493.
8. Diekhof EK, Kaps L, Falkai P, Gruber O. 2012. The role of the human ventral striatum and the medial orbitofrontal cortex in the representation of reward magnitude-an activation likelihood estimation meta-analysis of neuroimaging studies of passive reward expectancy and outcome processing. Neuropsychologia. 50:1252-1266.
9. Diekhof EK, Keil M, Obst KU, Henseler I, Dechent P, Falkai P, Gruber O. 2012. A functional neuroimaging study assessing gender differences in the neural mechanisms underlying the ability to resist impulsive desires. Brain Res. 1473:63-77.
10. Diekhof EK, Nerenberg L, Falkai P, Dechent P, Baudewig J, Gruber O. 2012. Impulsive personality and the ability to resist immediate reward: an fMRI study examining interindividual differences in the neural mechanisms underlying self-control. Hum Brain Mapp. 33:2768-2784.
11. Dinieri JA, Nemeth CL, Parsegian A, Carle T, Gurevich VV, Gurevich E, Neve RL, Nestler EJ, Carlezon WA Jr. 2009. Altered sensitivity to rewarding and aversive drugs in mice with inducible disruption of cAMP response element-binding protein function within the nucleus accumbens. J Neurosci. 29:1855-1859.
12. Dong Y, Green T, Saal D, Marie H, Neve R, Nestler EJ, Malenka RC. 2006. CREB modulates excitability of nucleus accumbens neurons. Nat Neurosci. 9:475-477.
13. Dowlatshahi D, MacQueen GM, Wang JF, Young LT. 1998. Increased temporal cortex CREB concentrations and antidepressant treatment in major depression. Lancet. 352: 1754-1755.
14. Dwivedi Y, Rao JS, Rizavi HS, Kotowski J, Conley RR, Roberts RC, Tamminga CA, Pandey GN. 2003. Abnormal expression and functional characteristics of cyclic adenosine monophosphate response element binding protein in postmortem brain of suicide subjects. Arch Gen Psychiatry. 60:273-282.
15. Green TA, Alibhai IN, Hommel JD, DiLeone RJ, Kumar A, Theobald DE, Neve RL, Nestler EJ. 2006. Induction of inducible cAMP early repressor expression in nucleus accumbens by stress or amphetamine increases behavioral responses to emotional stimuli. J Neurosci. 26:8235-8242.
16. Green TA, Alibhai IN, Roybal CN, Winstanley CA, Theobald DEH, Birnbaum SG, Graham AR, Unterberg S, Graham DL, Vialou V, et al. 2010. Environmental enrichment produces a behavioral phenotype mediated by low cyclic adenosine monophosphate response element binding (CREB) activity in the nucleus accumbens. Biol Psychiatry. 67:28-35.
17. Guo J, Liu Z, Dai H, Zhu Z, Wang H, Yang C, Xiao L, Huang Y, Wang G. 2014. Preliminary investigation of the influence of CREB1 gene polymorphisms on cognitive dysfunction in Chinese patients with major depression. Int J Neurosci. 124:22-29.
18. Hall J, Thomas KL, Everitt BJ. 2001. Fear memory retrieval induces CREB phosphorylation and Fos expression within the amygdala. Eur J Neurosci. 13:1453-1458.
19. Han JH, Kushner SA, Yiu AP, Cole CJ, Matynia A, Brown RA, Neve RL, Guzowski JF, Silva AJ, Josselyn SA. 2007. Neuronal competition and selection during memory formation. Science. 316:457-460.
20. Hyman SE, Malenka RC, Nestler EJ. 2006. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci. 29:565-598.
21. Jarcho JM, Benson BE, Plate RC, Guyer AE, Detloff AM, Pine DS, Leibenluft E, Ernst M. 2012. Developmental effects of decision-making on sensitivity to reward: an fMRI study. Dev Cogn Neurosci. 2:437-447.
22. Juhasz G, Dunham JS, McKie S, Thomas E, Downey D, Chase D, Lloyd-Williams K, Toth ZG, Platt H, Mekli K, et al. 2011. The CREB1-BDNF-NTRK2 pathway in depression: multiple genecognition-environment interactions. Biol Psychiatry. 69:762-771.
23. Kobayashi M, Masaki T, Hori K, Masuo Y, Miyamoto M, Tsubokawa H, Noguchi H, Nomura M, Takamatsu K. 2005. Hippocalcin-deficient mice display a defect in cAMP response element-binding protein activation associated with impaired spatial and associative memory. Neuroscience. 133:471-484.
24. Lazary J, Juhasz G, Anderson IM, Jacob CP, Nguyen TT, Lesch KP, Reif A, Deakin JF, Bagdy G. 2011. Epistatic interaction of CREB1 and KCNJ6 on rumination and negative emotionality. Eur Neuropsychopharmacol. 21:63-70.
25. Lee D, Seo H, JungMW. 2012. Neural basis of reinforcement learning and decision making. Annu Rev Neurosci. 35:287-308.
26. Leotti LA, Iyengar SS, Ochsner KN. 2010. Born to choose: the origins and value of the need for control. Trends Cogn Sci. 14:457-463.
27. Li M, Luo XJ, Rietschel M, Lewis CM, Mattheisen M, Muller-Myhsok B, Jamain S, Leboyer M, Landen M, Thompson PM, et al. 2014. Allelic differences between Europeans and Chinese for CREB1 SNPs and their implications in gene expression regulation, hippocampal structure and function, and bipolar disorder susceptibility. Mol Psychiatry. 19:452-461.
28. Li Y, Shaw CA, Sheffer I, Sule N, Powell SZ, Dawson B, Zaidi SN, Bucasas KL, Lupski JR, Wilhelmsen KC, et al. 2012. Integrated copy number and gene expression analysis detects a CREB1 association with Alzheimer's disease. Transl Psychiatry. 2: e192.
29. Liu X, Hairston J, Schrier M, Fan J. 2011. Common and distinct networks underlying reward valence and processing stages: a meta-analysis of functional neuroimaging studies. Neurosci Biobehav Rev. 35:1219-1236.
30. Mamiya N, Fukushima H, Suzuki A, Matsuyama Z, Homma S, FranklandPW, Kida S. 2009. Brain region-specific gene expression activation required for reconsolidation and extinction of contextual fear memory. J Neurosci. 29:402-413.
31. Muschamp JW, Van't Veer A, Parsegian A, Gallo MS, Chen M, Neve RL, Meloni EG, Carlezon WA Jr. 2011. Activation of CREB in the nucleus accumbens shell produces anhedonia and resistance to extinction of fear in rats. J Neurosci. 31:3095-3103.
32. Narita M, Matsushima Y, Niikura K, Takagi S, Nakahara K, Kurahashi K, Abe M, Saeki M, Asato M, Imai S, et al. 2010. Implication of dopaminergic projection from the ventral tegmental area to the anterior cingulate cortex in mu-opioidinduced place preference. Addict Biol. 15:434-447.
33. Nestler EJ, Carlezon WA Jr. 2006. The mesolimbic dopamine reward circuit in depression. Biol Psychiatry. 59:1151-1159.
34. Nishizawa D, Fukuda K, Kasai S, Hasegawa J, Aoki Y, Nishi A, Saita N, Koukita Y, Nagashima M, Katoh R, et al. 2014. Genome-wide association study identifies a potent locus associated with human opioid sensitivity. Mol Psychiatry. 19:55-62.
35. Perlis RH, Holt DJ, Smoller JW, Blood AJ, Lee S, Kim BW, Lee MJ, Sun M, Makris N, Kennedy DK, et al. 2008. Association of a polymorphism near CREB1 with differential aversion processing in the insula of healthy participants. Arch Gen Psychiatry. 65:882-892.
36. Pozzi L, Sacchetti G, Agnoli L, Mainolfi P, Invernizzi RW, Carli M. 2011. Distinct changes in CREB phosphorylation in frontal cortex and striatum during contingent and non-contingent performance of a visual attention task. Front Behav Neurosci. 5:65.
37. Ramos BP, Birnbaum SG, Lindenmayer I, Newton SS, Duman RS, Arnsten AF. 2003. Dysregulation of protein kinase a signaling in the aged prefrontal cortex: new strategy for treating agerelated cognitive decline. Neuron. 40:835-845.
38. Robison AJ, Nestler EJ. 2011. Transcriptional and epigenetic mechanisms of addiction. Nat Rev Neurosci. 12:623-637.
39. Shi Z, Chen L, Li S, Chen S, Sun X, Sun L, Li Y, Zeng J, He Y, Liu X. 2013. Chronic scopolamine-injection-induced cognitive deficit on reward-directed instrumental learning in rat is associated with CREB signaling activity in the cerebral cortex and dorsal hippocampus. Psychopharmacology (Berl). 230:245-260.
40. ShiflettMW, Mauna JC, Chipman AM, Peet E, Thiels E. 2009. Appetitive Pavlovian conditioned stimuli increase CREB phosphorylation in the nucleus accumbens. Neurobiol Learn Mem. 92:451-454.
41. Sun H, Green TA, Theobald DE, Birnbaum SG, Graham DL, Zeeb FD, Nestler EJ, Winstanley CA. 2010. Yohimbine increases impulsivity through activation of cAMP response element binding in the orbitofrontal cortex. Biol Psychiatry. 67:649-656.
42. Suzuki A, Fukushima H, Mukawa T, Toyoda H, Wu LJ, Zhao MG, Xu H, Shang Y, Endoh K, Iwamoto T, et al. 2011. Upregulation of CREB-mediated transcription enhances both short-and long-term memory. J Neurosci. 31:8786-8802.
43. Trost S, Diekhof EK, Zvonik K, Lewandowski M, Usher J, Keil M, Zilles D, Falkai P, Dechent P, Gruber O. 2014. Disturbed anterior prefrontal control of the mesolimbic reward system and increased impulsivity in bipolar disorder. Neuropsychopharmacology. 39:1914-1923.
44. Viosca J, Lopez de Armentia M, Jancic D, Barco A. 2009. Enhanced CREB-dependent gene expression increases the excitability of neurons in the basal amygdala and primes the consolidation of contextual and cued fear memory. Learn Mem. 16:193-197.
45. Viosca J, Malleret G, Bourtchouladze R, Benito E, Vronskava S, Kandel ER, Barco A. 2009. Chronic enhancement of CREB activity in the hippocampus interferes with the retrieval of spatial information. Learn Mem. 16:198-209.
46. Walters CL, Cleck JN, Kuo YC, Blendy JA. 2005. Mu-opioid receptor and CREB activation are required for nicotine reward. Neuron. 46:933-943.
47. Wei F, Qiu CS, Liauw J, Robinson DA, Ho N, Chatila T, Zhuo M. 2002. Calcium calmodulin-dependent protein kinase IV is required for fear memory. Nat Neurosci. 5:573-579.
48. Wolf C, Linden DE. 2012. Biological pathways to adaptability-interactions between genome, epigenome, nervous system and environment for adaptive behavior. Genes Brain Behav. 11:3-28.
49. Wu LJ, Zhang XH, Fukushima H, Zhang F, Wang H, Toyoda H, Li BM, Kida S, Zhuo M. 2008. Genetic enhancement of trace fear memory and cingulate potentiation in mice overexpressing Ca2+/calmodulin-dependent protein kinase IV. Eur J Neurosci. 27:1923-1932.
50. Yamamoto-Sasaki M, Ozawa H, Saito T, Rosler M, Riederer P. 1999. Impaired phosphorylation of cyclic AMP response element binding protein in the hippocampus of dementia of the Alzheimer type. Brain Res. 824:300-303.
51. Zhou Y, Won J, Karlsson MG, Zhou M, Rogerson T, Balaji J, Neve R, Poirazi P, Silva AJ. 2009. CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala. Nat Neurosci. 12:1438-1443.