Dopaminergic gene polymorphisms affect long-term forgetting in old age: Further support for the Magnification hypothesis

Journal of Cognitive Neuroscience

Volumn 25, Issue 4, 2013, Pages 571-579

  Papenberg, Goran ^a,b   Bäckman, Lars ^b   Nagel, Irene E ^a,d   Nietfeld, Wilfried ^c   Schröder, Julia ^c,e   Bertram, Lars ^c   Heekeren, Hauke R ^a,d   Lindenberger, Ulman ^a   Li, Shu Chen ^a,f  

^a MAX PLANCK INSTITUTE FOR HUMAN DEVELOPMENT   (Germany)

^b KAROLINSKA INSTITUTE   (Sweden)

^c MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^f NONE

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE 2 RECEPTOR; DOPAMINE 3 RECEPTOR;

ADULT; AGED; ARTICLE; EPISODIC MEMORY; EXECUTIVE FUNCTION; FEMALE; GENOTYPE; HUMAN; INTELLIGENCE; MAJOR CLINICAL STUDY; MALE; MEMORY DISORDER; PERCEPTION; PRIORITY JOURNAL; PSYCHOMETRY; SINGLE NUCLEOTIDE POLYMORPHISM; WORKING MEMORY;

EID: 84874568235     PISSN: 0898929X     EISSN: 15308898     Source Type: Journal    
DOI: 10.1162/jocn_a_00359     Document Type: Article

References (84)

1. Adcock, R. A., Thangavel, A., Whitfield-Gabrieli, S., Knutson, B., & Gabrieli, J. D. E. (2006). Reward-motivated learning: Mesolimbic activation precedes memory formation. Neuron, 50, 507-517.
2. Allen, N. C., Bagade, S., McQueen, M. B., Ioannidis, J. P., Kavvoura, F. K., Khoury, M. J., et al. (2008). Systematic meta-analyses and field synopsis of genetic association studies in schizophrenia: The SzGene database. Nature Genetics, 40, 827-834.
3. Bäckman, L., Ginovart, N., Dixon, R. A., Robins Wahlin, T.-B., Wahlin, A., Halldin, C., et al. (2000). Age-related cognitive deficits mediated by changes in the striatal dopamine system. American Journal of Psychiatry, 157, 635-637.
4. Bäckman, L., Lindenberger, U., Li, S.-C., & Nyberg, L. (2010). Linking cognitive aging to alterations in dopamine neurotransmitter functioning: Recent data and future avenues. Neuroscience & Biobehavioral Reviews, 34, 670-677.
5. Bäckman, L., Nyberg, L., Lindenberger, U., Li, S.-C., & Farde, L. (2006). The correlative triad among aging, dopamine, and cognition: Current status and future prospects. Neuroscience & Biobehavioral Reviews, 30, 791-807.
6. Barnett, J. H., Jones, P. B., Robbins, T. W., & Müller, U. (2007). Effects of the catechol-O-methyltransferase Val158Met polymorphism on executive function: A meta-analysis of the Wisconsin Card Sort Test in schizophrenia and healthy controls. Molecular Psychiatry, 12, 502-509.
7. Bethus, I., Tse, D., & Morris, R. G. M. (2010). Dopamine and memory: Modulation of the persistence of memory for novel hippocampal NMDA receptor-dependent paired associates. Journal of Neuroscience, 30, 1610-1618.
8. Bombin, I., Arango, C., Mayoral, M., Castro-Fornieles, J., Gonzalez-Pinto, A., Gonzalez-Gomez, C., et al. (2008). DRD3, but not COMT or DRD2, genotype affects executive functions in healthy and first-episode psychosis adolescents. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 147B, 873-879.
9. Brehmer, Y., Westerberg, H., Bellander, M., Fürth, D., Karlsson, S., & Bäckman, L. (2009). Working memory plasticity modulated by dopamine transporter genotype. Neuroscience Letters, 467, 117-120.
10. Castellano, C., Cestari, V., Cabib, S., & Puglisi-Allegra, S. (1991). Post-training dopamine receptor agonists and antagonists affect memory storage in mice irrespective of their selectivity for D1 or D2 receptors. Behavioral and Neural Biology, 56, 283-291.
11. Cervenka, S., Bäckman, L., Cselényi, Z., Halldin, C., & Farde, L. (2008). Associations between dopamine D2-receptor binding and cognitive performance indicate functional compartmentalization of the human striatum. Neuroimage, 40, 1287-1295.
12. Cestari, V., & Castellano, C. (1997). MK-801 potentiates morphine-induced impairment of memory consolidation in mice: Involvement of dopaminergic mechanisms. Psychopharmacology (Berlin), 133, 1-6.
13. Chen, P. S., Yang, Y. K., Lee, Y.-S., Yeh, T. L., Lee, I. H., Chiu, N. T., et al. (2005). Correlation between different memory systems and striatal dopamine D2/D3 receptor density: A single photon emission computed tomography study. Psychological Medicine, 35, 197-204.
14. Ciliax, B. J., Drash, G. W., Staley, J. K., Haber, S., Mobley, C. J., Miller, G. W., et al. (1999). Immunocytochemical localization of the dopamine transporter in human brain. Journal of Comparative Neurology, 409, 38-56.
15. Cools, R., & D'Esposito, M. (2011). Inverted-u-shaped dopamine actions on human working memory and cognitive control. Biological Psychiatry, 69, e113-e125.
16. de Lima, M. N., Presti-Torres, J., Dornelles, A., Scalco, F. S., Roesler, R., Garcia, V. A., et al. (2011). Modulatory influence of dopamine receptors on consolidation of object recognition memory. Neurobiology of Learning and Memory, 95, 305-310.
17. de Quervain, D. J., Henke, K., Aerni, A., Coluccia, D., Wollmer, M. A., Hock, C., et al. (2003). A functional genetic variation of the 5-HT2a receptor affects human memory. Nature Neuroscience, 6, 1141-1142.
18. de Quervain, D. J., & Papassotiropoulos, A. (2006). Identification of a genetic cluster influencing memory performance and hippocampal activity in humans. Proceedings of the National Academy of Sciences, U.S.A., 103, 4270-4274.
19. Egan, M. F., Kojima, M., Callicott, J. H., Goldberg, T. E., Kolachana, B. S., Bertolino, A., et al. (2003). The BDNF val66met polymorphism affects activity-dependent secretion of BDNF and human memory and hippocampal function. Cell, 112, 257-269.
20. Eppinger, B., Hämmerer, D., & Li, S.-C. (2011). Neuromodulation of reward-based learning and decision making in human aging. Annals of the New York Academy of Sciences, 1235, 1-17.
21. Erixon-Lindroth, N., Farde, L., Wahlin, T. B., Sovago, J., Halldin, C., & Bäckman, L. (2005). The role of the striatal dopamine transporter in cognitive aging. Psychiatry Research, 138, 1-12.
22. Fern, E. F., & Monroe, K. B. (1996). Effect-size estimates: Issues and problems in interpretation. Journal of Consumer Research, 23, 89-105.
23. Frey, U., Huang, Y.-Y., & Kandel, E. R. (1993). Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science, 260, 1661-1664.
24. Fujishiro, H., Umegaki, H., Suzuki, Y., Oohara-Kurotani, S., Yamaguchi, Y., & Iguchi, A. (2005). Dopamine D2 receptor plays a role in memory function: Implications of dopamine-acetylcholine interaction in the ventral hippocampus. Psychopharmacology (Berlin), 182, 253-261.
25. Hamrefors, V., Orho-Melander, M., Krauss, R. M., Hedblad, B., Almgren, P., Berglund, G., et al. (2010). A gene score of nine LDL and HDL regulating genes is associated with fluvastatin-induced cholesterol changes in women. Journal of Lipid Research, 51, 625-634.
26. Heinz, A., Goldman, D., Jones, D. W., Palmour, R., Hommer, D., Gorey, J. G., et al. (2000). Genotype influences in vivo dopamine transporter availability in human striatum. Neuropsychopharmacology, 22, 133-139.
27. Herlitz, A., Nilsson, L. G., & Bäckman, L. (1997). Gender differences in episodic memory. Memory & Cognition, 25, 801-811.
28. Hirvonen, M. M., Laakso, A., Någren, K., Rinne, J. O., Pohjalainen, T., & Hietala, J. (2004). C957T polymorphism of the dopamine D2 receptor (DRD2) gene affects striatal DRD2 availability in vivo. Molecular Psychiatry, 9, 1060-1061.
29. Hirvonen, M., Laakso, A., Någren, K., Rinne, J. O., Pohjalainen, T., & Hietala, J. (2005). Erratum: C957T polymorphism of the dopamine D2 receptor (DRD2) gene affects striatal DRD2 availability in vivo. Molecular Psychiatry, 10, 889.
30. Hirvonen, M. M., Laakso, A., Nagren, K., Rinne, J. O., Pohjalainen, T., & Hietala, J. (2009). C957T polymorphism of dopamine D2 receptor gene affects striatal DRD2 in vivo availability by changing the receptor affinity. Synapse, 63, 907-912.
31. Hirvonen, M. M., Lumme, V., Hirvonen, J., Pesonen, U., Någren, K., Vahlberg, T., et al. (2009). C957T polymorphism of the human dopamine D2 receptor gene predicts extrastriatal dopamine receptor availability in vivo. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 33, 630-636.
32. Huang, Y.-Y., & Kandel, E. R. (1995). D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proceedings of the National Academy of Sciences, U.S.A., 92, 2446-2450.
33. Karlsson, S., Rieckmann, A., Karlsson, P., Farde, L., Nyberg, L., & Bäckman, L. (2011). Relationship of dopamine D1 receptor binding in striatal and extrastriatal regions to cognitive functioning in healthy humans. Neuroimage, 57, 346-351.
34. Kauppi, K., Nilsson, L. G., Adolfsson, R., Eriksson, E., & Nyberg, L. (2011). KIBRA polymorphisma is related to enhanced memory and elevated hippocampal processing. Journal of Neuroscience, 31, 14218-14222.
35. Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (1997). International Affective Picture System (IAPS): Technical manual and affective ratings. Gainesville, FL: NIMH Center for the Study of Emotion and Attention, University of Florida.
36. Lannfelt, L., Sokoloff, P., Martres, M. P., Pilon, C., Giros, B., Jonsson, E., et al. (1992). Amino acid substitution in the dopamine D3 receptor as a useful polymorphism for investigating psychiatric disorders. Psychiatric Genetics, 2, 249-256.
37. Li, S., Cullen, W. K., Anwyl, R., & Rowan, M. J. (2003). Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty. Nature Neuroscience, 6, 526-531.
38. Li, S.-C., Chicherio, C., Nyberg, L., von Oertzen, T., Nagel, I. E., Papenberg, G., et al. (2010). Ebbinghaus revisited: Influences of the BDNF Val66Met polymorphism on backward serial recall are modulated by human aging. Journal of Cognitive Neuroscience, 22, 2164-2173.
39. Li, S.-C., Lindenberger, U., & Bäckman, L. (2010). Dopaminergic modulation of cognition across the life span. Neuroscience & Biobehavioral Reviews, 34, 625-630.
40. Li, S.-C., Lindenberger, U., & Sikström, S. (2001). Aging cognition: From neuromodulation to representation. Trends in Cognitive Sciences, 5, 479-486.
41. Li, S.-C., Naveh-Benjamin, M., & Lindenberger, U. (2005). Aging neuromodulation impairs associative binding: A neurocomputational account. Psychological Science, 16, 445-450.
42. Li, S.-C., Papenberg, G., Nagel, I. E., Preuschhof, C., Schröder, J., Nietfeld, W., et al. (2013). Aging magnifies the effects of dopamine transporter and D2 receptor genes on backward serial memory. Neurobiology of Aging, 34, 358.e1-358.e10.
43. Li, S.-C., & Sikström, S. (2002). Integrative neurocomputational perspectives on cognitive aging, neuromodulation, and representation. Neuroscience & Biobehavioral Reviews, 26, 795-808.
44. Lindenberger, U., Nagel, I. E., Chicherio, C., Li, S.-C., Heekeren, H. R., & Bäckman, L. (2008). Age-related decline in brain resources modulates genetic effects on cognitive functioning. Frontiers in Neuroscience, 2, 234-244.
45. Lisman, J. E., & Grace, A. A. (2005). The hippocampal-VTA loop: Controlling the entry of information into long-term memory. Neuron, 46, 703-713.
46. Lisman, J. E., Grace, A. A., & Düzel, E. (2011). A neoHebbian framework for episodic memory; role of dopaminedependent late LTP. Trend in Neurosciences, 34, 536-547.
47. Livak, K. J. (1999). Allelic discrimination using fluorogenic probes and the 50 nuclease assay. Genetic Analysis, 14, 143-149.
48. Loo, S. K., Specter, E., Smolen, A., Hopfer, C., Teale, P. D., & Reite, M. L. (2003). Functional effects of the DAT1 polymorphism on EEG measures in ADHD. Journal of the American Academy of Child and Adolescents Psychiatry, 42, 986-993.
49. MacDonald, S. W. S., Cervenka, S., Farde, L., Nyberg, L., & Bäckman, L. (2009). Extrastriatal dopamine D2 receptor binding modulates intraindividual variability in episodic recognition and executive functioning. Neuropsychologia, 47, 2299-2304.
50. MacDonald, S. W. S., Stigsdotter-Neely, A., Derwinger, A., & Bäckman, L. (2006). Rate of acquisition, adult age, and basic cognitive abilities predict forgetting: New views on a classic problem. Journal of Experimental Psychology: General, 135, 368-390.
51. Macmillan, N. A., & Creelman, C. D. (2005). Detection theory: A user's guide (2nd ed.). Mahwah, NJ: Lawrence Erlbaum Associates.
52. Magnusson, K. R., Brim, B. L., & Das, S. R. (2010). Selective vulnerabilities of N-methyl-D-aspartate (NMDA) receptors during brain aging. Frontiers in Aging Neuroscience, 2, 11.
53. Manago, F., Castellano, C., Oliverio, A., Mele, A., & De Leonibus, E. (2009). Role of dopamine receptors subtypes, D1-like and D2-like, within the nucleus accumbens subregions, core and shell, on memory consolidation in the one-trial inhibitory avoidance task. Learning & Memory, 16, 46-52.
54. Manahan-Vaughan, D., & Kulla, A. (2003). Regulation of depotentiation and long-term potentiation in the dentate gyrus of freely moving rats by dopamine D2-like receptors. Cerebral Cortex, 13, 123-135.
55. Mattay, V. S., Goldberg, T. E., Fera, F., Hariri, A. R., Tessitore, A., Egan, M. F., et al. (2003). Catechol O-methyltransferase val158-met genotype and individual variation in the brain response to amphetamine. Proceedings of the National Academy of Sciences, U.S.A., 100, 6186-6191.
56. McClearn, G. E., Johansson, B., Berg, S., Pedersen, N. L., Ahern, F., Petrill, S. A., et al. (1997). Substantial genetic influence on cognitive abilities in twins 80 or more years old. Science, 276, 1560-1563.
57. Mele, A., Castellano, C., Felici, A., Cabib, S., Caccia, S., & Oliverio, A. (1996). Dopamine-N-methyl-D-aspartate interactions in the modulation of locomotor activity and memory consolidation in mice. European Journal of Pharmacology, 308, 1-12.
58. Mill, J., Asherson, P., Browes, C., D'Souza, U., & Craig, I. (2002). Expression of the dopamine transporter gene is regulated by the 30 UTR VNTR: Evidence from brain and lymphocytes using quantitative RT-PCR. American Journal of Medical Genetics, 114, 975-979.
59. Mitchell, R. J., Howlett, S., Earl, L., White, N. G., McComb, J., Schanfield, M. S., et al. (2000). Distribution of the 30 VNTR polymorphism in the human dopamine transporter gene in world populations. Human Biology, 72, 295-304.
60. Morcom, A. M., Bullmore, E. T., Huppert, F. A., Lennox, B., Praseedom, A., Linnington, H., et al. (2010). Memory encoding and dopamine in the aging brain: A psychopharmacological neuroimaging study. Cerebral Cortex, 20, 743-757.
61. Mulert, C., Juckel, G., Giegling, I., Pogarell, O., Leicht, G., Karch, S., et al. (2006). A Ser9Gly polymorphism in the dopamine D3 receptor gene (DRD3) and event-related P300 potentials. Neuropsychopharmacology, 31, 1335-1344.
62. Nagel, I. E., Chicherio, C., Li, S.-C., von Oertzen, T., Sander, T., Villringer, A., et al. (2008). Human aging magnifies genetic effects on executive functioning and working memory. Frontier in Human Neuroscience, 2, 1.
63. Nunokawa, A., Watanabe, Y., Kaneko, N., Sugai, T., Yazaki, S., Arinami, T., et al. (2010). The dopamine D3 receptor (DRD3) gene and risk of schizophrenia: Case-control studies and an updated meta-analysis. Schizophrenia Research, 116, 61-67.
64. O'Bryant, S. E., Humphreys, J. D., Smith, G. E., Ivnik, R. J., Graff-Radford, N. R., Petersen, R. C., et al. (2008). Detecting dementia with the Mini-Mental State Examination (MMSE) in highly educated individuals. Archives of Neurology, 65, 963-967.
65. O'Carroll, C. M., Martin, S. J., Sandin, J., Frenguelli, B., & Morris, R. G. M. (2006). Dopaminergic modulation of the persistence of one-trial hippocampus-dependent memory. Learning & Memory, 13, 760-769.
66. Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9, 97-113.
67. Papassotiropoulos, A., Stephan, D. A., Huentelman, M. J., Hoerndli, F. J., Craig, D. W., Pearson, J. V., et al. (2006). Common Kibra alleles are associated with human memory performance. Science, 314, 475-478.
68. Papenberg, G., Bäckman, L., Chicherio, C., Nagel, I. E., Heekeren, H. R., Lindenberger, U., et al. (2011). Higher intraindividual variability is associated with more forgetting and dedifferentiated memory functions in old age. Neuropsychologia, 49, 1879-1888.
69. Payton, A. (2009). The impact of genetic research on our understanding of normal cognitive ageing: 1995 to 2009. Neuropsychology Review, 19, 451-477.
70. Prado-Alcalá, R. A., Ruiloba, M. I., Rubio, L., Solana-Figueroa, R., Medina, C., Salado-Castillo, R., et al. (2003). Regional infusions of serotonin into the striatum and memory consolidation. Synapse, 47, 169-175.
71. Rasch, B., Papassotiropoulos, A., & de Quervain, D. F. (2010). Imaging genetics of cognitive functions: Focus on episodic memory. Neuroimage, 53, 870-877.
72. Rissman, R. A., De Blas, A. L., & Armstrong, D. M. (2007). GABAA receptors in aging and Alzheimer's disease. Neurochemistry, 103, 1285-1292.
73. Rossato, J. I., Bevilaqua, L. R. M., Izquierdo, I., Medina, J. H., & Cammarota, M. (2009). Dopamine controls persistence of long-term memory storage. Science, 325, 1017-1020.
74. Roussos, P., Giakoumaki, S. G., & Bitsios, P. (2008). The dopamine D(3) receptor Ser9Gly polymorphism modulates prepulse inhibition of the acoustic startle reflex. Biological Psychiatry, 64, 235-240.
75. Schott, B. H., Seidenbecher, C. I., Fenker, D. B., Lauer, C. J., Bunzeck, N., Bernstein, H.-G., et al. (2006). The dopaminergic midbrain participates in human episodic memory formation: Evidence from genetic imaging. Journal of Neuroscience, 26, 1407-1417.
76. Schott, B. H., Seidenbecher, C. I., Richter, S., Wüstenberg, T., Debska-Vielhaber, G., Schubert, H., et al. (2011). Genetic variation of the serotonin 2a receptor affects hippocampal novelty processing in humans. PLoS One, 18, e15984.
77. Shohamy, D., & Adcock, R. A. (2010). Dopamine and adaptive memory. Trends in Cognitive Sciences, 14, 464-472.
78. Simon, J. R., Stollstorff, M., Westbay, L. C., Vaidya, C. J., Howard, J. H., Jr., & Howard, D. V. (2011). Dopamine transporter genotype predicts implicit sequence learning. Behavior Brain Research, 216, 452-457.
79. Swant, J., Stramiello, M., & Wagner, J. J. (2008). Postsynaptic dopamine D3 receptor modulation of evoked IPSCs via GABA(A) receptor endocytosis in rat hippocampus. Hippocampus, 18, 492-502.
80. Takahashi, H., Kato, M., Hayashi, M., Okubo, Y., Takano, A., Ito, H., et al. (2007). Memory and frontal lobe functions; possible relations with dopamine D2 receptors in the hippocampus. Neuroimage, 34, 1643-1649.
81. Takahashi, H., Kato, M., Takano, H., Arakawa, R., Okumura, M., Otsuka, T., et al. (2008). Differential contributions of prefrontal and hippocampal dopamine D(1) and D(2) receptors in human cognitive functions. Journal of Neuroscience, 28, 12032-12038.
82. Vandenbergh, D. J., Persico, A. M., Hawkins, A. L., Griffin, C. A., Li, X., Jabs, E. W., et al. (1992). Human dopamine transporter gene (DAT1) maps to chromosome 5p15.3 and displays a VNTR. Genomics, 14, 1104-1106.
83. Vijayraghavan, S., Wang, M., Birnbaum, S. G., Williams, G. V., & Arnsten, A. F. (2007). Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory. Nature Neuroscience, 10, 376-384.
84. Wittmann, B. C., Schott, B. H., Guderian, S., Frey, J. U., Heinze, H.-J., & Düzel, E. (2005). Reward-related fMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation. Neuron, 45, 459-467.