Aging affects acquisition and reversal of reward-based associative learning

Learning and Memory

Volumn 15, Issue 4, 2008, Pages 190-197

  Weiler, Julia A ^a   Bellebaum, Christian ^a   Daum, Irene ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGE DISTRIBUTION; AGED; AGING; ARTICLE; BRAIN CORTEX; BRAIN FUNCTION; BRAIN REGION; DOPAMINERGIC SYSTEM; FEMALE; HUMAN; LEARNING; MALE; MENTAL TASK; NORMAL HUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; REWARD; SHORT TERM MEMORY; STATISTICAL SIGNIFICANCE; TASK PERFORMANCE; WORKING MEMORY;

ADULT; AGED; AGING; ASSOCIATION LEARNING; COGNITION; HUMANS; MEMORY, SHORT-TERM; MENTAL RECALL; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; REACTION TIME; REWARD;

EID: 42149153885     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.890408     Document Type: Article

References (61)

1. Aron, A.R., Shohamy, D., Clark, J., Myers, C., Gluck, M.A., and Poldrack, R.A. 2004. Human midbrain sensitivity to cognitive feedback and uncertainty during classification learning. J. Neurophysiol. 92: 1144-1152.
2. Bäckman, L., Nyberg, L., Lindenberger, U., Li, S.C., and Farde, L. 2006. The correlative triad among aging, dopamine, and cognition: Current status and future prospects. Neurosci. Biobehav. Rev. 30: 791-807.
3. Beninger, R.J. and Gerdjikov, T. 2004. The role of signaling molecules in reward-related incentive learning. Neurotox. Res. 6: 91-104.
4. Cabeza, R., Anderson, N.D., Locantore, J.K., and McIntosh, A.R. 2002. Aging gracefully: Compensatory brain activity in high-performing older adults. Neuroimage 17: 1394-1402.
5. Chudasama, Y. and Robbins, T.W. 2003. Dissociable contributions of the orbitofrontal and infralimbic cortex to Pavlovian autoshaping and discrimination reversal learning: Further evidence for the functional heterogeneity of the rodent frontal cortex. J. Neurosci. 23: 8771-8780.
6. Dahl, G. 1972. WIP-Reduzierter Wechsler Intelligenztest: Anwendung, Auswertung Statistische Analysen, Normwerte. Hain, Meisenheim, Germany.
7. Daum, I., Schugens, M.M., Spieker, S., Poser, U., Schönle, P.W., and Birbaumer, N. 1995. Memory and skill acquisition in Parkinson's disease and frontal lobe dysfunction. Cortex 31: 413-432.
8. Delgado, M.R. 2007. Reward-related responses in the human striatum. Ann. N. Y. Acad. Sci. 1104: 70-88.
9. Delgado, M.R., Nystrom, L.E., Fissell, C., Noll, D.C., and Fiez, J.A. 2000. Tracking the hemodynamic responses to reward and punishment in the striatum. J. Neurophysiol. 84: 3072-3077.
10. Delgado, M.R., Locke, H.M., Stenger, V.A., and Fiez, J.A. 2003. Dorsal striatum responses to reward and punishment: Effects of valence and magnitude manipulations. Cogn. Affect. Behav. Neurosci. 3: 27-38.
11. Denburg, N.L., Tranel, D., and Bechara, A. 2005. The ability to decide advantageously declines prematurely in some normal older persons. Neuropsychologia 43: 1099-1106.
12. Elliott, R., Friston, K.J., and Dolan, R.J. 2000. Dissociable neural responses in human reward systems. J. Neurosci. 20: 6159-6165.
13. Elliott, R., Newman, J.L., Longe, O.A., and Deakin, J.F. 2003. Differential response patterns in the striatum and orbitofrontal cortex to financial reward in humans: A parametric functional magnetic resonance imaging study. J. Neurosci. 23: 303-307.
14. Fellows, L.K. and Farah, M.J. 2003. Ventromedial frontal cortex mediates affective shifting in humans: Evidence from a reversal learning paradigm. Brain 126: 1830-1837.
15. Fera, F., Weickert, T.W., Goldberg, T.E., Tessitore, A., Hariri, A., Das, S., Lee, S., Zoltick, B., Meeter, M., Myers, C.E., et al. 2005. Neural mechanisms underlying probabilistic category learning in normal aging. J. Neurosci. 25: 11340-11348.
16. Gunning-Dixon, F.M., Head, D., McQuain, J., Acker, J.D., and Raz, N. 1998. Differential aging of the human striatum: A prospective MR imaging study. AJNR Am. J. Neuroradiol. 19: 1501-1507.
17. Haug, H. and Eggers, R. 1991. Morphometry of the human cortex cerebri and corpus striatum during aging. Neurobiol. Aging 12: 336-338.
18. Hedden, T. and Gabrieli, J.D. 2004. Insights into the ageing mind: A view from cognitive neuroscience. Nat. Rev. Neurosci. 5: 87-96.
19. Herndon, J.G., Moss, M.B., Rosene, D.L., and Killiany, R.J. 1997. Patterns of cognitive decline in aged rhesus monkeys. Behav. Brain Res. 87: 25-34.
20. Hornak, J., O'Doherty, J., Bramham, J., Rolls, E.T., Morris, R.G., Bullock, P.R., and Polkey, C.E. 2004. Reward-related reversal learning after surgical excisions in orbito-frontal or dorsolateral prefrontal cortex in humans. J. Cogn. Neurosci. 16: 463-478.
21. Izquierdo, A., Suda, R.K., and Murray, E.A. 2004. Bilateral orbital prefrontal cortex lesions in rhesus monkeys disrupt choices guided by both reward value and reward contingency. J. Neurosci. 24: 7540-7548.
22. Keri, S., Nagy, O., Kelemen, O., Myers, C.E., and Gluck, M.A. 2005. Dissociation between medial temporal lobe and basal ganglia memory systems in schizophrenia. Schizophr. Res. 77: 321-328.
23. Knowlton, B.J., Mangels, J.A., and Squire, L.R. 1996. A neostriatal habit learning system in humans. Science 273: 1399-1402.
24. Knutson, B., Taylor, J., Kaufman, M., Peterson, R., and Glover, G. 2005. Distributed neural representation of expected value. J. Neurosci. 25: 4806-4812.
25. Kringelbach, M.L. 2005. The human orbitofrontal cortex: Linking reward to hedonic experience. Nat. Rev. Neurosci. 6: 691-702.
26. Lai, Z.C., Moss, M.B., Killiany, R.J., Rosene, D.L., and Herndon, J.G. 1995. Executive system dysfunction in the aged monkey: Spatial and object reversal learning. Neurobiol. Aging 16: 947-954.
27. Lamar, M., Yousem, D.M., and Resnick, S.M. 2004. Age differences in orbitofrontal activation: An fMRI investigation of delayed match and nonmatch to sample. Neuroimage 21: 1368-1376.
28. Larkin, G.R., Gibbs, S.E., Khanna, K., Nielsen, L., Carstensen, L.L., and Knutson, B. 2007. Anticipation of monetary gain but not loss in healthy older adults. Nat. Neurosci. 10: 787-791.
29. MacPherson, S.E., Phillips, L.H., and Della Sala, S. 2002. Age, executive function, and social decision making: A dorsolateral prefrontal theory of cognitive aging. Psychol. Aging 17: 598-609.
30. Marschner, A., Mell, T., Wartenburger, I., Villringer, A., Reischies, F.M., and Heekeren, H.R. 2005. Reward-based decision-making and aging. Brain Res. Bull. 67: 382-390.
31. Mell, T., Heekeren, H.R., Marschner, A., Wartenburger, I., Villringer, A., and Reischies, F.M. 2005. Effect of aging on stimulus-reward association learning. Neuropsychologia 43: 554-563.
32. Murphy Jr., G.M. 1985. The human corpus striatum and dentate nucleus: Volumetric analysis for hemispheric asymmetries, sex differences, and aging changes. Exp. Neurol. 89: 134-145.
33. Myers, C.E., Shohamy, D., Gluck, M.A., Grossman, S., Kluger, A., Ferris, S., Golomb, J., Schnirman, G., and Schwartz, R. 2003. Dissociating hippocampal versus basal ganglia contributions to learning and transfer. J. Cogn. Neurosci. 15: 185-193.
34. O'Doherty, J.P. 2004. Reward representations and reward-related learning in the human brain: Insights from neuroimaging. Curr. Opin. Neurobiol. 14: 769-776.
35. O'Doherty, J.P., Kringelbach, M.L., Rolls, E.T., Hornak, J., and Andrews, C. 2001. Abstract reward and punishment representations in the human orbitofrontal cortex. Nat. Neurosci. 4: 95-102.
36. Poldrack, R.A., Clark, J., Paré-Blagoev, E.J., Shohamy, D., Creso Moyano, J., Myers, C., and Gluck, M.A. 2001. Interactive memory systems in the human brain. Nature 414: 546-550.
37. Rapp, P.R. 1990. Visual discrimination and reversal learning in the aged monkey (Macaca mulatta). Behav. Neurosci. 104: 876-884.
38. Raz, N. and Rodrigue, K.M. 2006. Differential aging of the brain: Patterns, cognitive correlates and modifiers. Neurosci. Biobehav. Rev. 30: 730-748.
39. Raz, N., Gunning, F.M., Head, D., Dupuis, J.H., McQuain, J., Briggs, S.D., Loken, W.J., Thornton, A.E., and Acker, J.D. 1997. Selective aging of the human cerebral cortex observed in vivo: Differential vulnerability of the prefrontal gray matter. Cereb. Cortex 7: 268-282.
40. Raz, N., Rodrigue, K.M., Kennedy, K.M., Head, D., Gunning-Dixon, F., and Acker, J.D. 2003. Differential aging of the human striatum: Longitudinal evidence. AJNR Am. J. Neuroradiol. 24: 1849-1856.
41. Raz, N., Lindenberger, U., Rodrigue, K.M., Kennedy, K.M., Head, D., Williamson, A., Dahle, C., Gerstorf, D., and Acker, J.D. 2005. Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb. Cortex 15: 1676-1689.
42. Roesch, M.R. and Olson, C.R. 2004. Neuronal activity related to reward value and motivation in primate frontal cortex. Science 304: 307-310.
43. Rolls, E.T. 2000. The orbitofrontal cortex and reward. Cereb. Cortex 10: 284-294.
44. Rolls, E.T., Hornak, J., Wade, D., and McGrath, J. 1994. Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. J. Neurol. Neurosurg. Psychiatr. 57: 1518-1524.
45. Salat, D.H., Kaye, J.A., and Janowsky, J.S. 2001. Selective preservation and degeneration within the prefrontal cortex in aging and Alzheimer disease. Arch. Neurol. 58: 1403-1408.
46. Salat, D.H., Kaye, J.A., and Janowsky, J.S. 2002. Greater orbital prefrontal volume selectively predicts worse working memory performance in older adults. Cereb. Cortex 12: 494-505.
47. Schmitt-Eliassen, J., Ferstl, R., Wiesner, C., Deuschl, G., and Witt, K. 2007. Feedback-based versus observational classification learning in healthy aging and Parkinson's disease. Brain Res. 1142: 178-188.
48. Schoenbaum, G., Nugent, S., Saddoris, M.P., and Gallagher, M. 2002. Teaching old rats new tricks: Age-related impairments in olfactory reversal learning. Neurobiol. Aging 23: 555-564.
49. Schott, B.H., Niehaus, L., Wittmann, B.C., Schutze, H., Seidenbecher, C.I., Heinze, H.J., and Duzel, E. 2007. Ageing and early-stage Parkinson's disease affect separable neural mechanisms of mesolimbic reward processing. Brain 130: 2412-2424.
50. Schultz, W. 2000. Multiple reward signals in the brain. Nat. Rev. Neurosci. 1: 199-207.
51. Schultz, W. 2002. Getting formal with dopamine and reward. Neuron 36: 241-263.
52. Shohamy, D., Myers, C.E., Grossman, S., Sage, J., Gluck, M.A., and Poldrack, R.A. 2004. Cortico-striatal contributions to feedback-based learning: Converging data from neuroimaging and neuropsychology. Brain 127: 851-859.
53. Stalnaker, T.A., Franz, T.M., Singh, T., and Schoenbaum, G. 2007. Basolateral amygdala lesions abolish orbitofrontal-dependent reversal impairments. Neuron 54: 51-58.
54. Tapp, P.D., Siwak, C.T., Estrada, J., Head, E., Muggenburg, B.A., Cotman, C.W., and Milgram, N.W. 2003. Size and reversal learning in the beagle dog as a measure of executive function and inhibitory control in aging. Learn. Mem. 10: 64-73.
55. Tisserand, D.J. and Jolles, J. 2003. On the involvement of prefrontal networks in cognitive ageing. Cortex 39: 1107-1128.
56. Tisserand, D.J., Pruessner, J.C., Sanz Arigita, E.J., van Boxtel, M.P., Evans, A.C., Jolles, J., and Uylings, H.B. 2002. Regional frontal cortical volumes decrease differentially in aging: An MRI study to compare volumetric approaches and voxel-based morphometry. Neuroimage 17: 657-669.
57. Voytko, M.L. 1999. Impairments in acquisition and reversals of two-choice discriminations by aged rhesus monkeys. Neurobiol. Aging 20: 617-627.
58. Wallis, J.D. 2007. Orbitofrontal cortex and its contribution to decision-making. Annu. Rev. Neurosci. 30: 31-56.
59. Wallis, J.D. and Miller, E.K. 2003. Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task. Eur. J. Neurosci. 18: 2069-2081.
60. Wechsler, D. 1987. Wechsler memory scale-Revised. Psychological Corporation, London.
61. Zink, C.F., Pagnoni, G., Martin-Skurski, M.E., Chappelow, J.C., and Berns, G.S. 2004. Human striatal responses to monetary reward depend on saliency. Neuron 42: 509-517.