Parallel contributions of distinct human memory systems during probabilistic learning

NeuroImage

Volumn 55, Issue 1, 2011, Pages 266-276

  Dickerson, Kathryn C ^a   Li, Jian ^b   Delgado, Mauricio R ^a  

^a RUTGERS UNIVERSITY   (United States)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

Dopamine; FMRI; Hippocampus; Prediction error; Reward; Striatum

Indexed keywords

DOPAMINE; OXYGEN;

ADULT; ARTICLE; ASSOCIATION; BASAL GANGLION; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; DECISION MAKING; DECLARATIVE MEMORY; DOPAMINERGIC SYSTEM; EXPECTATION; FEEDBACK SYSTEM; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; HYPOTHESIS; LEARNING; MALE; MEMORY CONSOLIDATION; MESENCEPHALON; MOTIVATION; NORMAL HUMAN; OXYGEN BLOOD LEVEL; PREDICTION; PRIORITY JOURNAL; PROBABILITY; REINFORCEMENT; REWARD; SIGNAL PROCESSING; TEMPORAL LOBE;

CORPUS STRIATUM; CUES; FEMALE; HIPPOCAMPUS; HUMANS; MALE; MEMORY; NERVE NET; PROBABILITY LEARNING; YOUNG ADULT;

EID: 78951476827     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2010.10.080     Document Type: Article

References (75)

1. Abler B., Walter H., Erk S., Kammerer H., Spitzer M. Prediction error as a linear function of reward probability is coded in human nucleus accumbens. Neuroimage 2006, 31:790-795.
2. Adcock R.A., Thangavel A., Whitfield-Gabrieli S., Knutson B., Gabrieli J.D. Reward-motivated learning: mesolimbic activation precedes memory formation. Neuron 2006, 50:507-517.
3. Amso D., Davidson M.C., Johnson S.P., Glover G., Casey B.J. Contributions of the hippocampus and the striatum to simple association and frequency-based learning. Neuroimage 2005, 27:291-298.
4. Atallah H.E., Rudy J.W., O'Reilly R.C. The role of the dorsal striatum and dorsal hippocampus in probabilistic and deterministic odor discrimination tasks. Learn. Mem. 2008, 15:294-298.
5. Bakker A., Kirwan C.B., Miller M., Stark C.E. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 2008, 319:1640-1642.
6. Barto A.G. Adaptive critics and the basal ganglia. Models of Information Processing in the Basal Ganglia 1995, 215-232. MIT Press, Cambridge. J.C. Houk, J. Davis, D. Beiser (Eds.).
7. Bunzeck N., Duzel E. Absolute coding of stimulus novelty in the human substantia nigra/VTA. Neuron 2006, 51:369-379.
8. Cincotta C.M., Seger C.A. Dissociation between striatal regions while learning to categorize via feedback and via observation. J. Cogn. Neurosci. 2007, 19:249-265.
9. Delgado M.R. Reward-related responses in the human striatum. Ann. NY Acad. Sci. 2007, 1104:70-88.
10. Delgado M.R., Miller M.M., Inati S., Phelps E.A. An fMRI study of reward-related probability learning. Neuroimage 2005, 24:862-873.
11. Eldridge L.L., Engel S.A., Zeineh M.M., Bookheimer S.Y., Knowlton B.J. A dissociation of encoding and retrieval processes in the human hippocampus. J. Neurosci. 2005, 25:3280-3286.
12. Foerde K., Knowlton B.J., Poldrack R.A. Modulation of competing memory systems by distraction. Proc. Natl Acad. Sci. USA 2006, 103:11778-11783.
13. Forman S.D., Cohen J.D., Fitzgerald M., Eddy W.F., Mintun M.A., Noll D.C. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn. Reson. Med. 1995, 33:636-647.
14. Geweke J. Measurement of linear dependence and feedback between multiple time series. J. Am. Stat. Assoc. 1982, 77:304-313.
15. Gluck M.A., Shohamy D., Myers C. How do people solve the "weather prediction" task?: individual variability in strategies for probabilistic category learning. Learn. Mem. 2002, 9:408-418.
16. Goebel R., Roebroeck A., Kim D.S., Formisano E. Investigating directed cortical interactions in time-resolved fMRI data using vector autoregressive modeling and Granger causality mapping. Magn. Reson. Imaging 2003, 21:1251-1261.
17. Goebel R., Esposito F., Formisano E. Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: from single-subject to cortically aligned group general linear model analysis and self-organizing group independent component analysis. Hum. Brain Mapp. 2006, 27:392-401.
18. Greicius M.D., Krasnow B., Boyett-Anderson J.M., Eliez S., Schatzberg A.F., Reiss A.L., Menon V. Regional analysis of hippocampal activation during memory encoding and retrieval: fMRI study. Hippocampus 2003, 13:164-174.
19. Haber S.N. The primate basal ganglia: parallel and integrative networks. J. Chem. Neuroanat. 2003, 26:317-330.
20. Haruno M., Kawato M. Different neural correlates of reward expectation and reward expectation error in the putamen and caudate nucleus during stimulus-action-reward association learning. J. Neurophysiol. 2006, 95:948-959.
21. Heimer L., Alheid G.F., de Olmos J.S., Groenewegen H.J., Haber S.N., Harlan R.E., Zahm D.S. The accumbens: beyond the core-shell dichotomy. J. Neuropsychiatry Clin. Neurosci. 1997, 9:354-381.
22. Holm S. A simple sequentially rejective multiple test procedure. Scand. J. Stat. 1979, 6:65-70.
23. Huang Y.Y., Kandel E.R. D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus. Proc. Natl Acad. Sci. USA 1995, 92:2446-2450.
24. Jung Y., Hong S., Haber S.N. Organization of direct hippocampal projections to the different regions of the ventral striatum in primate. Korean J. Anat. 2003, 36:67-76.
25. Kelley A.E., Domesick V.B. The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: an anterograde- and retrograde-horseradish peroxidase study. Neuroscience 1982, 7:2321-2335.
26. Knowlton B.J., Squire L.R., Gluck M.A. Probabilistic classification learning in amnesia. Learn. Mem. 1994, 1:106-120.
27. Law J.R., Flanery M.A., Wirth S., Yanike M., Smith A.C., Frank L.M., Suzuki W.A., Brown E.N., Stark C.E. Functional magnetic resonance imaging activity during the gradual acquisition and expression of paired-associate memory. J. Neurosci. 2005, 25:5720-5729.
28. Lee A.S., Duman R.S., Pittenger C. A double dissociation revealing bidirectional competition between striatum and hippocampus during learning. Proc. Natl Acad. Sci. USA 2008, 105:17163-17168.
29. Lisman J.E., Grace A.A. The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 2005, 46:703-713.
30. Lynd-Balta E., Haber S.N. The organization of midbrain projections to the ventral striatum in the primate. Neuroscience 1994, 59:609-623.
31. Mattfeld A.T., Stark C.E. Striatal and medial temporal lobe functional interactions during visuomotor associative learning. Cereb. Cortex 2010.
32. McClure S.M., Berns G.S., Montague P.R. Temporal prediction errors in a passive learning task activate human striatum. Neuron 2003, 38:339-346.
33. Meeter M., Myers C.E., Shohamy D., Hopkins R.O., Gluck M.A. Strategies in probabilistic categorization: results from a new way of analyzing performance. Learn. Mem. 2006, 13:230-239.
34. Meeter M., Radics G., Myers C.E., Gluck M.A., Hopkins R.O. Probabilistic categorization: how do normal participants and amnesic patients do it?. Neurosci. Biobehav. Rev. 2008, 32:237-248.
35. Middleton F.A., Strick P.L. Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res. Brain Res. Rev. 2000, 31:236-250.
36. Middleton F.A., Strick P.L. Basal ganglia output and cognition: evidence from anatomical, behavioral, and clinical studies. Brain Cogn. 2000, 42:183-200.
37. Newell B.R., Lagnado D.A., Shanks D.R. Challenging the role of implicit processes in probabilistic category learning. Psychon. Bull. Rev. 2007, 14:505-511.
38. O'Doherty J.P., Dayan P., Friston K., Critchley H., Dolan R.J. Temporal difference models and reward-related learning in the human brain. Neuron 2003, 38:329-337.
39. O'Doherty J., Dayan P., Schultz J., Deichmann R., Friston K., Dolan R.J. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 2004, 304:452-454.
40. Packard M.G., Knowlton B.J. Learning and memory functions of the Basal Ganglia. Annu. Rev. Neurosci. 2002, 25:563-593.
41. Packard M.G., McGaugh J.L. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol. Learn. Mem. 1996, 65:65-72.
42. Packard M.G., White N.M. Dissociation of hippocampus and caudate nucleus memory systems by posttraining intracerebral injection of dopamine agonists. Behav. Neurosci. 1991, 105:295-306.
43. Pagnoni G., Zink C.F., Montague P.R., Berns G.S. Activity in human ventral striatum locked to errors of reward prediction. Nat. Neurosci. 2002, 5:97-98.
44. Pennartz C.M., Berke J.D., Graybiel A.M., Ito R., Lansink C.S., van der Meer M., Redish A.D., Smith K.S., Voorn P. Corticostriatal interactions during learning, memory processing, and decision making. J. Neurosci. 2009, 29:12831-12838.
45. Ploghaus A., Tracey I., Clare S., Gati J.S., Rawlins J.N., Matthews P.M. Learning about pain: the neural substrate of the prediction error for aversive events. Proc. Natl Acad. Sci. USA 2000, 97:9281-9286.
46. Poldrack R.A., Packard M.G. Competition among multiple memory systems: converging evidence from animal and human brain studies. Neuropsychologia 2003, 41:245-251.
47. Poldrack R.A., Clark J., Pare-Blagoev E.J., Shohamy D., Creso Moyano J., Myers C., Gluck M.A. Interactive memory systems in the human brain. Nature 2001, 414:546-550.
48. Poldrack R.A., Fletcher P.C., Henson R.N., Worsley K.J., Brett M., Nichols T.E. Guidelines for reporting an fMRI study. Neuroimage 2008, 40:409-414.
49. Rescorla R.A., Wagner A.R. A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. Classical Conditioning II: Current Research and Theory 1972, 64-99. Appleton Century Crofts, New York. A.H. Black, W.F. Prokasy (Eds.).
50. Rice W.R. Analyzing tables of statistical tests. Evolution 1989, 43:223-225.
51. Roebroeck A., Formisano E., Goebel R. Mapping directed influence over the brain using Granger causality and fMRI. Neuroimage 2005, 25:230-242.
52. Scatton B., Simon H., Le Moal M., Bischoff S. Origin of dopaminergic innervation of the rat hippocampal formation. Neurosci. Lett. 1980, 18:125-131.
53. Schultz W. Getting formal with dopamine and reward. Neuron 2002, 36:241-263.
54. Schultz W., Dayan P., Montague P.R. A neural substrate of prediction and reward. Science 1997, 275:1593-1599.
55. Seger C.A. How do the basal ganglia contribute to categorization? Their roles in generalization, response selection, and learning via feedback. Neurosci. Biobehav. Rev. 2008, 32:265-278.
56. Seger C.A., Cincotta C.M. The roles of the caudate nucleus in human classification learning. J. Neurosci. 2005, 25:2941-2951.
57. Seger C.A., Cincotta C.M. Dynamics of frontal, striatal, and hippocampal systems during rule learning. Cereb. Cortex 2006, 16:1546-1555.
58. Sherry D.F., Schacter D.L. The evolution of multiple memory systems. Psychol. Rev. 1987, 94:439-454.
59. Shohamy D., Adcock R.A. Dopamine and adaptive memory. Trends Cogn. Sci. 2010, 14.
60. Shohamy D., Wagner A.D. Integrating memories in the human brain: hippocampal-midbrain encoding of overlapping events. Neuron 2008, 60:378-389.
61. Shohamy D., Myers C.E., Grossman S., Sage J., Gluck M.A., Poldrack R.A. Cortico-striatal contributions to feedback-based learning: converging data from neuroimaging and neuropsychology. Brain 2004, 127:851-859.
62. Shohamy D., Myers C.E., Kalanithi J., Gluck M.A. Basal ganglia and dopamine contributions to probabilistic category learning. Neurosci. Biobehav. Rev. 2008, 32:219-236.
63. Squire L.R. Declarative and nondeclarative memory: multiple brain systems supporting learning and memory. J. Cogn. Neurosci. 1992, 4:232-243.
64. Squire L.R., Zola S.M. Structure and function of declarative and nondeclarative memory systems. Proc. Natl Acad. Sci. USA 1996, 93:13515-13522.
65. Swanson L.W. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res. Bull. 1982, 9:321-353.
66. Talairach J., Tournoux P. Co-Planar Stereotaxic Atlas of the Human Brain 1988, Thieme Medical Publishers, Inc., New York.
67. Toni I., Ramnani N., Josephs O., Ashburner J., Passingham R.E. Learning arbitrary visuomotor associations: temporal dynamic of brain activity. Neuroimage 2001, 14:1048-1057.
68. Tricomi E., Fiez J.A. Feedback signals in the caudate reflect goal achievement on a declarative memory task. Neuroimage 2008, 41:1154-1167.
69. Tricomi E.M., Delgado M.R., Fiez J.A. Modulation of caudate activity by action contingency. Neuron 2004, 41:281-292.
70. Vanni-Mercier G., Mauguiere F., Isnard J., Dreher J.C. The hippocampus codes the uncertainty of cue-outcome associations: an intracranial electrophysiological study in humans. J. Neurosci. 2009, 29:5287-5294.
71. Voermans N.C., Petersson K.M., Daudey L., Weber B., Van Spaendonck K.P., Kremer H.P., Fernandez G. Interaction between the human hippocampus and the caudate nucleus during route recognition. Neuron 2004, 43:427-435.
72. Watkins C.J.C.H. Learning from delayed rewards 1989, University of Cambridge, England.
73. White N.M., McDonald R.J. Multiple parallel memory systems in the brain of the rat. Neurobiol. Learn. Mem. 2002, 77:125-184.
74. Wittmann B.C., Schott B.H., Guderian S., Frey J.U., Heinze H.J., Duzel E. Reward-related FMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation. Neuron 2005, 45:459-467.
75. Wittmann B.C., Bunzeck N., Dolan R.J., Duzel E. Anticipation of novelty recruits reward system and hippocampus while promoting recollection. Neuroimage 2007, 38:194-202.