Reward-related fMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation

Neuron

Volumn 45, Issue 3, 2005, Pages 459-467

  Wittmann, Bianca C ^a   Schott, Björn H ^a   Guderian, Sebastian ^a   Frey, Julietta U ^b   Heinze, Hans Jochen ^a   Düzel, Emrah ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; DOPAMINERGIC SYSTEM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; LONG TERM MEMORY; MALE; MEMORY CONSOLIDATION; MESENCEPHALON; NORMAL HUMAN; PRIORITY JOURNAL; REWARD; SUBSTANTIA NIGRA; VISUAL STIMULATION;

ADULT; BRAIN MAPPING; DOPAMINE; EMOTIONS; FEMALE; HIPPOCAMPUS; HUMANS; LONG-TERM POTENTIATION; MAGNETIC RESONANCE IMAGING; MALE; MEMORY; MESENCEPHALON; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; PHOTIC STIMULATION; REWARD; SUBSTANTIA NIGRA; VENTRAL TEGMENTAL AREA;

EID: 13244279536     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2005.01.010     Document Type: Article

References (56)

1. M.E. Bach, M. Barad, H. Son, M. Zhuo, Y.F. Lu, R. Shih, I. Mansuy, R.D. Hawkins, and E.R. Kandel Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway Proc. Natl. Acad. Sci. USA 96 1999 5280 5285
2. L. Bäckman, N. Ginovart, R.A. Dixon, T.B. Wahlin, A. Wahlin, C. Halldin, and L. Farde Age-related cognitive deficits mediated by changes in the striatal dopamine system Am. J. Psychiatry 157 2000 635 637
3. R. Bernabeu, L. Bevilaqua, P. Ardenghi, E. Bromberg, P. Schmitz, M. Bianchin, I. Izquierdo, and J.H. Medina Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats Proc. Natl. Acad. Sci. USA 94 1997 7041 7046
4. J.B. Brewer, Z. Zhao, J.E. Desmond, G.H. Glover, and J.D. Gabrieli Making memories: brain activity that predicts how well visual experience will be remembered Science 281 1998 1185 1187
5. T. Canli, Z. Zhao, J. Brewer, J.D. Gabrieli, and L. Cahill Event-related activation in the human amygdala associates with later memory for individual emotional experience J. Neurosci. 20 2000 RC99
6. L. Davachi, and A.D. Wagner Hippocampal contributions to episodic encoding: insights from relational and item-based learning J. Neurophysiol. 88 2002 982 990
7. E. Düzel, A.P. Yonelinas, G.R. Mangun, H.J. Heinze, and E. Tulving Event-related brain potential correlates of two states of conscious awareness in memory Proc. Natl. Acad. Sci. USA 94 1997 5973 5978
8. E. Düzel, F. Vargha-Khadem, H.J. Heinze, and M. Mishkin Brain activity evidence for recognition without recollection after early hippocampal damage Proc. Natl. Acad. Sci. USA 98 2001 8101 8106
9. T. Eckert, M. Sailer, J. Kaufmann, C. Schrader, T. Peschel, N. Bodammer, H.J. Heinze, and M.A. Schoenfeld Differentiation of idiopathic Parkinson's disease, multiple system atrophy, progressive supranuclear palsy, and healthy controls using magnetization transfer imaging Neuroimage 21 2004 229 235
10. H. Eichenbaum The hippocampus and declarative memory: cognitive mechanisms and neural codes Behav. Brain Res. 127 2001 199 207
11. U. Frey, and R.G. Morris Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP Neuropharmacology 37 1998 545 552
12. U. Frey, H. Schroeder, and H. Matthies Dopaminergic antagonists prevent long-term maintenance of posttetanic LTP in the CA1 region of rat hippocampal slices Brain Res. 522 1990 69 75
13. U. Frey, H. Matthies, and K.G. Reymann The effect of dopaminergic D1 receptor blockade during tetanization on the expression of long-term potentiation in the rat CA1 region in vitro Neurosci. Lett. 129 1991 111 114
14. K.J. Friston, O. Josephs, G. Rees, and R. Turner Nonlinear event-related responses in fMRI Magn. Reson. Med. 39 1998 41 52
15. A. Gasbarri, A. Sulli, R. Innocenzi, C. Pacitti, and J.D. Brioni Spatial memory impairment induced by lesion of the mesohippocampal dopaminergic system in the rat Neuroscience 74 1996 1037 1044
16. A.I. Hersi, W. Rowe, P. Gaudreau, and R. Quirion Dopamine D1 receptor ligands modulate cognitive performance and hippocampal acetylcholine release in memory-impaired aged rats Neuroscience 69 1995 1067 1074
17. C. Hölscher, W. Jacob, and H.A. Mallot Reward modulates neuronal activity in the hippocampus of the rat Behav. Brain Res. 142 2003 181 191
18. G. Honey, and E. Bullmore Human pharmacological MRI Trends Pharmacol. Sci. 25 2004 366 374
19. Y.Y. Huang, and E.R. Kandel D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of the hippocampus Proc. Natl. Acad. Sci. USA 92 1995 2446 2450
20. T.M. Jay Dopamine: a potential substrate for synaptic plasticity and memory mechanisms Prog. Neurobiol. 69 2003 375 390
21. N. Kemppainen, M. Laine, M.P. Laakso, V. Kaasinen, K. Nagren, T. Vahlberg, T. Kurki, and J.O. Rinne Hippocampal dopamine D2 receptors correlate with memory functions in Alzheimer's disease Eur. J. Neurosci. 18 2003 149 154
22. P. Kirsch, A. Schienle, R. Stark, G. Sammer, C. Blecker, B. Walter, U. Ott, J. Burkart, and D. Vaitl Anticipation of reward in a nonaversive differential conditioning paradigm and the brain reward system: an event-related fMRI study Neuroimage 20 2003 1086 1095
23. S. Knecht, C. Breitenstein, S. Bushuven, S. Wailke, S. Kamping, A. Floel, P. Zwitserlood, and E.B. Ringelstein Levodopa: faster and better word learning in normal humans Ann. Neurol. 56 2004 20 26
24. B. Knutson, A. Westdorp, E. Kaiser, and D. Hommer FMRI visualization of brain activity during a monetary incentive delay task Neuroimage 12 2000 20 27
25. B. Knutson, C.M. Adams, G.W. Fong, and D. Hommer Anticipation of increasing monetary reward selectively recruits nucleus accumbens J. Neurosci. 21 2001 RC159
26. B. Knutson, G.W. Fong, C.M. Adams, J.L. Varner, and D. Hommer Dissociation of reward anticipation and outcome with event-related fMRI Neuroreport 12 2001 3683 3687
27. B. Knutson, G.W. Fong, S.M. Bennett, C.M. Adams, and D. Hommer A region of mesial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI Neuroimage 18 2003 263 272
28. S. Li, W.K. Cullen, R. Anwyl, and M.J. Rowan Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty Nat. Neurosci. 6 2003 526 531
29. J.E. Lisman, and N.A. Otmakhova Storage, recall, and novelty detection of sequences by the hippocampus: elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine Hippocampus 11 2001 551 568
30. S.M. McClure, G.S. Berns, and P.R. Montague Temporal prediction errors in a passive learning task activate human striatum Neuron 38 2003 339 346
31. R.G. Morris, and U. Frey Hippocampal synaptic plasticity: role in spatial learning or the automatic recording of attended experience? Philos. Trans. R. Soc. Lond. B Biol. Sci. 352 1997 1489 1503
32. R.G. Morris, E.I. Moser, G. Riedel, S.J. Martin, J. Sandin, M. Day, and C. O'Carroll Elements of a neurobiological theory of the hippocampus: the role of activity-dependent synaptic plasticity in memory Philos. Trans. R. Soc. Lond. B Biol. Sci. 358 2003 773 786
33. J.P. O'Doherty, R. Deichmann, H.D. Critchley, and R.J. Dolan Neural responses during anticipation of a primary taste reward Neuron 33 2002 815 826
34. K.A. Paller, and A.D. Wagner Observing the transformation of experience into memory Trends Cogn. Sci. 6 2002 93 102
35. S. Pappata, S. Dehaene, J.B. Poline, M.C. Gregoire, A. Jobert, J. Delforge, V. Frouin, M. Bottlaender, F. Dolle, L. Di Giamberardino, and A. Syrota In vivo detection of striatal dopamine release during reward: a PET study with [(11)C]raclopride and a single dynamic scan approach Neuroimage 16 2002 1015 1027
36. C. Pittenger, and E.R. Kandel In search of general mechanisms for long-lasting plasticity: Aplysia and the hippocampus Philos. Trans. R. Soc. Lond. B Biol. Sci. 358 2003 757 763
37. C. Ranganath, and G. Rainer Neural mechanisms for detecting and remembering novel events Nat. Rev. Neurosci. 4 2003 193 202
38. B. Rossion, and G. Pourtois Revisiting Snodgrass and Vanderwart's object pictorial set: the role of surface detail in basic-level object recognition Perception 33 2004 217 236
39. B.H. Schott, D.B. Sellner, C.J. Lauer, R. Habib, J.U. Frey, S. Guderian, H.J. Heinze, and E. Düzel Activation of midbrain structures by associative novelty and the formation of explicit memory in humans Learn. Mem. 11 2004 383 387
40. N. Schröder, S.J. O'Dell, and J.F. Marshall Neurotoxic methamphetamine regimen severely impairs recognition memory in rats Synapse 49 2003 89 96
41. W. Schultz Predictive reward signal of dopamine neurons J. Neurophysiol. 80 1998 1 27
42. W. Schultz, P. Apicella, E. Scarnati, and T. Ljungberg Neuronal activity in monkey ventral striatum related to the expectation of reward J. Neurosci. 12 1992 4595 4610
43. T. Straube, V. Korz, and J.U. Frey Bidirectional modulation of long-term potentiation by novelty-exploration in rat dentate gyrus Neurosci. Lett. 344 2003 5 8
44. T. Straube, V. Korz, D. Balschun, and J.U. Frey Requirement of beta-adrenergic receptor activation and protein synthesis for LTP-reinforcement by novelty in rat dentate gyrus J. Physiol. 552 2003 953 960
45. E.T. Tabuchi, A.B. Mulder, and S.I. Wiener Position and behavioural modulation of synchronization of hippocampal and accumbens neuronal discharges in freely moving rats Hippocampus 10 2000 717 728
46. J. Talairach, and P. Tournoux Co-Planar Stereotaxic Atlas of the Human Brain 1988 Thieme New York
47. I. Tracey Prospects for human pharmacological functional magnetic resonance imaging (phMRI) J. Clin. Pharmacol. 2001 21S 28S
48. E. Tulving Memory and consciousness Can. Psychol. 26 1985 1 12
49. E. Tulving, H.J. Markowitsch, F.E. Craik, R. Habib, and S. Houle Novelty and familiarity activations in PET studies of memory encoding and retrieval Cereb. Cortex 6 1996 71 79
50. H. Umegaki, J. Munoz, R.C. Meyer, E.L. Spangler, J. Yoshimura, H. Ikari, A. Iguchi, and D.K. Ingram Involvement of dopamine D(2) receptors in complex maze learning and acetylcholine release in ventral hippocampus of rats Neuroscience 103 2001 27 33
51. F. Vargha-Khadem, D.G. Gadian, K.E. Watkins, A. Connelly, W. Van Paesschen, and M. Mishkin Differential effects of early hippocampal pathology on episodic and semantic memory Science 277 1997 376 380
52. O.S. Vinogradova Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information Hippocampus 11 2001 578 598
53. N.D. Volkow, L. Chang, G.J. Wang, J.S. Fowler, M. Leonido-Yee, D. Franceschi, M.J. Sedler, S.J. Gatley, R. Hitzemann, and Y.S. Ding Association of dopamine transporter reduction with psychomotor impairment in methamphetamine abusers Am. J. Psychiatry 158 2001 377 382
54. H. Wan, J.P. Aggleton, and M.W. Brown Different contributions of the hippocampus and perirhinal cortex to recognition memory J. Neurosci. 19 1999 1142 1148
55. R.A. Wise Dopamine, learning and motivation Nat. Rev. Neurosci. 5 2004 483 494
56. A.P. Yonelinas, N.E. Kroll, J.R. Quamme, M.M. Lazzara, M.J. Sauve, K.F. Widaman, and R.T. Knight Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity Nat. Neurosci. 5 2002 1236 1241