Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty

Nature Neuroscience

Volumn 6, Issue 5, 2003, Pages 526-531

  Li, Shaomin ^a,b   Cullen, William K ^a   Anwyl, Roger ^a   Rowan, Michael J ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; DOPAMINE 1 RECEPTOR; DOPAMINE 5 RECEPTOR; GLUTAMIC ACID;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DEPTH PERCEPTION; ENVIRONMENTAL EXPOSURE; FACILITATION; HIPPOCAMPUS; INFORMATION RETRIEVAL; LONG TERM POTENTIATION; MALE; MEMORY; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPSE;

EID: 0037407956     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1049     Document Type: Article

References (48)

1. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Clarendon Press, Oxford, 1978).
2. Moser, E.I. & Paulsen, O. New excitement in cognitive space: between place cells and spatial memory. Curr. Opin. Neurobiol. 11, 745-751 (2001).
3. Lee, I. & Kesner, R. Differential contribution of NMDA receptors in hippocampal subregions to spatial working memory. Nat. Neurosci. 5, 162-168 (2002).
4. Knight, R. & Nakada, T. Cortico-limbic circuits and novelty: a review of EEG and blood flow data. Rev. Neurosci. 9, 57-70 (1998).
5. Tulving, E. & Markowitsch, H. Episodic and declarative memory: role of the hippocampus. Hippocampus 8, 198-204 (1998).
6. Ploghaus, A. et al. Learning about pain: the neural substrate of the prediction error for aversive events. Proc. Natl. Acad. Sci. USA 97, 9281-9286 (2000).
7. Vinogradova, O. Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11, 578-598 (2001).
8. Lisman, J.E. & Otmakova, N. 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, 551-558 (2001).
9. Moses, S., Sutherland, R. & McDonald, R. Differential involvement of amygdala and hippocampus in responding to novel objects and contexts. Brain Res. Bull. 58, 517-527 (2002).
10. Oswald, C. et al. The influence of selective lesions to components of the hippocampal system on the orientating response, habituation and latent inhibition. Eur. J. Neurosci. 15, 1983-1990 (2002).
11. Fischer, H. et al. Brain habituation during repeated exposure to fearful and neutral faces: a functional MRI study. Brain Res. Bull. 59, 387-392 (2003).
12. Martin, S.J., Grimwood, P. & Morris, R.G.M. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23, 649-711 (2000).
13. Bliss, T.V.P. & Lømo, T. Long-lasting potentiation of synaptic transmission in the dentate area of the anesthetized rabbit following stimulation of the perforant path. J. Physiol. (Lond.) 232, 331-356 (1973).
14. Pittenger, C. et al. Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory. Neuron 34, 447-462 (2002).
15. Buzsáki, G. Two stage model of memory trace formation: a role for noisy brain states. Neuroscience 31, 551-570 (1989).
16. Leung, L.S. Behavior-dependent evoked potentials in the hippocampal CA1 region of the rat. 1. Correlation with behavior and EEG. Brain Res. 198, 95-117 (1980).
17. Hargreaves, E., Cain, D. & Vanderwolf, C.H. Learning and behavioral long-term potentiation: importance of controlling for motor activity. J. Neurosci. 10, 1472-1478 (1990).
18. Moser, E.I., Mathiesen, I. & Andersen, P. Association between brain temperature and dentate field potentials in exploring and swimming rats. Science 259, 1324-1326 (1993).
19. Moser, E.I., Moser, M.-B. & Andersen, P. Potentiation of dentate synapses initiated by exploratory learning in rats: dissociation from brain temperature, motor activity and arousal. Learn. Mem. 1, 55-73 (1994).
20. Schultz, W., Apicella, P. & Ljungberg, T. Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. J. Neurosci. 13, 900-913 (1993).
21. Ihalainen, J., Riekkinen, P. & Feenstra, M. Comparison of dopamine and noradrenaline release in mouse prefrontal cortex, striatum and hippocampus using microdialysis. Neurosci. Lett. 277, 71-74 (1999).
22. Schultz, W. Multiple reward systems in the brain. Nat. Rev. Neurosci. 1, 199-207 (2000).
23. Frey, U., Huang, Y.-Y. & Kandel, E.R. Effects of cAMP simulate a late stage of LTP in hippocampal neurons. Nature 260, 1661-1664 (1993).
24. Otmakhova, N. & Lisman, J.E. D1/D5 Dopamine receptor activation increases the magnitude of early long-term potentiation at CA1 hippocampal synapses. J. Neurosci. 16, 7478-7486 (1996).
25. Swanson-Park, J. et al. A double dissociation within the hippocampus of dopamine D1/D5 receptor and beta-adrenergic receptor contributions to the persistence of long-term potentiation. Neuroscience 92, 485-497 (1999).
26. Frey, U., Matthies, H., Reyman, K.G. & Matthies, H. The effect of dopaminergic D1 blockade during tetanization on the expression of long-term potentiation in the rat CA1 region in vitro. Neurosci. Lett. 129, 111-114 (1991).
27. Otmakhova, N., Otmakhov, N., Mortenson, L. & Lisman, J.E. Inhibition of the cAMP pathway decreases early long-term potentiation at CA1 hippocampal synapses. J. Neurosci. 20, 4446-4451 (2000).
28. Acquas, E., Wilson, C. & Fibiger, H. Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: effects of novelty, habituation and fear. J. Neurosci. 16, 3089-3096 (1996).
29. Vankov, A., Herve-Minevielle, A. & Sara, S. Response to novelty and its rapid habituation in locus coeruleus neurons of the freely exploring rat. Eur. J. Neurosci. 7, 1180-1187 (1995).
30. Sah, P. & Bekkers, J. Apical dendritic location of slow after hyperpolarization current in hippocampal pyramidal neurons: Implications for the integration of long-term potentiation. J. Neurosci. 16, 4537-4542 (1996).
31. Watabe, A., Zaki, P. & O'Dell, T. Coactivation of beta-adrenergic and cholinergic receptors enhances the induction of long-term potentiation in the hippocampal CA1 region. J. Neurosci. 20, 5924-5931 (2000).
32. Xu, L., Anwyl, R. & Rowan, M.J. Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature 394, 891-894 (1998).
33. Horvitz, J. Mesolimbic and nigrostriatal dopamine responses to salient nonreward events. Neuroscience 96, 651-656 (2000).
34. Gasbarri, A., Sulli, A., Innocenzi, R., Pacitti, C. & Brioni, D. Spatial memory impairment induced by lesion of the mesohippocampal dopaminergic system in the rat. Neuroscience 74, 1037-1044 (1996).
35. Hersi, A., Rowe, W., Gaudreau, P. & Quirion, R. Dopamine D1 ligands modulate performance and hippocampal acetylcholine release in memoryimpaired aged rats. Neuroscience 69, 1067-1074 (1995).
36. Bach, M. et al. Age-related defects in spatial memory are correlated with defects in 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, 5280-5285 (1999).
37. Athos, J. et al. Hippocampal CRE-mediated gene expression is required for contextual memory formation. Nat. Neurosci. 5, 1119-1120 (2002).
38. Manahan-Vaughan, D. & Braunewell, K.-H. Novelty acquisition is associated with induction of hippocampal long-term depression. Proc. Natl. Acad. Sci. USA 96, 8739-8744 (1999).
39. Abraham, W.C., Logan, B., Greenwood, J.M. & Dragunow, M. Induction and experience-dependent consolidation of stable long-term potentiation lasting months in the hippocampus. J. Neurosci. 22, 9626-9634 (2002).
40. Li, S., Anwyl, R. & Rowan, M.J. Novelty exploration reverses early phase of long-term potentiation in hippocampal CA1 region of freely behaving rats. Irish J. Med. Sci. 171, 172 (2002).
41. Kim, J., Anwyl, R., Suh, Y., Djamgoz, M. & Rowan, M.J. Use-dependent effects of amyloidogenic fragments of β-amyloid precursor protein on synaptic plasticity in rat hippocampus in vivo. J. Neurosci. 21, 1327-1333 (2001).
42. Seidenbecher, T., Reyman, K.G. & Balschun, D. A post-tetanic time window for the reinforcement of long-term potentiation by appetitive and aversive stimuli. Proc. Natl. Acad. Sci. USA 94, 1494-1499 (1997).
43. Kusuki, T., Imahori, Y., Ueda, S. & Inokuchi, K. Dopaminergic modulation of LTP induction in the dentate gyrus of intact brain. Neuroreport 27, 2037-2040 (1997).
44. Kulla, A. & Manahan-Vaughan, D. Depotentiation in the dentate gyrus of freely moving rats is modulated by D1/D5 dopamine receptors. Cereb. Cortex 10, 614-620 (2000).
45. Frey, S., Bergado-Rosado, J., Seidenbecher, T., Pape, H.-C. & Frey, J.U. Reinforcement of early long-term potentiation (early-LTP) in dentate gyrus by stimulation of the basolateral amygdala: heterosynaptic induction mechanisms of late-LTP. J. Neurosci. 21, 3697-3703 (2001).
46. Dong, H.-W., Gan, Q. & Knuepfer, M. Central corticotropin releasing factor (CRF) and adrenergic receptors mediate hemodynamic responses to cocaine. Brain Res. 893, 1-10 (2001).
47. Li, S., Anwyl, R. & Rowan, M.J. Methoctramine induces a fast onset, long-lasting potentiation in the hippocampal CA1 region of the anaesthetized rat. Brit. J. Pharmacol. 34 (Suppl.), 150 (2001).
48. Xu, L., Anwyl, R. & Rowan, M.J. Behavioural stress facilitates the induction of long-term depression in the hippocampus. Nature 387, 497-500 (1997).