Stimulation in Hippocampal Region CA1 in Behaving Rats Yields Long-Term Potentiation when Delivered to the Peak of Theta and Long-Term Depression when Delivered to the Trough

Journal of Neuroscience

Volumn 23, Issue 37, 2003, Pages 11725-11731

  Hyman, James M ^a   Wyble, Bradley P ^a,b   Goyal, Vikas ^a,b   Rossi, Christina A ^a   Hasselmo, Michael E ^a  

^a BOSTON UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

Author keywords

CA1; Hippocampus; LTD; LTP; Plasticity; Theta rhythm

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN REGION; CENTRAL NERVOUS SYSTEM DEPRESSION; HIPPOCAMPUS; LEARNING; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; THETA RHYTHM;

EID: 0347694855     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-37-11725.2003     Document Type: Article

References (31)

1. Berry SD, Seager MA (2001) Hippocampal theta oscillations and classical conditioning. Neurobiol Learn Mem 76:298-313.
2. Brankack J, Stewart M, Fox SE (1993) Current source density analysis of the hippocampal theta rhythm: associated sustained potentials and candidate synaptic generators. Brain Res 615:310-327.
3. Brown TH, Chapman PF, Kairiss EW, Keenan CL (1988) Long-term synaptic potentiation. Science 242:724-728.
4. Buzsaki G, Leung LW, Vanderwolf CH (1983) Cellular bases of hippocampal EEG in the behaving rat. Brain Res 287:139-171.
5. 2+ signaling requirements for long-term depression in the hippocampus. Neuron 16:825-833.
6. Deadwyler SA, West JR, Cotman CW, Lynch GS (1975) A neurophysiological analysis of commisural projections to the dentate gyrus of the rat. J Neurophysiol 38:167-184.
7. Dudek SM, Bear MF (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci USA 89:4363-4367.
8. Fox SE, Wolfson S, Ranck Jr JB (1986) Hippocampal theta rhythm and the firing ofneurons in walking and urethane anesthetized rats. Exp Brain Res 62:495-508.
9. Golding NL, Staff NP, Spruston N (2002) Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418:326-331.
10. Green JD, Arduini AA (1954) Hippocampal electrical activity in arousal. J Neurophysiol 17:533-557.
11. Greenstein YJ, Pavlides C, Winson J (1988) Long-term potentiation in the dentate gyrus is preferentially induced at theta rhythm periodicity. Brain Res 438:331-334.
12. Hasselmo ME, Bodelon C, Wyble BP (2002) A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput 14:793-817.
13. Holscher C, McGlinchey L, Anwyl R, Rowan MJ (1997) HFS-induced long-term potentiation and LFS-induced depotentiation in area CA1 of the hippocampus are not good models for learning. Psychopharmacology (Berl) 130:174-182.
14. Huerta PT, Lisman JE (1995) Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro. Neuron 15:1053-1063.
15. Kaibara T, Leung S (1992) Basal versus apical dendritic long-term potentiation of commissural afferents to hippocampal CA1: a current-source density study. J Neurosci 13:2391-2404.
16. Kamondi A, Acsady L, Wang XJ, Buzsaki G (1998) Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus 8:244-261.
17. Larson J, Lynch G (1986) Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events. Science 232:985-988.
18. Leung LS, Shen B (1995) Long-term potentiation at the apical and basal dendritic synapses of CA1 after local stimulation in behaving rats. J Neurophysiol 73:1938-1946.
19. Leung LS, Shen B, Rajakumar N, Ma J (2003) Cholinergic activity enhances hippocampal long-term potentiation in CA1 during walking in rats. J Neurosci 23:9297-9304.
20. Levy WB, Steward O (1979) Synapses as associative memory elements in the hippocampal formation. Brain Res 175:233-245.
21. Lisman J (1989) A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. Proc Natl Acad Sci USA 86:9574-9578.
22. Macrides F, Eichenbaum HB, Forbes WB (1982) Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning. J Neurosci 2:1705-1717.
23. Malenka RC, Nicoll RA (1999) Long-term potentiation - a decade of progress? Science 285:1870-1874.
24. Martin SJ, Morris RG (2002) New life in an old idea: the synaptic plasticity and memory hypothesis revisited, Hippocampus 12:609-636.
25. Orr G, Rao G, Houston FP, McNaughton BL, Barnes CA (2001) Hippocampal synaptic plasticity is modulated by theta rhythm in the fascia dentata of adult and aged freely behaving rats. Hippocampus 11:647-654.
26. Pavlides C, Greenstein YJ, Grudman M, Winson J (1988) Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res 439:383-387.
27. Racine RJ, Milgram NW, Hafner S (1983) Long-term potentiation phenomena in the rat limbic forebrain. Brain Res 260:217-231.
28. Stewart M, Quirk GJ, Barry M, Fox SE (1992) Firing relations of medial entorhinal neurons to the hippocampal theta rhythm in urethane anesthetized and walking rats. Exp Brain Res 90:21-28.
29. Vanderwolf CH (1969) Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407-418.
30. Winson J (1978) Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 201:160-163.
31. Wyble BP, Linster C, Hasselmo ME (2000) Size of CA1-evoked synaptic potentials is related to theta rhythm phase in rat hippocampus. J Neurophysiol 83:2138-2144.