GABAergic inhibitory processes and hippocampal long-term potentiation

Neuroscientist

Volumn 3, Issue 4, 1997, Pages 226-236

  Schultz, Laura M ^a,b  

^a PRINCETON UNIVERSITY   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

CA1; Dentate; E S potentiation; GABA; LTP; Plasticity

Indexed keywords

EID: 0000833194     PISSN: 10738584     EISSN: None     Source Type: Journal    
DOI: 10.1177/107385849700300410     Document Type: Review

References (78)

1. Bliss TVP, Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 1973;232: 331-356.
2. Andersen P, Sundberg SH, Sveen O, Swann JW, Wigström H. Possible mechanisms for long-lasting potentiation of synaptic transmission in hippocampal slices from guinea pigs. J Physiol (Lond) 1980;302:463-482.
3. Schwartzkroin PA, Wester K. Long-lasting facilitation of a synaptic potential following tetanization in the in vitro hippocampal slice. Brain Res 1975;89:107-119.
4. Alger BE, Teyler TJ. Long-term and short-term plasticity in the CA1, CA3, and dentate regions of the rat hippocampal slice. Brain Res 1976;110:463-482.
5. Okada Y, Miyamoto T. Formation of long-term potentiation in superior colliculus slices from the guinea pig. Neurosci Lett 1989; 96:108-113.
6. Chapman PF, Kairiss EW, Keenan CL, Brown TH. Long-term synaptic potentiation in the amygdala. Synapse 1990;6:271-278.
7. Artola A, Singer W. Long-term potentiation and NMDA receptors in the rat visual cortex. Nature 1987;330:649-652.
8. Harris EW, Ganong AH, Cotman CW. Long-term potentiation in the hippocampus involves activation of N-methyl-D-aspartate receptors. Brain Res 1984;323:132-137.
9. Harris EW, Cotman CW. Long-term potentiation of guinea pig mossy fiber responses is not blocked by N-methyl-D-aspartate antagonists. Neurosci Lett 1986:70:132-137.
10. Larson J, Wong D, Lynch G. Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 1986;368:347-350.
11. Larson J, Lynch G. Induction of synaptic potentiation in hippocampus by patterned stimulation involves 2 events. Science 1986; 232:985-988.
12. Rose GM, Dunwiddie TV. Induction of hippocampal long-term potentiation using physiologically patterned stimulation. Neurosci Lett 1986;69:244-288.
13. Collingridge GL, Bliss, TVP. NMDA receptors - their role in long-term potentiation. Trends Neurosci 1987;10:288-293.
14. Collingridge GL, Kehl SJ, McLennan H. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol (Lond) 1983;334:33-46.
15. Errington ML, Lynch MA, Bliss TVP. Long-term potentiation in the dentate gyrus: induction and increased glutamate release are blocked by D (-) aminophosphonovalerate. Neuroscience 1987; 20:279-284.
16. Morris RG, Anderson E, Lynch GS, Baudry M. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 1986;319: 774-776.
17. Abraham WC, Mason SE. Long-term potentiation involves enhanced synaptic excitation relative to synaptic inhibition in guinea pig hippocampus. J Physiol (Lond) 1987;394:367-380.
18. Coan EJ, Saywood W, Collingridge GL. MK801 blocks NMDA receptor-mediated synaptic transmission and long-term potentiation in rat hippocampal slices. Neurosci Lett 1987;80:111-114.
19. Kauer JA, Malenka RC, Nicoll RA. NMDA application potentiates synaptic transmission in the hippocampus. Nature 1988;334: 250-252.
20. Bliss TVP, Collingridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993;361:31-39.
21. Coan EJ, Collingridge GL. Magnesium ions block an N-methyl-D-aspartate receptor-mediated component of synaptic transmission in rat hippocampus. Neurosci Lett 1985;53:21-26.
22. Huang Y-Y, Wigström H, Gustafsson B. Facilitated induction of hippocampal long-term potentiation in slices perfused with low concentrations of magnesium. Neurosci Lett 1987;22:9-16.
23. Neuman R, Cherubini E, Ben-Ari Y. Is activation of N-methyl-D-aspartate channels sufficient to induce long-term potentiation? Neurosci Lett 1987;80:283-288.
24. Dunwiddie TV, Lynch G. The relationship between extracellular calcium concentrations and the induction of hippocampal long-term potentiation. Brain Res 1979;169:103-110.
25. Lynch G, Larson J, Kelso S, Barrionuevo G, Schottler F. Intracellular injections of EGTA block induction of hippocampal long-term potentiation. Nature 1983;305:719-723.
26. Turner RW, Baimbridge KG, Miller JJ. Calcium-induced long-term potentiation in the hippocampus. Neuroscience 1982;7: 1411-1416.
27. Malenka RC, Kauer JA, Zucker RS, Nicoll RA. Postsynaptic calcium is sufficient for potentiation of hippocampal synaptic transmission. Science 1988;242:81-84.
28. Ghijsen WEJM, Besselsen E, Geukers V, Kamphuis W, Lopez da Silva FH. Enhancement of the endogenous release of glutamate and γ-atninobutyric acid from hippocampus CA1 slices after in vitro long-term potentiation. J Neurochem 1992;59:482-486.
29. Stelzer A, Simon G, Kovacs G, Rai R. Synaptic disinhibition during maintenance of long-term potentiation in the CA1 hippocampal subfield. Proc Natl Acad Sci U S A 1994;91:3058-3062.
30. Haas HL, Rose G. Long-term potentiation of excitatory synaptic transmission in the rat hippocampus: the role of inhibitory processes. J Physiol (Lond) 1982;329:541-552.
31. Haas HL, Rose G. The role of inhibitory mechanisms in hippocampal long-term potentiation. Neurosci Lett 1984;47:301-306.
32. Kairiss EW, Abraham WC, Bilkey DK, Goddard GV. Field potential evidence for long-term potentiation of feed-forward inhibition in the rat dentate gyrus. Brain Res 1987;401:87-94.
33. Taube JS, Schwartzkroin PA. Intracellular recording from hippocampal CA1 interneurons before and after the development of long-term potentiation. Brain Res 1987;419:32-38.
34. Andersen P, Eccles JC, Løyning Y. Pathway of synaptic inhibition in the hippocampus. J Neurophysiol 1964;27:608-619.
35. Kandel ER, Spencer WA, Brinley FJ. Electrophysiology of hippocampal neurons. I. Sequential invasion and synaptic organization. J Neurophysiol 1961;24:225-242.
36. Kapur J, Stringer JL, Lothman EW. Evidence that repetitive seizures in the hippocampus cause a lasting reduction of GABAergic inhibition. J Neurophysiol 1989;61:417-426.
37. Kanda M, Maru E, Ashida H, Tatsuno J, Takatini O. Effects of LTP-induced tetanic stimulations of the perforant path on the commissural inhibition and facilitation of dentate granule cell discharge. Brain Res 1989;484:325-332.
38. Maru E, Ashida H, Tatsuno J. Long-lasting reduction of dentate paired pulse depression following LTP-inducing tetanic stimulation of perforant path. Brain Res 1989;478:112-120.
39. Alger BE, Nicoll RA. Feed-forward inhibition in rat hippocampal pyramidal cells studied in vitro. J Physiol (Lond) 1982;394:105-123.
40. Seress L, Ribak CE. Direct commissural connections to the basket cells of the hippocampal dentate gyrus: anatomical evidence for feed-forward inhibition. J Neurocytol 1984;13:215-225.
41. Wigström H, Gustaffson B. Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition. Nature 1983;301:603-604.
42. Abraham WC, Goddard GV. Multiple traces of neural activity in the hippocampus. In: Weinberger NM, McGaugh JL, Lynch G, editors. Memory systems of the brain. New York: Guilford 1985;62-76.
43. Tomasulo RA, Levy WB, Steward O. LTP-associated EPSP/spike dissociation in the dentate gyrus: GABAergic and non-GABAergic components. Brain Res 1991;561:27-34.
44. Tomasulo RA, Ramirez JJ. Activity-mediated changes in feed-forward inhibition in the dentate commissural pathway: relationship to EPSP/spike dissociation in the converging perforant path. J Neurophysiol 1993;69:165-173.
45. Wilson RC. Changes in the translation of synaptic excitation to dentate cell discharge accompanying long-term potentiation. I. Differences between normal and reinnervated dentate gyrus. J Neurophysiol 1981;46:324-338.
46. Wilson RC, Levy WB, Steward O. Changes in the translation of synaptic excitation to dentate cell discharge accompanying long-term potentiation. II. An evaluation of mechanisms utilizing dentate gyrus dually innervated by surviving ipsilateral and sprouted crossed temporodentate inputs. J Neurophysiol 1981;46:339-355.
47. Abraham WC, Gustafsson B, Wigström H. Long-term potentiation involves enhanced synaptic excitation relative to synaptic inhibition in guinea pig hippocampus. J Physiol (Lond) 1987;394: 367-380.
48. Andersen P, Avoli M, Hvalby Ø. Evidence for both pre- and post-synaptic mechanisms during long-term potentiation in hippocampal slices. Exp Brain Res Suppl 1984;9:315-324.
49. Chavez-Noriega LE, Bliss TVP, Halliwell JV. The EPSP-spike (E-S) component of long-term potentiation in the rat hippocampal slice is modulated by GABAergic but not cholinergic mechanisms. Neurosci Lett 1989;104:58-64.
50. Taube JS, Schwartzkroin PA. Mechanisms of long-term potentiation: EPSP/spike dissociation, intradendritic recordings, and glutamate sensitivity. J Neurosci 1988;8:1632-1644.
51. 2+ facilitates long-term potentiation of hippocampal IPSPs. Neuroreport 1991;2:533-536.
52. Cooper JR, Bloom FE, Roth RH. The biochemical basis of neuropharmacology. 6th ed. New York: Oxford 1991.
53. A responses in rat hippocampus. Neuron 1993;10:189-200.
54. B receptors. Int Rev Neurobiol 1994;36:97-223.
55. Bowery NG, Hill DR, Hudson AL, et al. (-)Baclofen decreases neurotransmitter release in the mammalian CNS by an action at a novel GABA receptor. Nature 1980;283:92-94.
56. B receptors in the central nervous system. Nature 1988;332:156-158.
57. B receptors. Neurosci Lett 1988;92:92-96.
58. B receptor antagonists on long-term potentiation. Naunyn Schmiedebergs Arch Pharmacol 1990;342:194-197.
59. B receptors to the same channels in hippocampus. Science 1986;234:1261-1265.
60. Newberry NR, Nicoll RA. Direct hyperpolarizing action of baclofen on hippocampal pyramidal cells. Nature 1984;308:450-452.
61. B receptors mediate disinhibition and facilitate long-term potentiation in the dentate gynis. Epilepsy Res Suppl 1992;7:119-134.
62. Collingridge GL, Herron CE, Lester RAJ. Synaptic activation of N-methyl-D-aspartate receptors in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol (Lond) 1988;399: 283-300.
63. Collingridge GL, Singer W. Excitatory amino acid receptors and synaptic plasticity. Trends Pharmacol Sci 1990:11:290-296.
64. Mott DD, Lewis DV, Ferrari CM, Wilson WA, Swartzwelder HS. Baclofen facilitates the development of long-term potentiation in the rat dentate gyms. Neurosci Lett 1990;113:222-226.
65. McNamara RK, dePape GE, Skelton RW. Differential effects of benzodiazepine receptor agonists on hippocampal long-term potentiation and spatial learning in the Morris water maze. Brain Res 1993;626:63-70.
66. Del Cerro S, Jung M, Lynch G. Benzodiazepines block long-term potentiation in slices of hippocampus and piriform cortex. Neuroscience 1992;49:1-6.
67. Tremwel MF, Hunter BE. Effects of chronic ethanol ingestion on long-term potentiation remain even after prolonged recovery from ethanol exposure. Synapse 1994;17:141-148.
68. Wigström H, Gustaisson B. Large long-lasting potentiation in the dentate gyrus in vitro during blockade of inhibition. Brain Res 1983:275;153-158.
69. Ballyk BA, Goh JW. Elevation of extracellular potassium facilitates the induction of long-term potentiation. J Neurosci Res 1992; 33:594-604.
70. B receptors in long-term potentiation. Experientia 1993;49:542-546.
71. B autoreceptors regulate the induction of LTP. Nature 1991;349:609-611.
72. Mott DD, Lewis DV. Facilitation of the induction of long-term potentiation by GABAB receptors. Science 1991;252:1718-1720.
73. Morrisett RA, Swartzwelder HS. Attenuation of hippocampal long-term potentiation by ethanol: a patch clamp analysis of glutamatergic and GABAergic mechanisms. J Neurosci 1993;13: 2264-2272.
74. Davies CH, Davies SN, Collingridge GL. Paired-pulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in rat hippocampus. J Physiol (Lond) 1990;424:513-531.
75. Hirai H, Okada Y. Ipsilateral corticotectal pathway inhibits the formation of long-term potentiation (LTP) in the rat superior colliculus through a GABAergic mechanism. Brain Res 1993;629: 23-30.
76. Hirai H, Tomita H, Okada Y. Inhibitory effect of GABA (γ-aminobutyric acid) on the induction of long-term potentiation in guinea pig superior colliculus slices. Neurosci Lett 1993;149: 198-200.
77. Bear MF, Press WA, Connors BW. Long-term potentiation in slices of kitten visual cortex and the effects of NMDA receptor blockade. J Neurophysiol 1992;67:841-851.
78. A blockade. J Neurosci 1993;13: 2477-2482.