NMDA-dependent modulation of CA1 local circuit inhibition

Journal of Neuroscience

Volumn 16, Issue 6, 1996, Pages 2034-2043

  Grunze, Heinz C R ^a   Rainnie, Donald G ^a   Hasselmo, Michael E ^b   Barkai, Eddie ^b   Hearn, Elizabeth F ^a   McCarley, Robert W ^a   Greene, Robert W ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

AP5; long term potentiation; N acetylaspartyl glutamate; phencyclidine; recurrent inhibition; schizophrenia; signal processing

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; N ACETYLASPARTYLGLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; COMPUTER SIMULATION; CONTROLLED STUDY; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIAL; LEARNING; LONG TERM POTENTIATION; MALE; NONHUMAN; PATTERN RECOGNITION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

EID: 0029880412     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-06-02034.1996     Document Type: Article

References (72)

1. Abraham WC, Gustafsson B, Wigström H (1987) Long-term potentiation involves enhanced synaptic excitation relative to synaptic inhibition in guinea-pig hippocampus. J Physiol (Lond) 394:367-380.
2. Alger BE, Nicoll RA (1982) Feed-forward dendritic inhibition in rat hippocampal pyramidal cells studied in vitro. J Physiol (Lond) 328:105-123.
3. Amaral DG, Witter M (1989) The three dimensional organization of the rat hippocampal formation: a review of anatomical data. Neuroscience 31:571-591.
4. Andersen P, Eccles JC, Løyning Y (1963) Recurrent inhibition in the hippocampus with identification of the inhibitory cell and its synapses. Nature 198:540-542.
5. Anderson P, Sundberg SH, Sveen O, Wigström H (1977) Specific long-lasting potentiation of synaptic transmission in hippocampal slices. Nature 266:736-737.
6. Barkai E, Hasselmo ME (1994) Modulation of the input output function of rat piriform cortex pyramidal cells. J Neurophysiol 72:644-658.
7. Barkai E, Bergman RE, Horwitz G, Hasselmo ME (1994) Modulation of associative memory function in a biophysical simulation of rat piriform cortex. J Neurophysiol 72:659-677.
8. Blakely RD, Coyle JT (1988) The neurobiology of N-acetylaspartylglutamate. Int Rev Neurobiol 30:39-100.
9. Blanton MG, Lo Turco JJ, Kriegstein AR (1989) Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex. J Neurosci Methods 30:203-210.
10. Bliss TVP, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39.
11. Bliss TVP, Lømo T (1973) Long lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 232:331-356.
12. Bochet P, Audinat E, Lambolez B, Crépel F, Rossier J, Iino M, Tsuzuki K, Ozawa S (1994) Subunit composition at the single- cell level explains functional properties of a glutamate-gated channel. Neuron 12:383-388.
13. Bourne GW, Théorêt Y, Esplin B, Čapek R (1983) Effect of phencyclidine on inhibition in the hippocampal slice. Naunyn-Schmiedebergs Arch Pharmacol 323:168-172.
14. Bower JM, Beeman D (1995) The book of genesis: exploring realistic neural models with the general neural simulation system. New York: Telos/Springer-Verlag.
15. Buhl EH, Halasy K, Somogyi P (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368:823-828.
16. Buzsáki G, Eidelberg E (1982) Direct afferent excitation and long-term potentiation of hippocampal interneurons. J Neurophysiol 48:597-607.
17. Buzsáki G, Horváth Z, Urioste R, Hetke J, Wise K (1992) High-frequency network oscillation in the hippocampus. Science 256:1025-1027.
18. Collingridge GL, Keel SJ, McLennan H (1983) Excitatory amino acids in synaptic transmission in the Chaffer collateral-commissural pathway of the rat hippocampus. J Physiol (Lond) 334:33-46.
19. Collingridge GL, Herron CE, Lester RAJ (1988) Synaptic activation of N-methyl-D-aspartate receptors in the Chaffer collateral-commissural pathway of rat hippocampus. J Physiol (Lond) 399:283-300.
20. Curtis DR, Felix D, McLellan H (1970) GABA and hippocampal inhibition. Br J Pharmacol 40:881-883.
21. Davis S, Butcher SP, Morris RGM (1992) The NMDA receptor antagonist D-″-amino-%-phosphopentanoate (D-APV) impairs spatial learning and LTP in vivo at intracerebral concentrations comparable to those that block LTP in vitro. J Neurosci 12:21-34.
22. Dingledine R, Langmoen IA (1980) Conductance changes and inhibitory actions of hippocampal recurrent i.p.s.p.s. Brain Res 185:277-287.
23. Frotscher M, Zimmer J (1983) Commissural fibers terminate on non-pyramidal neurons in the guinea pig hippocampus - a combined Golgi/EM degeneration study. Brain Res 265:289-293.
24. Gruenthal M, Armstrong DR, Ault B, Nadler JC (1986) Comparison of seizures and brain lesions produced by intracerebroventricular kainic acid and bicuculline methiodide. Exp Neurol 93:621-630.
25. Haas HL, Rose G (1982) Long-term potentiation of excitatory synaptic transmission in the rat hippocampus: the role of inhibitory processes. J Physiol (Lond) 329:541-552.
26. Hablitz JJ, Langmoen IA (1986) N-methyl-D-aspartate receptor antagonists reduce synaptic excitation in the hippocampus. J Neurosci 6:102-106.
27. Harris W, Ganong AH, Cotman CW (1984) Long-term potentiation in the hippocampus involves activation of N-methyl-D-aspartate receptors. Brain Res 323:132-137.
28. Hasselmo ME, Barkai E (1996) Cholinergic modulation of activity-dependent synaptic plasticity in the piriform cortex and associative memory function in a network biophysical simulation. J Neurosci. in press.
29. Hasselmo ME, Bower JM (1993) Acetylcholine and memory. Trends Neurosci 16:218-222.
30. Herron CE, Lester RAJ, Coan EJ, Collingridge GL (1986) Frequency-dependent involvement of NMDA receptors in the hippocampus: a novel synaptic mechanism. Nature 322:265-268.
31. Hestrin S, Nicoll RA, Perkel DJ, Sah P (1990) Analysis of excitatory synaptic action in pyramidal cells using whole cell recordings fro rat hippocampal slices. J Physiol (Lond) 422:203-225.
32. Javitt DC, Zukin SR (1991) Recent advances in the phencyclidine model of schizophrenia. Am J Psychiatry 148:1301-1308.
33. Johnston D, Wu, SM-S (1995) Foundations of cellular neurophysiology. Cambridge, MA: MIT.
34. Korn H, Oda Y, Faber DS (1992) Long-term potentiation of inhibitory circuits and synapses in the central nervous system. Proc Natl Acad Sci USA 89:440-443.
35. Krystal JH, Karper LP, Seibyl JP, Freeman GK, Delaney R, Brenner JD, Heninger GR, Bowers MB Jr, Charney DS (1994) Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Arch Gen Psychiatry 51:199-214.
36. Lacaille JC (1991) Postsynaptic potentials mediated by excitatory and inhibitory amino acids in interneurons of stratum pyramidale of the CA1 region of rat hippocampal slices in vitro. J Neurophysiol 66:1441-1454.
37. Lacaille JC, Williams S (1990) Membrane properties of interneurons in stratum oriens-alveus of the CA1 region of rat hippocampus in vitro. Neuroscience 36:349-359.
38. Laurie DJ, Seeburg H (1994) Regional and developmental heterogeneity in slicing of the rat brain NMDAR1 mRNA. J Neurosci 14:3180-3194.
39. Léránth CS, Frotscher M (1983) Commissural afferents to the rat hippocampus terminate on vasoactive intestinal polypeptide-like immunoreactive non-pyramidal neurons: an EM immunocytochemical degeneration study. Brain Res 276:357-361.
40. Li XG, Somogyi P, Ylinen A, Buzsáki G (1994) The hippocampal CA3 network: an in vivo intracellular labeling study. J Comp Neurol 339:181-208.
41. Lodge D, Ands NA, Berry SC, Burton NR (1983) Arylcyclohexylamines selectively reduce excitation of mammalian neurones by aspartate-like amino acids. In: Phencyclidine and related arylcyclohexylamines (Kamenka JM, Domino EF, Geneste P, eds), pp 595-616. Ann Arbor, MI:NPP Books.
42. Malenka RC, Nicoll RA (1993) NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trends Neurosci 16:521-527.
43. Malinow R, Miller JP (1986) Postsynaptic hyperpolarization during conditioning reversibly blocks induction of long-term potentiation. Nature 320:529-530.
44. Miles R (1990) Synaptic excitation if inhibitory cells by single CA3 hippocampal pyramidal cells of the Guinea-pig in vitro. J Physiol (Lond) 428:61-77.
45. Miles R, Wong RKS (1986) Excitatory synaptic interactions between CA3 neurones in the guinea-pig hippocampus. J Physiol (Lond) 373:397-418.
46. Miles R, Wong RKS (1987a) Inhibitory control of local excitatory circuits in the guinea-pig hippocampus. J Physiol (Lond) 388:611-629.
47. Miles R, Wong RKS (1987b) Latent synaptic pathways revealed after tetanic stimulation in the hippocampus. Nature 329:724-726.
48. Monyer H, Sprengel R, Schoepfer R, Herb A, Higuchi M, Lomeli H, Burnashev N, Sakmann B, Seeburg PH (1992) Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256:1217-1221.
49. Monyer H, Burnashev N, Laurie DJ, Sakmann B, Seeburg PH (1994) Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12:529-540.
50. Mori-Okamoto J, Okamoto K, Sekiguchi M (1987) Electrophysiological and pharmacological actions of N-acetylaspartylglutamate intracellularly studied in cultured chick cerebellar neurons. Brain Res 401:60-67.
51. Moriyoshi K, Masu M, Ishii T, Shigemoto R, Mizuno N, Nakanishi S (1991) Molecular cloning and characterization of the rat NMDA receptor. Nature 354:31-37.
52. Nakanishi N, Axel R, Schneider NA (1992) Alternative splicing generates functionally distinct N-methyl-D-aspartate receptors. Proc Natl Acad Sci USA 89:8552-8556.
53. Olney JW, Labruyere J, Wang G, Wozniak DF, Price MT, Sesma MA (1991) NMDA antagonist neurotoxicity: mechanism and prevention. Science 254:1515-1518.
54. 3H] MK 801 binding in rat hippocampal membranes. Soc Neurosci Abstr 15:942.
55. 3H] norepinephrine release from rat hippocampal slices. J Pharmacol Exp Ther 266:796-803.
56. Radpour S, Thomson AM (1991) Co-activation of local circuit NMDA receptor mediated EPSPs induces lasting enhancement of minimal Chaffer collateral EPSPs in slices of rat hippocampus. Eur J Neurosci 3:602-613.
57. Rainnie DG, Asprodini EK, Shinnick-Gallagher P (1991) Excitatory transmission in the basolateral amygdala. J Neurophysiol 66:986-998.
58. Sah P, Hestrin S, Nicoll RA (1990) Properties of excitatory postsynaptic currents recorded in vitro from rat hippocampal interneurones. J Physiol (Lond) 430, 605-616.
59. Schwartzkroin PA, Prince DA (1977) Penicillin-induced epileptiform activity in the hippocampal in vitro preparation. Ann Neurol 1:463-469.
60. Sekiguchi M, Okamoto K, Sakai Y (1989) Low-concentration N-acetylaspartylgtutamate suppresses the climbing fiber response of Purkinje cells in guinea pig cerebellar slices and the response to excitatory amino acids of Xenopus laevis oocytes injected with cerebellar mRNA. Brain Res 482, 87-96.
61. Spencer WA, Kandel ER (1961) Hippocampal neuron responses to selective activation of recurrent collaterals of hippocampofugal axons. Exp Neurol 4:149-161.
62. Stauch-Slusher BS, Tsai G, Voo G, Coyle JT (1992) Immunocytochemical localization of the N-acetyl-aspartyl-glutamate (NAAG) hydrolyzing enzyme N-acetylated alpha-linked acidic dipeptidase (NAALA-Dase). J Comp Neurol 315:217-229.
63. A receptors control the excitability of neuronal populations. Int Rev Neurobiol 33:195-287.
64. Stelzer A, Simon G, Kovacs G, Rai R (1994) Synaptic disinhibition during maintenance of long-term potentiation in the CA 1 hippocampal subfield. Proc Natl Acad Sci USA 91:3058-3062.
65. Stringer JL, Greenfield LJ, Hackett JT, Guyenet PG (1983) Blockade of long-term potentiation by phencyclidine and σ opiates in the hippocampus in vivo and in vitro. Brain Res 280:127-138.
66. Thomson AM, Radpour S (1991) Excitatory connections between CA 1 pyramidal cells revealed by spike triggered averaging in slices of rat hippocampus are partially NMDA receptor mediated. Eur J Neurosci 3:587-601.
67. Traub R, Miles R, Buzsáki G (1992) Computer simulation of carbachol-driven rhythmic population oscillations in the CA3 region of the in vitro rat hippocampus. J Physiol (Lond) 451:653-672.
68. Traub R, Miles R, Jeffereys JGR (1993) Synaptic and intrinsic conductances shape picrotoxin-induced synchronized after discharges in the guinea-pig hippocampal slice. J Physiol (Lond) 461:525-547.
69. Tsai G, Passani LA, Slusher BS, Carter R, Kleinman JE, Coyle JT (1996) Changes of excitatory neurotransmitter metabolism in schizophrenic brains. Arch Gen Psychiatry, in press
70. Watanabe M, Mishina M, Inoue Y (1994) Distinct spatiotemporal expressions of five NMDA receptor channel subunit mRNAs in the cerebellum. J Comp Neurol 343:513-519.
71. Whittington MA, Traub RD, Jeffereys JGR (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373:612-615.
72. Wilson MA, Bower JM (1992) Cortical oscillations and temporal interactions in a computer simulation of piriform cortex. J Neurophysiol 67:981-995.