Medial septal benzodiazepine receptors modulate hippocampal evoked responses and long-term potentiation

Brain Research

Volumn 717, Issue 1-2, 1996, Pages 12-21

  Stackman, Robert W ^a,d   Walsh, Thomas J ^a   Brucato, Frederic H ^b,c   Swartzwelder, H Scott ^b,c  

^a RUTGERS UNIVERSITY   (United States)

^b DURHAM VA MEDICAL CENTER   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Dartmouth College   (United States)

Author keywords

benzodiazepine; chlordiazepoxide; dentate gyrus; field potential; flumazenil; hippocampus; long term potentiation; medial septum; synaptic plasticity

Indexed keywords

BENZODIAZEPINE RECEPTOR; BENZODIAZEPINE RECEPTOR BLOCKING AGENT; BENZODIAZEPINE RECEPTOR STIMULATING AGENT; CHLORDIAZEPOXIDE; FLUMAZENIL;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EVOKED RESPONSE; FEMALE; HIPPOCAMPUS; INTRACEREBRAL DRUG ADMINISTRATION; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SEPTUM NUCLEUS;

EID: 0030002373     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/0006-8993(95)01455-1     Document Type: Article

References (49)

1. Abe, K., Ishiyama, J. and Saito, H., Effects of epidermal growth factor and basic fibroblast growth factor on generation of long-term potentiation in the dentate gyrus of fimbria-fornix lesioned rats, Brain Res., 593 (1992) 335-338.
2. Abe, K., Nakata, A., Mizutani, A. and Saito, H., Facilitatory but nonessential role of the muscarinic cholinergic system in the generation of long-term potentiation of population spikes in the dentate gyrus in vivo, Neuropharmacology, 33 (1994) 847-852.
3. Adamec, R.E., McNaughton, B.L., Racine, R. and Livingston, K.E., Effects of diazepam on hippocampal excitability in the rat: action in the dentate area, Epilepsia, 22 (1981) 205-215.
4. Alvarez-Leefmans, F.J. and Gardner-Medwin, A.R., Influences of the septum on the hippocampal dentate area which are unaccompanied by field potentials, J. Physiol., 249 (1975) 14P-16P.
5. Andersen, P., Bliss, T.V.P. and Skrede, K.K., Unit analysis of hippocampal population spikes, Exp. Brain Res., 13 (1971) 208-221.
6. Andersen, P., Sundberg, S.H., Sveen, O., Swann, J.W. and Wigström, Possible mechanisms for long-lasting potentiation of synaptic transmission in hippocampal slices from guinea pigs, J. Physiol., 302 (1980) 463-482.
7. Ben-Ari, Y., Krnjevic, K., Reinhart, W. and Ropert, N., Intracellular observations on the disinhibitory action of acetylcholine in the hippocampus, Neuroscience, 6 (1981) 2475-2484.
8. Bilkey, D.K. and Goddard, G.V., Medial septal facilitation of hippocampal granule cell activity is mediated by inhibition of inhibitory interneurones. Brain Res., 361 (1985) 99-106.
9. Bliss, T.V.P. and Lomo, T., Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path, J. Physiol., 232 (1973) 331-356.
10. Brioni, J.D., Arolfo, M.P., Jerusalinsky, D., Medina, J.H. and Izquierdo, I., The effect of flumazenil on acquisition, retention, and retrieval of spatial information, Behav. Neural Biol., 56 (1991) 329-335.
11. Brucato, F.H., Morrisett, R.A., Wilson, W.A. and Swartzwelder, H.S., The GABA-B receptor antagonist, CGP-35348, inhibits paired-pulse disinhibition in the rat dentate gyrus in vivo, Brain Res., 588 (1992) 150-153.
12. Caudarella, M., Durkin, T., Galey, D., Jeantet, Y. and Jaffard, R., The effect of diazepam on hippocampal EEG in relation to behavior, Brain Res., 435 (1987) 202-212.
13. Del Cerro, S., Jung, M. and Lynch, G., Benzodiazepines block long-term potentiation in slices of hippocampus and piriform cortex, Neuroscience, 49 (1992) 1-6.
14. Fantie, B.D. and Goddard, G.V., Septal modulation of the population spike in the fascia dentata produced by perforant path stimulation in the rat, Brain Res., 252 (1982) 227-237.
15. Foster, T.C. and Deadwyler, S.A., Acetylcholine modulates averaged sensory evoked responses and perforant path evoked field potentials in the rat dentate gyrus, Brain Res., 587 (1992) 95-101.
16. Freund, T. F. and Antal, M., GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus, Nature. 336 (1988) 170-173.
17. Frotscher, M. and Léránth, C., The cholinergic innervation of the rat fascia dentata: identification of target structures on granule cells by combining choline acetyltransferase immunocytochemistry and golgi impregnation, J. Comp. Neurol., 243 (1986) 58-70.
18. Herron, C.E., Lester, R.A.J., Coan, E.J. and Collingridge, G.L., Frequency-dependent involvement of NMDA receptors in the hippocampus: a novel synaptic mechanism, Nature, 322 (1986) 265-268.
19. Imperato, A., Dazzi, L., Obinu, M.C., Cessa, G.L. and Biggio, G., The benzodiazepine receptor antagonist flumazenil increases acetylcholine release in rat hippocampus, Brain Res., 647 (1994) 167-171.
20. Krnjevic, K., Reiffenstein, R.J. and Ropert, N., Disinhibitory action of acetylcholine in the rat's hippocampus: extracellular observations, Neuroscience, 6 (1981) 2465-2474.
21. Lal, H., Kumar, B. and Forster, M.J., Enhancement of learning and memory in mice by a benzodiazepine antagonist, FASEB J., 11 (1988) 2707-2711.
22. Larson, J., Wong, D. and Lynch, G., Pattern stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation, Brain Res., 368 (1986) 347-350.
23. Lee, H.K., Dunwiddie, T.V. and Hoffer, B.J., Interaction of diazepam with synaptic transmission in the in vitro rat hippocampus, Naunyn-Schmied. Arch. Pharmacol., 309 (1979) 131-136.
24. Lister, R.G., The amnesic action of benzodiazepines in man, Neurosci. Biobehav. Rev., 9 (1985) 87-94.
25. McNamara, R.K., dePape, G.E. and Skelton, R.W., Differential effects of benzodiazepine receptor agonists on hippocampal long-term potentiation and spatial learning in the Morris water maze, Brain Res., 626 (1993) 63-70.
26. McNamara, R.K. and Skelton, R.W., Effects of intracranial infusions of chlordiazepoxide on spatial learning in the Morris water maze. I. Neuroanatomical specificity, Behav. Brain Res., 59 (1993) 175-191.
27. Mizumori, S.J.Y., McNaughton, B.L. and Barnes, C.A., A comparison of supramammillary and medial septal influences on hippocampal field potentials and single-unit activity, J. Neurophysiol., 61 (1989) 15-31.
28. Mott, D.D. and Lewis, D.V., Facilitation of the induction of long-term potentiation by GABA-B receptors, Science, 252 (1991) 1718-1720.
29. B autoreceptors mediate activity-dependent disinhibition and enhance signal transmission in the dentate gyrus, J. Neurophysiol., 69 (1993) 674-691.
30. Nathan, T., Jensen, M.S. and Lambert, J.D.C., GABA-B receptors play a major role in paired-pulse facilitation in area CA1 of the rat hippocampus, Brain Res., 531 (1990) 55-65.
31. Paxinos, G. and Watson, C., The rat brain in stereotaxic coordinates, Academic Press, New York, 1982.
32. Rock, D. and Taylor, C.P., Effects of diazepam, pentobarbital, phenytoin and pentylenetetrazol on hippocampal paired-pulse inhibition in vivo, Neurosci. Lett., 65 (1986) 265-270.
33. Satoh, M., Ishihara, K., Iwama, T. and Takagi, H., Aniracetam augments, and midazolam inhibits, the long-term potentiation in guinea-pig hippocampal slices, Neurosci. Lett., 68 (1986) 216-220.
34. Stackman, R.W. and Walsh, T.J., Anatomical specificity and temporal dependence of chlordiazepoxide induced spatial memory impairments, Behav. Neurosci., 109 (1995) 436-445.
35. Stackman, R.W. and Walsh, T.J., Chlordiazepoxide-induced working memory impairments: site specificity and reversal by flumazenil, Behav. Neural Biol., 57 (1992) 233-243.
36. Steffensen, S.C. and Henriksen, S.J., Comparison of the effects of ethanol and chlordiazepoxide on electrophysiological activity in the fascia dentata and hippocampus regio superior. Hippocampus, 2 (1992) 201-212.
37. Stewart, M. and Fox, S.E., Two populations of rhythmically bursting neurons in rat medial septum are revealed by atropine, J. Neurophysiol., 61 (1989) 982-993.
38. Stringer, J.L. and Guyenet, P.G., Elimination of long-term potentiation in hippocampus by phencyclidine and ketamine, Brain Res., 258 (1983) 159-164.
39. Taube, J.S. and Schwartzkroin, P.A., Mechanisms of long-term potentiation: EPSP/spike dissociation, intradendritic recordings, and glutamate sensitivity, J. Neurosci., 8 (1988) 1632-1644.
40. Teyler, T.J. and DiScenna, P., Long-term potentiation as a candidate mnemonic device, Brain Res. Rev., 7 (1984) 15-28.
41. Thiébot, M.-H., Some evidence for amnesic-like effects of benzodiazepines in animals, Neurosci. Biobehav. Rev., 9 (1985) 95-100.
42. Valjakka, A., Lukkarinen, K., Koivisto, E., Lammintausta, R., Airaksinen, M.M. and Riekkinen, P., Evoked field responses, recurrent inhibition, long-term potentiation and immobility-related non-rhythmical EEG in dentate gyrus of fimbria-fornix-lesioned and control rats, Brain Res. Bull., 26 (1991) 525-532.
43. Van der Zee, E.A. and Luiten, P.G.M., Cholinergic and GABAergic neurons in the rat medial septum express muscarinic acetylcholine receptors, Brain Res., 652 (1994) 263-272.
44. Walsh, T.J., Site-specific pharmacology for the treatment of Alzheimer's Disease, Exp. Neurol., 124 (1993) 43-46.
45. Walsh, T.J. and Stackman, R.W., Modulation of memory by benzodiazepine-acetylcholine interactions. In E.D. Levin, M.W. Decker and L.L. Butcher (Eds.), Neurotransmitter Interactions and Cognitive Function, Birkhäuser, Boston, 1992, pp. 312-328.
46. Walsh, T.J., Stackman, R.W., Emerich, D.F. and Taylor, L.A., Intraseptal injection of GABA and benzodiazepine receptor ligands alters high-affinity choline transport in the hippocampus. Brain Res. Bull., 31 (1993) 267-271.
47. Wolfman, C., Da Cunha, C., Jerusalinsky, D., Levi de Stein, M., Viola, H., Izquierdo, I. and Medina, J.H., Habituation and inhibitory avoidance training alter brain regional levels of benzodiazepine-like molecules and are affected by intracerebral flumazenil microinjection, Brain Res., 548 (1991) 74-80.
48. Yasui, M., Kawasaki, K., Matsushita, A. and Satoh, M., Benzodiazepine inverse agonists augment long-term potentiation in CA1 and CA3 of guinea pig hippocampal slices, Neuropharmacology, 32 (1993) 127-131.
49. Záborszky, L., Heimer, L., Eckenstein, F. and Léránth, C., GABAergic input to cholinergic forebrain neurons: an ultrastructural study using retrograde tracing of HRP and double immunolabelling. J. Comp. Neurol., 250 (1986) 282-295.