Inescapable stress enhances extracellular acetylcholine in the rat hippocampus and prefrontal cortex but not the nucleus accumbens or amygdala

Neuroscience

Volumn 74, Issue 3, 1996, Pages 767-774

  Mark, G P ^a,b   Rada, P V ^a,c   Shors, T J ^a  

^a PRINCETON UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c UNIVERSIDAD DE LOS ANDES   (Venezuela)

Author keywords

Acetylcholine release; Microdialysis; Restraint stress; Tail shock

Indexed keywords

ACETYLCHOLINE;

ADOLESCENT; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; MALE; MICRODIALYSIS; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; STRESS;

EID: 0030564962     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/0306-4522(96)00211-4     Document Type: Article

References (66)

1. Abercrombie E.D., Keefe K.A., DiFrischia D.S., Zigmond M.J. Differential effect of stress on in vivo dopamine release in striatum, nucleus accumbens and medial prefrontal cortex. J. Neurochem. 52:1989;1655-1658.
2. Amaral D.G., Kurz J. An analysis of the origins of the cholinergic and non-cholinergic septal projections to the hippocampal formation of the rat. J. comp. Neurol. 240:1985;37-59.
3. Arendt H.J., Allen Y., Marchbanks R.M., Schugens M.M., Sinden J., Lantos P.L., Gray J.A. Cholinergic system and memory in the rat: effects of chronic ethanol, embryonic basal forebrain transplants, and excitotoxic lesions of the cholinergic basal forebrain projection system. Neuroscience. 33:1989;435-462.
4. Bartus R. T., Dean R. L. and Flicker C. (1987) Cholinergic psychopharmacology: an integration of human and animal research on memory. In Psychopharmacology: The Third Generation of Progress (ed. Meltzer H. Y.), pp. 219-232. Raven Press, New York.
5. Bland B.H., Seto M.G., Sinclair B.R., Fraser S.M. The pharmacology of hippocampal theta cells: evidence that the sensory processing correlate is cholinergic. Brain Res. 299:1984;121-131.
6. Butcher S.G., Butcher L.L. Origin and modulation of acetylcholine activity in the neostriatum. Brain Res. 71:1974;167-171.
7. Cooper D.O., Schmidt D.E., Barrett R.J. Strain specific cholinergic changes in response to stress: analysis of a time-dependent avoidance variation. Pharmac. Biochem. Behav. 19:1983;457-462.
8. Costa E., Panula P., Thompson H.K., Cheney D.L. The transsynaptic regulation of the septo-hippocampal cholinergic neurons. Life Sci. 32:1983;165-179.
9. Damsma G., De Boer P., Westerink B.H.C., Fibiger H.C. Dopaminergic regulation of striatal cholinergic interneurons. Naunyn-Schmiedeberg's Arch. Pharmac. 342:1990;523-527.
10. Damsma G., Tham C., Robertson G.S., Fibiger H.C. Dopamine D1 receptor stimulation increases acetylcholine release in the rat. Eur. J. Pharmac. 186:1990;335-338.
11. Day J., Damsma G., Fibiger H.C. Cholinergic activity in the rat hippocampus, cortex and striatum correlates with locomotor activity: an in vivo microdialysis study. Pharmac. Biochem. Behav. 38:1991;723-729.
12. Deutch A.Y., Tam S.-Y., Roth R.H. Footshock and conditioned stress increase 3,4-dihydroxyphenylacetic acid (DOPAC) in the ventral tegmental area but not substantia nigra. Brain Res. 333:1985;143-146.
13. Dudar J.D., Whishaw I.Q., Szerb J.C. Release of acetylcholine from the hippocampus of freely moving rats during sensory stimulation and running. Neuropharmacology. 18:1979;673-678.
14. Dutar P., Lamour Y., Jobert A. Activation of identified septo-hippocampal neurons by noxious peripheral stimulation. Brain Res. 328:1985;15-21.
15. Fatranska M., Budai D., Gulya K., Kvetnansky R. Changes in acetylcholine content, release and muscarinic receptors in rat hippocampus under cold stress. Life Sci. 45:1989;143-149.
16. Fatranska M., Budai D., Oprsalova Z., Kvetnansky R. Acetylcholine and its enzymes in some brain areas of the rat under stress. Brain Res. 424:1987;109-114.
17. Fibiger H.C. The organization and some projections of cholinergic neurons of the mammalian forebrain. Brain Res. Rev. 4:1982;327-388.
18. Fibiger H.C., Lynch G.S., Cooper H.P. A biphasic action of central cholinergic stimulation on behavioral arousal in the rat. Psychopharmacologia. 20:1971;366-382.
19. Finkelstein Y., Koffler B., Rabey J.M., Gilad G.M. Dynamics of cholinergic synaptic mechanisms in the rat hippocampus after stress. Brain Res. 343:1985;314-319.
20. Fox S.E., Wolfson S., Ranck J.B. Hippocampal theta rhythm and the firing of neurons in walking and urethane anesthetized rats. Expl Brain Res. 62:1986;495-508.
21. Gilad G.M., Gilad V.H., Rabey J.M. Dopaminergic modulation of the septo-hippocampal cholinergic system activity under stress. Life Sci. 39:1986;2387-2393.
22. Gilad G.M., Mahom B.D., Finkelstein Y., Koffler B., Gilad V. Stress-induced activation of the hippocampal cholinergic system and the pituitary-adrenocortical axis. Brain Res. 347:1985;404-408.
23. Gilad G.M., Rabey J.M., Gilad V.M. Presynaptic effects of glucocorticoids on dopaminergic and cholinergic synaptosomes: implications for rapid endocrine-neural interactions in stress. Life Sci. 40:1987;2401-2408.
24. Gilad G.M., Rabey J.M., Shenkman L. Strain-dependent and stress induced changes in rat hippocampal cholinergic system. Brain Res. 267:1983;171-174.
25. Hadfield M.G. Mesocortical vs nigrostriatal dopamine uptake in isolated fighting mice. Brain Res. 222:1981;172-176.
26. Hata T., Kita T., Higashiguchi T., Ichida S. Total acetylcholine content, and activities of choline acetyltransferase and acetylcholinesterase in brain and duodenum of SART-stressed (repeated cold stressed) rat. Jpn. J. Pharmac. 41:1986;475-485.
27. Hernandez L., Stanley B.G., Hoebel B.G. A small, removable microdialysis probe. Life Sci. 39:1986;2629-2637.
28. Hoover D.B., Muth E.A., Jacobowitz D.M. A mapping of the distribution of acetylcholine, choline acetyltransferase and acetylcholinesterase in discrete areas of rat brain. Brain Res. 153:1978;295-306.
29. Imperato A., Stefano P.-A., Casolini P., Angelucci L. Changes in brain dopamine and acetylcholine release during and following stress are independent of the pituitary-adrenocortical axis. Brain Res. 538:1991;111-117.
30. Inglis F.M., Fibiger H.C. Increases in hippocampal and frontal cortical acetylcholine release associated with presentation of sensory stimuli. Neuroscience. 66:1995;81-86.
31. Jasper H.H., Tessier J. Acetlycholine liberation from cerebral cortex during paradoxical (REM) sleep. Science. 172:1971;601-602.
32. Kametani H., Kawamura H. Circadian rhythm of cortical acetylcholine release as measured by in vivo microdialysis in freely moving rats. Neurosci. Lett. 132:1991;263-266.
33. Koslow S.H., Racagni G., Costa E. Mass fragmentographic measurement of norepinephrine, dopamine, serotonin and acetylcholine in seven discrete nuclei of the rat tel-diencephalon. Neuropharmacology. 13:1974;1123-1130.
34. Krnejeivc K., Rieffenstein R.J., Robert N. Disinhibitory action of acetylcholine in the rat's hippocampus: extracellular observations. Neuroscience. 6:1981;2465-2474.
35. Kurosawa M., Okada K., Sato A., Uchida S. Extracellular release of acetylcholine, noradrenaline and serotonin increases in the cerebral cortex during walking in conscious rats. Neurosci. Lett. 161:1993;73-76.
36. Leith M.J., Barrett R.J. Effects of hippocampal microinjections of d-amphetamine and scopolamine on active avoidance behavior in rats. J. comp. physiol. Psychol. 88:1975;285-299.
37. Lin Q., Li P. Rostral medullary cholinergic mechanisms and chronic stress-induced hypertension. J. auton. nerv. Syst. 31:1990;211-217.
38. Lindvall O., Stenevi U. Dopamine and noradrenaline neurons projecting to the septal area in the rat. Cell Tissue Res. 190:1978;383-405.
39. Mark G., Rada P., Pothos E., Hoebel B.G. Effects of feeding and drinking on acetylcholine release in the nucleus accumbens, striatum and hippocampus of freely-behaving rats. J. Neurochem. 58:1992;2269-2274.
40. Mark G. P., Schwartz D. H., Hernandez L., West H. L. and Hoebel B. G. (1991) Application of microdialysis to the study of motivation and conditioning: measurements of dopamine and serotonin in freely-behaving rats. In Microdialysis in the Neurosciences (eds Robinson T. E. and Justice J. B.), pp. 369-385. Elsevier, Amsterdam.
41. Mesulam M.-M., Mufson E.J., Wainer B.H., Levey E.I. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience. 10:1983;1185-1201.
42. Mizukawa K., Takayama H., Sato H., Ota Z., Haba K., Ogawa N. Alterations of muscarinic cholinergic receptors in the hippocampal formation of stressed rat: in vitro quantitative autoradiographic analysis. Brain Res. 478:1989;187-192.
43. Mizuno T., Endo Y., Arita J., Kimura F. Acetylcholine release in the rat hippocampus as measured by the microdialysis method correlates with motor activity and exhibits a diurnal variation. Neuroscience. 44:1991;607-612.
44. Nicoll R. The septo-hippocampal projection: a model cholinergic pathway. Trends Neurosci. 8:1985;533-536.
45. Nilsson O.G., Bjorklund A. Behaviour-dependent changes in acetylcholine release in normal and graft-reinnervated hippocampus: evidence for host regulation of grafted cholinergic neurons. Neuroscience. 49:1992;33-44.
46. Nilsson O.G., Kalen P., Rosengren E., Bjorklund A. Acetylcholine release in the rat hippocampus as studied by microdialysis is dependent on axonal impulse flow and increases during behavioural activation. Neuroscience. 36:1990;325-338.
47. Nilsson O.G., Leanza G., Bjorklund A. Acetylcholine release in the hippocampus: regulation by monoaminergic afferents as assessed by in vivo microdialysis. Brain Res. 584:1992;132-140.
48. Onteniente B., Geffard M., Calas A. Ultrastructural immunocytochemical study of the dopaminergic innervation of the rat lateral septum with anti-dopamine antibodies. Neuroscience. 13:1984;385-393.
49. Paxinos G. and Watson C. (1982) The Rat Brain in Stereotaxic Coordinates. Academic Press, Sydney.
50. Robinson S.E., Malthe-Sorensen D., Wood P.L., Commissiong J. Dopaminergic control of the septo-hippocampal cholinergic pathway. J. Pharmac. exp. Ther. 208:1979;476-479.
51. Rosenblad C., Nilsson O.G. Basal forebrain grafts in the rat neocortex restore in vivo acetylcholine release and respond to behavioural activation. Neuroscience. 55:1993;353-362.
52. Saavedra J.M. Changes in dopamine, noradrenaline and adrenaline in specific septal and preoptic nuclei after acute immobilization stress. Neuroendocrinology. 35:1982;396-401.
53. Saper C.B. Organization of cerebral cortical afferent systems in the rat. II. Magnocellular basal nucleus. J. comp. Neurol. 222:1984;313-342.
54. Schallert T., Whishaw I.Q., Ramirez V.D., Teitelbaum P. Compulsive, abnormal walking caused by anticholinergics in akinetic, 6-hyroxydopamine-treated rats. Science. 199:1978;1461-1463.
55. Schmidt E.D., Cooper D.O., Barrett R.J. Strain specific alterations in hippocampal cholinergic function following acute footshock. Pharmac. Biochem. Behav. 12:1979;277-280.
56. Servatius R.J., Shors T.J. Exposure to inescapable stress persistently facilitates associative and nonassociative learning in rats. Behav. Neurosci. 108:1994;1011-1016.
57. Shors T. J., Gallegos R. and Breindl A. (1996) Transient and persistent consequences of inescapable stress on long-term potentiation (LTP), synaptic responses, theta rhythms and burst in area CA1 of the hippocampus. Submitted.
58. Shors T.J., Mark G., Selcher J., Servatiius R.J. Stress-induced sensitization, but not the facilitated learning, is cholinergically-mediated. Neurosci. Abstr. 21:1995;1674.
59. Shors T.J., Weiss C., Thompson R.F. Stress-induced facilitation of classical conditioning. Science. 257:1992;537-539.
60. Swanson L.W., Cowan W.M. The connections of the septal region in the rat. J. comp. Neurol. 186:1979;621-656.
61. Szerb J.C. Cortical acetylcholine release and electroencephalographic arousal. J. Physiol. 192:1967;329-343.
62. Takayama H., Mizukawa K., Ota Z., Ogawa N. Regional responses of rat brain muscarinic cholinergic receptors to immobilization stress. Brain Res. 436:1987;291-295.
63. Toide K. Effects of scopolamine on extracellular acetylcholine and choline levels and on spontaneous motor activity in freely moving rats measured by brain dialysis. Pharmac. Biochem. Behav. 33:1989;109-113.
64. Vanderwolf C.H. Hippocampal electrical activity and voluntary movement in the rat. Electroenceph. clin. Neurophysiol. 26:1969;407-418.
65. Vanderwolf C.H. Cerebral activity and behavior: control by central cholinergic and serotonergic systems. Int. Rev. Neurobiol. 30:1988;225-340.
66. Welner S.A., Dunnett S.B., Salamone J.D., MacLean B., Iverson S.D. Transplantation of embryonic ventral forebrain grafts to the neocortex of rats with bilateral lesions of the nucleus basalis magnocellularis ameliorates a lesion-induced deficit in spatial memory. Brain Res. 463:1988;192-197.