Summary
Norepinephrine (NE)-induced, long-lasting facilitation of the perforant path evoked population spike amplitude in the dentate gyrus (DG) has been reported to occur following iontophoresis of norepinephrine in the DG in vivo and following application of 10 or 20 μM NE to the hippocampal slice in vitro. The present study employs glutamatergic activation of the locus coeruleus (LC) to induce NE release in the DG. Thirty-three female rats served as subjects. The perforant path-evoked potential was elicited once every 10 s and monitored in the DG cell body layer. Following appropriate control periods, 100–150 nL of 0.5 M 1-glutamate were pressure ejected in the vicinity of the LC. All placements in or within 300 μM of the LC produced significant facilitation (140%) of the population spike amplitude. Facilitation lasted more than 20 min in 37% of the animals tested. The facilitation effects on population spike amplitude were replicated with up to four ejections of glutamate at the same site. Propranolol (30 mg/kg i.p.) blocked this facilitation of population spike amplitude. Changes in EPSP slope were variable. Glutamate-activation of LC was not accompanied by blood pressure increases. These data suggest that physiological NE release via LC activation induces a beta receptor mediated facilitation of the perforant path-evoked population spike which parallels that obtained with direct application of NE to the DG in vivo or in vitro. LC-NE may provide one mechanism in the mammalian brain for long-lasting heterosynaptic modulation of neural inputs.
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References
Armstrong-James M, Fox K (1983) Effects of iontophoresed noradrenaline on the spontaneous activity of neurones in rat primary somatosensory cortex. J Physiol (Lond) 335: 427–447
Assaf SY, Mason ST, Miller JJ (1979) Noradrenergic modulation of neuronal transmission between the entorhinal cortex and the dentate gyrus of the rat. J Physiol (Lond) 292: 52P
Berecek KH, Olpe HR, Jones RSG, Hofbauer KG (1984) Microinjection of vasopressin into the locus coeruleus of conscious rats. Am J Physiol 247: H675-H681
Bliss TYP, Wendlandt S (1977) Effects of stimulation of locus coeruleus on synaptic transmission in the hippocampus. Proc XIII Cong IUPS (Abstr) 225: 81
Cedarbaum JM, Aghajanian GK (1976) Noradrenergic neurons of the locus coeruleus: inhibition by epinephrine and activation by the α-antagonist piperoxane. Brain Res 112: 413–419
Church AC (1983) Vasopressin potentiates the stimulation of cyclic AMP accumulation by norepinephrine. Peptides 4: 261–263
Crawley JN, Maas JW, Roth RH (1980) Evidence against specificity of electrical stimulation of the nucleus locus coeruleus in activating the sympathetic nervous system in the rat. Brain Res 183: 301–311
Dahl D, Winson J (1985) Action of norepinephrine in the dentate gyms. I. Stimulation of locus coeruleus. Exp Brain Res 59: 491–496
Foote SL, Aston-Jones G, Bloom FE (1980) Impulse activity of locus coeruleus in awake rats and monkey is a function of sensory stimulation and arousal. Proc Natl Acad Sci USA 77: 3033–3037
Freedman R, Hoffer BJ, Woodward DJ, Puro D (1977) Interaction of norepinephrine with cerebellar activity evoked by mossy and climbing fibers. Exp Neurol 55: 269–288
Goodchild AK, Dampney RAL, Bandler R (1982) A method for evoking physiological responses by stimulation of cell bodies, but not axons of passage, within localized regions of the central nervous system. J Neurosci Meth 6: 351–363
Gurtu S, Pant KK, Sinha JN, Bhargava KP (1984) An investigation into the mechanism of cardiovascular responses elicited by electrical stimulation of locus coeruleus and subcoeruleus in the cat. Brain Res 301: 59–64
Guyenet PG, Aghajanian GK (1979) ACh, substance P and metenkephalin in the locus coeruleus: pharmalogical evidence for independent sites of action. Eur J Pharmacol 53: 319–328
Harley CW, Lacaille JC, Milway S (1982) Potentiation of the perforant path evoked potential in the dentate gyrus by locus coeruleus stimulation. Neurosci Abstr 8: 483
Hawkins RD, Kandel ER (1984) Is there a cell biological alphabet for simple forms of learning? Psych Rev 91: 375–391
Hopkins WF, Johnston D (1984) Frequency-dependent noradrenergic modulation of long-term potentiation in the hippocampus. Science 226: 350–351
Kasamatsu T (1983) Neuronal plasticity maintained by the central norepinephrine system in the cat visual cortex. Prog Psychobiol Physiol Psychol 10: 1–112
Keller EL, Smith MJ (1983) Suppressed visual adaptation of the vestibulo-ocular reflex in catecholamine-depleted cats. Brain Res 258: 323–326
Lacaille JC, Harley CW (1985) The action of norepinephrine in the dentate gyrus: beta-mediated facilitation of evoked potentials in vitro. Brain Res 358: 210–220
Magistretti PJ, Schorderet M (1985) Norepinephrine and histamine potentiate the increases in cyclic adenosine 3′: 5′-monophosphate elicited by vasoactive intestinal polypeptide in mouse cerebral cortical slices: mediation by an adrenergic and H-histaminergic receptor. J Neurosci 5: 362–368
Michael AJ, Waterhouse BD, Woodward DJ (1983) D-amphetamine produces long-lasting potentiation of Purkinje cell response to iontophoretically applied gamma-aminobutyric acid. Neurosci Abstr 9: 1145
Moises HC, Woodward DJ, Hoffer BJ, Freedman R (1979) Interactions of norepinephrine with Purkinje cell responses to putative amino acid neurotransmitters applied by microiontophoresis. Exp Neurol 64: 493–515
Mueller AL, Hoffer BJ, Dunwiddie TV (1981) Noradrenergic responses in rat hippocampus: evidence for mediation by α and β receptors in the in vitro slice. Brain Res 214: 113–126
Neuman RS, Harley CW (1983) Long-lasting potentiation of the dentate gyrus population spike by norepinephrine. Brain Res 273: 162–165
Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Academic Press, New York
Roberts DCS (1981) An evaluation of the role of noradrenaline in learning. In: Cooper SJ (ed) Theory in psychopharmacology, Vol 1. Academic Press, New York
Segal M, Bloom FE (1976) The action of norepinephrine in the rat hippocampus. IV. The effects of locus coeruleus stimulation on evoked hippocampal unit activity. Brain Res 107: 513–525
Stanton PK, Sarvey JM (1986) Blockade of norepinephrine-induced long-lasting potentiation in the hippocampal dentate gyrus by an inhibitor of protein synthesis. Brain Res 361: 276–283
Walters ET, Byrne JH (1985) Long-term enhancement produced by activity-dependent modulation of Aplysia sensory neurons. J Neurosci 5: 662–672
Ward DG, Gunn CG (1976) Locus coeruleus complex: elicitation of a pressor response and a brain stem region necessary for its occurrence. Brain Res 107: 401–406
Waterhouse BD, Azizi SA, Burne RA, Woodward DJ (1983) Interactions of norepinephrine and serotonin with visually evoked responses of simple and complex cells in area 17 of rat cortex. Neurosci Abstr 9: 1001
Waterhouse BD, Moises HC, Woodward DJ (1981) Alpha-receptor-mediated facilitation of somatosensory cortical neuronal responses to excitatory synaptic inputs and iontophoretically applied acetylcholine. Neuropharmacology 20: 907–920
Waterhouse BD, Moises HC, Yen HH, Woodward DJ (1982) Norepinephrine enhancement of inhibitory synaptic mechanisms in cerebellum and cerebral cortex: mediation by beta adrenergic receptors. J Pharmacol Exp Ther 221: 495–506
Waterhouse BD, Woodward DJ (1980) Interaction of norepinephrine with cerebrocortical activity evoked by stimulation of somatosensory afferent pathways in the rat. Exp Neurol 67: 11–34
Watson M, McElligott JG (1984) Cerebellar norepinephrine depletion and impaired acquisition of specific locomotor tasks in rats. Brain Res 296: 129–138
Welzl H, Tolle TR, Huston JP (1985) Intracranial application of substances in the unrestrained, awake rat by pressure injection through glass micropipettes. J Neurosci Meth 13: 1–8
Winson J, Abzug C (1978) Neuronal transmission through hippocampal pathways dependent on behavior. J Neurophysiol 41: 716–732
Winson J, Dahl D (1985) Action of norepinephrine in the dentate gyrus. II. Iontophoretic studies. Exp Brain Res 59: 497–506
Woodward DJ, Moises HC, Waterhouse BD, Hoffer BJ, Freedman R (1979) Modulatory actions of norepinephrine in the central nervous system. Fed Proc 38: 2109–2116
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Harley, C.W., Milway, J.S. Glutamate ejection in the locus coeruleus enhances the perforant path-evoked population spike in the dentate gyrus. Exp Brain Res 63, 143–150 (1986). https://doi.org/10.1007/BF00235656
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DOI: https://doi.org/10.1007/BF00235656