Abstract
The medial septal area of conscious rats was stimulated through previously implanted electrodes at a frequency of 7.7 Hz for 20 min each day for 7 days to evoke rhythmic slow activity in CA1 at a similar frequency to spontaneous theta. Two weeks later in the anaesthetized rats the effects of a single subcutaneous injection of nicotine (0.4 mg/kg) on fEPSPs, evoked in the dentate gyrus by separate stimulation of the MPP and LPP, were studied and compared with those obtained in controls. Nicotine increased the firing of locus coeruleus neurons and the slope of the fEPSPs evoked by LPP stimulation, but not by MPP stimulation. Prior theta driving considerably increased the effect of nicotine on the responses evoked by stimulation of the MPP and abolished the nicotine-induced potentiation of the responses evoked by stimulation of the LPP. The results are attributed to theta driving increasing the amount of noradrenaline released by nicotine and to noradrenaline producing a β-adrenoceptor long-lasting potentiation at the medial perforant path synapse and a long-lasting depression at the lateral perforant path synapse.
Similar content being viewed by others
References
W. C. Abraham and N. McNaughton, “Differences in synaptic transmission between medial and lateral components of the perforant path,” Brain Res., 303, 251–260 (1984).
T. V. P. Bliss and G. L. Collingridge, “A synaptic model of memory: long-term potentiation in the hippocampus,” Nature, 361, 31–39 (1993).
C. R. Bramham, K. Bacher-Svendsen, and J. M. Sarvey, “LTP in the lateral perforant path is beta-adrenergic receptor-dependent,” Neuroreport, 8, 719–724 (1997).
M. P. Brazell, S. N. Mitchell, and J. A. Gray “Effect of acute administration of nicotine on in vivo release of noradrenaline in the hippocampus of freely moving rats: a dose-response and antagonist study,” Neuropharmacology, 30, 823–833 (1991).
J. M. Cedarbaum and G. K. Aghajanian, “Afferent projections to the rat locus coeruleus as determined by a retrograde tracing technique,” J. Comp. Neurol., 178, 1–16 (1978).
P. C. Chaulk and C. W. Harley, “Intracerebroventricular norepinephrine potentiation of the perforant path-evoked potential in dentate gyrus of anesthetized and awake rats: A role for both alpha-and beta-adrenoceptor activation,” Brain Res., 787, 59–70 (1998).
Z. Chen and G. Engberg, “The rat nucleus paragigantocellularis as a relay station to mediate peripherally induced central effects of nicotine,” Neurosci. Lett., 101, 67–71 (1989).
D. Dahl and J. M. Sarvey, “Norepinephrine induces pathway-specific long-lasting potentiation and depression in the hippocampal dentate gyrus,” Proc. Natl. Acad. Sci., USA, 86, 4776–4780 (1989).
V. Doyere, B. Srebro, and S. Laroche, “Heterosynaptic LTD and depotentiation in the medial perforant path of the dentate gyrus in the freely moving rat,” J. Neurophysiol., 77, No. 2, 571–578 (1997).
S. M. Florin-Lechner, J. P. Druhan, G. Aston-Jones, and R. J. Valentino, “Enhanced norepinephrine release in prefrontal cortex with burst stimulation of the locus coeruleus,” Brain Res., 742, 89–97 (1996).
S. Fujii, Z. Ji, N. Morita, and K. Sumikawa, “Acute and chronic nicotine exposure differentially facilitate the induction of LTP,” Brain Res., 846, 137–143 (1999).
A. A. Grace and B. S. Bunney, “The control of firing pattern in nigral dopamine neurons: burst firing,” J. Neurosci., 4, 2877–2890 (1984).
S. Graham-Jones, L. Holt, J. A. Gray, and M. Fillenz, “Low-frequency septal stimulation increases tyrosine hydroxylase activity in the hippocampus,” Pharmacol. Biochem. Behav., 23, 489–493 (1985).
R. Gray and D. Johnston, “Noradrenaline and β-adrenoceptor agonists increase activity of voltage-dependent calcium channels in hippocampal neurons,” Nature, 327, 620–623 (1987).
R. Gray, A. S. Rajan, K. A. Radcliffe, M. Yakehiro, and J. A. Dani, “Hippocampal synaptic transmission enhanced by low concentrations of nicotine,” Nature, 383, 713–716 (1996).
G. A. Grigoryan and J. A. Gray, “A single dose of nicotine proactively enhances the partial reinforcement extinction effect in the rat,” Psychobiology, 24, 136–146 (1996).
H. L. Haas and G. M. Rose, “Noradrenaline blocks potassium conductance in rat dentate granule cells in vitro,” Neurosci. Lett., 78, 171–174 (1987).
S. Hamid, G. S. Dawe, J. A. Gray, and J. D. Stephenson, “Nicotine induces long-lasting potentiation in the dentate gyrus of nicotine-primed rats,” Neurosci. Res., 29, 81–85 (1997).
R. Kramis, C. H. Vanderwolf, and B. H. Bland, “Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital, ” Exp. Neurol., 49, 58–85 (1975)
T. A. Macek, D. G. Winder, R. W. Gereau, C. O. Ladd, and P. J. Conn, “Differential involvement of group II and group III mGluRs as autoreceptors at lateral and medial perforant path synapses,” J. Neurophysiol., 76, 3798–3806 (1996).
L. Maggi, E. Sola, F. Minneci, et al., “Persistent decrease in synaptic efficacy induced by nicotine at Schaffer collateral-CA1 synapses in the immature rat hippocampus,” J. Physiol., 559, No. 3, 863–874 (2004).
B. L. McNaughton, “Evidence for two physiological distinct perforant pathways to the fascia dentate, ” Brain Res., 199, 1–19 (1980).
T. A Milner, P. Shah, and J. P. Pierce, “Beta-adrenergic receptors primarily are located on the dendrites of granule cells and interneurons but also are found on astrocytes and a few presynaptic profiles in the rat dentate gyrus,” Synapse, 36, 178–193 (2000).
S. N. Mitchel, K. M. Smith, M. H. Joseph, and J. A. Gray, “Increases in tyrosine hydroxylase messenger RNA in the locus coeruleus after a single dose of nicotine are followed by time-dependent increases in enzyme activity and noradrenaline release,” Neuroscience, 56, 989–997 (1993).
R. S. Neuman, and C. W. Harley, “Long-lasting potentiation of the dentate gyrus population spike by norepinephrine,” Brain Res., 273, 162–165 (1983).
R. A. Nicoll and R. C. Malenka, “Contrasting properties of two forms of long-term potentiation in the hippocampus,” Nature, 377, 115–118 (1995).
W. X. Pan and N. McNaughton, “The medial supramammillary nucleus, spatial learning and the frequency of hippocampal theta activity,” Brain Res., 764, 101–108 (1997).
G. Paxinos and C. Watson, The Rat Brain in Stereotaxic Coordinates, Acad. Press, New York, London (1986).
M. Snape, G. Grigoryan, J. D. Sinden, and J. A. Gray, “Dependence of the proactive behavioural effects of theta-driving septal stimulation upon stimulation frequency and behavioural experience. II Continuously and partially reinforced running,” Psychobiology, 24, 22–32 (1996).
C. S. Tung, L. Ugedo, J. Grenhoff, G. Engberg, and T. H. Svensson, “Peripheral induction of burst firing in locus coeruleus neurons by nicotine mediated via excitatory amino acids,” Synapse, 4, 313–318 (1989).
Author information
Authors and Affiliations
Additional information
Published in Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 56, No. 2, pp. 257–263, March–April, 2006.
Rights and permissions
About this article
Cite this article
Markevich, V.A., Grigoryan, G.A., Dawe, G.S. et al. Theta driving both inhibits and potentiates the effects of nicotine on dentate gyrus responses. Neurosci Behav Physiol 37, 403–409 (2007). https://doi.org/10.1007/s11055-007-0027-2
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11055-007-0027-2