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The Journal of Neurophysiology Vol. 82 No. 5 November 1999, pp. 2590-2601
Copyright ©1999 by the American Physiological Society
1Montreal Neurological Institute and Departments of Neurology and Neurosurgery and of Physiology, McGill University, Montreal, Quebec H3A 2B4 Canada; and 2Centro per l'Epilessia, Ospedale San Paolo, Università degli Studi di Milano, 20142 Milan, Italy
Kawasaki, Hiroto,
Carmela Palmieri, and
Massimo Avoli.
Muscarinic Receptor Activation Induces Depolarizing Plateau
Potentials in Bursting Neurons of the Rat Subiculum. J. Neurophysiol. 82: 2590-2601, 1999. Acetylcholine
functions as a neuromodulator in the mammalian brain by binding to
specific receptors and thus bringing about profound changes in neuronal
excitability. Activation of muscarinic receptors often results in an
increased excitability of cortical cells. It is, however, unknown
whether such an action is present in the subiculum, a limbic structure
that may be involved in cognitive processes as well as in seizure
propagation. Most rat subicular neurons are endowed of intrinsic
membrane properties that make them fire action potential bursts. Using
intracellular recordings from these bursting cells in a slice
preparation, we report here that application of the cholinergic agonist
carbachol (CCh, 30-100 µM) to medium containing ionotropic
excitatory amino acid receptor antagonists reduces
burst-afterhyperpolarizations (burst-AHPs) and discloses depolarizing
plateau potentials that outlast the triggering current pulses by
140-2,800 ms. These plateau potentials appear with CCh concentrations
>50 µM and are dependent on the resting membrane potential and on
the intensity/duration of the triggering pulse; are recorded during
application of tetrodotoxin (1 µM, n = 5 neurons); but are
markedly reduced by replacing 82% of extracellular Na+
with equimolar choline (n = 6). Plateau potentials
also are abolished by Co2+ (2 mM; n = 5) or Cd2+ (1 mM; n = 2) application
and by recording with electrodes containing the Ca2+
chelator bis(2-aminophenoxy)ethane-N,
N,N',N'-tetraacetic acid (0.2 M; n = 6).
CCh-induced burst-AHP reduction and plateau potentials are reversed by
the muscarinic antagonist atropine (0.5 µM, n = 7). In conclusion, our findings demonstrate a powerful muscarinic modulation of the intrinsic excitability of subicular bursting cells
that is predominated by the appearance of plateau potentials. These
changes in excitability may contribute to physiological processes such
as learning or memory and play a role in the generation of epileptiform
depolarizations. We propose that, as in other limbic structures,
muscarinic plateau potentials in the subiculum are mainly due to a
Ca2+-dependent nonselective cationic conductance.
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