Network and intrinsic contributions to carbachol-induced oscillations in the rat subiculum.
Low-frequency network oscillations occur in several areas of the limbic system where they contribute to synaptic plasticity and mnemonic functions that are in turn modulated by cholinergic mechanisms. Here we used slices of the rat subiculum (a limbic area involved in cognitive functions) to establish how network and single neuron (intrinsic) membrane mechanisms participate to the rhythmic oscillations elicited by the cholinergic agent carbachol (CCh, 50-100 microM). We have found that CCh-induced network oscillations (intraoscillatory frequency = 5-16 Hz) are abolished by an antagonist of non-N-methyl-D-aspartate (NMDA) glutamatergic receptors (n = 6 slices) but persist during blockade of GABA receptors (n = 16). In addition, during application of glutamate and GABA receptor antagonists, single subicular cells generate burst oscillations at 2.1-6.8 Hz when depolarized with steady current injection. These intrinsic burst oscillations disappear during application of a Ca(2+) channel blocker (n = 6 cells), intracellular Ca(2+) chelation (n = 6), or replacement of extracellular Na(+) (n = 4) but persist in recordings made with electrodes containing a blocker of voltage-gated Na(+) channels (n = 7). These procedures cause similar effects on CCh-induced depolarizing plateau potentials that are contributed by a Ca(2+)-activated nonselective cationic conductance (I(CAN)). Network and intrinsic oscillations along with depolarizing plateau potentials were abolished by the muscarinic receptor antagonist atropine. In conclusion, our findings demonstrate that low-frequency oscillations in the rat subiculum rely on the muscarinic receptor-dependent activation of an intrinsic oscillatory mechanism that is presumably contributed by I(CAN) and are integrated within the network via non-NMDA receptor-mediated transmission.
D'Antuono
M
M
Montreal Neurological Institute, Department of Neurology and Neurosurgery, McGill University, Montreal, Quebec H3A 2B4, Canada.
Kawasaki
H
H
Palmieri
C
C
Avoli
M
M
D018750:6-Cyano-7-nitroquinoxaline-2,3-dione / Q000494:pharmacology; D000200:Action Potentials / Q000187:drug effects / Q000502:physiology; D000818:Animals; D001285:Atropine / Q000494:pharmacology; D001640:Bicuculline / Q000031:analogs & derivatives* / Q000494:pharmacology; D002217:Carbachol / Q000494:pharmacology*; D002614:Chelating Agents / Q000494:pharmacology; D018679:Cholinergic Agonists / Q000494:pharmacology*; D004533:Egtazic Acid / Q000031:analogs & derivatives* / Q000494:pharmacology; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D018756:GABA Antagonists / Q000494:pharmacology; D006624:Hippocampus / Q000166:cytology* / Q000502:physiology*; D008297:Male; D018727:Muscarinic Antagonists / Q000494:pharmacology; D009434:Neural Pathways / Q000502:physiology*; D009943:Organophosphorus Compounds / Q000494:pharmacology; D010507:Periodicity; D010852:Picrotoxin / Q000494:pharmacology; D010879:Piperazines / Q000494:pharmacology; D051381:Rats; D017207:Rats, Sprague-Dawley; D017470:Receptors, Glutamate / Q000502:physiology
D018750:6-Cyano-7-nitroquinoxaline-2,3-dione; D001285:Atropine; D001640:Bicuculline; D002217:Carbachol; D002614:Chelating Agents; D018679:Cholinergic Agonists; D004533:Egtazic Acid; D018691:Excitatory Amino Acid Antagonists; D018756:GABA Antagonists; D018727:Muscarinic Antagonists; D009943:Organophosphorus Compounds; D010852:Picrotoxin; D010879:Piperazines; D017470:Receptors, Glutamate; C017069:bicuculline methiodide; C066430:CGP 35348; C050592:3-(2-carboxypiperazin-4-yl)propyl-1-phosphonic acid; C025603:1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid