Muscarinic responses of rat basolateral amygdaloid neurons recorded in vitro.

Abstract

SUMMARY1. Intracellular recordings were obtained from pyramidal-type neurons in the basolateral amygdaloid nucleus (BLA) in slices of rat ventral forebrain and used to compare the actions of exogenously applied cholinomimetics to the effects produced by electrical stimulation of amygdalopetal cholinergic afferents from basal forebrain.2. Bath application of carbachol depolarized pyramidal cells with an associated increase in input resistance (Ri), reduced the slow after-hyperpolarization (AHP)that followed a series of current-evoked action potentials and blocked spike frequency accommodation. All of these effects were reversed by the muscarinic antagonist atropine but not by the nicotinic antagonist hexamethonium. 3. Electrical stimulation of amygdaloid afferents within the external capsule evoked a series of synaptic potentials consisting of a non-cholinergic fast excitatory postsynaptic potential (EPSP), followed by early and late inhibitory postsynaptic potentials (IPSPs). Each of these synaptic potentials was reduced by carbachol in an atropine-sensitive manner.4. Local application of carbachol to pyramidal cells produced a short-latency hyperpolarization followed by a prolonged depolarization. The hyperpolarization and depolarization to carbachol were blocked by atropine but not hexamethonium.5. The carbachol-induced hyperpolarization was associated with a decrease in Ri and had a reversal potential nearly identical to that of the early IPSP. The inhibitory response was blocked by perfusion of medium containing tetrodotoxin (TTX), bicuculline or picrotoxin, while the subsequent depolarization was unaffected. On the basis of these data, it is concluded that the muscarinic hyperpolarization is mediated through the rapid excitation of presynaptic GABAergic interneurons in the slice.6. The findings that the carbachol-induced depolarization was associated with an increase in Ri, often had a reversal potential below -80 mV, was sensitive to changes in extracellular potassium concentration and was blocked by intracellular ionophoresis of the potassium channel blocker caesium suggest that it resulted from a muscarinic blockade of one or more potassium conductances. M. S. WASHBURN AND H. C MOISES evoked a series of fast EPSPs followed by IPSPs. These non-cholinergic potentials were followed by a slow EPSP that lasted from 10 s-4 min. The slow EPSP was enhanced by eserine and blocked by atropine. It was also blocked by TTX or cadmium, indicating that it was dependent on spike propagation and calciumdependent release of acetylcholine (ACh).8. Stimulation of cholinergic afferents in the slice mimicked other effects produced by carbachol including blockade of the slow AHP and accommodation of action potential discharge and these actions were potentiated by eserine and blocked by atropine.9. The present results provide the first demonstration of muscarinic cholinergic actions in an area of the amygdala known to receive cholinergic innervation. These effects appear to involve both direct and indirect mechanisms.

Input-specific contributions to valence processing in the amygdala

“…Studies have provided a variety of mechanisms by which signaling through muscarinic receptors in BLA neurons promotes neuronal excitability, such as the suppression of potassium currents and reduction of the slow afterhyperpolarization of action potentials (Washburn and Moises 1992;Womble and Moises 1993). In agreement with these data, long-term potentiation in the lateral amygdala was reduced by muscarinic receptor blockade.…”

A Cholinergic Synaptically Triggered Event Participates in the Generation of Persistent Activity Necessary for Eye Fixation

“…Duration and amplitude of this depolarization depend on membrane potential due to cholinergic effects on voltage-dependent K ϩ currents (i.e., an M current) (Seeger and Alzheimer, 2001) or to a K ϩ inward rectification current (Washburn and Moises, 1992). A decrease in the amplitude of the action potentials, similar to that observed in the entorhinal and prefrontal cortices, was also observed (Cantrell et al, 1996;Klink and Alonso, 1997) and was attributed to a decrease in Na ϩ conductance, resulting from the increased availability of intracellular Ca 2ϩ (Bulatko and Greeff, 1995;Klink and Alonso, 1997).…”

A Potential Cholinergic Mechanism of Procaine's Limbic Activation

“…Amygdalar neurons via muscarinic mediation have been associated with bursting phenomena (Yajeya et al, 1997), postsynaptically (Washburn and Moises, 1992) and presynaptically (Sugita et al, 1991). Bursting activity was further tied to a complement of presynaptic muscarinic receptors that were estimated to be comprised of 50% M 3 , 30% M 2 , and 20% or less M 1 , but most likely not due to the well characterized M-current (Yajeya et al, 1997).…”