Serotonergic modulation of neurotransmission in the rat basolateral amygdala

Serotonergic modulation of neurotransmission in the rat basolateral amygdal a. J. Neurophysiol. 82. 69-85, 1999. Whole cell patch-clamp recordings were obtained from projection neurons and interneurons of the rat basolateral a mygdala (BLA) to understand local network interactions in morphologically i dentified neurons and their modulation by serotonin. Projection neurons and interneurons were characterized morphologically and electrophysiologically according to their intrinsic membrane properties and synaptic characterist ics. Syn aptic activity in projection neurons was dominated by spontaneous inhibitory postsynaptic currents (IPSCs) that were multiphasic, reached 181 +/- 38 pA in amplitude, lasted 296 +/- 27 mS, and were blocked by the GABA (A) receptor antagonist, bicuculline methiodide (30 mu M). In interneurons, spontaneous synaptic activity was characterized by a burst-firing discharg e patterns (200 +/- 40 Hz) that correlated with the occurrence of 6-cyano-7 -nitroquinoxaline-2,3-dione-sensitive high-amplitude (260 +/- 42 pA), long- duration (139 +/- 19 mS) inward excitatory postsynaptic currents (EPSCs). T he interevent interval of 831 +/- 344 mS for compound inhibitory postsynapt ic potentials (IPSPs), and 916 +/- 270 mS for EPSC bursts, suggested that s pontaneous IPSP/Cs in projection neurons are driven by burst of action pote ntials in interneurons. Hence, BLA interneurons may regulate the excitabili ty of projection neurons and thus determine the degree of synchrony within ensembles of BLA neurons. In interneurons 5-hydroxytryptamine oxalate (5-HT ) evoked a direct, dose-dependent. membrane depolarization mediated by a 45 +/- 6.9 pA inward current, which had a reversal potential of -90 mV. The e ffect of 5-HT was mimicked by the 5-HT2 receptor agonist, alpha-methyl-5-hy droxytryptamine (alpha-methyl-5-HT), but not by the 5-HT1A receptor agonist , (+/-) 8-hydroxydipropylaminotetralin hydrobromide (8-QH-DPAT), or the 5-H T1B agonist, CGS 12066A. In projection neurons, 5-HT evoked an indirect mem brane hyperpolarization (similar to 2 mV) that was associated with a 75 +/- 42 pA outward current and had a reversal potential of -70 mV. The response was independent of 5-HT concentration, blocked;ed by TTX, mimicked by alph a-methyl-5-HT but nut by 8-OH-DPAT. In interneurons, 5-HT reduced the ampli tude of the evoked EPSC and in the presence of TTX (0.6 mu M) reduced the f requency of miniature EPSCs but not their quantal content. In projection ne urons, 5-HT also caused a dose-dependent reduction in the amplitude of stim ulus evoked EPSCs and IPSCs. These results suggest that acute serotonin rel ease would directly activate GABAergic interneurons of the BLA, via an acti vation of 5-HT2 receptors, and increase the frequency of inhibitory synapti c events in projection neurons. Chronic serotonin release, or high levels o f serotonin, would reduce the excitatory drive onto interneurons and may ac t as a feedback mechanism to prevent excess inhibition within the nucleus.