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Volume 16, Number 23, Issue of December 1, 1996 pp. 7566-7573
Copyright ©1996 Society for Neuroscience

Differential Actions of Serotonin, Mediated by 5-HT_1B and 5-HT_2C Receptors, on GABA-Mediated Synaptic Input to Rat Substantia Nigra Pars Reticulata Neurons In Vitro

Received Aug. 1, 1996; revised Sept. 11, 1996; accepted Sept. 30, 1996.

Ian M. Stanford and Michael G. Lacey

Department of Pharmacology, The Medical School, University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom

The ability of serotonin to modulate GABA-mediated synaptic input to substantia nigra pars reticulata (SNr) neurons was investigated with the use of whole-cell patch-clamp recording from slices of rat midbrain. Fast evoked GABA_A receptor-mediated synaptic currents (IPSCs) were attenuated reversibly ~60% by serotonin, which also caused an inward current with reversal potential of 25 mV. This inward current was blocked by the 5-HT₂ receptor antagonist ritanserin, whereas the IPSC depression was blocked by the 5-HT_1B receptor antagonist pindolol. The amplitude ratio of IPSC pairs (50 msec interpulse interval) was enhanced by serotonin (in ritanserin) and also by the GABA_B receptor agonist baclofen (which also depressed the IPSC), consistent with a presynaptic site of action in both cases. In contrast, spontaneous tetrodotoxin-sensitive GABA_A synaptic currents (sIPSCs) were increased in frequency by serotonin (an action that was sensitive to ritanserin, but not pindolol) but reduced in frequency by baclofen. SNr neurons therefore receive inhibitory synaptic input mediated by GABA_A receptors from at least two distinct sources. One, probably originating from the striatum, may be depressed via presynaptic 5-HT_1B and GABA_B receptors. The second is likely to arise from axon collaterals of SNr neurons themselves and is facilitated by an increase in firing via postsynaptic, somatodendritic 5-HT_2C receptor activation, but it is depressed by GABA_B receptor activation. Thus, serotonin can both depolarize and disinhibit SNr neurons via 5-HT_2C and 5-HT_1B receptors, respectively, but excitation may be limited by GABA released from axon collaterals.

Key words: serotonin; substantia nigra pars reticulata; GABA_A IPSPs; presynaptic receptors; baclofen; basal ganglia

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