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GABA_B Receptor Modulation of Rapid Inhibitory and Excitatory Neurotransmission From Subfornical Organ and Other Afferents to Median Preoptic Nucleus Neurons

¹Neuroscience Program, Ottawa Health Research Institute and University of Ottawa, Ottawa, Ontario K1Y 4E9; and ²Department of Physiology and Pharmacology, University of Western Ontario, London, Ontario N6A 5C1, Canada

Submitted 6 January 2004; accepted in final form 12 February 2004

Cardiovascular and behavioral responses to circulating angiotensin require intact connectivity along the upper lamina terminalis joining the subfornical organ (SFO) with the median preoptic nucleus (MnPO). Whole cell patch-clamp recordings in sagittal rat brain slice preparations revealed that 28/40 MnPO neurons responded to electrical stimulation of SFO efferents with bicuculline-sensitive GABA_A receptor-mediated inhibition and glutamate-mediated postsynaptic excitation involving AMPA and N-methyl-D-aspartate (NMDA) receptor subtypes, blockable with 2,3-dioxo-6nitro-1, 2,3,4-tetrahydrobenzo [f] quinoxaline-7-sulfoamide disodium (NBQX) and D-2-amino-4-phosphonovaleric acid (D-APV), respectively. Bath applications of baclofen induced a concentration-dependent (0.3–10 µM) reduction in these SFO-evoked postsynaptic currents, attenuation of SFO-evoked paired-pulse depression, and reduction in frequency (but not amplitude) of miniature postsynaptic currents, consistent with an action at presynaptic GABA_B receptors. Baclofen's effects on miniature currents lacked sensitivity to barium, -conotoxin GVIA, and cadmium. Acting at postsynaptic GABA_B receptors, baclofen hyperpolarized a majority of MnPO neurons by increasing a G protein–coupled inwardly rectifying potassium conductance and suppressing an N-type high-voltage–activated calcium conductance. The latter contributed to reduction in action potential afterhyperpolarization and enhanced cell firing and spike frequency adaptation when tested with a depolarizing stimulus. All baclofen-induced effects were blockable with CGP52432 CGP52432alone had no significant effect on SFO-evoked postsynaptic current amplitudes or paired-pulse ratios, but did induce an increase in miniature inhibitory postsynaptic current (mIPSC) frequency in 2/4 cells tested, indicating that ambient levels of GABA could activate presynaptic GABA_B receptors on undefined inputs. These observations indicate that MnPO neurons receive both a GABAergic and glutamatergic innervation from SFO. Both forms of rapid neurotransmission are subject to modulation via pre- and postsynaptic GABA_B receptors.

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