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J Neurophysiol (March 1, 2003). 10.1152/jn.00914.2002
Submitted on Submitted 11 October 2002; accepted in final form 1 November 2002
Department of Physiology, Queen's University, Kingston, Ontario K7L 3N6, Canada
Latchford, Kevin J. and
Alastair V. Ferguson.
Angiotensin II Activates a Nitric-Oxide-Driven Inhibitory
Feedback in the Rat Paraventricular Nucleus. J. Neurophysiol. 89: 1238-1244, 2003. The hypothalamic
paraventricular nucleus (PVN) has been shown to play major obligatory
roles in autonomic and neuroendocrine regulation. Angiotensin II (ANG)
acts as a neurotransmitter regulating the excitability of magnocellular
neurons in this nucleus. We report here that ANG also activates a
nitric-oxide-mediated negative feedback loop in the PVN that acts to
regulate the functional output of magnocellular neurons. Thus in
addition to its depolarizing actions on magnocellular neurons, ANG
application results in an increase in the frequency of inhibitory
postsynaptic potentials in a population of these neurons without effect
on the amplitude of these events. ANG was also without significant
effect on the mean frequency or amplitude of mini synaptic currents
analyzed in voltage-clamp experiments. This increase in inhibitory
input after ANG can be abolished by the nitric oxide synthase inhibitor N
-nitro-L-arginine methylester, demonstrating a
requisite role for nitric oxide in the activation of this pathway. The
depolarization of magnocellular neurons that show increased inhibitory
postsynaptic potential (IPSP) frequency in response to ANG is
significantly smaller than that observed in neurons in which IPSPs
frequency was unaffected (3.2 ± 1.1 vs. 8.0 ± 0.5mV,
P < 0.05). Correspondingly, after nitric oxide
synthase inhibition, the depolarizing effects of ANG on magnocellular
neurons are augmented (2.0 ± 0.7 vs. 6.7 ± 0.7mV,
P < 0.05). The depolarization was also enhanced in the presence of the GABAergic antagonist bicuculline (1.9 ± 1.2 vs. 11.9 ± 2.3, P < 0.001). These data demonstrate
that there exists within the PVN an intrinsic negative feedback loop
that modulates neuronal excitability in response to peptidergic excitation.
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