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The Journal of Neurophysiology Vol. 83 No. 4 April 2000, pp. 1796-1808
Copyright ©2000 by the American Physiological Society
Departments of Neuroscience and Psychiatry, Center for Neuroscience, University of Pittsburgh, Pittsburgh, Pennsylvania 15260
West, Anthony R. and
Anthony A. Grace.
Striatal Nitric Oxide Signaling Regulates the Neuronal Activity
of Midbrain Dopamine Neurons In Vivo. J. Neurophysiol. 83: 1796-1808, 2000. A major component of the
cortical regulation of the nigrostriatal dopamine (DA) system is known
to occur via activation of striatal efferent systems projecting to the
substantia nigra. The potential intermediary role of striatal nitric
oxide synthase (NOS)-containing interneurons in modulating the efferent
regulation of DA neuron activity was examined using single-unit
recordings of DA neurons performed concurrently with striatal
microdialysis in anesthetized rats. The response of DA neurons recorded
in the substantia nigra to intrastriatal artificial cerebrospinal fluid (ACSF) or drug infusion was examined in terms of mean firing rate, percent of spikes fired in bursts, cells/track, and response to electrical stimulation of the orbital prefrontal cortex (oPFC) and
striatum. Intrastriatal infusion of NOS substrate concurrently with
intermittent periods of striatal and cortical stimulation increased the
mean DA cell population firing rate as compared with ACSF controls.
This effect was reproduced via intrastriatal infusion of a NO
generator. Infusion of either a NOS inhibitor or NO chelator via
reverse microdialysis did not affect basal firing rate but increased
the percentage of DA neurons responding to striatal stimulation with an
initial inhibition followed by a rebound excitation (IE response) from
40 to 74%. NO scavenger infusion also markedly decreased the
stimulation intensity required to elicit an IE response to electrical
stimulation of the striatum. In single neurons in which the effects of
electrical stimulation were observed before and after drug delivery, NO
antagonist infusion was observed to decrease the onset latency and
extend the duration of the initial inhibitory phase induced by either
oPFC or striatal stimulation. This is the first report showing that
striatal NO tone regulates the basal activity and responsiveness of DA
neurons to cortical and striatal inputs. These studies also indicate
that striatal NO signaling may play an important role in the
integration of information transmitted to basal ganglia output centers
via corticostriatal and striatal efferent pathways.
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