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The Journal of Neurophysiology Vol. 82 No. 2 August 1999, pp. 925-933
Copyright ©1999 by the American Physiological Society
Center for Molecular and Behavioral Neuroscience, Program in Cellular and Molecular Biodynamics, Rutgers, The State University of New Jersey, Newark, New Jersey 07102
Iribe, Yuji,
Kevin Moore,
Kevin C. H. Pang, and
James M. Tepper.
Subthalamic Stimulation-Induced Synaptic Responses in Substantia
Nigra Pars Compacta Dopaminergic Neurons In Vitro. J. Neurophysiol. 82: 925-933, 1999. The subthalamic
nucleus (STN) is one of the principal sources of excitatory
glutamatergic input to dopaminergic neurons of the substantia nigra,
yet stimulation of the STN produces both excitatory and inhibitory
effects on nigral dopaminergic neurons recorded extracellularly in
vivo. The present experiments were designed to determine the sources of
the excitatory and inhibitory effects. Synaptic potentials were
recorded intracellularly from substantia nigra pars compacta
dopaminergic neurons in parasagittal slices in response to stimulation
of the STN. Synaptic potentials were analyzed for onset latency,
amplitude, duration, and reversal potential in the presence and absence
of GABA and glutamate receptor antagonists. STN-evoked depolarizing
synaptic responses in dopaminergic neurons reversed at approximately
31 mV, intermediate between the expected reversal potential for an
excitatory and an inhibitory postsynaptic potential (EPSP and IPSP).
Blockade of GABAA receptors with bicuculline caused a
positive shift in the reversal potential to near 0 mV, suggesting that
STN stimulation evoked a near simultaneous EPSP and IPSP. Both synaptic
responses were blocked by application of the glutamate receptor
antagonist, 6-cyano-7-nitroquinoxalene-2,3-dione. The confounding
influence of inhibitory fibers of passage from globus pallidus and/or
striatum by STN stimulation was eliminated by unilaterally transecting
striatonigral and pallidonigral fibers 3 days before recording. The
reversal potential of STN-evoked synaptic responses in dopaminergic
neurons in slices from transected animals was approximately 30 mV.
Bath application of bicuculline shifted the reversal potential to ~5
mV as it did in intact animals, suggesting that the source of the IPSP
was within substantia nigra. These data indicate that electrical
stimulation of the STN elicits a mixed EPSP-IPSP in nigral dopaminergic
neurons due to the coactivation of an excitatory monosynaptic and an
inhibitory polysynaptic connection between the STN and the dopaminergic
neurons of substantia nigra pars compacta. The EPSP arises from a
direct monosynaptic excitatory glutamatergic input from the STN. The
IPSP arises polysynaptically, most likely through STN-evoked excitation
of GABAergic neurons in substantia nigra pars reticulata, which
produces feed-forward GABAA-mediated inhibition of
dopaminergic neurons through inhibitory intranigral axon collaterals.
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