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The Journal of Neuroscience, October 1, 1998, 18(19):8003-8015
Electrophysiological Characterization of GABAergic Neurons in the
Ventral Tegmental Area
Scott C.
Steffensen1,
Adena L.
Svingos2,
Virginia
M.
Pickel2, and
Steven J.
Henriksen1
1 The Scripps Research Institute, La Jolla, California
92037, and 2 Cornell University Medical College, New
York, New York 10021
GABAergic neurons in the ventral tegmental area (VTA) play a
primary role in local inhibition of mesocorticolimbic dopamine (DA)
neurons but are not physiologically or anatomically well characterized.
We used in vivo extracellular and intracellular recordings in the rat VTA to identify a homogeneous population of
neurons that were distinguished from DA neurons by their rapid-firing, nonbursting activity (19.1 ± 1.4 Hz), short-duration action
potentials (310 ± 10 µsec), EPSP-dependent spontaneous spikes,
and lack of spike accommodation to depolarizing current pulses. These
non-DA neurons were activated both antidromically and orthodromically by stimulation of the internal capsule (IC; conduction velocity, 2.4 ± 0.2 m/sec; refractory period, 0.6 ± 0.1 msec) and
were inhibited by stimulation of the nucleus accumbens septi (NAcc).
Their firing rate was moderately reduced, and their IC-driven activity
was suppressed by microelectrophoretic application or systemic
administration of NMDA receptor antagonists. VTA non-DA neurons were
recorded intracellularly and showed relatively depolarized resting
membrane potentials ( 61.9 ± 1.8 mV) and small action potentials
(68.3 ± 2.1 mV). They were injected with neurobiotin and shown by
light microscopic immunocytochemistry to be multipolar cells and by electron microscopy to contain GABA but not the
catecholamine-synthesizing enzyme tyrosine hydroxylase (TH).
Neurobiotin-filled dendrites containing GABA received asymmetric
excitatory-type synapses from unlabeled terminals and symmetric
synapses from terminals that also contained GABA. These findings
indicate that VTA non-DA neurons are GABAergic, project to the cortex,
and are controlled, in part, by a physiologically relevant NMDA
receptor-mediated input from cortical structures and by GABAergic
inhibition.
Key words:
ventral tegmental area; nondopamine; intracellular; immunocytochemistry; GABA; neurobiotin; refractory period; superexcitability
Copyright © 1998 Society for Neuroscience 0270-6474/98/18198003-13$05.00/0
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