Simultaneous recording of substantia nigra neurons and voltammetric release of dopamine in the caudate of behaving cats

doi:10.1016/0361-9230(85)90140-6

Brain Research Bulletin

Volume 15, Issue 2, August 1985, Pages 221-223

https://doi.org/10.1016/0361-9230(85)90140-6 Get rights and content

Abstract

Simultaneous electrophysiological recordings of single dopamine-containing neurons in the pars compacta of the substantia nigra and the voltammetric release of dopamine in the caudate were made in the behaving cat. Unit activity showed no significant changes during sleep and small changes during active waking, while the release of dopamine in post-synaptic target regions of the caudate nucleus decreased by approximately 35% during sleep and increased approximately 50% during movement. These data demonstrate that recording the electrophysiological activity of single dopamine-containing neurons alone does not accurately reflect the functional state of the central dopamine system. The present study is the first report on the simultaneous measurement of the post-synaptic release of a neurotransmitter and the electrophysiological recording of neurons identified to contain that transmitter substance.

References (22)

S.M. Antelman et al.
Tail pinch-induced eating, gnawing and licking behavior in rats: Dependence on the nigrostriatal dopamine system
Brain Res
(1975)
R.J. Beninger
The role of dopamine in locomotor activity and learning
Brain Res Rev
(1983)
A.G. Ewing et al.
In vivo voltammetry with electrodes that discriminate between dopamine and ascorbate
Brain Res
(1982)
D.C. German et al.
Electrophysiological examination of the ventral tegmental (A10) area in the rat
Brain Res
(1980)
D.C. German et al.
A system for chronic single unit recording in the behaving rat
Brain Res Bull
(1982)
J.D. Miller et al.
Activity of mesencephalic dopamine and non-dopamine neurons across stages of sleep and waking in the rat
Brain Res
(1983)
M.K. Sanghera et al.
Electrophysiological properties of mouse dopamine neurons: In vivo and in vitro studies
Neuroscience
(1984)
M.E. Trulson
Activity of dopamine-containing substantia nigra neurons in freely moving cats
Neurosci Biobehav Rev
(1985)
M.E. Trulson et al.
Effects of D-amphetamine on striatal unit activity and behavior in freely moving cats
Neuropharmacology
(1979)
M.E. Trulson et al.
Activity of substantia nigra units across the sleep waking cycle in freely moving cats
Neurosci Lett
(1981)

S. Barasi

Effect of noxious stimulation on a population of substantia nigra neurons

J Physiol (Lond)

(1978)

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Rapid communicationSimultaneous recording of substantia nigra neurons and voltammetric release of dopamine in the caudate of behaving cats

Abstract

Brain Res

Brain Res Rev

Brain Res

Brain Res

Brain Res Bull

Brain Res

Neuroscience

Neurosci Biobehav Rev

Neuropharmacology

Neurosci Lett

Effect of noxious stimulation on a population of substantia nigra neurons

J Physiol (Lond)

Rapid communication
Simultaneous recording of substantia nigra neurons and voltammetric release of dopamine in the caudate of behaving cats