Journal of Neuroscience, Vol 6, 613-619, Copyright © 1986 by Society for Neuroscience
Stimulation of the lateral habenula inhibits dopamine-containing neurons in the substantia nigra and ventral tegmental area of the rat
GR Christoph, RJ Leonzio and KS Wilcox
Neurons in the lateral habenula (LHb) of rats have efferent projections
that terminate in the substantia nigra pars compacta (SNC) and ventral
tegmental area (VTA), where cell bodies of dopamine-containing neurons are
located. In order to study the influence of the habenula on dopaminergic
activity, single-cell electrophysiological techniques were used to record
unit discharge of dopamine-containing neurons in the SNC and VTA during
electrical stimulation of the LHb or adjacent structures.
Dopamine-containing neurons in the SNC and VTA were identified by their
characteristic spike duration (greater than 2 msec), discharge rate (2-8
spikes/sec), and irregular firing pattern. Analysis of peristimulus time
histograms showed that 85% of SNC cells and 91% of VTA neurons were
inhibited after single pulse stimulation (0.25 mA, 0.1 msec) of the LHb.
The mean time between stimulation and onset of inhibition was 11 msec
(range, 2-22 msec) and mean duration of maximal suppression was 76 msec
(range, 20-250 msec). Stimulation of structures adjacent to the LHb
(hippocampus, lateral thalamus, medial dorsal thalamus, medial habenula)
had little or no effect. Destruction of the fasciculus retroflexus, the
fiber pathway that contains most habenular efferents, blocked the
stimulation effects on dopamine- containing neurons. Destruction of the
stria medullaris, which contains most habenular afferents, did not alter
the inhibitory effect of habenular stimulation. Injection of a cytotoxin,
kainic acid, in the LHb 1 week before recording sessions blocked the
inhibitory consequences of habenular stimulation. These experiments show
that activation of neuronal perikarya in the LHb causes orthodromic
inhibition of dopamine-containing neurons in SNC and VTA via the fasciculus
retroflexus.
