Cerebral Cortex, Vol 8, 321-345, Copyright © 1998 by Oxford University Press
SM Williams and PS Goldman-Rakic
The dopaminergic innervation of the frontal cortex, commonly implicated in
psychiatric and neurological disorders, has traditionally been associated
with a circumscribed midline group of ventral tegmental area (VTA) neurons.
We have employed a combination of retrograde tracing, using fluorescent
dyes, and tyrosine hydroxylase (TH) immunohistochemistry to amplify
knowledge of frontal cortex-projecting dopamine (DA) neurons in non-human
primates. Injections of retrograde fluorochromes were made in areas 46,
8B/6M, 12, 4, 24, and the prelimbic (PL) and infralimbic areas (IL) of the
rhesus monkey. The mesencephalic distribution of neurons exhibiting both
retrograde labeling and TH immunoreactivity or retrograde labeling alone
was examined from the level of the mammillary bodies to the locus
coeruleus. DA afferents innervating the macaque frontal cortex as a whole
originate from an unexpectedly widespread continuum of neurons distributed
in the dorsal aspects of all three of the mesencephalic DA cell groups [A9,
A10 and A8; generally corresponding to the DA cells of the substantia nigra
(SN), VTA, and the retrorubral area (RRA) respectively]. A large number of
these retrogradely labeled neurons are non-dopaminergic. The dorsal frontal
cortex (areas 46, BB/6M and 4) receive DA projections primarily from the
full medial-lateral extent of A9 cells dorsal to the SN pars compacta (i.e.
A9 dorsalis), the RRA and to a lesser extent from the A10 parabrachial
pigmented nucleus (PBPG) and linear nuclei, the latter of which have been
associated with the mesocortical DA system. In contrast, the ventromedial
PL and IL exhibit a significantly more robust input from the PBPG and
midline linear VTA nuclei than from the lateral groups. The anterior
cingulate cortex (area 24) is innervated by a group of DA neurons primarily
located between these laterally and medially concentrated populations.
These findings demonstrate a degree of compartmentalization of the
mesofrontal DA system in primates, and suggest that this projection should
no longer be viewed as a unitary midline system.
ARTICLES
Widespread origin of the primate mesofrontal dopamine system
Section of Neurobiology, Yale University School of Medicine, New Haven, CT 06510, USA.
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