Journal of Neuroscience, Vol 12, 2079-2103, Copyright © 1992 by Society for Neuroscience
Compartmental distribution of ventral striatal neurons projecting to the mesencephalon in the rat
HW Berendse, HJ Groenewegen and AH Lohman
Department of Anatomy and Embryology, Vrije Universiteit, Amsterdam, The Netherlands.
The ventral striatum is characterized by an intricate neurochemical
compartmentation that is reflected in the distribution of most of its
afferent fiber systems. In the present study, the compartmental
relationships of ventral striatal neurons projecting to the mesencephalon
were studied by combining tract tracing with the immunohistochemical
localization of leu-enkephalin. Injections of the retrograde tracer cholera
toxin subunit B were placed at various sites in the ventral mesencephalon.
The anterograde tracer Phaseolus vulgaris leucoagglutinin was injected in
single compartments in the rostrolateral part of the nucleus accumbens. The
projections from the ventral striatum to the dopaminergic cell groups in
the ventral mesencephalon and those to the substantia nigra pars reticulata
originate from distinct subpopulations of ventral striatal neurons that
respect neurochemically defined compartmental boundaries. In the "shell" of
the nucleus accumbens, neurons that project to the dopaminergic cell groups
are located outside areas of high cell density and weak enkephalin
immunoreactivity (ENK-IR). Rostrolaterally in the "core" of the nucleus
accumbens, neurons inside large areas of strong ENK-IR surrounding the
anterior commissure project to the dorsomedial part of the substantia nigra
pars reticulata, whereas neurons outside these areas innervate the ventral
tegmental area and/or the medial part of the substantia nigra pars
compacta. By contrast, more caudally in the dorsal part of the nucleus
accumbens and in the ventral part of the caudate-putamen, the relationships
are reversed: neurons in- or outside small patches of strong ENK-IR project
respectively to the pars compacta or the pars reticulata of the substantia
nigra. Since the thalamic and cortical afferents of the ventral striatum
are compartmentally ordered as well, the present results imply that through
the ventral striatal compartments information from disparate combinations
of cortical and thalamic sources may be conveyed to distinct mesencephalic
targets. The component of the ventral striatomesencephalic system reaching
the dopaminergic cell groups A10, A9, and A8 may modulate the dopaminergic
input to virtually the entire striatum. The other component can, by way of
the pars reticulata of the substantia nigra, participate in nigrothalamic
and nigrotectal output pathways of the basal ganglia.