Heterogeneous distribution of the limbic system-associated membrane protein in the caudate nucleus and substantia nigra of the cat

Abstract

The limbic system-associated membrane protein is a glycoprotein selectively associated, in the adult, with dendrites and cell bodies of neurons of the limbic system and related brain regions. In the present study, the distribution of the limbic system-associated membrane protein was studied by immunohistochemistry in the caudate nucleus and substantia nigra of the cat to determine how its expression relates to the compartmentalization of these areas. In all areas of the caudate nucleus, the pattern of limbic system-associated membrane protein immunoreactivity was highly heterogeneous, labeling zones that were in register with areas expressing neurochemical markers that classically identify striosomes. The extrastriosomal matrix exhibited low levels of staining. The results show that the limbic system-associated membrane protein is expressed by neurons within the target areas (striosomes) of subsets of limbic afferents (originating mainly from the basolateral nucleus of the amygdala and the prefrontal cortex), whereas regions of the caudate nucleus (extrastriosomal matrix) receiving inputs from other subdivisions of the limbic system, such as the cingulate cortex and the ventral tegmental area, contain relatively low levels of limbic system-associated membrane protein immunoreactivity. Thus the expression of this antigen may reflect the targeting of specific groups of limbic afferents to regions that are intimately associated with distinct components of the limbic system. The presence of limbic system-associated membrane protein in neurons of the substantia nigra pars compacta does not appear to be related to the presence or absence of the protein in their striatal target areas. In the substantia nigra, immunoreactivity to the limbic system-associated membrane protein was intense in the cell-sparse zone of the pars compacta, an area known to project to the extrastriosomal matrix of the caudate nucleus. This contrasted with the absence of immunostaining in areas containing dense clusters of dopaminergic neurons (densocellular zone), which project to the limbic system-associated protein-rich striosomes. By analogy to findings in the caudate nucleus and in other brain areas, the results suggest that subgroups of nigral dopaminergic neurons identified on the basis of their terminal fields in the caudate nucleus, may also differ in their limbic afferents.