Substance P: Localization within paleostriatal-tegmental pathways in the pigeon

Abstract

Immunohistochemical techniques were used to determine the distribution of substance P-like immunoreactivity within the paleostriatal complex and within the projection targets of the paleostriatal complex in the pigeon. The density of substance P-like immunoreactivity was found to be much greater in the paleostriatal complex than in immediately overlying portions of the telencephalon (such as the neostriatum and ectostriatum). The small-celled zone of the paleostriatal complex (equivalent to the mammalian caudate-putamen) is characterized by the presence of numerous neurons and fibers that show intense substance P-like immunoreactivity. A higher density of neurons containing substance P-like immunoreactivity was observed within the more medial subdivision of the small-celled zone of the paleostriatal complex (termed the lobus parolfactorius), than in the more lateral subdivision of the small-celled zone of the paleostriatal complex (termed the paleostriatum augmentatum). Many of the substance P-containing fibers within the neuropil of lobus parolfactorius and paleostriatum augmentatum appeared to represent the processes of the substance P-containing neurons of those regions. A dense network of seemingly thick, coarse substance P-containing fibers was observed in the large-celled zone of the avian paleostriatal complex (termed the paleostriatum primitivum). A few medium-sized substance P-containing neurons were evident in the latter area. In addition to fine substance P-containing fibers, numerous thick substance P-immunoreactive fibers were observed in the lobus parolfactorius. The substance P-containing fibers of this region appeared to contribute to a dense substance P-containing fiber plexus in the ventromedial floor of the telencephalon. This region, through which the medial forebrain bundle courses, has been termed the ventral paleostriatum by Kitt & Brauth. 36 The medial forebrain bundle could be traced as a substance P-positive fiber bundle from within the ventral paleostriatum to the midbrain tegmentum. Within the midbrain tegmentum, the fibers of the medial forebrain bundle could be traced into prominent substance P-immunoreactive terminal fields over the cell bodies and neuropil of the catecholaminergic cell groups of the tegmentum, including the ventral tegmental area of Tsai and the nucleus tegmentipedunculopontinus. Within the latter nucleus, substance P-containing fibers and terminals were most densely concentrated within the dorsomedial portion of the nucleus. Kitt & Brauth 36have recently shown by horseradish peroxidase and autoradiographic pathway tracing techniques that the lobus parolfactorius projects to the portions of the ventral tegmental area and nucleus pedunculopontinus that were observed to contain a dense field of substance P-containing fibers and terminals. Unilateral knife cuts of the medial forebrain bundle at rostral diencephalic levels were found to eliminate nearly totally the substance P-immunoreactivity from the neuropil of the ventral tegmental area and nucleus pendunculopontinus on the ipsilateral side of the brain. The present findings argue that, as in mammals, portions of the small-celled zone of the basal ganglia (or paleostriatal complex) in birds may utilize substance P as a neurotransmitter or modulator in their projections upon catecholaminergic cell groups of the midbrain. The present data further suggest that the lobus parolfactorius and paleostriatum augmentatum together in birds are to be considered equivalent to the mammalian caudate-putamen and nucleus accumbens. Previous studies had only emphasized the similarity of paleostriatum augmentatum to the mammalian caudate-putamen. 4,33