Primate cingulostriatal projection: Limbic striatal versus sensorimotor striatal input

Abstract

The organization of the projections from the cingulate cortex to the striatum in the monkey was studied using the retrograde tracers Lucifer Yellow conjugated to dextran amines and horseradish peroxidase conjugated to wheat germ agglutinin. These tracers were injected into the different regions of the ventral (limbic) striatum and the dorsal (sensorimotor) striatum. The shell region of the nucleus accumbens was defined using calbindin‐D_28K immunohistochemistry. Following injections into the ventral striatum, there are numerous retrogradely labeled neurons in the various regions of the primate cingulate cortex, most of which are derived from layer V. The cytoarchitectural subdivisions of cingulate cortex include the anterior cingulate cortex, areas 25, 24a–c, and 24a'–c', and the posterior cingulate cortex, areas 23a–c, 29, 30, and 31. There is a topographical organization of the projections from these different cingulate areas to the ventral and dorsal striatum. The medial ventral striatum receives input from the rostral part of the anterior cingulate cortex (areas 25 and 24a, b). The shell region of the nucleus accumbens receives fibers from areas 25, 24a,b, and 24a',b'. Projections to the central ventral striatum including the core of the nucleus accumbens are derived primarily from areas 25, 24a, 24b, and the medial part of area 24c. However, few labeled cells are detected in areas 24c and 24c'. The lateral ventral striatum receives input primarily from areas 24b, 24b' and 23b and medial portion of area 24c. The medial ventral striatum and the shell of the nucleus accumbens have a similar distribution of labeled cells, such that these regions derive their input almost entirely from the rostral anterior cingulate cortex. In contrast to the ventral striatum, the dorsal sensorimotor striatum receives projections from areas 24c, 24c' 23c and 31. These arise primarily from the lateral portion of lower bank and the fundus of the cingulate sulcus. Our results demonstrate that areas 24c, 24c' and 23c, the lateral portion of the lower bank and the fundus of the cingulate sulcus project to the dorsal sensorimotor striatum. The medial portion of the lower bank of the cingulate cortex projects to the ventral striatum including the core of the nucleus accumbens. Different projections to striatum from discrete subdivisions of cingulate cortex indicate that these areas are heterogeneous and have different functions such that the fundus of the cingulate sulcus is related to skeletomotor function, whereas the medial portion of the lower bank of the cingulate sulcus is associated with the limbic‐related and association cortical function. The lateral portion of the lower bank may be a transition area and related to both motor and limbic functions.