Preferential localization of self-stimulation sites in striosomes/patches in the rat striatum

Abstract

Histological sections of the mammalian striatum reveal a "matrix" that is histochemically distinguishable from patches, or "striosomes". The latter are cross sections of a compartment that consists primarily of tube-shaped structures radiating through the matrix. As a test of the hypothesis that the function of the striosome/patch compartment includes the mediation of behaviors related to reward, the present study examined electrical self-stimulation of the caudoputamen in rats with electrodes in either of the two compartments. Rats acquired and maintained bar-pressing responses that were contingent on stimulation through electrodes making contact with striosomes/patches more reliably than animals with electrodes terminating exclusively in the matrix. The results provide in vivo evidence that the striosome/patch compartment is functionally differentiated from the matrix compartment: Stimulation centered in or around the striosome/patch compartment but not in the matrix led to rapid acquisition of a new behavior.

Figure 1

Placement of electrode tips for 75 subjects. In 22 cases (stars), the tip was localized in a striosome/patch (see text and Fig. 3), and in 9 cases (inverted triangles), the tip was in the matrix; the remaining 44 cases (circles) were unidentified. Filled symbols represent subjects that made >99 responses in three sessions (self-stimulators); open symbols indicate lower response rates. The cases identified by their rank-order and bar-press rates in parentheses (see Fig. 2) are illustrated in Fig. 3.

Figure 2

Rank-ordering of self-stimulation rates for 31 rats in which the location of the electrode tip with respect to a striosome/patch was determined (see text and Fig. 3). The numbers of responses shown for each rat are the totals made during the three consecutive 30-min sessions with the highest rates of responding. Cases in which the electrode tip contacted a striosome/patch (S) and those with the tip in the matrix (M) are indicated. Asterisks identify cases illustrated in Fig. 3 (every fourth case is illustrated). A median split (ranks 1–15 vs. ranks 17–31) of the rank-ordered data was used to determine the statistical relationship of self-stimulation rate to electrode location (see text).

Figure 3

Illustrations of electrode tip locations in relation to striosomes/patches for cases ranked 1, 5, 9, 13, 17, 21, 25, and 29 in Fig. 2 (self-stimulation rates in parentheses). (A, Left and B, Left) A relatively dark background stained for calbindin-D 28k (matrix) with irregularly shaped and placed lighter areas marked by arrows not expressing this stain (striosomes/patches). (A, Right and B, Right) Higher magnification illustrations in which individual cells expressing calbindin are visible. The absence or presence of these cells between the electrode track and a striosome/patch was an important criterion for determining whether a tip contacted or did not contact a striosome/patch. (Bars = 250 μm.)