Insular and gustatory inputs to the caudal ventral striatum in primates

Abstract

The ventral striatum mediates goal-directed behaviors based, in part, on inputs from the amygdala. However, striatal areas caudal to the ventral striatum also receive inputs from the amygdala. In primates, the amygdala projects to the central ventral putamen, lateral amygdalostriatal area, and caudal ventral putamen, suggesting that these regions are also "limbic-related." The anterior insula, which integrates sensory and amygdaloid inputs, projects to the classic ventral striatum. We used retrograde and anterograde tract tracing techniques to determine the extent to which specific subdivisions of the insula influence the caudal ventral striatum in the primate. The anterior (agranular and rostral dysgranular) insula has significant inputs to caudal ventral striatal regions that receive projections from the amygdala. In contrast, the posterior (granular) insula has sparse projections. Within the agranular insula, the posteromedial agranular (Iapm), lateral agranular (Ial), and posterolateral agranular (Iapl) subdivisions have the strongest inputs. These subdivisions mediate olfactory, gustatory, and visceral information processing (Carmichael and Price JL [1996b] J. Comp. Neurol. 363:642-640). In contrast, the intermediate agranular subdivision (Iai) is relatively devoid of visceral/gustatory inputs and has few inputs. In summary, caudal ventral striatal areas that receive amygdaloid inputs also receive significant innervation by agranular and dysgranular insula subdivisions that are themselves connected with the amygdala. Within this projection, the Ial, Iapm, and Iapl make the strongest contribution, suggesting that highly processed visceral/autonomic information, taste, and olfaction influence behavioral responses mediated by the caudal ventral striatum.

Fig. 1

Photomicrographs of sections through the rostral (A–C) and caudal (D–F) ventral striatum stained for AChE (A,D), CaBP (B,E), and TH (C,F). Intermediate to high AChE activity is found in the ventral striatum both rostrally and caudally (A,D) Low CaBP immunoreactivity is found in the shell of the rostral ventral striatum (B) and lateral amygdalostriatal area (E), overlapping areas of intermediate to high AChE staining. Dotted line depicts the CaBP-poor shell and lateral amygdalostriatal area. The medial amygdalostriatal area contains very low to absent AChE activity (D) and TH immunostaining (F) and high CaBP immunoreactivity (E). For abbreviations, see list. Scale bars = 1 mm in A–F.

Fig. 2

Nissl-stained sections at several rostrocaudal levels of the insula. A: The rostral agranular insula is found on the caudal orbital surface and is bordered laterally by the gustatory cortex. The Iapm has three rudimentary layers, and the Ial has five layers including a sublaminated layer V. Iai has a partially sublaminated layer V. B: Further caudally, the Iapm and Iapl extend into the sylvian fissure. They are bordered dorsally by the Id. C: The Iac, Id, and Ig at the level of the decussation of the anterior commissure. D: Dense parvalbumin immunoreactivity in layers III/IV distinguishes the gustatory cortex. Iapm is distinguished by low parvalbumin staining. Photographs were digitally captured and tiled by using ImagePro software. For abbreviations, see list. Scale bars = 1 mm in A–D.

Fig. 3

Schematic of retrograde injection sites in the caudal striatum and central nucleus (A–C, top) and anterograde injection sites in the insula and gustatory cortex (D, bottom). Photomicrographs of several injection sites are shown for each series. For abbreviations, see list. Scale bars = 1 mm in A,B,D.

Fig. 4

A–F: Schematic of retrogradely labeled cells in the insula following an injection of WGA-HRP into the central ventromedial putamen (case J8WGA). Boxed area in C depicts the area photographed in Figure 5. For abbreviations, see list. Each dot = 1 cell.

Fig. 5

Photomicrographs of retrogradely labeled cells in Iapl in case J8WGA. A: Macroscopic view of labeled cells in the Iapl (boxed area in Fig. 4C). The photograph was digitally captured using a 4× objective and tiled into a montage by using ImagePro software. B: Higher power views of labeled cells in boxed area in A. For abbreviations, see list. Scale bars = 1 mm in A; 100 µm in B.

Fig. 6

A–F: Schematic of retrogradely labeled cells in the insula following an injection of WGA-HRP into the caudal ventromedial putamen (case J12WGA). For abbreviations, see list. Each dot = 1 cell.

Fig. 7

A–F: Schematic of WGA-HRP-positive cells in the insula in case J4WGA. D′: Labeled cells in layer V (box in D). The CaBP-poor lateral amygdalostriatal area is illustrated with a dotted line. Each dot = 1 cell. For abbreviations, see list. Scale bar = 100 µm in D′

Fig. 8

A–C: Retrogradely labeled cells in the insula following an FR injection into the lateral amygdalostriatal area near the emerging tail of the caudate nucleus (injection site shown in Fig. 3). The CaBP-poor lateral amygdalostriatal area is illustrated with a dotted line. Each dot = 1 cell. B′: FR-labeled cells in the Iac (boxed area in B). Lightly labeled cells (small arrows) are seen in addition to darkly staining cells (large arrows). For abbreviations, see list. Scale bar = 100 µm in B′.

Fig. 9

A–E: Schematic of retrogradely labeled cells in case J4FR, following an injection into the ventromedial caudal striatum. The CaBP-poor lateral amygdalostriatal area is illustrated with a dotted line. Each dot = 1 cell. D′: Labeled cells in layer V of the dysgranular insula (boxed area in D). For abbreviations, see list. Scale bar = 100 µm in D′.

Fig. 10

Schematic showing retrogradely labeled cells after injections into the central nucleus: case J1FR (left, A–D) and case J1 LY (right, E). The CaBP-poor lateral amygdalostriatal area is illustrated with a dotted line. Each dot = 1 cell. C′: Retrogradely labeled cells in the Iapl in case J1FR (boxed area in C). For abbreviations, see list. Scale bar = 1 mm in C′.

Fig. 11

A–E: Schematic of the distribution of silver grains in the striatum following a tritiated amino acid injection into the rostral dysgranular insula (case J9AA). The injection site is pictured in Figure 3. For abbreviations, see list.

Fig. 12

A–G: Schematic of labeled fibers in the striatum following an FR injection into the gustatory cortex/Iapl (case J6FR). For abbreviations, see list.