Amygdaloid inputs define a caudal component of the ventral striatum in primates

Abstract

The ventral striatum mediates goal-directed behavior through limbic afferents. One well-established afferent to the ventral striatum is the amygdaloid complex, which projects throughout the shell and core of the nucleus accumbens, the rostral ventromedial caudate nucleus, and rostral ventromedial putamen. However, striatal regions caudal to the anterior commissure also receive inputs from the amygdala. These caudal areas contain histochemical and cytoarchitectural features that resemble the shell and core, based on our recent studies. Specifically, there is a calcium binding protein (CaBP)-poor region in the lateral amygdalostriatal area that resembles the "shell." To examine the idea that the caudal ventral striatum is part of the "classic" ventral striatum, we placed small injections of retrograde tracers throughout the caudal ventral striatum/amygdalostriatal area and charted the distribution of specific amygdaloid inputs. Amygdaloid inputs to the CaBP-poor zone in the lateral amygdalostriatal area arise from the basal nucleus, the magnocellular subdivision of the accessory basal nucleus, the periamygdaloid cortex, and the medial subdivision of the central nucleus, resembling that of the shell of the ventral striatum found in our previous studies. There are also amygdaloid inputs to CaBP-positive areas outside the shell, which originate mainly in the basal nucleus. Taken together, the "limbic-related" striatum forms a continuum from the rostral ventral striatum through the caudal ventral striatum/lateral amygdalostriatal area based on histochemical and cellular similarities, as well as inputs from the amygdala.

Fig. 1

A,B: Coronal sections through the rostral ventral striatum (A) and caudal ventral striatum (B) of the macaque, immunoreacted for CaBP. The CaBP-poor shell in (A) and the CaBP-poor “shell-like” lateral amygdalostriatal area in (B) are outlined. Note that the medial amygdalostriatal area is CaBP-positive, similar to the lateral core of the central nucleus (CeLcn). C,D: Coronal sections through the central (C) and caudal (D) amygdala stained for acetylcholinesterase (AChE), and labeled for various nuclei. For other abbreviations, see list. Scale bars = 1 mm in A–D.

Fig. 2

A–C: Schematic of retrograde injection sites in the central (A,B) and caudal (C) ventral striatum and central nucleus, with photomicrographs of representative injection sites. DAB staining of electrode tracks is a nonspecific response to gliosis and is not due to leakage of tracer. The dotted line in C represents the CaBP-poor zone. D: Schematic of anterograde tracer injection site placement in the amygdala, with photomicrographs of each. Scale bars = 1 mm in B–D.

Fig. 3

Case J9FR. A–C: Schematic of the distribution of retrogradely labeled cells at three rostrocaudal levels of the amygdala following an injection in the ventral CaBP-poor zone. Each dot = 1 cell. D–E: Photomicrograph of retrogradely labeled cells in the Bpc (D) and Bi (E). For abbreviations, see list. Scale bar = 25 µm in D,E.

Fig. 4

Case J4WGA. A–C: Schematic of the distribution of retrogradely labeled cells at three rostrocaudal levels of the amygdala following an injection in the CaBP-poor zone. Each dot = 1 cell. D: Photomicrograph of labeled cells in the PACs transition with the Bpc. For abbreviations, see list. Scale bar = 25 µm in D.

Fig. 5

Case J6WGA. A–C: Schematic of the distribution of retrogradely labeled cells at three rostrocaudal levels of the amygdala. Each dot = 1 cell. For abbreviations, see list.

Fig. 6

Case J4FR. A,B: Schematic of the distribution of retrogradely labeled cells at two rostrocaudal levels of the amygdala following an injection in the CaBP-positive ventral striatum. Case J4FS. C,D: Schematic of the distribution of retrogradely labeled cells at two rostrocaudal levels of the amygdala following an injection in the CaBP-positive ventral striatum, slightly lateral to the injection in case J4FR above. Each dot = 1 cell. For abbreviations, see list.

Fig. 7

Case J1LY. A,B: Schematic of the distribution of retrogradely labeled cells at two rostrocaudal levels of the amygdala following an injection into the central nucleus (A,B). Each dot = 1 cell. C,D: Photomicrographs of labeled cells in the ABmc (C) and ABpc (D). Case J1FR. E,F: Schematic of the distribution of retrogradely labeled cells at two rostrocaudal levels of the amygdala after a slightly larger injection into the central nucleus. Each dot = 1 cell. For abbreviations, see list. Scale bar = 25 µm in C,D.

Fig. 8

Case J8FR. A–H: Distribution of anterogradely labeled fibers in the striatum following an injection into the basal nucleus, magnocellular subdivision. In D, labeled fibers in the ventromedial putamen are in the region of the putative IPAC. For abbreviations, see list.

Fig. 9

Case J8FR. A,B: Macroscopic photomicrographs of adjacent sections through the caudal ventral striatum in Case J8FR immunoreacted for CaBP (A) and anterograde tracer (B). Asterisk indicates same blood vessel. Dense patches of anterogradely labeled in the CaBP-poor zone compared with the CaBP-positive striatum is apparent even at low magnification. C: Higher power image of labeled fibers in the CaBP-poor zone (boxed area in B). D: Photomicroscopic image at 100× of labeled fibers (boxed area in C) showing numerous boutons. For abbreviations, see list. Scale bar = 1 mm in A,B; 25 µm in C; 10 µm in D.

Fig. 10

Case J8LY. A–G: Distribution of anterogradely labeled fibers in the striatum following an injection into the accessory basal nucleus, magnocellular subdivision. Dense patches of labeled fibers near the posterior limb of the anterior commissure (D) are in the vicinity corresponding to the IPAC in the rodent. For abbreviations, see list.

Fig. 11

The functional gradient formed in the rostral ventral striatum (A) is reflected in the caudal ventral striatum (B), based on amygdaloid inputs. The “shell” (dotted line) is in close proximity to the ventricle both rostrally and caudally, suggesting another rostrocaudal symmetry. Schematic of the ventral striatum adapted from Haber and Fudge (1997).