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. Keywordsshell; nucleus accumbens; central nucleus; amygdalostriatal area; extended amygdala; limbicThe concept of the "ventral striatum" originated with Heimer (Heimer and Wilson, 1975;Heimer, 1978) and has been further elaborated over the last decade. In addition to the "nucleus accumbens," the ventromedial caudate nucleus and ventromedial putamen are considered part of the ventral striatum in primates, based on afferent inputs from brain regions mediating motivation and reward (Haber et al., 1995;Chikama et al., 1997;Kunishio and Haber, 1994). Consistent with its anatomic connections, the ventral striatum mediates operant responses to natural and drug rewards (Dickinson, 1994;Kelley and Holahan, 1997;Corbit et al., 2001). Functional neuroimaging studies confirm that the ventral striatum is involved in goal-directed behaviors in humans, for example, in tasks involving financial or other rewards (Koepp et al., 1998;Elliott et al., 2000;Breiter et al., 2001). Across species, the ventral striatum contains a unique subregion known as the "shell," which is tightly connected to the limbic system (Kunishio and Haber, 1994;Haber et al., 1995 1995;Chikama et al., 1997;Haber et al., 2000). The shell is best characterized by its relatively low levels of calbindin-D28k immunoreactivity but is also distinguished by other cytoarchitectural and histochemical features (Meredith et al., 1996;Heimer et al., 199...

Striatal dopamine D2/3 receptor-mediated neurotransmission in major depression: Implications for anhedonia, anxiety and treatment response

“…We show that increments in baseline DA D 2/3 BP ND in the more caudal portion of the NAc were associated with higher anxiety levels in MDD patients. These effects are consistent with the notion that caudal ventromedial striatal regions, which receive inputs from several “limbic” brain regions, including the amygdala and anterior cingulate cortex (Fudge et al, 2004; Russchen et al, 1985; Shammah-Lagnado et al, 2001), are involved in fear generation. In fact, preclinical evidence suggests that fear generation requires simultaneous stimulation of D1 and D2 receptors at caudal sites of the NAc (Richard and Berridge, 2011).…”

The organization of the human striatum estimated by intrinsic functional connectivity

“…There are strong projections to the striatum from subcortical structures, which we have not considered here, such as the amygdala (Fudge et al 2002(Fudge et al , 2004Russchen et al 1985) and the cerebellum via the thalamus (Hoshi et al 2005). We refer interested readers to another study examining the functional connectivity of the amygdala to the striatum (Roy et al 2009).…”

“…We expand on these organizational properties in DISCUSSION. Fourth, the parcellation parallels monkey anatomical projections in the posterior ventral striatum. In addition to projections to the ventral putamen from the tongue region of the motor cortex, monkey anatomy reveals projections to the posteriormost portion of the ventral striatum from association and limbic cortices [there are also projections from subcortical structures, such as the amygdala (Fudge et al 2002(Fudge et al , 2004Russchen et al 1985), but we will not address them here]. Figure 10 shows the 7-network parcellation of the posterior ventral striatum and the corresponding fcMRI maps, showing that the posterior ventral striatum is functionally coupled to the motor and, further ventrally, association cortical networks.…”

Connectivity between the central nucleus of the amygdala and the bed nucleus of the stria terminalis in the non-human primate: neuronal tract tracing and developmental neuroimaging studies

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