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. . 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. Keywordslimbic; gustatory; caudate; putamen; amygdalostriatal area; amygdala; tract tracingThe rostral ventral striatum is considered a substrate for goal-directed behaviors based on its inputs from multiple brain regions mediating motivation and reward (Mogenson et al., 1980;Nauta, 1986;Ferry et al., 2000;Haber et al., 2000). However, it is increasingly recognized that caudal ventromedial striatal regions also receive inputs from several "limbic" brain regions, including the amygdala and anterior cingulate cortex (Russchen et al., 1985;Selemon and Goldman-Rakic, 1985;Nauta, 1986;McDonald et al., 1999;Ferry et al., 2000; ShammahLagnado et al., 2001;Fudge et al., 2004). We have previously defined the primate "caudal ventral striatum" based on amygdaloid afferent inputs and histochemical markers typical of the ventral striatum (Fudge and Haber, 2002;Fudge et al., 2004). Based on these criteria, the NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript caudal ventral striatum includes the ventromedial putamen surrounding, and caudal to, the decussation of the anterior commissure, the lateral amygdalostriatal area, and the medial tail of the caudate nucleus.The anterior insula is involved in emotional and multisensory processing (Lane et al., 1997;Phillips et a...

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