Abstract
The prefrontal cortex (PFC) and insula, amygdala, and striatum form interconnected networks that drive motivated behaviors. We previously found a connectional trend in which granularity of the ventromedial and orbital PFC/insula predicted connections to the amygdala and also the scope of amygdalo-striatal efferents, including projections beyond the ‘classic’ ventral striatum. To further interrogate this triad and define the ‘limbic (amygdala-recipient) striatum’, we conducted tract tracing studies in two cohorts of primates to define the scope of cortico-amygdalo-striatal (indirect) and cortico-‘limbic’ striatal (direct) paths originating in the entire PFC and insula. With larger data sets and a quantitative approach, we found that the level of cortical granularity predicts the complexity and location of projections to both the amygdala and striatum. Remarkably, ‘cortical-like’ basal nucleus subdivisions also followed these rules in their projections to the striatum. In both ‘direct’ and ‘indirect’ paths to the ‘limbic’ striatum, agranular cortices formed a ‘foundational’, broad projection, and were joined by inputs from progressively more differentiated cortices. In amygdalo-striatal paths, the ventral basal nucleus was the ‘foundational’ input, with progressively more dorsal basal nucleus regions gradually adding inputs as the ‘limbic striatum’ extended caudally. Together, the ‘indirect’ and ‘direct’ paths follow consistent rules dictating projection strength and complexity to their targets. In the ‘indirect’ path, the agranular ‘interoceptive’ cortices consistently dominate amygdala inputs to the striatum. In contrast, ‘direct’ cortical inputs to the ‘limbic’ (amygdala-recipient) striatum create gradual shifts in connectivity fingerprints to provide clues to functional differences in the classic versus caudal ventral ‘limbic’ striatum.
Significance Statement The ‘limbic system’ broadly refers to brain circuits that coordinate emotional responses. Here, we investigate circuits of the amygdala, which is involved in coding the emotional value of external cues, and their influence on the striatum. Regions of prefrontal cortex and insula form gradients of overlapping inputs to basal nucleus of the amygdala, which are fed forward to the striatum. Direct cortical inputs to these ‘amygdala-recipient’ striatal areas are surprisingly organized according to similar principles, but subtly shift from the classic ventral striatum to the caudal ventral striatum. Together, these distinct subsystems—cortico-amygdala-striatal circuits and direct cortico-striatal circuits— provide substantial opportunity for different levels of internal, sensory, and external experiences to be integrated within the striatum, a major motor-behavioral interface.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
Conflict of interest statement: The authors declare no competing financial interests.