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Articles, Systems/Circuits

Cortico–Amygdala–Striatal Circuits Are Organized as Hierarchical Subsystems through the Primate Amygdala

Youngsun T. Cho, Monique Ernst and Julie L. Fudge
Journal of Neuroscience 28 August 2013, 33 (35) 14017-14030; DOI: https://doi.org/10.1523/JNEUROSCI.0170-13.2013
Youngsun T. Cho
1Department of Neurobiology and Anatomy and
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Monique Ernst
3National Institute of Mental Health/National Institutes of Health, Emotional Development and Affective Neuroscience Branch, Bethesda, Maryland 20892
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Julie L. Fudge
1Department of Neurobiology and Anatomy and
2Department of Psychiatry, University of Rochester Medical Center, Rochester, New York 14642, and
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Abstract

The prefrontal and insula cortex, amygdala, and striatum are key regions for emotional processing, yet the amygdala's role as an interface between the cortex and striatum is not well understood. In the nonhuman primate (Macaque fascicularis), we analyzed a collection of bidirectional tracer injections in the amygdala to understand how cortical inputs and striatal outputs are organized to form integrated cortico–amygdala–striatal circuits. Overall, diverse prefrontal and insular cortical regions projected to the basal and accessory basal nuclei of the amygdala. In turn, these amygdala regions projected to widespread striatal domains extending well beyond the classic ventral striatum. Analysis of the cases in aggregate revealed a topographic colocalization of cortical inputs and striatal outputs in the amygdala that was additionally distinguished by cortical cytoarchitecture. Specifically, the degree of cortical laminar differentiation of the cortical inputs predicted amygdalostriatal targets, and distinguished three main cortico–amygdala–striatal circuits. These three circuits were categorized as “primitive,” “intermediate,” and “developed,” respectively, to emphasize the relative phylogenetic and ontogenetic features of the cortical inputs. Within the amygdala, these circuits appeared arranged in a pyramidal-like fashion, with the primitive circuit found in all examined subregions, and subsequent circuits hierarchically layered in discrete amygdala subregions. This arrangement suggests a stepwise integration of the functions of these circuits across amygdala subregions, providing a potential mechanism through which internal emotional states are managed with external social and sensory information toward emotionally informed complex behaviors.

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The Journal of Neuroscience: 33 (35)
Journal of Neuroscience
Vol. 33, Issue 35
28 Aug 2013
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Cortico–Amygdala–Striatal Circuits Are Organized as Hierarchical Subsystems through the Primate Amygdala
Youngsun T. Cho, Monique Ernst, Julie L. Fudge
Journal of Neuroscience 28 August 2013, 33 (35) 14017-14030; DOI: 10.1523/JNEUROSCI.0170-13.2013

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Cortico–Amygdala–Striatal Circuits Are Organized as Hierarchical Subsystems through the Primate Amygdala
Youngsun T. Cho, Monique Ernst, Julie L. Fudge
Journal of Neuroscience 28 August 2013, 33 (35) 14017-14030; DOI: 10.1523/JNEUROSCI.0170-13.2013
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