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Cortico–Amygdala–Striatal Circuits Are Organized As Hierarchical Subsystems Through the Primate Amygdala

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Cortico–Amygdala–Striatal Circuits Are Organized As Hierarchical Subsystems Through the Primate Amygdala The Journal of Neuroscience, August 28, 2013 • 33(35):14017–14030 • 14017 Systems/Circuits Cortico–Amygdala–Striatal Circuits Are Organized as Hierarchical Subsystems through the Primate Amygdala Youngsun T. Cho,1 Monique Ernst,3 and Julie L. Fudge1,2 1Department of Neurobiology and Anatomy and 2Department of Psychiatry, University of Rochester Medical Center, Rochester, New York 14642, and 3National Institute of Mental Health/National Institutes of Health, Emotional Development and Affective Neuroscience Branch, Bethesda, Maryland 20892 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 mech- anism through which internal emotional states are managed with external social and sensory information toward emotionally informed complex behaviors. Introduction 1981; Amaral and Price, 1984; Ghashghaei et al., 2007; Ho¨istad Emotions color everyday experiences, providing direction and and Barbas, 2008). Medial (mPFC) and orbital (OFC) PFC sub- motivation for action (Damasio, 1996). The amygdala is a key divisions, which are less differentiated than nearby isocortex structure in emotional processing (LeDoux, 1992; Lang and Da- (Sanides, 1964; Pandya and Yeterian, 1990; Carmichael and vis, 2006). Consistent with its complex structure and connec- Price, 1994), have the strongest connections (Carmichael and tions, the amygdala mediates a range of functions, including fear Price, 1995; Ghashghaei and Barbas, 2002; Ghashghaei et al., conditioning and extinction (Phillips and LeDoux, 1992; Maren 2007). These relatively primitive (i.e., phylogenetically older) re- and Quirk, 2004; Phelps et al., 2004; Herry et al., 2006), updating gions are associated with more automatic, unconscious pro- value representations (Ma´lkova´ et al., 1997), recognition of facial cesses, compared with the cognitive functions of isocortex (Ray expressions (Whalen et al., 1998), and affective responses to pri- and Zald, 2012). Although a separate lobe, the insula cortex is mary rewards (Nishijo et al., 1988; Belova et al., 2007). Classic analogously organized with a relatively undifferentiated anterior tract-tracing studies in primates (Carmichael and Price, 1995; subdivision that progresses to a granular organization posteriorly Ghashghaei et al., 2007) and neuroimaging work in humans (Say- (Mesulam and Mufson, 1982). Like more primitive PFC regions, gin et al., 2011; 2012) indicate that these diverse functions depend the anterior insula mediates awareness of internal states (May- on specific combinations of precise neuronal inputs. berg et al., 1999; Damasio et al., 2000; Craig, 2002; Paulus and In primates, the expanded prefrontal cortex (PFC) and insular Stein, 2006). Not surprisingly, abnormal PFC-amygdala and cortices send large projections to the amygdala (Mufson et al., insula-amygdala functional connectivity is well documented in individuals with mood and anxiety disorders, suggesting Received Jan. 10, 2013; revised July 14, 2013; accepted July 18, 2013. ineffective communication between these nodes during states Author contributions: J.L.F. designed research; Y.T.C. and J.L.F. performed research; Y.T.C. and J.L.F. analyzed of emotional disturbance (Etkin et al., 2010; Fonzo et al., 2010; data; Y.T.C., M.E., and J.L.F. wrote the paper. Moses-Kolko et al., 2010; Almeida et al., 2011). This work was funded through support of the National Institutes of Mental Health F30 MH09126 (Y.T.C.) and R01MH63291 (J.L.F.), and the Clinical and Translational Sciences Institute TL1RR024135 (Y.T.C.). We thank Owen The ventral striatum, historically conceptualized as an inter- Zacharias for his photography and Daniel Tylee for assistance with histology and immunocytochemistry. We also face for translating emotional information into complex motor acknowledge helpful criticisms and comments on a draft of this manuscript from Dr. Lizabeth Romanski. responses (Mogenson et al., 1980), receives strong inputs from The authors declare no competing financial interests. the amygdala, particularly from the basal and accessory basal Correspondence should be addressed to Julie L. Fudge, Department of Neurobiology and Anatomy, University of Rochester Medical Center, 601 Elmwood Avenue, Rochester, NY 14642. E-mail: [email protected]. nuclei (Russchen et al., 1985; Friedman et al., 2002; Fudge et al., DOI:10.1523/JNEUROSCI.0170-13.2013 2002). Afferents from these nuclei are thought to facilitate re- Copyright © 2013 the authors 0270-6474/13/3314017-14$15.00/0 sponse selection in the striatum by influencing striatal plastic- 14018 • J. Neurosci., August 28, 2013 • 33(35):14017–14030 Cho et al. • Cortico–Amygdala–Striatal Circuits Figure 1. Schematic of injection sites in the macaque amygdala. A, Coronal section of the macaque amygdala stained with AChE. Scale bar, 1 mm. Amygdala nuclei and subnuclei display differential AChE immunoreactivity. B, Schematic of injection sites in the accessory basal (green) and basal nuclei (yellow) at approximately the same level as A. C, Schematic of injection sites in the caudal amygdala. D, Coronal section of the caudal amygdala at approximately the same level as C stained with AChE. Scale bar, 1 mm. E, Photomicrograph of J15LY injection into the centromedial Bpc taken with dark-field microscopy. Scale bar, 0.5 mm. Arrow points to the center of the injection site. F, AChE-stained section adjacent to E. Scale bar, 0.5 mm. G, Photomicrograph of J20FS injection encompassing both ABmc and ABpc taken with dark-field microscopy. Scale bar, 0.5 mm. Arrow points to the center of the injection site. H, AChE-stained section adjacent to G. Scale bar, 0.5mm.AHA,amygdalohippocampalarea;Bi,basalnucleus,intermediatesubdivision;CeL,centralnucleus,lateralcore;CeM,centralnucleus,medialsubdivision;H,hippocampus;L,lateralnucleus; M, medial nucleus; OT, optic tract; P, putamen; PAC, periamygdaloid cortex; V, ventricle. ity during corticostriatal throughput, and by coordinating (Fudge et al., 2004, 2012). Before surgery, animals were placed under cue-outcome associations (Popescu et al., 2007, 2009; Am- deep surgical anesthesia with intravenous pentobarbital (initial dose broggi et al., 2008; McGinty and Grace, 2009; Li et al., 2011; 20 mg/kg, i.v.) following an initial intramuscular injection of ket- Stuber et al., 2011). Amygdalostriatal projections also target amine (10 mg/kg). Monkeys were stabilized in a stereotactic head the caudoventral striatum posterior to the anterior commis- frame, and sterile procedure was followed. To visualize cortical sur- sure (Russchen et al., 1985; Fudge et al., 2002, 2004), suggest- face landmarks, a craniotomy was done. Internal landmarks were ing engagement of additional striatal domains in motivated determined with electrophysiologic mapping. Small injections (40 nl) of the bidirectional tracers Lucifer yellow (LY), Fluorescein (FS), and behaviors. Fluoro-Ruby (FR; Invitrogen) were pressure injected into subregions Cortical inputs are key influences on amygdala function, and of the amygdala nuclei. in turn, on the gating of striatal responses (Cardinal et al., 2002; Ten to 12 d after surgery the animals were deeply anesthetized and Ernst and Fudge, 2009). Although connections between the PFC/ killed by intracardiac perfusion with 0.9% saline containing 0.5 ml of insula and amygdala, and amygdala and striatum, have previ- heparin sulfate (200 ml/min for 10 min), followed by a cold solution of ously been detailed in separate studies, these two arms of the 4% paraformaldehyde in 0.1 M phosphate buffer (PB)/30% sucrose solu- cortical–amygdala–striatal circuit have yet to be described within tion (100 ml/min for 1 h). Brains were postfixed overnight and cryopro- the same animal. Using bidirectional tracers in various amygdala tected in increasing gradients of sucrose (10, 20, and 30%). After sites, we examined both circuits simultaneously within the same perfusion and postfixation, brains were sectioned on a freezing, sliding animal and amygdala subregion to more fully understand the microtome
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