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Cortical Connections Position Primate Area 25 As a Keystone for Interoception, Emotion, and Memory

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Cortical Connections Position Primate Area 25 As a Keystone for Interoception, Emotion, and Memory The Journal of Neuroscience, February 14, 2018 • 38(7):1677–1698 • 1677 Systems/Circuits Cortical Connections Position Primate Area 25 as a Keystone for Interoception, Emotion, and Memory X Mary Kate P. Joyce1,2 and XHelen Barbas1,2 1Graduate Program in Neuroscience, Boston University and School of Medicine, Boston, Massachusetts 02215, and 2Neural Systems Laboratory, Department of Health Sciences, Boston University, Boston, Massachusetts 02215 The structural and functional integrity of subgenual cingulate area 25 (A25) is crucial for emotional expression and equilibrium. A25 has a key role in affective networks, and its disruption has been linked to mood disorders, but its cortical connections have yet to be systematically or fully studied. Using neural tracers in rhesus monkeys, we found that A25 was densely connected with other ventrome- dial and posterior orbitofrontal areas associated with emotions and homeostasis. A moderate pathway linked A25 with frontopolar area 10, an area associated with complex cognition, which may regulate emotions and dampen negative affect. Beyond the frontal lobe, A25 was connected with auditory association areas and memory-related medial temporal cortices, and with the interoceptive-related anterior insula. A25 mostly targeted the superficial cortical layers of other areas, where broadly dispersed terminations comingled with modula- tory inhibitory or disinhibitory microsystems, suggesting a dominant excitatory effect. The architecture and connections suggest that A25 is the consummate feedback system in the PFC. Conversely, in the entorhinal cortex, A25 pathways terminated in the middle-deep layers amid a strong local inhibitory microenvironment, suggesting gating of hippocampal output to other cortices and memory storage. The graded cortical architecture and associated laminar patterns of connections suggest how areas, layers, and functionally distinct classes of inhibitory neurons can be recruited dynamically to meet task demands. The complement of cortical connections of A25 with areas associated with memory, emotion, and somatic homeostasis provide the circuit basis to understand its vulnerability in psychiatric and neurologic disorders. Key words: connectome; cortical systematic variation; inhibitory neurons; mood disorders; subgenual cingulate; tract-tracing Significance Statement Integrity of the prefrontal subgenual cingulate cortex is crucial for healthy emotional function. Subgenual area 25 (A25) is mostly linkedwithotherprefrontalareasassociatedwithemotioninadensenetworkpositionedtorecruitlargefieldsofcortex.Inhealthy states, A25 is associated with internal states, autonomic function, and transient negative affect. Constant hyperactivity in A25 is a biomarker for depression in humans and may trigger extensive activation in its dominant connections with areas associated with emotions and internal balance. A pathway between A25 and frontopolar area 10 may provide a critical link to regulate emotions and dampen persistent negative affect, which may be explored for therapeutic intervention in depression. Introduction function (Drevets et al., 2008a,b; Hamani et al., 2011; Myers- Area 25, found deep in the ventral and posterior aspect of the Schulz and Koenigs, 2012; Gold, 2015; Palomero-Gallagher et al., subgenual cingulate region of the ventromedial prefrontal cortex 2015). Classical studies have shown that stimulation of A25 elicits (vmPFC), has a significant role in emotion and visceromotor changes in autonomic function (Kaada et al., 1949; Showers and Crosby, 1958), consistent with its dense projections to the hypo- Received Aug. 21, 2017; revised Nov. 10, 2017; accepted Dec. 8, 2017. thalamus (Nauta, 1971; Ongu¨r et al., 1998; Rempel-Clower and Author contributions: M.K.P.J. and H.B. designed research; M.K.P.J. and H.B. performed research; M.K.P.J. and Barbas, 1998) and brainstem monoaminergic systems (Freedman H.B. analyzed data; M.K.P.J. and H.B. wrote the paper. et al., 2000; Chiba et al., 2001). These structures have global ef- This work was supported by National Institute of Neurological Disorders and Stroke, National Institute of Mental Health,NationalInstitutesofHealth.WethankDrs.MiguelA´.García-Cabezas,BasilisZikopoulos,andYohanJohnfor fects on the brain and somatic states, such as the stress response. helpful discussions. Unlike most of the PFC, A25 has both a very strong sender and The authors declare no competing financial interests. receiver relationship with the amygdala (Ghashghaei et al., 2007), CorrespondenceshouldbeaddressedtoDr.HelenBarbas,BostonUniversity,635CommonwealthAvenue,Room which is associated with affective states and projects to auto- 431, Boston, MA 02215. E-mail: [email protected]. DOI:10.1523/JNEUROSCI.2363-17.2017 nomic structures as well (Sah et al., 2003; Salzman and Fusi, 2010; Copyright © 2018 the authors 0270-6474/18/381677-22$15.00/0 Pessoa, 2017). Further, A25 receives direct input from the hip- 1678 • J. Neurosci., February 14, 2018 • 38(7):1677–1698 Joyce and Barbas • Cortical Connections of Subgenual Cortex Figure 1. Experimental design. A, Bidirectional tracer transport to study connections. B, Exhaustive mapping of tracer-labeled neurons in sections of cortex, a small portion of which is depicted bythethickblackoutline.ArrowheadindicatesaBDAneuronvisualizedwithDAB.Scalebar,250␮m.C,Strategyforunbiased,systematicstereologicsamplingincorticalareasofinterest(thickblack outline)toquantifydensityoftracer-labeledterminations(axonboutons)fromA25.Terminationsinblanksquaresarenotcounted.ArrowheadsindicateBDAboutonsvisualizedwithDAB.Scalebar, 75 ␮m. D, Schematic depicts five different cortical types based on architectural differences. Agranular areas are three layered cortices with poorly defined lamination, whereas eulaminate II ϩ depicts areas with the highest level of laminar definition within areas with label in this study. pocampus (Rosene and Van Hoesen, 1977; Barbas and Blatt, Materials and Methods 1995; Insausti and Mun˜oz, 2001), a region known for its essential Experimental design and statistical analysis overview role in long-term and contextual memory (for review, see Murray Figure 1 depicts the experimental design. The goal was to map the cortical and Wise, 2010; Schiller et al., 2015), and heavily innervates the pathways of A25 in rhesus monkeys and investigate their laminar pattern ventral striatum, associated with motivation and reward-driven of connections. To map incoming and outgoing pathways of A25, we behavior (Heimer and Van Hoesen, 2006; Heilbronner et al., injected four distinct neural tracers in medial or orbital A25 (Table 1). 2016). Dysfunction of A25 is associated with psychiatric disor- The tracers labeled neurons (incoming) and boutons (outgoing) in cor- ders characterized by abnormal affect and emotional expression. tical areas connected with the injection site (Fig. 1A). The extent of each Accordingly, accumulating evidence has highlighted a role of A25 injection site was reconstructed from serial coronal sections, as described in major depression, accompanied by functional and morpho- in Results. logical pathology (Mayberg, 1997; Drevets, 2001; Mayberg et al., The rhesus monkeys were young adult (age 3–4 years old, n ϭ 4, 3 2005; Drevets et al., 2008a). female). Cortical connections in this species are already in place within Despite the involvement of A25 in vital autonomic systems the first postnatal year in visual as well as prefrontal cortices (Goldman and Nauta, 1977; Schwartz and Goldman-Rakic, 1991; Rodman, 1994). and its relevance for affective processes, its cortical connections ϳ have yet to be investigated systematically. Limited information White matter changes continue until 4 years (Malkova et al., 2006) and may be associated with the protracted myelination in primates (Yakovlev on the cortical connections of A25 has been obtained incidentally and Lecours, 1967). After perfusion and coronal sectioning of each brain, from studies with a focus elsewhere (for review, see Hamani et al., we used systematic sampling of coronal series to map labeled neurons by 2011; Yeterian et al., 2012), leaving several questions unad- cortical area in the entire cortex using exhaustive plotting (Fig. 1B; n ϭ dressed. Which cortical areas are connected with A25, and what 42–88 sections/case; the sampling rate was determined by case based on are their relative strengths? Do these pathways interact with spe- labeling distribution). Cortical areas were parcellated using matched se- cific cortical layers in a systematic way and within functionally ries stained with architectural markers (n ϭ 3, 1 female; Table 1). We distinct local environments of inhibitory neurons? We addressed used the coronal plots from each section to compute labeled neuron these questions at the areal and laminar level in rhesus monkeys. density for each cortical area. We then used the normalized densities What emerges is a comprehensive and quantitatively based cor- from sections to reconstruct detailed quantitative maps on the brain tical map at high resolution that positions A25 within the sub- surfaces for each case; this method allowed direct comparison across strate circuitry for interoception, emotion, and memory, and cases. provides insight into the circuitry that becomes disrupted in psy- Because cortical connections are reciprocal but differ across directions chiatric and neurologic diseases. in strength and laminar distribution, we also quantified several comple- Joyce and Barbas • Cortical Connections of Subgenual Cortex J. Neurosci., February
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