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Increased Functional Connectivity of the Posterior Cingulate Cortex with the Lateral Orbitofrontal Cortex in Depression Wei Cheng1, Edmund T

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Cheng et al. Translational Psychiatry (2018) 8:90 DOI 10.1038/s41398-018-0139-1 Translational Psychiatry ARTICLE Open Access Increased functional connectivity of the posterior cingulate cortex with the lateral orbitofrontal cortex in depression Wei Cheng1, Edmund T. Rolls2,3,JiangQiu4,5, Xiongfei Xie6,DongtaoWei5, Chu-Chung Huang7,AlbertC.Yang8, Shih-Jen Tsai 8,QiLi9,JieMeng5, Ching-Po Lin 1,7,10,PengXie9,11,12 and Jianfeng Feng1,2,13 Abstract To analyze the functioning of the posterior cingulate cortex (PCC) in depression, we performed the first fully voxel- level resting state functional-connectivity neuroimaging analysis of depression of the PCC, with 336 patients with major depressive disorder and 350 controls. Voxels in the PCC had significantly increased functional connectivity with the lateral orbitofrontal cortex, a region implicated in non-reward and which is thereby implicated in depression. In patients receiving medication, the functional connectivity between the lateral orbitofrontal cortex and PCC was decreased back towards that in the controls. In the 350 controls, it was shown that the PCC has high functional connectivity with the parahippocampal regions which are involved in memory. The findings support the theory that the non-reward system in the lateral orbitofrontal cortex has increased effects on memory systems, which contribute to the rumination about sad memories and events in depression. These new findings provide evidence that a key target to ameliorate depression is the lateral orbitofrontal cortex. 1234567890():,; 1234567890():,; Introduction pathophysiology of major depression and it appears to be Depression characterized by persistently sad or related to rumination and depression severity in MDD6. depressed mood is a major personal burden to sufferers The posterior cingulate cortex is a key region of the and their families, and is a major economic burden to default mode network with strong connectivity in pri- society1. Neuroimaging studies have highlighted a number mates with the entorhinal cortex and parahippocampal – of large-scale functional networks, such as the default gyrus, and thus with the hippocampal memory system7 9. mode network (DMN)2, the salience network3, the fron- The posterior cingulate region (including the retrosplenial toparietal network4, and also the interactions between cortex) is consistently engaged by a range of tasks that these networks, contributing to the pathophysiology of examine episodic memory including autobiographical depression, as recently reviewed5. Considerable evidence memory, and imagining the future; and also spatial navi- has shown the important role of the DMN in the gation and scene processing10,11. It has also been shown that the functional connectivity of the posterior cingulate cortex is related to the rumination in depression12. Fur- ther we detected some voxels in the posterior cingulate Correspondence: Edmund T Rolls ([email protected])orC- cortex and precuneus with different functional con- P Lin ([email protected]) or Peng Xie ([email protected]) or Jianfeng Feng nectivity in depression in a study involving very stringent ([email protected]) 1Institute of Science and Technology for Brain-inspired Intelligence, Fudan correction for multiple comparisons for every voxel pair University, Shanghai 200433, China across the whole brain, but did not attempt to separate 2 Department of Computer Science, University of Warwick, Coventry CV4 7AL, out the posterior cingulate cortex from the precuneus, nor UK Full list of author information is available at the end of the article These authors contributed equally: Wei Cheng, Edmund T. Rolls, Jiang Qiu, Xiongfei Xie © The Author(s) 2018 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a linktotheCreativeCommons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Cheng et al. Translational Psychiatry (2018) 8:90 Page 2 of 10 to analyze how the posterior cingulate cortex may be parietal cortical areas, and from temporal cortical related to depression13. areas8,9,15. Further, there are direct connections between Given this background, the aim of the current investi- the parahippocampal gyrus and the PCC, providing a gation was to focus on the posterior cingulate cortex, and major route via PCC into hippocampal circuitry9. The to analyze how voxels in it may have altered functional vPCC is activated during self-reflection and self- – connectivity in depression; how any different functional imagery16 19. The PCC also has direct connections from connectivities in depression may be related to the symp- the orbitofrontal cortex8,9,15. toms of depression; whether there are differences in The focus here is on the posterior cingulate cortex, effective connectivity in unmedicated patients with major because not only is it implicated in depression, as depressive disorder; and the effects of medication on described above, but also it is implicated in emotion and functional connectivity in depression. processes fundamental to emotion such as the processing – In this investigation, we performed the first voxel-level of rewards and non-rewards20 22. We relate the dis- resting state functional-connectivity neuroimaging ana- coveries described here to a new theory of depression in lysis of depression of voxels in the posterior cingulate which an area that projects to the posterior cingulate cortex (PCC) with all other voxels in the brain in a large cortex, the lateral orbitofrontal cortex, has increased sample of 336 patients with depression and 350 matched sensitivity of a non-reward attractor in depression; and controls. With this large dataset, we are able to analyze the medial orbitofrontal cortex reward system is under- every posterior cingulate voxel for significantly different active in depression23,24. functional connectivity with every voxel throughout the rest of the brain in depressed people vs controls, in order Methods to advance understanding of the posterior cingulate cor- Participants tex and depression. In this paper we utilize what we term There were 336 patients with a diagnosis of major “hypothesis-based voxel-level functional connectivity depression, and 350 controls. The patients were from analysis” in which we select a brain region of interest, but Taiwan (Veteran General Hospital, Taipei) and Xinan then calculate for every voxel in that region whether it has (First Affiliated Hospital of Chongqing Medical School in functional connectivity with individual voxels in every Chongqing,China). All participants were diagnosed other brain region. In the present paper, we select the according to the Diagnostic and Statistical Manual of posterior cingulate cortex as the region of interest, given Mental Disorder-IV criteria for major depressive disorder. the research on it described above implicating it in Depression severity and symptomatology were evaluated depression, and then we show exactly which posterior by the Hamilton Depression Rating Scale (HAMD, 17 cingulate voxels have altered functional connectivity in items)25 and the Beck Depression Inventory (BDI)26.In depression with which individual voxels in every other total 211 patients were receiving medication at the time of brain area. The advantage over previous seed-wise the neuroimaging. The medication consisted in most approaches is that this new method enables identifica- cases of selective serotonin reuptake inhibitors (SSRIs) tion of which voxels within the posterior cingulate have including fluoxetine, paroxetine, sertraline, citalopram, altered connectivity with other brain regions. Given that and escitalopram; or serotonin-norepinephrine reuptake the posterior cingulate cortex has 241 voxels, and that inhibitors (SNRIs) such as venflaxine, or a tetracyclic there are 47619 3 × 3 × 3 mm3 voxels in the automated antidepressant such as mirtazepine. Table S2 provides a anatomical atlas (AAL2) brain14, the number of voxel summary of the demographic information and the psy- pairs in this study was approximately (241 × 47619/2). chiatric diagnosis of the participants, and fuller informa- This methodology is quite different from, and more sta- tion is provided in Supplementary Material. tistically powerful than, a whole brain voxel-to voxel functional connectivity analysis, which, because there are Image acquisition and preprocessing so many voxels pairs in the whole brain, is rather insen- Data for resting state functional connectivity analysis sitive, for it carries a huge burden to correct for the were collected in 3T MRI scanners in an 8 min period in multiple comparisons (1,133,760,771 voxel pairs requiring which the participants were awake in the scanner not − normally p <10 8 for any effect to be significant13). The performing a task using standard protocols described in AAL2 atlas14 was used to provide names for brain areas in Supplementary
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