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Structural changes in brain regions involved in executive-control and self-referential processing after sleeve gastrectomy in obese patients

  • Li Liu
  • Gang Ji
  • Guanya Li
  • Yang Hu
  • Qingchao Jin
  • Chunxin Hu
  • Jizheng Zhao
  • Qianqian Meng
  • Karen M. von Deneen
  • Antao Chen
  • Guangbin Cui
  • Huaning Wang
  • Qingchuan Zhao
  • Kaichun Wu
  • Jie Tian
  • Ehsan Shokri-Kojori
  • Dardo Tomasi
  • Nora D. Volkow
  • Yongzhan Nie
  • Yi Zhang
  • Gene-Jack Wang
Original Research

Abstract

Obesity-related brain gray (GM) and white matter (WM) abnormalities have been reported in regions associated with food-intake control and cognitive-emotional regulation. Bariatric surgery (BS) is the most effective way to treat obesity and induce structural recovery of GM/WM density and WM integrity. It is unknown whether the surgery can promote structural changes in cortical morphometry along with weight-loss. Structural Magnetic Resonance Imaging and surface-based morphometry analysis were used to investigate BS-induced alterations of cortical morphometry in 22 obese participants who were tested before and one month post-BS, and in 21 obese controls (Ctr) without surgery who were tested twice (Baseline and One-month). Results showed that fasting plasma ghrelin, insulin, and leptin levels were significantly reduced post-BS (P < 0.001). Post-BS there were significant decreases in cortical thickness in the precuneus (PFDR < 0.05) that were associated with decreases in BMI. There were also significant increases post-BS in cortical thickness in middle (MFG) and superior (SFG) frontal gyri, superior temporal gyrus (STG), insula and ventral anterior cingulate cortex (vACC); and in cortical volume in left postcentral gyrus (PostCen) and vACC (PFDR < 0.05). Post-BS changes in SFG were associated with decreases in BMI. These findings suggest that structural changes in brain regions implicated in executive control and self-referential processing are associated with BS-induced weight-loss.

Keywords

Obesity Bariatric surgery Cortical morphometry Linear mixed effects 

Notes

Acknowledgements

This work is supported by the National Natural Science Foundation of China under Grant Nos. 61431013, 81470816, 81501543, 81601563, and 81730016; National Clinical Research Center for Digestive Diseases, Xi’an, China under Grant No. 2015BAI13B07; and support in part from the Intramural Research Program of the United States National Institute on Alcoholism and Alcohol Abuse, Z01AA3009 (ESK, DT, NDV, GJW). We thank Mingzhu Xu and Long Qian for their contribution to the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Ethical statements

Informed consent was obtained from all patients included in the study.

Ethics approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Supplementary material

11682_2018_9904_MOESM1_ESM.doc (23 kb)
ESM 1 (DOC 22 kb)
11682_2018_9904_MOESM2_ESM.tif (5.6 mb)
ESM 2 (TIF 5686 kb)
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High resolution image (PNG 8 kb)

References

  1. Benjamini, Y., Krieger, A. M., & Yekutieli, D. (2006). Adaptive linear step-up procedures that control the false discovery rate. Biometrika, 93(3), 491–507.Google Scholar
  2. Bernal-Rusiel, J. L., Greve, D. N., Reuter, M., Fischl, B., & Sabuncu, M. R. (2013). Statistical analysis of longitudinal neuroimage data with linear mixed effects models. Neuroimage, 66, 249–260.PubMedGoogle Scholar
  3. Bluher, S., & Mantzoros, C. S. (2009). Leptin in humans: Lessons from translational research. American Journal of Clinical Nutrition, 89(3), 991S–997S.PubMedPubMedCentralGoogle Scholar
  4. Bush, G., Luu, P., & Posner, M. I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences, 4(6), 215–222.PubMedGoogle Scholar
  5. Clark, S. M., & Saules, K. K. (2013). Validation of the Yale food addiction scale among a weight-loss surgery population. Eating Behaviors, 14(2), 216–219.PubMedGoogle Scholar
  6. Cohen, M. X., Heller, A. S., & Ranganath, C. (2005). Functional connectivity with anterior cingulate and orbitofrontal cortices during decision-making. Cognitive Brain Research, 23(1), 61–70.PubMedGoogle Scholar
  7. Craig, A. D. (2011). Significance of the insula for the evolution of human awareness of feelings from the body. Annals of the New York Academy of Sciences, 1225, 72–82.PubMedGoogle Scholar
  8. Dale, A. M., Fischl, B., & Sereno, M. I. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage, 9(2), 179–194.PubMedGoogle Scholar
  9. van de Sande-Lee, S., Pereira, F. R., Cintra, D. E., Fernandes, P. T., Cardoso, A. R., Garlipp, C. R., Chaim, E. A., Pareja, J. C., Geloneze, B., Li, L. M., et al. (2011). Partial reversibility of hypothalamic dysfunction and changes in brain activity after body mass reduction in obese subjects. Diabetes, 60(6), 1699–1704.PubMedPubMedCentralGoogle Scholar
  10. Desikan, R. S., Segonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., Buckner, R. L., Dale, A. M., Maguire, R. P., Hyman, B. T., et al. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage, 31(3), 968–980.PubMedGoogle Scholar
  11. Diamantis, T., Apostolou, K. G., Alexandrou, A., Griniatsos, J., Felekouras, E., & Tsigris, C. (2014). Review of long-term weight loss results after laparoscopic sleeve gastrectomy. Surgery for Obesity and Related Diseases, 10(1), 177–183.PubMedGoogle Scholar
  12. Fischl, B., & Dale, A. M. (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceeding of the National Academy Sciences United States of America, 97(20), 11050–11055.Google Scholar
  13. Fischl, B., Sereno, M. I., & Dale, A. M. (1999). Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. Neuroimage, 9(2), 195–207.PubMedGoogle Scholar
  14. Fischl, B., Salat, D. H., van der Kouwe, A. J., Makris, N., Segonne, F., Quinn, B. T., & Dale, A. M. (2004). Sequence-independent segmentation of magnetic resonance images. Neuroimage, 23(Suppl 1), S69–S84.PubMedGoogle Scholar
  15. Frank, S., Kullmann, S., & Veit, R. (2013). Food related processes in the insular cortex. Frontiers in Human Neuroscience, 7, 499.PubMedPubMedCentralGoogle Scholar
  16. Frank, S., Wilms, B., Veit, R., Ernst, B., Thurnheer, M., Kullmann, S., Fritsche, A., Birbaumer, N., Preissl, H., & Schultes, B. (2014). Altered brain activity in severely obese women may recover after roux-en Y gastric bypass surgery. International Journal of Obesity (London), 38(3), 341–348.Google Scholar
  17. Freund, H. J. (2003). Somatosensory and motor disturbances in patients with parietal lobe lesions. Advances in Neurology, 93, 179–193.PubMedGoogle Scholar
  18. Gearhardt, A. N., Corbin, W. R., & Brownell, K. D. (2009). Preliminary validation of the Yale food addiction scale. Appetite, 52(2), 430–436.PubMedGoogle Scholar
  19. Grabenhorst, F., & Rolls, E. T. (2009). Different representations of relative and absolute subjective value in the human brain. Neuroimage, 48(1), 258–268.PubMedGoogle Scholar
  20. Grabenhorst, F., & Rolls, E. T. (2011). Value, pleasure and choice in the ventral prefrontal cortex. Trends in Cognitive Sciences, 15(2), 56–67.PubMedGoogle Scholar
  21. Grosshans, M., Vollmert, C., Vollstadt-Klein, S., Tost, H., Leber, S., Bach, P., Buhler, M., von der Goltz, C., Mutschler, J., Loeber, S., et al. (2012). Association of leptin with food cue-induced activation in human reward pathways. Archives of General Psychiatry, 69(5), 529–537.PubMedGoogle Scholar
  22. Hamilton, M. (1959). The assessment of anxiety states by rating. British Journal of Medical Psychology, 32(1), 50–5.Google Scholar
  23. Hamilton, M. (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry, 23(1), 56–62.Google Scholar
  24. Hao, X., Xu, D., Bansal, R., Dong, Z., Liu, J., Wang, Z., Kangarlu, A., Liu, F., Duan, Y., Shova, S., Gerber, A. J., & Peterson, B. S. (2013). Multimodal magnetic resonance imaging: The coordinated use of multiple, mutually informative probes to understand brain structure and function. Human Brain Mapping, 34(2), 253–271.PubMedGoogle Scholar
  25. Hassenstab, J. J., Sweet, L. H., Del, P. A., McCaffery, J. M., Haley, A. P., Demos, K. E., Cohen, R. A., & Wing, R. R. (2012). Cortical thickness of the cognitive control network in obesity and successful weight loss maintenance: A preliminary MRI study. Psychiatry Research, 202(1), 77–79.PubMedPubMedCentralGoogle Scholar
  26. Hu, S., Ide, J. S., Zhang, S., & Li, C. R. (2016). The right superior frontal gyrus and individual variation in proactive control of impulsive response. Journal of Neuroscience, 36(50), 12688–12696.PubMedPubMedCentralGoogle Scholar
  27. Kaur, S., Gonzales, M. M., Strasser, B., Pasha, E., McNeely, J., Tanaka, H., & Haley, A. P. (2015). Central adiposity and cortical thickness in midlife. Psychosomatic Medicine, 77(6), 671–678.PubMedGoogle Scholar
  28. Killgore, W. D., Weber, M., Schwab, Z. J., Kipman, M., DelDonno, S. R., Webb, C. A., & Rauch, S. L. (2013). Cortico-limbic responsiveness to high-calorie food images predicts weight status among women. International Journal of Obesity (London), 37(11), 1435–1442.Google Scholar
  29. Kim, J., Muller, K. R., Chung, Y. G., Chung, S. C., Park, J. Y., Bulthoff, H. H., & Kim, S. P. (2014). Distributed functions of detection and discrimination of vibrotactile stimuli in the hierarchical human somatosensory system. Frontiers in Human Neuroscience, 8, 1070.PubMedGoogle Scholar
  30. Kullmann, S., Heni, M., Veit, R., Ketterer, C., Schick, F., Haring, H. U., Fritsche, A., & Preissl, H. (2012). The obese brain: Association of body mass index and insulin sensitivity with resting state network functional connectivity. Human Brain Mapping, 33(5), 1052–1061.PubMedGoogle Scholar
  31. Kurth, F., Levitt, J. G., Phillips, O. R., Luders, E., Woods, R. P., Mazziotta, J. C., Toga, A. W., & Narr, K. L. (2013). Relationships between gray matter, body mass index, and waist circumference in healthy adults. Human Brain Mapping, 34(7), 1737–1746.PubMedGoogle Scholar
  32. Lepping, R. J., Bruce, A. S., Francisco, A., Yeh, H. W., Martin, L. E., Powell, J. N., Hancock, L., Patrician, T. M., Breslin, F. J., Selim, N., Donnelly, J. E., Brooks, W. M., Savage, C. R., Simmons, W. K., & Bruce, J. M. (2015). Resting-state brain connectivity after surgical and behavioral weight loss. Obesity (Silver Spring), 23(7), 1422–1428.Google Scholar
  33. Li, C. S., Morgan, P. T., Matuskey, D., Abdelghany, O., Luo, X., Chang, J. L., Rounsaville, B. J., Ding, Y. S., & Malison, R. T. (2010). Biological markers of the effects of intravenous methylphenidate on improving inhibitory control in cocaine-dependent patients. Proceeding of the National Academy Sciences United States of America, 107(32), 14455–14459.Google Scholar
  34. Makaronidis, J. M., & Batterham, R. L. (2018). Obesity, body weight regulation and the brain: Insights from fMRI. British Journal of Radiology.  https://doi.org/10.1259/bjr.20170910.
  35. Marques-Iturria, I., Pueyo, R., Garolera, M., Segura, B., Junque, C., Garcia-Garcia, I., Jose, S. M., Vernet-Vernet, M., Narberhaus, A., Ariza, M., et al. (2013). Frontal cortical thinning and subcortical volume reductions in early adulthood obesity. Psychiatry Research, 214(2), 109–115.PubMedGoogle Scholar
  36. Mata, F., Verdejo-Roman, J., Soriano-Mas, C., & Verdejo-Garcia, A. (2015). Insula tuning towards external eating versus interoceptive input in adolescents with overweight and obesity. Appetite, 93, 24–30.PubMedGoogle Scholar
  37. Medic, N., Ziauddeen, H., Ersche, K. D., Farooqi, I. S., Bullmore, E. T., Nathan, P. J., Ronan, L., & Fletcher, P. C. (2016). Increased body mass index is associated with specific regional alterations in brain structure. International Journal of Obesity (London), 40(7), 1177–1182.Google Scholar
  38. Nakamura, Y., & Ikuta, T. (2017). Caudate-Precuneus functional connectivity is associated with obesity preventive eating tendency. Brain Connectivity, 7(3), 211–217.PubMedGoogle Scholar
  39. Navas, J. F., Barros-Loscertales, A., Costumero-Ramos, V., Verdejo-Roman, J., Vilar-Lopez, R., & Verdejo-Garcia, A. (2017). Excessive body fat linked to blunted somatosensory cortex response to general reward in adolescents. International Journal of Obesity (London), 42, 88–94.Google Scholar
  40. Ochner, C. N., Kwok, Y., Conceicao, E., Pantazatos, S. P., Puma, L. M., Carnell, S., Teixeira, J., Hirsch, J., & Geliebter, A. (2011). Selective reduction in neural responses to high calorie foods following gastric bypass surgery. Annals of Surgery, 253(3), 502–507.PubMedPubMedCentralGoogle Scholar
  41. Ochner, C. N., Stice, E., Hutchins, E., Afifi, L., Geliebter, A., Hirsch, J., & Teixeira, J. (2012). Relation between changes in neural responsivity and reductions in desire to eat high-calorie foods following gastric bypass surgery. Neuroscience, 209, 128–135.PubMedPubMedCentralGoogle Scholar
  42. Ojemann, G. A., Schoenfield-McNeill, J., & Corina, D. P. (2002). Anatomic subdivisions in human temporal cortical neuronal activity related to recent verbal memory. Nature Neuroscience, 5(1), 64–71.PubMedGoogle Scholar
  43. Pannacciulli, N., Le, D. S., Chen, K., Reiman, E. M., & Krakoff, J. (2007). Relationships between plasma leptin concentrations and human brain structure: A voxel-based morphometric study. Neuroscience Letters, 412(3), 248–253.PubMedGoogle Scholar
  44. Pleger, B., Blankenburg, F., Ruff, C. C., Driver, J., & Dolan, R. J. (2008). Reward facilitates tactile judgments and modulates hemodynamic responses in human primary somatosensory cortex. Journal of Neuroscience, 28(33), 8161–8168.PubMedPubMedCentralGoogle Scholar
  45. Reuter, M., & Fischl, B. (2011). Avoiding asymmetry-induced bias in longitudinal image processing. Neuroimage, 57(1), 19–21.PubMedPubMedCentralGoogle Scholar
  46. Reuter, M., Rosas, H. D., & Fischl, B. (2010). Highly accurate inverse consistent registration: A robust approach. Neuroimage, 53(4), 1181–1196.PubMedPubMedCentralGoogle Scholar
  47. Reuter, M., Schmansky, N. J., Rosas, H. D., & Fischl, B. (2012). Within-subject template estimation for unbiased longitudinal image analysis. Neuroimage, 61(4), 1402–1418.PubMedPubMedCentralGoogle Scholar
  48. Segonne, F., Dale, A. M., Busa, E., Glessner, M., Salat, D., Hahn, H. K., & Fischl, B. (2004). A hybrid approach to the skull stripping problem in MRI. Neuroimage, 22(3), 1060–1075.PubMedGoogle Scholar
  49. Sharkey, R. J., Karama, S., & Dagher, A. (2015). Overweight is not associated with cortical thickness alterations in children. Frontiers in Neuroscience, 9, 24.PubMedPubMedCentralGoogle Scholar
  50. Sjostrom, L., Narbro, K., Sjostrom, C. D., Karason, K., Larsson, B., Wedel, H., Lystig, T., Sullivan, M., Bouchard, C., Carlsson, B., et al. (2007). Effects of bariatric surgery on mortality in Swedish obese subjects. New England Journal of Medicine, 357(8), 741–752.PubMedGoogle Scholar
  51. Steele, K. E., Prokopowicz, G. P., Schweitzer, M. A., Magunsuon, T. H., Lidor, A. O., Kuwabawa, H., Kumar, A., Brasic, J., & Wong, D. F. (2010). Alterations of central dopamine receptors before and after gastric bypass surgery. Obesity Surgery, 20(3), 369–374.PubMedGoogle Scholar
  52. Tuulari, J. J., Karlsson, H. K., Antikainen, O., Hirvonen, J., Pham, T., Salminen, P., Helmio, M., Parkkola, R., Nuutila, P., & Nummenmaa, L. (2016). Bariatric surgery induces white and Grey matter density recovery in the morbidly obese: A voxel-based morphometric study. Human Brain Mapping, 37(11), 3745–3756.PubMedGoogle Scholar
  53. Veit, R., Kullmann, S., Heni, M., Machann, J., Haring, H. U., Fritsche, A., & Preissl, H. (2014). Reduced cortical thickness associated with visceral fat and BMI. Neuroimage Clinical, 6, 307–311.PubMedPubMedCentralGoogle Scholar
  54. Vidal, P., Ramon, J. M., Goday, A., Benaiges, D., Trillo, L., Parri, A., Gonzalez, S., Pera, M., & Grande, L. (2013). Laparoscopic gastric bypass versus laparoscopic sleeve gastrectomy as a definitive surgical procedure for morbid obesity. Mid-term results. Obesity Surgery, 23(3), 292–299.PubMedGoogle Scholar
  55. Vitaglione, P., Mennella, I., Ferracane, R., Rivellese, A. A., Giacco, R., Ercolini, D., Gibbons, S. M., La Storia, A., Gilbert, J. A., Jonnalagadda, S., et al. (2015). Whole-grain wheat consumption reduces inflammation in a randomized controlled trial on overweight and obese subjects with unhealthy dietary and lifestyle behaviors: Role of polyphenols bound to cereal dietary fiber. American Journal of Clinical Nutrition, 101(2), 251–261.PubMedGoogle Scholar
  56. Vogt, B. A. (2005). Pain and emotion interactions in subregions of the cingulate gyrus. Nature Reviews Neuroscience, 6(7), 533–544.PubMedPubMedCentralGoogle Scholar
  57. Volkow, N. D., & Fowler, J. S. (2000). Addiction, a disease of compulsion and drive: Involvement of the orbitofrontal cortex. Cerebral Cortex, 10(3), 318–325.PubMedGoogle Scholar
  58. Wallis, C. U., Cardinal, R. N., Alexander, L., Roberts, A. C., & Clarke, H. F. (2017). Opposing roles of primate areas 25 and 32 and their putative rodent homologs in the regulation of negative emotion. Proceeding of the National Academy Sciences United States of America, 114(20), E4075–E4084.Google Scholar
  59. Wang, G. J., Volkow, N. D., Felder, C., Fowler, J. S., Levy, A. V., Pappas, N. R., Wong, C. T., Zhu, W., & Netusil, N. (2002). Enhanced resting activity of the oral somatosensory cortex in obese subjects. Neuroreport, 13(9), 1151–1155.PubMedGoogle Scholar
  60. Wang, G. J., Tomasi, D., Backus, W., Wang, R., Telang, F., Geliebter, A., Korner, J., Bauman, A., Fowler, J. S., Thanos, P. K., & Volkow, N. D. (2008). Gastric distention activates satiety circuitry in the human brain. Neuroimage, 39(4), 1824–1831.PubMedGoogle Scholar
  61. Weilbacher, R. A., & Gluth, S. (2016). The interplay of Hippocampus and ventromedial prefrontal cortex in memory-based decision making. Brain Sciences, 7(1), 4.PubMedCentralGoogle Scholar
  62. Wiemerslage, L., Zhou, W., Olivo, G., Stark, J., Hogenkamp, P. S., Larsson, E. M., Sundbom, M., & Schioth, H. B. (2017). A resting-state fMRI study of obese females between pre- and postprandial states before and after bariatric surgery. European Journal of Neuroscience, 45(3), 333–341.PubMedGoogle Scholar
  63. Yokum, S., & Stice, E. (2013). Cognitive regulation of food craving: Effects of three cognitive reappraisal strategies on neural response to palatable foods. International Journal of Obesity (London), 37(12), 1565–1570.Google Scholar
  64. Zhang, Y., Ji, G., Xu, M., Cai, W., Zhu, Q., Qian, L., Zhang, Y. E., Yuan, K., Liu, J., Li, Q., Cui, G., Wang, H., Zhao, Q., Wu, K., Fan, D., Gold, M. S., Tian, J., Tomasi, D., Liu, Y., Nie, Y., & Wang, G. J. (2016). Recovery of brain structural abnormalities in morbidly obese patients after bariatric surgery. International Journal of Obesity (London), 40(10), 1558–1565.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Li Liu
    • 1
  • Gang Ji
    • 2
  • Guanya Li
    • 1
  • Yang Hu
    • 1
  • Qingchao Jin
    • 1
  • Chunxin Hu
    • 1
  • Jizheng Zhao
    • 3
  • Qianqian Meng
    • 1
  • Karen M. von Deneen
    • 1
  • Antao Chen
    • 4
  • Guangbin Cui
    • 5
  • Huaning Wang
    • 6
  • Qingchuan Zhao
    • 2
  • Kaichun Wu
    • 2
  • Jie Tian
    • 1
    • 7
  • Ehsan Shokri-Kojori
    • 8
  • Dardo Tomasi
    • 8
  • Nora D. Volkow
    • 8
  • Yongzhan Nie
    • 2
  • Yi Zhang
    • 1
  • Gene-Jack Wang
    • 8
  1. 1.Center for Brain Imaging, School of Life Science and TechnologyXidian UniversityXi’anChina
  2. 2.Xijing Gastrointestinal HospitalThe Fourth Military Medical UniversityXi’anChina
  3. 3.College of Mechanical and Electronic EngineeringNorthwest A&F UniversityYanglingChina
  4. 4.Department of PsychologySouthwest UniversityChongqingChina
  5. 5.Department of Radiology, Tangdu HospitalThe Fourth Military Medical UniversityXi’anChina
  6. 6.Depart of Psychiatry, Xijing HospitalFourth Military Medical UniversityXi’anChina
  7. 7.Institute of AutomationChinese Academy of SciencesBeijingChina
  8. 8.Laboratory of NeuroimagingNational Institute on Alcohol Abuse and AlcoholismBethesdaUSA

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