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Published in: Endocrine 2/2023

Open Access 02-12-2022 | Hypoglycemia | Original Article

Effects of gastric bypass surgery on brain connectivity responses to hypoglycemia

Authors: Giovanni Fanni, Christakis Kagios, Erika Roman, Magnus Sundbom, Johan Wikström, Sven Haller, Jan W. Eriksson

Published in: Endocrine | Issue 2/2023

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Abstract

Introduction

Roux-en-Y gastric bypass (RYGB) leads to beneficial effects on glucose homeostasis, and attenuated hormonal counterregulatory responses to hypoglycemia are likely to contribute. RYGB also induces alterations in neural activity of cortical and subcortical brain regions. We aimed to characterize RYGB-induced changes in resting-state connectivity of specific brain regions of interest for energy homeostasis and behavioral control during hypoglycemia.

Method

Ten patients with BMI > 35 kg/m2 were investigated with brain PET/MR imaging during a hyperinsulinemic normo- and hypoglycemic clamp, before and 4 months after RYGB. Hormonal levels were assessed throughout the clamp. Resting-state (RS) fMRI scans were acquired in the glucose-lowering phase of the clamp, and they were analyzed with a seed-to-voxel approach.

Results

RS connectivity during initiation of hypoglycemia was significantly altered after RYGB between nucleus accumbens, thalamus, caudate, hypothalamus and their crosstalk with cortical and subcortical regions. Connectivity between the nucleus accumbens and the frontal pole was increased after RYGB, and this was associated with a reduction of ACTH (r = −0.639, p = 0.047) and cortisol (r = −0.635, p = 0.048) responses. Instead, connectivity between the caudate and the frontal pole after RYGB was reduced and this was associated with less attenuation of glucagon response during the hypoglycemic clamp (r = −0.728, p = 0.017), smaller reduction in fasting glucose (r = −0.798, p = 0.007) and less excess weight loss (r = 0.753, p = 0.012). No other significant associations were found between post-RYGB changes in ROI-to-voxel regional connectivity hormonal responses and metabolic or anthropometric outcomes.

Conclusion

RYGB alters brain connectivity during hypoglycemia of several neural pathways involved in reward, inhibitory control, and energy homeostasis. These changes are associated with altered hormonal responses to hypoglycemia and may be involved in the glucometabolic outcome of RYGB.
Literature
1.
go back to reference D.E. Arterburn, A.P. Courcoulas, Bariatric surgery for obesity and metabolic conditions in adults. BMJ 349, g3961 (2014).CrossRef D.E. Arterburn, A.P. Courcoulas, Bariatric surgery for obesity and metabolic conditions in adults. BMJ 349, g3961 (2014).CrossRef
2.
go back to reference H. Buchwald, R. Estok, K. Fahrbach, D. Banel, M.D. Jensen, W.J. Pories, J.P. Bantle, I. Sledge, Weight and Type 2 Diabetes after Bariatric Surgery: Systematic Review and Meta-analysis. Am. J. Med 122, 248 (2009).CrossRef H. Buchwald, R. Estok, K. Fahrbach, D. Banel, M.D. Jensen, W.J. Pories, J.P. Bantle, I. Sledge, Weight and Type 2 Diabetes after Bariatric Surgery: Systematic Review and Meta-analysis. Am. J. Med 122, 248 (2009).CrossRef
3.
go back to reference I. Cornejo-Pareja, M. Clemente-Postigo, F.J. Tinahones, Metabolic and Endocrine Consequences of Bariatric Surgery. Front Endocrinol. (Lausanne) 10, 626 (2019).CrossRef I. Cornejo-Pareja, M. Clemente-Postigo, F.J. Tinahones, Metabolic and Endocrine Consequences of Bariatric Surgery. Front Endocrinol. (Lausanne) 10, 626 (2019).CrossRef
4.
go back to reference L.E. Sewaybricker, E.A. Schur, Is Bariatric Surgery Brain Surgery? Diabetes 70, 1244 (2021).CrossRef L.E. Sewaybricker, E.A. Schur, Is Bariatric Surgery Brain Surgery? Diabetes 70, 1244 (2021).CrossRef
5.
go back to reference C. Broberger, Brain regulation of food intake and appetite: Molecules and networks. J. Intern Med 258, 301 (2005).CrossRef C. Broberger, Brain regulation of food intake and appetite: Molecules and networks. J. Intern Med 258, 301 (2005).CrossRef
6.
go back to reference C. Diepenbroek, M.J. Serlie, E. Fliers, A. Kalsbeek, S.E. la Fleur, Brain areas and pathways in the regulation of glucose metabolism. BioFactors 39, 505 (2013).CrossRef C. Diepenbroek, M.J. Serlie, E. Fliers, A. Kalsbeek, S.E. la Fleur, Brain areas and pathways in the regulation of glucose metabolism. BioFactors 39, 505 (2013).CrossRef
7.
go back to reference D. Vallöf, Glucagon-like peptide-1 and alcohol-mediated behaviors in rodents. Glucagon-like Peptide-1 and Alcohol-Mediated Behaviors in Rodents, Univeristy of Gothenburg, 2019. D. Vallöf, Glucagon-like peptide-1 and alcohol-mediated behaviors in rodents. Glucagon-like Peptide-1 and Alcohol-Mediated Behaviors in Rodents, Univeristy of Gothenburg, 2019.
8.
go back to reference J.F. Davis, D.L. Choi, S.C. Benoit, Insulin, leptin and reward. Trends Endocrinol. Metab. 21, 68 (2010).CrossRef J.F. Davis, D.L. Choi, S.C. Benoit, Insulin, leptin and reward. Trends Endocrinol. Metab. 21, 68 (2010).CrossRef
9.
go back to reference K.P. Skibicka, C. Hansson, E. Egecioglu, S.L. Dickson, Role of ghrelin in food reward: impact of ghrelin on sucrose self-administration and mesolimbic dopamine and acetylcholine receptor gene expression. Addiction Biol. 17, 95 (2012).CrossRef K.P. Skibicka, C. Hansson, E. Egecioglu, S.L. Dickson, Role of ghrelin in food reward: impact of ghrelin on sucrose self-administration and mesolimbic dopamine and acetylcholine receptor gene expression. Addiction Biol. 17, 95 (2012).CrossRef
10.
go back to reference C.M. Olsen, Natural rewards, neuroplasticity, and non-drug addictions. Neuropharmacology 61, 1109 (2011).CrossRef C.M. Olsen, Natural rewards, neuroplasticity, and non-drug addictions. Neuropharmacology 61, 1109 (2011).CrossRef
11.
go back to reference R.M. O’Connor, P.J. Kenny, Utility of ‘substance use disorder’ as a heuristic for understanding overeating and obesity. Prog. Neuropsychopharmacol. Biol. Psychiatry 118, 110580 (2022).CrossRef R.M. O’Connor, P.J. Kenny, Utility of ‘substance use disorder’ as a heuristic for understanding overeating and obesity. Prog. Neuropsychopharmacol. Biol. Psychiatry 118, 110580 (2022).CrossRef
12.
go back to reference G.F. Koob, N.D. Volkow, Neurobiology of addiction: a neurocircuitry analysis. Lancet Psychiatry 3, 760 (2016).CrossRef G.F. Koob, N.D. Volkow, Neurobiology of addiction: a neurocircuitry analysis. Lancet Psychiatry 3, 760 (2016).CrossRef
13.
go back to reference K. Coveleskie, A. Gupta, L.A. Kilpatrick, E.D. Mayer, C. Ashe-Mcnalley, J. Stains, J.S. Labus, E.A. Mayer, Altered functional connectivity within the central reward network in overweight and obese women. Nutr. Diabetes 5(1), e148 (2015).CrossRef K. Coveleskie, A. Gupta, L.A. Kilpatrick, E.D. Mayer, C. Ashe-Mcnalley, J. Stains, J.S. Labus, E.A. Mayer, Altered functional connectivity within the central reward network in overweight and obese women. Nutr. Diabetes 5(1), e148 (2015).CrossRef
14.
go back to reference G.J. Morton, T.H. Meek, M.W. Schwartz, Neurobiology of food intake in health and disease. Nat. Rev. Neurosci. 15, 367 (2014).CrossRef G.J. Morton, T.H. Meek, M.W. Schwartz, Neurobiology of food intake in health and disease. Nat. Rev. Neurosci. 15, 367 (2014).CrossRef
15.
go back to reference Y. Zeighami, S. Iceta, M. Dadar, M. Pelletier, M. Nadeau, L. Biertho, A. Lafortune, A. Tchernof, S. Fulton, A. Evans, D. Richard, A. Dagher, A. Michaud, Spontaneous neural activity changes after bariatric surgery: A resting-state fMRI study. Neuroimage 241, 118419 (2021).CrossRef Y. Zeighami, S. Iceta, M. Dadar, M. Pelletier, M. Nadeau, L. Biertho, A. Lafortune, A. Tchernof, S. Fulton, A. Evans, D. Richard, A. Dagher, A. Michaud, Spontaneous neural activity changes after bariatric surgery: A resting-state fMRI study. Neuroimage 241, 118419 (2021).CrossRef
16.
go back to reference R.J. Lepping, A.S. Bruce, A. Francisco, H.-W. Yeh, L.E. Martin, J.N. Powell, L. Hancock, T.M. Patrician, F.J. Breslin, N. Selim, J.E. Donnelly, W.M. Brooks, C.R. Savage, W.K. Simmons, J.M. Bruce, Resting-state brain connectivity after surgical and behavioral weight loss. Obesity 23, 1422 (2015).CrossRef R.J. Lepping, A.S. Bruce, A. Francisco, H.-W. Yeh, L.E. Martin, J.N. Powell, L. Hancock, T.M. Patrician, F.J. Breslin, N. Selim, J.E. Donnelly, W.M. Brooks, C.R. Savage, W.K. Simmons, J.M. Bruce, Resting-state brain connectivity after surgical and behavioral weight loss. Obesity 23, 1422 (2015).CrossRef
17.
go back to reference G. Li, G. Ji, Y. Hu, M. Xu, Q. Jin, L. Liu, K.M. Deneen, J. Zhao, A. Chen, G. Cui, H. Wang, Q. Zhao, K. Wu, E. Shokri‐Kojori, D. Tomasi, N.D. Volkow, Y. Nie, Y. Zhang, G. Wang, Bariatric surgery in obese patients reduced resting connectivity of brain regions involved with self‐referential processing. Hum. Brain Mapp. 39, 4755 (2018).CrossRef G. Li, G. Ji, Y. Hu, M. Xu, Q. Jin, L. Liu, K.M. Deneen, J. Zhao, A. Chen, G. Cui, H. Wang, Q. Zhao, K. Wu, E. Shokri‐Kojori, D. Tomasi, N.D. Volkow, Y. Nie, Y. Zhang, G. Wang, Bariatric surgery in obese patients reduced resting connectivity of brain regions involved with self‐referential processing. Hum. Brain Mapp. 39, 4755 (2018).CrossRef
18.
go back to reference G. Olivo, W. Zhou, M. Sundbom, C. Zhukovsky, P. Hogenkamp, L. Nikontovic, J. Stark, L. Wiemerslage, E.-M. Larsson, C. Benedict, H.B. Schiöth, Resting-state brain connectivity changes in obese women after Roux-en-Y gastric bypass surgery: A longitudinal study. Sci. Rep. 7, 6616 (2017).CrossRef G. Olivo, W. Zhou, M. Sundbom, C. Zhukovsky, P. Hogenkamp, L. Nikontovic, J. Stark, L. Wiemerslage, E.-M. Larsson, C. Benedict, H.B. Schiöth, Resting-state brain connectivity changes in obese women after Roux-en-Y gastric bypass surgery: A longitudinal study. Sci. Rep. 7, 6616 (2017).CrossRef
19.
go back to reference J.J. Tuulari, H.K. Karlsson, J. Hirvonen, J.C. Hannukainen, M. Bucci, M. Helmiö, J. Ovaska, M. Soinio, P. Salminen, N. Savisto, L. Nummenmaa, P. Nuutila, Weight loss after bariatric surgery reverses insulin-induced increases in brain glucose metabolism of the morbidly obese. Diabetes 62, 2747 (2013).CrossRef J.J. Tuulari, H.K. Karlsson, J. Hirvonen, J.C. Hannukainen, M. Bucci, M. Helmiö, J. Ovaska, M. Soinio, P. Salminen, N. Savisto, L. Nummenmaa, P. Nuutila, Weight loss after bariatric surgery reverses insulin-induced increases in brain glucose metabolism of the morbidly obese. Diabetes 62, 2747 (2013).CrossRef
20.
go back to reference K.F. Hunt, J.T. Dunn, C.W. le Roux, L.J. Reed, P.K. Marsden, A.G. Patel, S.A. Amiel, Differences in Regional Brain Responses to Food Ingestion After Roux-en-Y Gastric Bypass and the Role of Gut Peptides: A Neuroimaging Study. Diabetes Care 39, 1787 (2016).CrossRef K.F. Hunt, J.T. Dunn, C.W. le Roux, L.J. Reed, P.K. Marsden, A.G. Patel, S.A. Amiel, Differences in Regional Brain Responses to Food Ingestion After Roux-en-Y Gastric Bypass and the Role of Gut Peptides: A Neuroimaging Study. Diabetes Care 39, 1787 (2016).CrossRef
21.
go back to reference K.E. Almby, M.H. Lundqvist, N. Abrahamsson, S. Kvernby, M. Fahlström, M.J. Pereira, M. Gingnell, F.A. Karlsson, G. Fanni, M. Sundbom, U. Wiklund, S. Haller, M. Lubberink, J. Wikström, J.W. Eriksson, Effects of Gastric Bypass Surgery on the Brain: Simultaneous Assessment of Glucose Uptake, Blood Flow, Neural Activity, and Cognitive Function During Normo- and Hypoglycemia. Diabetes 70, 1265 (2021).CrossRef K.E. Almby, M.H. Lundqvist, N. Abrahamsson, S. Kvernby, M. Fahlström, M.J. Pereira, M. Gingnell, F.A. Karlsson, G. Fanni, M. Sundbom, U. Wiklund, S. Haller, M. Lubberink, J. Wikström, J.W. Eriksson, Effects of Gastric Bypass Surgery on the Brain: Simultaneous Assessment of Glucose Uptake, Blood Flow, Neural Activity, and Cognitive Function During Normo- and Hypoglycemia. Diabetes 70, 1265 (2021).CrossRef
22.
go back to reference S. Whitfield-Gabrieli, A. Nieto-Castanon, Conn: A Functional Connectivity Toolbox for Correlated and Anticorrelated Brain Networks. Brain Connect 2, 125 (2012).CrossRef S. Whitfield-Gabrieli, A. Nieto-Castanon, Conn: A Functional Connectivity Toolbox for Correlated and Anticorrelated Brain Networks. Brain Connect 2, 125 (2012).CrossRef
23.
go back to reference K.C. Berridge, T.E. Robinson, What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Rev. 28, 309 (1998).CrossRef K.C. Berridge, T.E. Robinson, What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Rev. 28, 309 (1998).CrossRef
24.
go back to reference M. Morales, E.B. Margolis, Ventral tegmental area: cellular heterogeneity, connectivity and behaviour. Nat. Rev. Neurosci. 18, 73 (2017).CrossRef M. Morales, E.B. Margolis, Ventral tegmental area: cellular heterogeneity, connectivity and behaviour. Nat. Rev. Neurosci. 18, 73 (2017).CrossRef
25.
go back to reference R. Al-Hasani, R. Gowrishankar, G.P. Schmitz, C.E. Pedersen, D.J. Marcus, S.E. Shirley, T.E. Hobbs, A.J. Elerding, S.J. Renaud, M. Jing, Y. Li, V.A. Alvarez, J.C. Lemos, M.R. Bruchas,, Ventral tegmental area GABAergic inhibition of cholinergic interneurons in the ventral nucleus accumbens shell promotes reward reinforcement. Nat. Neurosci. 24(10), 1414 (2021).CrossRef R. Al-Hasani, R. Gowrishankar, G.P. Schmitz, C.E. Pedersen, D.J. Marcus, S.E. Shirley, T.E. Hobbs, A.J. Elerding, S.J. Renaud, M. Jing, Y. Li, V.A. Alvarez, J.C. Lemos, M.R. Bruchas,, Ventral tegmental area GABAergic inhibition of cholinergic interneurons in the ventral nucleus accumbens shell promotes reward reinforcement. Nat. Neurosci. 24(10), 1414 (2021).CrossRef
26.
go back to reference G. Chahine, E.K. Diekhof, A. Tinnermann, O. Gruber, On the role of the anterior prefrontal cortex in cognitive “branching”: An fMRI study. Neuropsychologia 77, 421 (2015).CrossRef G. Chahine, E.K. Diekhof, A. Tinnermann, O. Gruber, On the role of the anterior prefrontal cortex in cognitive “branching”: An fMRI study. Neuropsychologia 77, 421 (2015).CrossRef
27.
go back to reference L.M. Yager, A.F. Garcia, A.M. Wunsch, S.M. Ferguson, The ins and outs of the striatum: Role in drug addiction. Neuroscience 301, 529 (2015).CrossRef L.M. Yager, A.F. Garcia, A.M. Wunsch, S.M. Ferguson, The ins and outs of the striatum: Role in drug addiction. Neuroscience 301, 529 (2015).CrossRef
28.
go back to reference A. de Groote and A. de Kerchove d’Exaerde, Thalamo-Nucleus Accumbens Projections in Motivated Behaviors and Addiction. Front Syst. Neurosci. 15, (2021). A. de Groote and A. de Kerchove d’Exaerde, Thalamo-Nucleus Accumbens Projections in Motivated Behaviors and Addiction. Front Syst. Neurosci. 15, (2021).
29.
go back to reference B. Kim, H. Im, The role of the dorsal striatum in choice impulsivity. Ann. N. Y. Acad. Sci. 1451, 92 (2019).CrossRef B. Kim, H. Im, The role of the dorsal striatum in choice impulsivity. Ann. N. Y. Acad. Sci. 1451, 92 (2019).CrossRef
30.
go back to reference S.N. Haber, Corticostriatal circuitry. Dialogues Clin. Neurosci. 18, 7 (2016).CrossRef S.N. Haber, Corticostriatal circuitry. Dialogues Clin. Neurosci. 18, 7 (2016).CrossRef
31.
go back to reference R. Leech, D.J. Sharp, The role of the posterior cingulate cortex in cognition and disease. Brain 137, 12 (2014).CrossRef R. Leech, D.J. Sharp, The role of the posterior cingulate cortex in cognition and disease. Brain 137, 12 (2014).CrossRef
32.
go back to reference J.A. Brewer, K.A. Garrison, S. Whitfield-Gabrieli, What about the “Self” is Processed in the Posterior Cingulate Cortex? Front Hum. Neurosci. 7, 647 (2013).CrossRef J.A. Brewer, K.A. Garrison, S. Whitfield-Gabrieli, What about the “Self” is Processed in the Posterior Cingulate Cortex? Front Hum. Neurosci. 7, 647 (2013).CrossRef
33.
go back to reference J.N. Zhu, J.J. Wang, The cerebellum in feeding control: possible function and mechanism. Cell Mol. Neurobiol. 28, 469 (2008).CrossRef J.N. Zhu, J.J. Wang, The cerebellum in feeding control: possible function and mechanism. Cell Mol. Neurobiol. 28, 469 (2008).CrossRef
34.
go back to reference A.Y.T. Low, N. Goldstein, J.R. Gaunt, K.-P. Huang, N. Zainolabidin, A.K.K. Yip, J.R.E. Carty, J.Y. Choi, A.M. Miller, H.S.T. Ho, C. Lenherr, N. Baltar, E. Azim, O.M. Sessions, T.H. Ch’ng, A.S. Bruce, L.E. Martin, M.A. Halko, R.O. Brady, L.M. Holsen, A.L. Alhadeff, A.I. Chen, J.N. Betley, Reverse-translational identification of a cerebellar satiation network. Nature 600, 269 (2021).CrossRef A.Y.T. Low, N. Goldstein, J.R. Gaunt, K.-P. Huang, N. Zainolabidin, A.K.K. Yip, J.R.E. Carty, J.Y. Choi, A.M. Miller, H.S.T. Ho, C. Lenherr, N. Baltar, E. Azim, O.M. Sessions, T.H. Ch’ng, A.S. Bruce, L.E. Martin, M.A. Halko, R.O. Brady, L.M. Holsen, A.L. Alhadeff, A.I. Chen, J.N. Betley, Reverse-translational identification of a cerebellar satiation network. Nature 600, 269 (2021).CrossRef
35.
go back to reference E.M. Marron, R. Viejo-Sobera, G. Cuatrecasas, D. Redolar-Ripoll, P.G. Lorda, A. Datta, M. Bikson, G. Magerowski, M. Alonso-Alonso, Prefronto-cerebellar neuromodulation affects appetite in obesity. Int. J. Obes. 43, 2119 (2019).CrossRef E.M. Marron, R. Viejo-Sobera, G. Cuatrecasas, D. Redolar-Ripoll, P.G. Lorda, A. Datta, M. Bikson, G. Magerowski, M. Alonso-Alonso, Prefronto-cerebellar neuromodulation affects appetite in obesity. Int. J. Obes. 43, 2119 (2019).CrossRef
36.
go back to reference J. Cheng, J. Wang, X. Ma, R. Ullah, Y. Shen, Y.-D. Zhou, Anterior Paraventricular Thalamus to Nucleus Accumbens Projection Is Involved in Feeding Behavior in a Novel Environment. Front Mol. Neurosci. 11, 202 (2018).CrossRef J. Cheng, J. Wang, X. Ma, R. Ullah, Y. Shen, Y.-D. Zhou, Anterior Paraventricular Thalamus to Nucleus Accumbens Projection Is Involved in Feeding Behavior in a Novel Environment. Front Mol. Neurosci. 11, 202 (2018).CrossRef
37.
go back to reference G. Labouèbe, B. Boutrel, D. Tarussio, B. Thorens, Glucose-responsive neurons of the paraventricular thalamus control sucrose-seeking behavior. Nat. Neurosci. 19(8), 999 (2016).CrossRef G. Labouèbe, B. Boutrel, D. Tarussio, B. Thorens, Glucose-responsive neurons of the paraventricular thalamus control sucrose-seeking behavior. Nat. Neurosci. 19(8), 999 (2016).CrossRef
38.
go back to reference D.J. Christoffel, J.J. Walsh, B.D. Heifets, P. Hoerbelt, S. Neuner, G. Sun, V.K. Ravikumar, H. Wu, C.H. Halpern, R.C. Malenka, Input-specific modulation of murine nucleus accumbens differentially regulates hedonic feeding. Nat. Commun. 12(1), 1 (2021).CrossRef D.J. Christoffel, J.J. Walsh, B.D. Heifets, P. Hoerbelt, S. Neuner, G. Sun, V.K. Ravikumar, H. Wu, C.H. Halpern, R.C. Malenka, Input-specific modulation of murine nucleus accumbens differentially regulates hedonic feeding. Nat. Commun. 12(1), 1 (2021).CrossRef
39.
go back to reference D. Milardi, A. Quartarone, A. Bramanti, G. Anastasi, S. Bertino, G.A. Basile, P. Buonasera, G. Pilone, G. Celeste, G. Rizzo, D. Bruschetta, A. Cacciola, The Cortico-Basal Ganglia-Cerebellar Network: Past, Present and Future Perspectives. Front Syst. Neurosci. 13, 61 (2019).CrossRef D. Milardi, A. Quartarone, A. Bramanti, G. Anastasi, S. Bertino, G.A. Basile, P. Buonasera, G. Pilone, G. Celeste, G. Rizzo, D. Bruschetta, A. Cacciola, The Cortico-Basal Ganglia-Cerebellar Network: Past, Present and Future Perspectives. Front Syst. Neurosci. 13, 61 (2019).CrossRef
40.
go back to reference D. Ballotta, F. Talami, F. Pizza, A.E. Vaudano, F. Benuzzi, G. Plazzi, S. Meletti, Hypothalamus and amygdala functional connectivity at rest in narcolepsy type 1. Neuroimage Clin. 31, 102748 (2021).CrossRef D. Ballotta, F. Talami, F. Pizza, A.E. Vaudano, F. Benuzzi, G. Plazzi, S. Meletti, Hypothalamus and amygdala functional connectivity at rest in narcolepsy type 1. Neuroimage Clin. 31, 102748 (2021).CrossRef
41.
go back to reference E.E. Noble, Z. Wang, C.M. Liu, E.A. Davis, A.N. Suarez, L.M. Stein, L. Tsan, S.J. Terrill, T.M. Hsu, A.H. Jung, L.M. Raycraft, J.D. Hahn, M. Darvas, A.M. Cortella, L.A. Schier, A.W. Johnson, M.R. Hayes, D.P. Holschneider, S.E. Kanoski, Hypothalamus-hippocampus circuitry regulates impulsivity via melanin-concentrating hormone. Nat. Commun. 10(1), 1 (2019).CrossRef E.E. Noble, Z. Wang, C.M. Liu, E.A. Davis, A.N. Suarez, L.M. Stein, L. Tsan, S.J. Terrill, T.M. Hsu, A.H. Jung, L.M. Raycraft, J.D. Hahn, M. Darvas, A.M. Cortella, L.A. Schier, A.W. Johnson, M.R. Hayes, D.P. Holschneider, S.E. Kanoski, Hypothalamus-hippocampus circuitry regulates impulsivity via melanin-concentrating hormone. Nat. Commun. 10(1), 1 (2019).CrossRef
42.
go back to reference O. Contreras-Rodríguez, R. Vilar-López, Z.B. Andrews, J.F. Navas, C. Soriano-Mas, A. Verdejo-García, Altered cross-talk between the hypothalamus and non-homeostatic regions linked to obesity and difficulty to lose weight. Sci. Rep. 7(1), 1 (2017).CrossRef O. Contreras-Rodríguez, R. Vilar-López, Z.B. Andrews, J.F. Navas, C. Soriano-Mas, A. Verdejo-García, Altered cross-talk between the hypothalamus and non-homeostatic regions linked to obesity and difficulty to lose weight. Sci. Rep. 7(1), 1 (2017).CrossRef
43.
go back to reference M.H. Lundqvist, K. Almby, N. Abrahamsson, J.W. Eriksson, Is the Brain a Key Player in Glucose Regulation and Development of Type 2 Diabetes? Front Physiol. 10, 1 (2019).CrossRef M.H. Lundqvist, K. Almby, N. Abrahamsson, J.W. Eriksson, Is the Brain a Key Player in Glucose Regulation and Development of Type 2 Diabetes? Front Physiol. 10, 1 (2019).CrossRef
Metadata
Title
Effects of gastric bypass surgery on brain connectivity responses to hypoglycemia
Authors
Giovanni Fanni
Christakis Kagios
Erika Roman
Magnus Sundbom
Johan Wikström
Sven Haller
Jan W. Eriksson
Publication date
02-12-2022
Publisher
Springer US
Keyword
Hypoglycemia
Published in
Endocrine / Issue 2/2023
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-022-03253-y

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