Functional connectivity of insula, basal ganglia, and prefrontal executive control networks during hypoglycemia in type 1 diabetes

Journal of Neuroscience

Volumn 35, Issue 31, 2015, Pages 11012-11023

  Bolo, Nicolas R ^a,b,e   Musen, Gail ^b,c   Simonson, Donald C ^b,d   Nickerson, Lisa D ^a,b   Flores, Veronica L ^c   Siracusa, Tamar ^a   Hager, Brandon ^e   Lyoo, In Kyoon ^f   Renshaw, Perry F ^a,b,h   Jacobson, Alan M ^b,c,g  

^a MCLEAN HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c JOSLIN DIABETES CENTER   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^f Ewha Womans University   (South Korea)

^g WINTHROP UNIVERSITY HOSPITAL   (United States)

^h UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Executive control resting state network; Functional connectivity; Functional magnetic resonance imaging; Hypoglycemia; Independent component analysis; Type 1 diabetes

Indexed keywords

HEMOGLOBIN A1C;

ADULT; ARTICLE; BASAL GANGLION; CLINICAL ARTICLE; CONNECTOME; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXECUTIVE FUNCTION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GLYCEMIC CONTROL; HUMAN; HYPERGLYCEMIA; HYPOGLYCEMIA; INSULA; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PREFRONTAL CORTEX; PRIORITY JOURNAL; QUESTIONNAIRE; RADIOIMMUNOASSAY; SCORING SYSTEM; YOUNG ADULT; BRAIN CORTEX; BRAIN MAPPING; NERVE CELL NETWORK; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY;

ADULT; BASAL GANGLIA; BRAIN MAPPING; CEREBRAL CORTEX; DIABETES MELLITUS, TYPE 1; EXECUTIVE FUNCTION; FEMALE; HUMANS; HYPOGLYCEMIA; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NERVE NET; PREFRONTAL CORTEX; YOUNG ADULT;

EID: 84938817505     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0319-15.2015     Document Type: Article

References (45)

1. Albert NB, Robertson EM, Miall RC (2009) The resting human brain and motor learning. Curr Biol 19:1023–1027. CrossRef Medline
2. Allen EA, Erhardt EB, Wei Y, Eichele T, Calhoun VD (2012) Capturing inter-subject variability with group independent component analysis of fMRI data: a simulation study. Neuroimage 59:4141–4159. CrossRef Medline
3. Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005) Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 360:1001–1013. CrossRef Medline
4. Bingham EM, Hopkins D, Smith D, Pernet A, Hallett W, Reed L, Marsden PK, Amiel SA (2002) The role of insulin in human brain glucose metabolism: an 18fluoro-deoxyglucose positron emission tomography study. Diabetes 51:3384–3390. CrossRef Medline
5. Bischof MG, Brehm A, Bernroider E, Krssák M, Mlynárik V, Krebs M, Roden M (2006) Cerebral glutamate metabolism during hypoglycaemia in healthy and type 1 diabetic humans. Eur J Clin Invest 36:164–169. CrossRef Medline
6. Bolo NR, Musen G, Jacobson AM, Weinger K, McCartney RL, Flores V, Renshaw PF, Simonson DC (2011) Brain activation during working memory is altered in patients with type 1 diabetes during hypoglycemia. Diabetes 60:3256–3264. CrossRef Medline
7. Clarke WL, Cox DJ, Gonder-Frederick LA, Julian D, Schlundt D, Polonsky W (1995) Reduced awareness of hypoglycemia in adults with IDDM. A prospective study of hypoglycemic frequency and associated symptoms. Diabetes Care 18:517–522. CrossRef Medline
8. Corbetta M (2012) Functional connectivity and neurological recovery. Dev Psychobiol 54:239–253. CrossRef Medline
9. Craft S, Watson GS (2004) Insulin and neurodegenerative disease: shared and specific mechanisms. Lancet Neurol 3:169–178. CrossRef Medline
10. Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3:655–666. CrossRef Medline
11. Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ (2004) Neural systems supporting interoceptive awareness. Nat Neurosci 7:189–195. CrossRef Medline
12. Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci U S A 103:13848–13853. CrossRef Medline
13. Filippini N, MacIntosh BJ, Hough MG, Goodwin GM, Frisoni GB, Smith SM, Matthews PM, Beckmann CF, Mackay CE (2009) Distinct patterns of brain activity in young carriers of the APOE-epsilon4 allele. Proc Natl Acad Sci U S A 106:7209–7214. CrossRef Medline
14. Fornito A, Bullmore ET (2010) What can spontaneous fluctuations of the blood oxygenation-level-dependent signal tell us about psychiatric disorders? Curr Opin Psychiatry 23:239–249. CrossRef Medline
15. Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711. CrossRef Medline
16. Grabner G, Janke AL, Budge MM, Smith D, Pruessner J, Collins DL (2006) Symmetric atlasing and model based segmentation: an application to the hippocampus in older adults. Med Image Comput Comput Assist Interv 9:58–66. Medline
17. Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825–841. CrossRef Medline
18. Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM (2012) FSL. Neuroimage 62:782–790. CrossRef Medline
19. Kapogiannis D, Reiter DA, Willette AA, Mattson MP (2013) Posteromedial cortex glutamate and GABA predict intrinsic functional connectivity of the default mode network. Neuroimage 64:112–119. CrossRef Medline
20. Kullmann S, Heni M, Veit R, Ketterer C, Schick F, Häring HU, Fritsche A, Preissl H (2012) The obese brain: association of body mass index and insulin sensitivity with resting state network functional connectivity. Hum Brain Mapp 33:1052–1061. CrossRef Medline
21. Kullmann S, Pape AA, Heni M, Ketterer C, Schick F, Häring HU, Fritsche A, Preissl H, Veit R (2013) Functional network connectivity underlying food processing: disturbed salience and visual processing in overweight and obese adults. Cereb Cortex 23:1247–1256. CrossRef Medline
22. Laird AR, Fox PM, Eickhoff SB, Turner JA, Ray KL, McKay DR, Glahn DC, Beckmann CF, Smith SM, Fox PT (2011) Behavioral interpretations of intrinsic connectivity networks. J Cogn Neurosci 23:4022–4037. CrossRef Medline
23. Lewis CM, Baldassarre A, Committeri G, Romani GL, Corbetta M (2009) Learning sculpts the spontaneous activity of the resting human brain. Proc Natl Acad Sci U S A 106:17558–17563. CrossRef Medline
24. Lyoo IK, Yoon SJ, Musen G, Simonson DC, Weinger K, Bolo N, Ryan CM, Kim JE, Renshaw PF, Jacobson AM (2009) Altered prefrontal glutamateglutamine- gamma-aminobutyric acid levels and relation to low cognitive performance and depressive symptoms in type 1 diabetes mellitus. Arch Gen Psychiatry 66:878–887. CrossRef Medline
25. Lyoo IK, Yoon S, Jacobson AM, Hwang J, Musen G, Kim JE, Simonson DC, Bae S, Bolo N, Kim DJ, Weinger K, Lee JH, Ryan CM, Renshaw PF (2012) Prefrontal cortical deficits in type 1 diabetes mellitus: brain correlates of comorbid depression. Arch Gen Psychiatry 69:1267–1276. CrossRef Medline
26. Musen G, Simonson DC, Bolo NR, Driscoll A, Weinger K, Raji A, Théberge J, Renshaw PF, Jacobson AM (2008) Regional brain activation during hypoglycemia in type 1 diabetes. J Clin Endocrinol Metab 93:1450–1457. CrossRef Medline
27. Nichols T, Hayasaka S (2003) Controlling the familywise error rate in func-tional neuroimaging: a comparative review. Stat Methods Med Res 12: 419–446. CrossRef Medline
28. Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1–25. CrossRef Medline
29. Öz G, Tesfaye N, Kumar A, Deelchand DK, Eberly LE, Seaquist ER (2012) Brain glycogen content and metabolism in subjects with type 1 diabetes and hypoglycemia unawareness. J Cereb Blood Flow Metab 32:256–263. CrossRef Medline
30. Page KA, Seo D, Belfort-DeAguiar R, Lacadie C, Dzuira J, Naik S, Amarnath S, Constable RT, Sherwin RS, Sinha R (2011) Circulating glucose levels modulate neural control of desire for high-calorie foods in humans. J Clin Invest 121:4161–4169. CrossRef Medline
31. Perneger TV (1998) What’s wrong with Bonferroni adjustments. BMJ 316: 1236–1238.
32. CrossRef Medline
33. Redgrave P, Rodriguez M, Smith Y, Rodriguez-Oroz MC, Lehericy S, Bergman H, Agid Y, DeLong MR, Obeso JA (2010) Goal-directed and habitual control in the basal ganglia: implications for Parkinson’s disease. Nat Rev Neurosci 11:760–772. CrossRef Medline
34. Schulingkamp RJ, Pagano TC, Hung D, Raffa RB (2000) Insulin receptors and insulin action in the brain: review and clinical implications. Neurosci Biobehav Rev 24:855–872. CrossRef Medline
35. Seaquist ER, Öz G (2013) Diabetes: does lactate sustain brain metabolism during hypoglycaemia? Nat Rev Endocrinol 9:386–387. CrossRef Medline
36. Simmons WK, Avery JA, Barcalow JC, Bodurka J, Drevets WC, Bellgowan P (2013) Keeping the body in mind: insula functional organization and functional connectivity integrate interoceptive, exteroceptive, and emotional awareness. Hum Brain Mapp 34:2944–2958. CrossRef Medline
37. Smith SM (2002) Fast robust automated brain extraction.HumBrain Mapp 17:143–155. CrossRef Medline
38. Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structuralMRimage analysis and implementation as FSL. Neuroimage 23 [1]:S208–S219. CrossRef
39. Smith SM, Beckmann CF, Ramnani N, Woolrich MW, Bannister PR, Jenkinson M, Matthews PM, McGonigle DJ (2005) Variability in fMRI: A reexamination of inter-session differences. Hum Brain Mapp 24:248–257. CrossRef Medline
40. Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF (2009) Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci U S A 106:13040–13045. CrossRef Medline
41. Teh MM, Dunn JT, Choudhary P, Samarasinghe Y, Macdonald I, O’Doherty M, Marsden P, Reed LJ, Amiel SA (2010) Evolution and resolution of human brain perfusion responses to the stress of induced hypoglycemia. Neuroimage 53:584–592. CrossRef Medline
42. Terpstra M, Moheet A, Kumar A, Eberly LE, Seaquist E, Öz G (2014) Changes in human brain glutamate concentration during hypoglycemia: insights into cerebral adaptations in hypoglycemia-associated autonomic failure in type 1 diabetes. J Cereb Blood Flow Metab 34:876–882. CrossRef Medline
43. van de Ven K, Tack CJ, Heerschap A, van der Graaf M, de Galan BE (2013) Patients with type 1 diabetes exhibit altered cerebral metabolism during hypoglycemia. J Clin Invest 123:623–629. CrossRef Medline
44. van Duinkerken E, Schoonheim MM, Sanz-Arigita EJ, Ijzerman RG, Moll AC, Snoek FJ, Ryan CM, Klein M, Diamant M, Barkhof F (2012) Restingstate brain networks in type 1 diabetic patients with and without microangiopathy and their relation to cognitive functions and disease variables. Diabetes 61:1814–1821. CrossRef Medline
45. Yin HH, Knowlton BJ (2006) The role of the basal ganglia in habit formation. Nat Rev Neurosci 7:464–476. CrossRef Medline