Functional Neuroanatomy and Sleep-Disordered Breathing: Implications for Autonomic Regulation

Anatomical Record

Volumn 295, Issue 9, 2012, Pages 1385-1395

  Harper, Ronald M ^a,b   Kumar, Rajesh ^a   Macey, Paul M ^b   Ogren, Jennifer A ^b   Richardson, Heidi L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Congenital central hypoventilation syndrome; Diabetes; Magnetic resonance imaging; Obstructive sleep apnea

Indexed keywords

AMYGDALOID NUCLEUS; ARTICLE; AUTONOMIC DYSFUNCTION; AUTONOMIC NERVOUS SYSTEM FUNCTION; CENTRAL APNEA; CEREBELLUM; CONGENITAL CENTRAL HYPOVENTILATION SYNDROME; CORPUS CALLOSUM; DIABETIC PATIENT; HORMONE RELEASE; HUMAN; HYPOTHALAMUS; INSULA; NEUROANATOMY; NON INSULIN DEPENDENT DIABETES MELLITUS; NUCLEAR MAGNETIC RESONANCE IMAGING; OXYGENATION; PANCREAS; PRIORITY JOURNAL; SLEEP APNEA SYNDROME; SLEEP DISORDERED BREATHING; SYMPATHETIC FUNCTION; VISCERA;

ANIMALS; AUTONOMIC NERVOUS SYSTEM; BRAIN; BRAIN INJURIES; DIABETES MELLITUS; HUMANS; SLEEP APNEA SYNDROMES;

EID: 84865281936     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.22514     Document Type: Article

References (77)

1. Allison KC, Ahima RS, O'Reardon JP, Dinges DF, Sharma V, Cummings DE, Heo M, Martino NS, Stunkard AJ. 2005. Neuroendocrine profiles associated with energy intake, sleep, and stress in the night eating syndrome. J Clin Endocrinol Metab 90: 6214-6217.
2. Amin A, Dhillo WS, Murphy KG. 2011. The central effects of thyroid hormones on appetite. J Thyroid Res 2011: 306510.
3. Araki Y, Nomura M, Tanaka H, Yamamoto H, Yamamoto T, Tsukaguchi I, Nakamura H. 1994. MRI of the brain in diabetes mellitus. Neuroradiology 36: 101-103.
4. Aronsohn RS, Whitmore H, Van Cauter E, Tasali E. 2010. Impact of untreated obstructive sleep apnea on glucose control in type 2 diabetes. Am J Respir Crit Care Med 181: 507-513.
5. Aurora RN, Punjabi NM. 2007. Sleep apnea and metabolic dysfunction: cause or co-relation? Sleep Med Clin 2: 237-250.
6. Barbe F, Duran-Cantolla J, Capote F, de la Pena M, Chiner E, Masa JF, Gonzalez M, Marin JM, Garcia-Rio F, de Atauri JD, Teran J, Mayos M, Monasterio C, del Campo F, Gomez S, de la Torre MS, Martinez M, Montserrat JM. 2010. Long-term effect of continuous positive airway pressure in hypertensive patients with sleep apnea. Am J Respir Crit Care Med 181: 718-726.
7. Bedard MA, Montplaisir J, Richer F, Rouleau I, Malo J. 1991. Obstructive sleep apnea syndrome: pathogenesis of neuropsychological deficits. J Clin Exp Neuropsychol 13: 950-964.
8. Berry-Kravis EM, Zhou L, Rand CM, Weese-Mayer DE. 2006. Congenital central hypoventilation syndrome: PHOX2B mutations and phenotype. Am J Respir Crit Care Med 174: 1139-1144.
9. Berry DT, Webb WB, Block AJ, Bauer RM, Switzer DA. 1986. Nocturnal hypoxia and neuropsychological variables. J Clin Exp Neuropsychol 8: 229-238.
10. Biessels GJ, Koffeman A, Scheltens P. 2006. Diabetes and cognitive impairment. Clinical diagnosis and brain imaging in patients attending a memory clinic. J Neurol 253: 477-482.
11. Bradley TD, Floras JS. 2003a. Sleep apnea and heart failure: Part I: obstructive sleep apnea. Circulation 107: 1671-1678.
12. Bradley TD, Floras JS. 2003b. Sleep apnea and heart failure: Part II: central sleep apnea. Circulation 107: 1822-1826.
13. Canessa N, Castronovo V, Cappa SF, Aloia MS, Marelli S, Falini A, Alemanno F, Ferini-Strambi L. 2011. Obstructive sleep apnea: brain structural changes and neurocognitive function before and after treatment. Am J Respir Crit Care Med 35: 41-48.
14. Coughlin SR, Mawdsley L, Mugarza JA, Calverley PM, Wilding JP. 2004. Obstructive sleep apnoea is independently associated with an increased prevalence of metabolic syndrome. Eur Heart J 25: 735-741.
15. Cross RL, Kumar R, Macey PM, Doering LV, Alger JR, Yan-Go FL, Harper RM. 2008. Neural alterations and depressive symptoms in obstructive sleep apnea patients. Sleep 31: 1103-1039.
16. Curb JD, Rodriguez BL, Burchfiel CM, Abbott RD, Chiu D, Yano K. 1995. Sudden death, impaired glucose tolerance, and diabetes in Japanese American men. Circulation 91: 2591-2595.
17. den Heijer T, Vermeer SE, van Dijk EJ, Prins ND, Koudstaal PJ, Hofman A, Breteler MM. 2003. Type 2 diabetes and atrophy of medial temporal lobe structures on brain MRI. Diabetologia 46: 1604-1610.
18. Felver-Gant JC, Bruce AS, Zimmerman M, Sweet LH, Millman RP, Aloia MS. 2007. Working memory in obstructive sleep apnea: construct validity and treatment effects. J Clin Sleep Med 3: 589-594.
19. Ferini-Strambi L, Baietto C, Di Gioia MR, Castaldi P, Castronovo C, Zucconi M, Cappa SF. 2003. Cognitive dysfunction in patients with obstructive sleep apnea (OSA): partial reversibility after continuous positive airway pressure (CPAP). Brain Res Bull 61: 87-92.
20. Foster GD, Sanders MH, Millman R, Zammit G, Borradaile KE, Newman AB, Wadden TA, Kelley D, Wing RR, Sunyer FX, Darcey V, Kuna ST. 2009. Obstructive sleep apnea among obese patients with type 2 diabetes. Diabetes Care 32: 1017-1019.
21. Gami AS, Pressman G, Caples SM, Kanagala R, Gard JJ, Davison DE, Malouf JF, Ammash NM, Friedman PA, Somers VK. 2004. Association of atrial fibrillation and obstructive sleep apnea. Circulation 110: 364-367.
22. Harper RM, Bandler R, Spriggs D, Alger JR. 2000. Lateralized and widespread brain activation during transient blood pressure elevation revealed by magnetic resonance imaging. J Comp Neurol 417: 195-204.
23. Harper RM, Macey PM, Henderson LA, Woo MA, Macey KE, Frysinger RC, Alger JR, Nguyen KP, Yan-Go FL. 2003. FMRI responses to cold pressor challenges in control and obstructive sleep apnea subjects. J Appl Physiol 94: 1583-1595.
24. Harper RM, Macey PM, Kumar R, Woo MA. 2009. Neural injury in diabetic versus non-diabetic obstructive sleep apnea patients: a pilot study. Sleep 32: A341.
25. Henderson LA, Woo MA, Macey PM, Macey KE, Frysinger RC, Alger JR, Yan-Go F, Harper RM. 2003. Neural responses during Valsalva maneuvers in obstructive sleep apnea syndrome. J Appl Physiol 94: 1063-1074.
26. Hiestand DM, Britz P, Goldman M, Phillips B. 2006. Prevalence of symptoms and risk of sleep apnea in the US population: results from the national sleep foundation sleep in America 2005 poll. Chest 130: 780-786.
27. Hsu JL, Chen YL, Leu JG, Jaw FS, Lee CH, Tsai YF, Hsu CY, Bai CH, Leemans A. 2012. Microstructural white matter abnormalities in type 2 diabetes mellitus: a diffusion tensor imaging study. Neuroimage 59: 1098-1105.
28. Joo EY, Tae WS, Lee MJ, Kang JW, Park HS, Lee JY, Suh M, Hong SB. 2010. Reduced brain gray matter concentration in patients with obstructive sleep apnea syndrome. Sleep 33: 235-241.
29. Kamba M, Inoue Y, Higami S, Suto Y, Ogawa T, Chen W. 2001. Cerebral metabolic impairment in patients with obstructive sleep apnoea: an independent association of obstructive sleep apnoea with white matter change. J Neurol Neurosurg Psychiatry 71: 334-339.
30. Kumar R, Birrer BV, Macey PM, Woo MA, Gupta RK, Yan-Go FL, Harper RM. 2008a. Reduced mammillary body volume in patients with obstructive sleep apnea. Neurosci Lett 438: 330-334.
31. Kumar R, Chavez AS, Macey PM, Woo MA, Yan-Go F, Harper RM. 2012. Altered global and regional mean diffusivity alterations in patients with obstructive sleep apnea. J Neurosci Res: DOI: 10.1002/jnr.23083.
32. Kumar R, Macey PM, Cross RL, Woo MA, Yan-Go FL, Harper RM. 2009. Neural alterations associated with anxiety symptoms in obstructive sleep apnea syndrome. Depress Anxiety 26: 480-491.
33. Kumar R, Macey PM, Woo MA, Alger JR, Harper RM. 2006a. Elevated mean diffusivity in widespread brain regions in congenital central hypoventilation syndrome. J Magn Reson Imaging 24: 1252-1258.
34. Kumar R, Macey PM, Woo MA, Alger JR, Harper RM. 2008b. Diffusion tensor imaging demonstrates brainstem and cerebellar abnormalities in congenital central hypoventilation syndrome. Pediatr Res 64: 275-280.
35. Kumar R, Macey PM, Woo MA, Alger JR, Keens TG, Harper RM. 2005. Neuroanatomic deficits in congenital central hypoventilation syndrome. J Comp Neurol 487: 361-371.
36. Kumar R, Macey PM, Woo MA, Harper RM. 2010. Rostral brain axonal injury in congenital central hypoventilation syndrome. J Neurosci Res 88: 2146-2154.
37. Kumar R, Macey PM, Woo MA, Harper RM. 2011. Selectively diminished corpus callosum fibers in congenital central hypoventilation syndrome. Neuroscience 178: 261-269.
38. Kumar R, Macey PM, Woo MA, Valladares E, Alger JR, Yan-Go F, Harper R. 2006b. Abnormal T2 values in obstructive sleep apnea. Soc Neurosci Abs:308.10.
39. Lee W, Nagubadi S, Kryger MH, Mokhlesi B. 2008. Epidemiology of obstructive sleep apnea: a population-based perspective. Expert Rev Respir Med 2: 349-364.
40. Leung RS. 2009. Sleep-disordered breathing: autonomic mechanisms and arrhythmias. Prog Cardiovasc Dis 51: 324-338.
41. Lutherer LO, Lutherer BC, Dormer KJ, Janssen HF, Barnes CD. 1983. Bilateral lesions of the fastigial nucleus prevent the recovery of blood pressure following hypotension induced by hemorrhage or administration of endotoxin. Brain Res 269: 251-257.
42. Macefield VG, Rundqvist B, Sverrisdottir YB, Wallin BG, Elam M. 1999. Firing properties of single muscle vasoconstrictor neurons in the sympathoexcitation associated with congestive heart failure. Circulation 100: 1708-1713.
43. Macey PM, Harper RM. 2005. OSA brain morphology differences: magnitude of loss approximates age-related effects. Am J Respir Crit Care Med 172: 1056-1057.
44. Macey PM, Henderson LA, Macey KE, Alger JR, Frysinger RC, Woo MA, Harper RK, Yan-Go FL, Harper RM. 2002. Brain morphology associated with obstructive sleep apnea. Am J Respir Crit Care Med 166: 1382-1387.
45. Macey PM, Kumar R, Woo MA, Valladares EM, Yan-Go FL, Harper RM. 2008. Brain structural changes in obstructive sleep apnea. Sleep 31: 967-977.
46. Macey PM, Wu P, Kumar R, Ogren JA, Richardson HL, Woo MA, Harper RM. 2012. Differential responses of the insular cortex gyri to autonomic challenges. Auton Neurosci 168:72-81.
47. Marshall NS, Won KKH, Liu PY, Cullen SRJ, Knuiman MW, Grunstein RR. 2008. Sleep apnea as an independent risk factor for all-cause mortality: the Busselton Health Study. Sleep 31: 1079-1085.
48. Matera I, Bachetti T, Puppo F, Di Duca M, Morandi F, Casiraghi GM, Cilio MR, Hennekam R, Hofstra R, Schober JG, Ravazzolo R, Ottonello G, Ceccherini I. 2004. PHOX2B mutations and polyalanine expansions correlate with the severity of the respiratory phenotype and associated symptoms in both congenital and late onset Central Hypoventilation syndrome. J Med Genet 41: 373-380.
49. Morrell MJ, Jackson ML, Twigg GL, Ghiassi R, McRobbie DW, Quest RA, Pardoe H, Pell GS, Abbott DF, Rochford PD, Jackson GD, Pierce RJ, O'Donoghue FJ, Corfield DR. 2010. Changes in brain morphology in patients with obstructive sleep apnoea. Thorax 65: 908-914.
50. Morrell MJ, McRobbie DW, Quest RA, Cummin AR, Ghiassi R, Corfield DR. 2003. Changes in brain morphology associated with obstructive sleep apnea. Sleep Med 4: 451-454.
51. Naegele B, Pepin JL, Levy P, Bonnet C, Pellat J, Feuerstein C. 1998. Cognitive executive dysfunction in patients with obstructive sleep apnea syndrome (OSAS) after CPAP treatment. Sleep 21: 392-397.
52. O'Donoghue FJ, Wellard RM, Rochford PD, Dawson A, Barnes M, Ruehland WR, Jackson ML, Howard ME, Pierce RJ, Jackson GD. 2012. Magnetic resonance spectroscopy and neurocognitive dysfunction in obstructive sleep apnea before and after CPAP treatment. Sleep 35: 41-48.
53. Ohga E, Tomita T, Wada H, Yamamoto H, Nagase T, Ouchi Y. 2003. Effects of obstructive sleep apnea on circulating ICAM-1, IL-8, and MCP-1. J Appl Physiol 94: 179-184.
54. Oppenheimer SM. 2006. Cerebrogenic cardiac arrhythmias: cortical lateralization and clinical significance. Clin Auton Res 16: 6-11.
55. Oppenheimer SM, Gelb A, Girvin JP, Hachinski VC. 1992. Cardiovascular effects of human insular cortex stimulation. Neurology 42: 1727-1732.
56. Oppenheimer SM, Wilson JX, Guiraudon C, Cechetto DF. 1991. Insular cortex stimulation produces lethal cardiac arrhythmias: a mechanism of sudden death? Brain Res 550: 115-121.
57. Patel DG. 1984. Role of sympathetic nervous system in glucagon response to insulin hypoglycemia in normal and diabetic rats. Diabetes 33: 1154-1159.
58. Peppard PE, Young T, Palta M, Skatrud J. 2000. Prospective study of the association between sleep-disordered breathing and hypertension. N Engl J Med 342: 1378-1384.
59. Popovic V, Duntas LH. 2005. Leptin TRH and ghrelin: influence on energy homeostasis at rest and during exercise. Horm Metab Res 37: 533-537.
60. Redeker NS, Muench U, Zucker MJ, Walsleben J, Gilbert M, Freudenberger R, Chen M, Campbell D, Blank L, Berkowitz R, Adams L, Rapoport DM. 2010. Sleep disordered breathing, daytime symptoms, and functional performance in stable heart failure. Sleep 33: 551-560.
61. Saper CB. 2002. The central autonomic nervous system: conscious visceral perception and autonomic pattern generation. Annu Rev Neurosci 25: 433-469.
62. Saper CB, Scammell TE, Lu J. 2005. Hypothalamic regulation of sleep and circadian rhythms. Nature 437: 1257-1263.
63. Saunamaki T, Himanen SL, Polo O, Jehkonen M. 2010. Executive dysfunction and learning effect after continuous positive airway pressure treatment in patients with obstructive sleep apnea syndrome. Eur Neurol 63: 215-220.
64. Sforza E, de Saint Hilaire Z, Pelissolo A, Rochat T, Ibanez V. 2002. Personality, anxiety and mood traits in patients with sleep-related breathing disorders: effect of reduced daytime alertness. Sleep Med 3: 139-145.
65. Shahar E, Whitney CW, Redline S, Lee ET, Newman AB, Javier Nieto F, O'Connor GT, Boland LL, Schwartz JE, Samet JM. 2001. Sleep-disordered breathing and cardiovascular disease: cross-sectional results of the Sleep Heart Health Study. Am J Respir Crit Care Med 163: 19-25.
66. Somers VK, Dyken ME, Clary MP, Abboud FM. 1995. Sympathetic neural mechanisms in obstructive sleep apnea. J Clin Invest 96: 1897-1904.
67. Steiger A, Dresler M, Schussler P, Kluge M. 2011. Ghrelin in mental health, sleep, memory. Mol Cell Endocrinol 340: 88-96.
68. Tasali E, Mokhlesi B, Van Cauter E. 2008. Obstructive sleep apnea and type 2 diabetes: interacting epidemics. Chest 133: 496-506.
69. Thompson PM, Hayashi KM, De Zubicaray GI, Janke AL, Rose SE, Semple J, Hong MS, Herman DH, Gravano D, Doddrell DM, Toga AW. 2004. Mapping hippocampal and ventricular change in Alzheimer disease. Neuroimage 22: 1754-1766.
70. Torelli F, Moscufo N, Garreffa G, Placidi F, Romigi A, Zannino S, Bozzali M, Fasano F, Giulietti G, Djonlagic I, Malhotra A, Marciani MG, Guttmann CR. 2011. Cognitive profile and brain morphological changes in obstructive sleep apnea. Neuroimage 54: 787-793.
71. Weese-Mayer DE, Berry-Kravis EM, Ceccherini I, Keens TG, Loghmanee DA, Trang H. 2010. An official ATS clinical policy statement: congenital central hypoventilation syndrome: genetic basis, diagnosis, and management. Am J Respir Crit Care Med 181: 626-644.
72. Woo MS, Woo MA, Gozal D, Jansen MT, Keens TG, Harper RM. 1992. Heart rate variability in congenital central hypoventilation syndrome. Pediatr Res 31: 291-296.
73. Wu P, Macey PM, Kumar R, Harper RM. 2010. Axonal projections between insular gyri and the hypothalamus. Soc Neurosci Abs:694.7.
74. Wu P, Macey PM, Kumar R, Woo MA, Harper RM. 2011. Functional topography of insular cortex responses to the Valsalva maneuver is impaired in obstructive sleep apnea. Soc Neurosci Abs:283.05.
75. Yaouhi K, Bertran F, Clochon P, Mezenge F, Denise P, Foret J, Eustache F, Desgranges B. 2009. A combined neuropsychological and brain imaging study of obstructive sleep apnea. J Sleep Res 18: 36-48.
76. Young T, Finn L, Peppard PE, Szklo-Coxe M, Austin D, Nieto FJ, Stubbs R, Hla KM. 2008. Sleep disordered breathing and mortality: eighteen-year follow-up of the Wisconsin sleep cohort. Sleep 31: 1071-1078.
77. Young T, Peppard PE, Gottlieb DJ. 2002. Epidemiology of obstructive sleep apnea: a population health perspective. Am J Respir Crit Care Med 165: 1217-1239.