Hippocampal hypertrophy and sleep apnea: A role for the ischemic preconditioning?

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Rosenzweig, Ivana ^a,b   Kempton, Matthew J ^a   Crum, William R ^a   Glasser, Martin ^c,d   Milosevic, Milan ^e   Beniczky, Sandor ^b,f   Corfield, Douglas R ^g   Williams, Steven C ^a   Morrell, Mary J ^c,d  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b DANISH EPILEPSY CENTRE   (Denmark)

^c NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^d ROYAL BROMPTON AND HAREFIELD NHS FOUNDATION TRUST   (United Kingdom)

^e UNIVERSITY OF ZAGREB   (Croatia)

^f AARHUS UNIVERSITY HOSPITAL   (Denmark)

^g UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BRAIN DISEASE; BRAIN SIZE; CEREBELLUM; CEREBELLUM CORTEX; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; HIPPOCAMPAL HYPERTROPHY; HUMAN; HYPERTROPHY; ISCHEMIC PRECONDITIONING; MIDDLE AGED; SLEEP DISORDERED BREATHING; THALAMUS; CLINICAL TRIAL; FEMALE; HIPPOCAMPUS; MALE; PATHOPHYSIOLOGY; RADIOGRAPHY;

ADULT; FEMALE; HIPPOCAMPUS; HUMANS; HYPERTROPHY; ISCHEMIC PRECONDITIONING; MALE; MIDDLE AGED; SLEEP APNEA SYNDROMES;

EID: 84892661047     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0083173     Document Type: Article

References (72)

1. Ayalon L, Ancoli-Israel S, Drummond SP (2010) Obstructive sleep apnea and age: a double insult to brain function? Am J Respir Crit Care Med 182: 413-419. doi:10.1164/rccm.200912-1805OC. PubMed: 20395556.
2. Li Y, Veasey SC (2012) Neurobiology and neuropathophysiology of obstructive sleep apnea. Neuromolecular Med 14: 168-179. doi: 10.1007/s12017-011-8165-7. PubMed: 22169915.
3. Durgan DJ, Bryan RM Jr. (2012) Cerebrovascular consequences of obstructive sleep apnea. J Am Heart Assoc 1: e000091.
4. Haddad GG, Yu SP (2009) Brain hypoxia and ischemia : with special emphasis on development. xi. New York: Humana Press. 343 pp.
5. Redline S, Yenokyan G, Gottlieb DJ, Shahar E, O'Connor GT et al. (2010) Obstructive sleep apnea-hypopnea and incident stroke: the sleep heart health study. Am J Respir Crit Care Med 182: 269-277. doi: 10.1164/rccm.200911-1746OC. PubMed: 20339144.
6. Yaggi HK, Concato J, Kernan WN, Lichtman JH, Brass LM et al. (2005) Obstructive sleep apnea as a risk factor for stroke and death. N Engl J Med 353: 2034-2041. doi:10.1056/NEJMoa043104. PubMed: 16282178.
7. Munoz R, Duran-Cantolla J, Martínez-Vila E, Gallego J, Rubio R et al. (2006) Severe sleep apnea and risk of ischemic stroke in the elderly. Stroke 37: 2317-2321. doi:10.1161/01.STR.0000236560.15735.0f. PubMed: 16888274.
8. Somers VK, White DP, Amin R, Abraham WT, Costa F, et al. (2008) Sleep apnea and cardiovascular disease: an American Heart Association/american College Of Cardiology Foundation Scientific Statement from the American Heart Association Council for High Blood Pressure Research Professional Education Committee, Council on Clinical Cardiology, Stroke Council, and Council On Cardiovascular Nursing. In collaboration with the National Heart, Lung, and Blood Institute National Center on Sleep Disorders Research (National Institutes of Health). Circulation 118: 1080-1111.
9. Gozal D (2013) CrossTalk proposal: The intermittent hypoxia attending severe obstructive sleep apnoea does lead to alterations in brain structure and function. J Physiol 591: 379-381. doi:10.1113/jphysiol.2012.241216. PubMed: 23322286.
10. Rosenzweig I, Williams SC, Morrell MJ (2013) CrossTalk opposing view: The intermittent hypoxia attending severe obstructive sleep apnoea does not lead to alterations in brain structure and function. J Physiol 591: 383-385. doi:10.1113/jphysiol.2012.241224. PubMed: 23322287.
11. Fotuhi M, Hachinski V, Whitehouse PJ (2009) Changing perspectives regarding late-life dementia. Nat. Rev Neurol 5: 649-658.
12. Morrell MJ, Glasser M (2011) The brain in sleep-disordered breathing: a vote for the chicken? Am J Respir Crit Care Med 183: 1292-1294. doi:10.1164/rccm.201103-0562ED. PubMed: 21596831.
13. Sforza E, Roche F (2012) Sleep apnea syndrome and cognition. Front Neurol 3: 87. PubMed: 22661967.
14. Morrell MJ, Jackson ML, Twigg GL, Ghiassi R, McRobbie DW et al. (2010) Changes in brain morphology in patients with obstructive sleep apnoea. Thorax 65: 908-914. doi:10.1136/thx.2009.126730. PubMed: 20861295.
15. Canessa N, Castronovo V, Cappa SF, Aloia MS, Marelli S et al. (2011) Obstructive sleep apnea: brain structural changes and neurocognitive function before and after treatment. Am J Respir Crit Care Med 183: 1419-1426. doi:10.1164/rccm.201005-0693OC. PubMed: 21037021.
16. Canessa N, Ferini-Strambi L (2011) Sleep-disordered breathing and cognitive decline in older adults. JAMA 306: 654-655. doi:10.1001/jama.2011. 1124. PubMed: 21828331.
17. Kushida CA, Nichols DA, Holmes TH, Quan SF, Walsh JK et al. (2012) Effects of continuous positive airway pressure on neurocognitive function in obstructive sleep apnea patients: The Apnea Positive Pressure Long-term Efficacy Study (APPLES). Sleep 35: 1593-1602. PubMed: 23204602.
18. Twigg GL, Papaioannou I, Jackson M, Ghiassi R, Shaikh Z et al. (2010) Obstructive sleep apnea syndrome is associated with deficits in verbal but not visual memory. Am J Respir Crit Care Med 182: 98-103. doi: 10.1164/rccm.200901- 0065OC. PubMed: 20299536.
19. Lavie L, Lavie P (2006) Ischemic preconditioning as a possible explanation for the age decline relative mortality in sleep apnea. Med Hypotheses 66: 1069-1073. doi:10.1016/j.mehy.2005.10.033. PubMed: 16513285.
20. Rosenzweig I, Williams SC, Morrell MJ (2013) Rebuttal from ivana rosenzweig, steven C Williams and Mary j Morrell. J Physiol 591: 389. doi:10.1113/jphysiol.2012.246157.
21. Dirnagl U, Becker K, Meisel A (2009) Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol 8: 398-412. doi:10.1016/S1474-4422(09)70054-7. PubMed: 19296922.
22. Nanduri J, Yuan G, Kumar GK, Semenza GL, Prabhakar NR (2008) Transcriptional responses to intermittent hypoxia. Respir Physiol Neurobiol 164: 277-281. doi:10.1016/j.resp.2008.07.006. PubMed: 18692603.
23. Papadakis M, Hadley G, Xilouri M, Hoyte LC, Nagel S et al. (2013) Tsc1 (hamartin) confers neuroprotection against ischemia by inducing autophagy. Nat Med 19: 351-357. doi:10.1038/nm.3097. PubMed: 23435171.
24. Tsai YW, Yang YR, Wang PS, Wang RY (2011) Intermittent hypoxia after transient focal ischemia induces hippocampal neurogenesis and c-Fos expression and reverses spatial memory deficits in rats. PLOS ONE 6: e24001. doi:10.1371/journal.pone.0024001. PubMed: 21887361.
25. Tsai YW, Yang YR, Sun SH, Liang KC, Wang RY (2013) Post ischemia intermittent hypoxia induces hippocampal neurogenesis and synaptic alterations and alleviates long-term memory impairment. J Cereb Blood Flow Metab, 33: 764-73. PubMed: 23443175.
26. Aviles-Reyes RX, Angelo MF, Villarreal A, Rios H, Lazarowski A et al. (2010) Intermittent hypoxia during sleep induces reactive gliosis and limited neuronal death in rats: implications for sleep apnea. J Neurochem 112: 854-869. doi:10.1111/j.1471-4159.2009.06535.x. PubMed: 20002528.
27. Seki T (2011) Neurogenesis in the adult brain. Tokyo; New York: Springer.
28. Lledo PM, Alonso M, Grubb MS (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7: 179-193. doi:10.1038/nrn1867. PubMed: 16495940.
29. Lichtenwalner RJ, Parent JM (2006) Adult neurogenesis and the ischemic forebrain. J Cereb Blood Flow Metab 26: 1-20. doi:10.1038/sj.jcbfm.9600170. PubMed: 15959458.
30. Gozal D, Row BW, Kheirandish L, Liu R, Guo SZ et al. (2003) Increased susceptibility to intermittent hypoxia in aging rats: changes in proteasomal activity, neuronal apoptosis and spatial function. J Neurochem 86: 1545-1552. doi:10.1046/j.1471-4159.2003.01973.x. PubMed: 12950463.
31. Gozal D, Row BW, Gozal E, Kheirandish L, Neville JJ et al. (2003) Temporal aspects of spatial task performance during intermittent hypoxia in the rat: evidence for neurogenesis. Eur J Neurosci 18: 2335-2342. doi:10.1046/j.1460-9568.2003.02947.x. PubMed: 14622195.
32. Jung ME, Simpkins JW, Wilson AM, Downey HF, Mallet RT (2008) Intermittent hypoxia conditioning prevents behavioral deficit and brain oxidative stress in ethanol-withdrawn rats. J Appl Physiol (1985) 105: 510-517. doi:10.1152/ japplphysiol.90317.2008. PubMed: 18499779.
33. Zhu XH, Yan HC, Zhang J, Qu HD, Qiu XS et al. (2010) Intermittent hypoxia promotes hippocampal neurogenesis and produces antidepressant-like effects in adult rats. J Neurosci 30: 12653-12663. doi:10.1523/JNEUROSCI.6414-09.2010. PubMed: 20861371.
34. Ross HH, Sandhu MS, Cheung TF, Fitzpatrick GM, Sher WJ et al. (2012) In vivo intermittent hypoxia elicits enhanced expansion and neuronal differentiation in cultured neural progenitors. Exp Neurol 235: 238-245. doi:10.1016/j.expneurol.2012.01.027. PubMed: 22366327.
35. Macey PM, Henderson LA, Macey KE, Alger JR, Frysinger RC et al. (2002) Brain morphology associated with obstructive sleep apnea. Am J Respir Crit Care Med 166: 1382-1387. doi:10.1164/rccm.200201-050OC. PubMed: 12421746.
36. Macey PM, Kumar R, Woo MA, Valladares EM, Yan-Go FL et al. (2008) Brain structural changes in obstructive sleep apnea. Sleep 31: 967-977. PubMed: 18652092.
37. Morrell MJ, McRobbie DW, Quest RA, Cummin AR, Ghiassi R et al. (2003) Changes in brain morphology associated with obstructive sleep apnea. Sleep Med 4: 451-454. doi:10.1016/S1389-9457(03)00159-X. PubMed: 14592287.
38. Yaouhi K, Bertran F, Clochon P, Mézenge F, Denise P et al. (2009) A combined neuropsychological and brain imaging study of obstructive sleep apnea. J Sleep Res 18: 36-48. doi:10.1111/j.1365-2869.2008.00705.x. PubMed: 19250174.
39. Joo EY, Tae WS, Lee MJ, Kang JW, Park HS et al. (2010) Reduced brain gray matter concentration in patients with obstructive sleep apnea syndrome. Sleep 33: 235-241. PubMed: 20175407.
40. Torelli F, Moscufo N, Garreffa G, Placidi F, Romigi A et al. (2011) Cognitive profile and brain morphological changes in obstructive sleep apnea. NeuroImage 54: 787-793. doi:10.1016/j.neuroimage.2010.09.065. PubMed: 20888921.
41. O'Donoghue FJ, Briellmann RS, Rochford PD, Abbott DF, Pell GS et al. (2005) Cerebral structural changes in severe obstructive sleep apnea. Am J Respir Crit Care Med 171: 1185-1190. doi:10.1164/rccm.200406-738OC. PubMed: 15699018.
42. O'Donoghue FJ, Wellard RM, Rochford PD, Dawson A, Barnes M et al. (2012) Magnetic resonance spectroscopy and neurocognitive dysfunction in obstructive sleep apnea before and after CPAP treatment. Sleep 35: 41-48. PubMed: 22215917.
43. Gozal D (2013) Rebuttal from david gozal. J Physiol 591: 387. doi: 10.1113/jphysiol.2012.246017.
44. Doring TM, Kubo TT, Cruz LC Jr., Juruena MF, Fainberg J et al. (2011) Evaluation of hippocampal volume based on MR imaging in patients with bipolar affective disorder applying manual and automatic segmentation techniques. J Magn Reson Imaging 33: 565-572. doi: 10.1002/jmri.22473. PubMed: 21563239.
45. Pengas G, Pereira JM, Williams GB, Nestor PJ (2009) Comparative reliability of total intracranial volume estimation methods and the influence of atrophy in a longitudinal semantic dementia cohort. J Neuroimaging 19: 37-46. doi:10.1111/j.1552-6569.2008.00246.x. PubMed: 18494772.
46. McDonald CR, Hagler DJ Jr., Ahmadi ME, Tecoma E, Iragui V et al. (2008) Subcortical and cerebellar atrophy in mesial temporal lobe epilepsy revealed by automatic segmentation. Epilepsy Res 79: 130-138. doi:10.1016/j.eplepsyres.2008. 01.006. PubMed: 18359198.
47. Tae WS, Kim SS, Lee KU, Nam EC, Kim KW (2008) Validation of hippocampal volumes measured using a manual method and two automated methods (FreeSurfer and IBASPM) in chronic major depressive disorder. Neuroradiology 50: 569-581. doi:10.1007/s00234-008-0383-9. PubMed: 18414838.
48. Walhovd KB, Fjell AM, Reinvang I, Lundervold A, Dale AM et al. (2005) Effects of age on volumes of cortex, white matter and subcortical structures. Neurobiol Aging 26: 1261-1275; discussion: 16005549.
49. Cerasa A, Messina D, Nicoletti G, Novellino F, Lanza P et al. (2009) Cerebellar atrophy in essential tremor using an automated segmentation method. AJNR Am J Neuroradiol 30: 1240-1243. doi: 10.3174/ajnr.A1544. PubMed: 19342539.
50. Fischl B, Salat DH, Busa E, Albert M, Dieterich M et al. (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33: 341-355. doi:10.1016/S0896-6273(02)00569-X. PubMed: 11832223.
51. Webb EA, O'Reilly MA, Clayden JD, Seunarine KK, Chong WK et al. (2012) Effect of growth hormone deficiency on brain structure, motor function and cognition. Brain 135: 216-227. doi:10.1093/brain/awr305. PubMed: 22120144.
52. Gronenschild EH, Habets P, Jacobs HI, Mengelers R, Rozendaal N et al. (2012) The effects of FreeSurfer version, workstation type, and Macintosh operating system version on anatomical volume and cortical thickness measurements. PLOS ONE 7: e38234. doi:10.1371/journal.pone.0038234. PubMed: 22675527.
53. Plessen KJ, Bansal R, Zhu H, Whiteman R, Amat J et al. (2006) Hippocampus and amygdala morphology in attention-deficit/ hyperactivity disorder. Arch Gen Psychiatry 63: 795-807. doi:10.1001/archpsyc.63.7.795. PubMed: 16818869.
54. Hajak G, Klingelhöfer J, Schulz-Varszegi M, Sander D, Rüther E (1996) Sleep apnea syndrome and cerebral hemodynamics. Chest 110: 670-679. doi:10.1378/chest.110.3.670. PubMed: 8797410.
55. Bålfors EM, Franklin KA (1994) Impairment of cerebral perfusion during obstructive sleep apneas. Am J Respir Crit Care Med 150: 1587-1591. doi:10.1164/ajrccm.150.6.7952619. PubMed: 7952619.
56. Meadows GE, Kotajima F, Vazir A, Kostikas K, Simonds AK et al. (2005) Overnight changes in the cerebral vascular response to isocapnic hypoxia and hypercapnia in healthy humans: protection against stroke. Stroke 36: 2367-2372. doi:10.1161/01.STR.0000185923.49484.0f. PubMed: 16224083.
57. Joo EY, Tae WS, Han SJ, Cho JW, Hong SB (2007) Reduced cerebral blood flow during wakefulness in obstructive sleep apnea-hypopnea syndrome. Sleep 30: 1515-1520. PubMed: 18041484.
58. Ferriero DM (2005) Protecting neurons. Epilepsia 46 Suppl 7: 45-51. doi:10.1111/j.1528-1167.2005.00302.x. PubMed: 16201995.
59. Comi AM (2003) Pathophysiology of Sturge-Weber syndrome. J Child Neurol 18: 509-516. doi:10.1177/08830738030180080701. PubMed: 13677575.
60. Goldbart AD, Row BW, Kheirandish-Gozal L, Cheng Y, Brittian KR et al. (2006) High fat/refined carbohydrate diet enhances the susceptibility to spatial learning deficits in rats exposed to intermittent hypoxia. Brain Res 1090: 190-196. doi:10.1016/j.brainres.2006.03.046. PubMed: 16674930.
61. Schönwald SV, Carvalho DZ, de Santa-Helena EL, Lemke N, Gerhardt GJ (2012) Topography-specific spindle frequency changes in obstructive sleep apnea. BMC Neurosci 13: 89. doi: 10.1186/1471-2202-13-S1-P89. PubMed: 22985414.
62. Sica AL, Greenberg HE, Scharf SM, Ruggiero DA (2000) Chronic-intermittent hypoxia induces immediate early gene expression in the midline thalamus and epithalamus. Brain Res 883: 224-228. doi: 10.1016/S0006-8993(00)02800-6. PubMed: 11074051.
63. McKenna JT, Vertes RP (2004) Afferent projections to nucleus reuniens of the thalamus. J Comp Neurol 480: 115-142. doi:10.1002/cne.20342. PubMed: 15514932.
64. Eleore L, López-Ramos JC, Guerra-Narbona R, Delgado-García JM (2011) Role of reuniens nucleus projections to the medial prefrontal cortex and to the hippocampal pyramidal CA1 area in associative learning. PLOS ONE 6: e23538. doi:10.1371/journal.pone.0023538. PubMed: 21858159.
65. Aggleton JP, O'Mara SM, Vann SD, Wright NF, Tsanov M et al. (2010) Hippocampal-anterior thalamic pathways for memory: uncovering a network of direct and indirect actions. Eur J Neurosci 31: 2292-2307. doi:10.1111/j.1460- 9568.2010.07251.x. PubMed: 20550571.
66. Kumar R, Chavez AS, Macey PM, Woo MA, Yan-Go FL et al. (2012) Altered global and regional brain mean diffusivity in patients with obstructive sleep apnea. J Neurosci Res 90: 2043-2052. doi:10.1002/jnr.23083. PubMed: 22715089.
67. Rosenzweig I, Vukadinovic Z, Turner AJ, Catani M (2012) Neuroconnectivity and valproic acid: the myelin hypothesis. Neurosci Biobehav Rev 36: 1848-1856. doi:10.1016/j.neubiorev.2012.05.006. PubMed: 22652270.
68. Schmahmann JD, Sherman JC (1998) The cerebellar cognitive affective syndrome. Brain 121 (4): 561-579. doi:10.1093/brain/121.4.561.
69. Newman PP, Reza H (1979) Functional relationships between the hippocampus and the cerebellum: an electrophysiological study of the cat. J Physiol 287: 405-426. PubMed: 430426.
70. Hoffmann LC, Berry SD (2009) Cerebellar theta oscillations are synchronized during hippocampal theta-contingent trace conditioning. Proc Natl Acad Sci U S A 106: 21371-21376. doi:10.1073/pnas.0908403106. PubMed: 19940240.
71. Devisser A, Yang C, Herring A, Martinez JA, Rosales-Hernandez A et al. (2011) Differential impact of diabetes and hypertension in the brain: adverse effects in grey matter. Neurobiol Dis 44: 161-173. doi:10.1016/j.nbd.2011.06. 005. PubMed: 21742034.
72. Bonnici HM, Chadwick MJ, Kumaran D, Hassabis D, Weiskopf N et al. (2012) Multi-voxel pattern analysis in human hippocampal subfields. Front Hum Neuroscience 6: 290. PubMed: 23087638.