Progressive sleep and electroencephalogram changes in mice carrying the Huntington's disease mutation

Brain

Volumn 136, Issue 7, 2013, Pages 2147-2158

  Kantor, Sandor ^a   Szabo, Lajos ^a   Varga, Janos ^a,b   Cuesta, Marc ^a,c   Morton, A Jennifer ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

Author keywords

EEG; gamma activity; R6 2 mice; REM sleep theta; slow wave activity

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN REGION; CONTROLLED STUDY; ELECTROENCEPHALOGRAPHY; FEMALE; GENE MUTATION; GENOTYPE; HUNTINGTON CHOREA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PSYCHOSIS; QUALITY OF LIFE; REM SLEEP; SCHIZOPHRENIA; SLEEP WAKING CYCLE; SLOW WAVE SLEEP; WAKEFULNESS; WILD TYPE;

EID: 84879928399     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt128     Document Type: Article

References (75)

1. Adler CM, Goldberg TE, Malhotra AK, Pickar D, Breier A. Effects of ketamine on thought disorder, working memory, and semantic memory in healthy volunteers. Biol Psychiatry 1998; 43: 811-16
2. Allain P, Havet-Thomassin V, Verny C, Gohier B, Lancelot C, Besnard J, et al. Evidence for deficits on different components of theory of mind in Huntington's disease. Neuropsychology 2011; 25: 741-51
3. Arnulf I, Nielsen J, Lohmann E, Schiefer J, Wild E, Jennum P, et al. Rapid eye movement sleep disturbances in Huntington disease. Arch Neurol 2008; 65: 482-8
4. Aziz NA, Anguelova GV, Marinus J, Lammers GJ, Roos RA. Sleep and circadian rhythm alterations correlate with depression and cognitive impairment in Huntington's disease. Parkinsonism Relat Disord 2010; 16: 345-50
5. Beersma DG, Dijk DJ, Blok CG, Everhardus I. REM sleep deprivation during 5 hours leads to an immediate REM sleep rebound and to suppression of non-REM sleep intensity. Electroencephalogr Clin Neurophysiol 1990; 76: 114-22
6. Benington JH, Heller HC. REM-sleep timing is controlled homeostatically by accumulation of REM-sleep propensity in non-REM sleep. Am J Physiol 1994; 266: R1992-R2000
7. Berry SD, Seager MA. Hippocampal theta oscillations and classical conditioning. Neurobiol Learn Mem 2001; 76: 298-313
8. Berry SD, Thompson RF. Prediction of learning rate from the hippocampal electroencephalogram. Science 1978; 200: 1298-300
9. Beuckmann CT, Sinton CM, Williams SC, Richardson JA, Hammer RE, Sakurai T, et al. Expression of a poly-glutamine-Ataxin-3 transgene in orexin neurons induces narcolepsy-cataplexy in the rat. J Neurosci 2004; 24: 4469-77
10. Bode FJ, Stephan M, Wiehager S, Nguyen HP, Bjorkqvist M, von Horsten S, et al. Increased numbers of motor activity peaks during light cycle are associated with reductions in adrenergic alpha(2)-receptor levels in a transgenic Huntington's disease rat model. Behav Brain Res 2009; 205: 175-82
11. Brune M. "Theory of mind" in schizophrenia: A review of the literature. Schizophr Bull 2005; 31: 21-42
12. Buzsaki G. Memory consolidation during sleep: A neurophysiological perspective. J Sleep Res 1998; 7 (Suppl 1): 17-23
13. Buzsaki G. Theta oscillations in the hippocampus. Neuron 2002; 33: 325-40
14. Buzsaki G. Theta rhythm of navigation: Link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 2005; 15: 827-40
15. Buzsaki G, Draguhn A. Neuronal oscillations in cortical networks. Science 2004; 304: 1926-9
16. Bylsma FW, Peyser CE, Folstein SE, Folstein MF, Ross C, Brandt J. EEG power spectra in Huntington's disease: Clinical and neuropsychological correlates. Neuropsychologia 1994; 32: 137-50
17. Caplan JB, Madsen JR, Schulze-Bonhage A, Aschenbrenner-Scheibe R, Newman EL, Kahana MJ. Human theta oscillations related to sensorimotor integration and spatial learning. J Neurosci 2003; 23: 4726-36
18. Carskadon MA, Dement WC. Sleepiness and sleep state on a 90-min schedule. Psychophysiology 1977; 14: 127-33
19. Chemelli RM, Willie JT, Sinton CM, Elmquist JK, Scammell T, Lee C, et al. Narcolepsy in orexin knockout mice: Molecular genetics of sleep regulation. Cell 1999; 98: 437-51
20. Dantz B, Edgar DM, Dement WC. Circadian rhythms in narcolepsy: Studies on a 90 minute day. Electroencephalogr Clin Neurophysiol 1994; 90: 24-35
21. Dijk DJ, Czeisler CA. Contribution of the circadian pacemaker and the sleep homeostat to sleep propensity, sleep structure, electroencephalographic slow waves, and sleep spindle activity in humans. J Neurosci 1995; 15: 3526-38
22. Ehrnhoefer DE, Butland SL, Pouladi MA, Hayden MR. Mouse models of Huntington disease: Variations on a theme. Dis Model Mech 2009; 2: 123-9
23. Endo T, Schwierin B, Borbely AA, Tobler I. Selective and total sleep deprivation: Effect on the sleep EEG in the rat. Psychiatry Res 1997; 66: 97-110
24. Engel AK, Fries P, Singer W. Dynamic predictions: Oscillations and synchrony in top-Down processing. Nat Rev Neurosci 2001; 2: 704-16
25. Etholm L, Arabadzisz D, Lipp HP, Heggelund P. Seizure logging: A new approach to synchronized cable-free EEG and video recordings of seizure activity in mice. J Neurosci Methods 2010; 192: 254-60
26. Fell J, Fernandez G, Klaver P, Elger CE, Fries P. Is synchronized neuronal gamma activity relevant for selective attention? Brain Res Brain Res Rev 2003; 42: 265-72
27. Franken P, Malafosse A, Tafti M. Genetic determinants of sleep regulation in inbred mice. Sleep 1999; 22: 155-69
28. Frith CD. Schizophrenia and theory of mind. Psychol Med 2004; 34: 385-9
29. Gerbrandt LK, Lawrence JC, Eckardt MJ, Lloyd RL. Origin of the neocortically monitored theta rhythm in the curarized rat. Electroencephalogr Clin Neurophysiol 1978; 45: 454-67
30. Gibson HE, Reim K, Brose N, Morton AJ, Jones S. A similar impairment in CA3 mossy fibre LTP in the R6/2 mouse model of Huntington's disease and in the complexin II knockout mouse. Eur J Neurosci 2005; 22: 1701-12
31. Goodman AO, Morton AJ, Barker RA. Identifying sleep disturbances in Huntington's disease using a simple disease-focused questionnaire. PLoS Curr 2010; 2: RRN1189
32. Goodman AO, Rogers L, Pilsworth S, McAllister CJ, Shneerson JM, Morton AJ, et al. Asymptomatic sleep abnormalities are a common early feature in patients with Huntington's disease. Curr Neurol Neurosci Rep 2011; 11: 211-7
33. Gruber T, Muller MM, Keil A. Modulation of induced gamma band responses in a perceptual learning task in the human EEG. J Cogn Neurosci 2002; 14: 732-44
34. Hara J, Beuckmann CT, Nambu T, Willie JT, Chemelli RM, Sinton CM, et al. Genetic ablation of orexin neurons in mice results in narcolepsy, hypophagia, and obesity. Neuron 2001; 30: 345-54
35. Hennenlotter A, Schroeder U, Erhard P, Haslinger B, Stahl R, Weindl A, et al. Neural correlates associated with impaired disgust processing in pre-symptomatic Huntington's disease. Brain 2004; 127: 1446-53
36. Herrmann CS, Demiralp T. Human EEG gamma oscillations in neuropsychiatric disorders. Clin Neurophysiol 2005; 116: 2719-33
37. Hetem LA, Danion JM, Diemunsch P, Brandt C. Effect of a subanesthetic dose of ketamine on memory and conscious awareness in healthy volunteers. Psychopharmacology (Berl) 2000; 152: 283-8
38. Ho AK, Sahakian BJ, Brown RG, Barker RA, Hodges JR, Ane MN, et al. Profile of cognitive progression in early Huntington's disease. Neurology 2003; 61: 1702-6
39. Holsheimer J, Feenstra BW. Volume conduction and EEG measurements within the brain: A quantitative approach to the influence of electrical spread on the linear relationship of activity measured at different locations. Electroencephalogr Clin Neurophysiol 1977; 43: 52-8
40. Hong SL, Cossyleon D, Hussain WA, Walker LJ, Barton SJ, Rebec GV. Dysfunctional behavioral modulation of corticostriatal communication in the R6/2 mouse model of Huntington's disease. PLoS One 2012; 7: E47026
41. Johnson SA, Stout JC, Solomon AC, Langbehn DR, Aylward EH, Cruce CB, et al. Beyond disgust: Impaired recognition of negative emotions prior to diagnosis in Huntington's disease. Brain 2007; 130: 1732-44
42. Jones MW, Wilson MA. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol 2005; 3: E402
43. Kantor S, Jakus R, Molnar E, Gyongyosi N, Toth A, Detari L, et al. Despite similar anxiolytic potential, the 5-hydroxytryptamine 2C receptor antagonist SB-242084 [6-chloro-5-methyl-1-[2-(2-methylpyrid-3-yloxy)-pyrid-5-yl carbamoyl] indoline] and chlordiazepoxide produced differential effects on electroencephalogram power spectra. J Pharmacol Exp Ther 2005; 315: 921-30
44. Kantor S, Mochizuki T, Janisiewicz AM, Clark E, Nishino S, Scammell TE. Orexin neurons are necessary for the circadian control of REM sleep. Sleep 2009; 32: 1127-34
45. Kittelberger K, Hur EE, Sazegar S, Keshavan V, Kocsis B. Comparison of the effects of acute and chronic administration of ketamine on hippocampal oscillations: Relevance for the NMDA receptor hypofunction model of schizophrenia. Brain Struct Funct 2012; 217: 395-409
46. Kocsis B. Differential role of NR2A and NR2B subunits in N-methyl-Daspartate receptor antagonist-induced aberrant cortical gamma oscillations. Biol Psychiatry 2012a; 71: 987-95
47. Kocsis B. State-Dependent increase of cortical gamma activity during REM sleep after selective blockade of NR2B subunit containing NMDA receptors. Sleep 2012b; 35: 1011-6
48. Krystal JH, Karper LP, Seibyl JP, Freeman GK, Delaney R, Bremner JD, et al. Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Psychotomimetic, perceptual, cognitive, and neuroendocrine responses. Arch Gen Psychiatry 1994; 51: 199-214
49. Kudo T, Schroeder A, Loh DH, Kuljis D, Jordan MC, Roos KP, et al. Dysfunctions in circadian behavior and physiology in mouse models of Huntington's disease. Exp Neurol 2011; 228: 80-90
50. Lione LA, Carter RJ, Hunt MJ, Bates GP, Morton AJ, Dunnett SB. Selective discrimination learning impairments in mice expressing the human Huntington's disease mutation. J Neurosci 1999; 19: 10428-37
51. Mochizuki T, Crocker A, McCormack S, Yanagisawa M, Sakurai T, Scammell TE. Behavioral state instability in orexin knock-out mice. J Neurosci 2004; 24: 6291-300
52. Morton AJ. Circadian and sleep disorder in Huntington's disease. Exp Neurol 2013; 243: 34-44
53. Morton AJ, Lagan MA, Skepper JN, Dunnett SB. Progressive formation of inclusions in the striatum and hippocampus of mice transgenic for the human Huntington's disease mutation. J Neurocytol 2000; 29: 679-702
54. Morton AJ, Wood NI, Hastings MH, Hurelbrink C, Barker RA, Maywood ES. Disintegration of the sleep-wake cycle and circadian timing in Huntington's disease. J Neurosci 2005; 25: 157-63
55. Newcomer JW, Farber NB, Jevtovic-Todorovic V, Selke G, Melson AK, Hershey T, et al. Ketamine-induced NMDA receptor hypofunction as a model of memory impairment and psychosis. Neuropsychopharmacology 1999; 20: 106-18
56. Nguyen L, Bradshaw JL, Stout JC, Croft RJ, Georgiou-Karistianis N. Electrophysiological measures as potential biomarkers in Huntington's disease: Review and future directions. Brain Res Rev 2010; 64: 177-94
57. Peinemann A, Schuller S, Pohl C, Jahn T, Weindl A, Kassubek J. Executive dysfunction in early stages of Huntington's disease is associated with striatal and insular atrophy: A neuropsychological and voxel-based morphometric study. J Neurol Sci 2005; 239: 11-9
58. Petit D, Gagnon JF, Fantini ML, Ferini-Strambi L, Montplaisir J. Sleep and quantitative EEG in neurodegenerative disorders. J Psychosom Res 2004; 56: 487-96
59. Pignatelli M, Lebreton F, Cho YH, Leinekugel X. "Ectopic" theta oscillations and interictal activity during slow-wave state in the R6/1 mouse model of Huntington's disease. Neurobiol Dis 2012; 48: 409-17
60. Pinault D. N-methyl d-Aspartate receptor antagonists ketamine and MK-801 induce wake-related aberrant gamma oscillations in the rat neocortex. Biol Psychiatry 2008; 63: 730-5
61. Rudenko O, Tkach V, Berezin V, Bock E. Detection of early behavioral markers of Huntington's disease in R6/2 mice employing an automated social home cage. Behav Brain Res 2009; 203: 188-99
62. Sammer G, Blecker C, Gebhardt H, Bischoff M, Stark R, Morgen K, et al. Relationship between regional hemodynamic activity and simultaneously recorded EEG-Theta associated with mental arithmetic-induced workload. Hum Brain Mapp 2007; 28: 793-803
63. Shea JL, Mochizuki T, Sagvaag V, Aspevik T, Bjorkum AA, Datta S. Rapid eye movement (REM) sleep homeostatic regulatory processes in the rat: Changes in the sleep-wake stages and electroencephalographic power spectra. Brain Res 2008; 1213: 48-56
64. Silvestri R, Raffaele M, De Domenico P, Tisano A, Mento G, Casella C, et al. Sleep features in Tourette's syndrome, neuroacanthocytosis and Huntington's chorea. Neurophysiol Clin 1995; 25: 66-77
65. Snowden JS, Gibbons ZC, Blackshaw A, Doubleday E, Thompson J, Craufurd D, et al. Social cognition in frontotemporal dementia and Huntington's disease. Neuropsychologia 2003; 41: 688-701
66. Sprengelmeyer R, Young AW, Calder AJ, Karnat A, Lange H, Homberg V, et al. Loss of disgust. Perception of faces and emotions in Huntington's disease. Brain 1996; 119: 1647-65
67. Trachsel L, Tobler I, Achermann P, Borbely AA. Sleep continuity and the REM-nonREM cycle in the rat under baseline conditions and after sleep deprivation. Physiol Behav 1991; 49: 575-80
68. Videnovic A, Leurgans S, Fan W, Jaglin J, Shannon KM. Daytime somnolence and nocturnal sleep disturbances in Huntington disease. Parkinsonism Relat Disord 2009; 15: 471-4
69. Wiegand M, Moller AA, Lauer CJ, Stolz S, Schreiber W, Dose M, et al. Nocturnal sleep in Huntington's disease. J Neurol 1991a; 238: 203-8
70. Wiegand M, Moller AA, Schreiber W, Lauer C, Krieg JC. Brain morphology and sleep EEG in patients with Huntington's disease. Eur Arch Psychiatry Clin Neurosci 1991b; 240: 148-52
71. Williams RH, Morton AJ, Burdakov D. Paradoxical function of orexin/ hypocretin circuits in a mouse model of Huntington's disease. Neurobiol Dis 2011; 42: 438-45
72. Winson J. Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science 1978; 201: 160-3
73. Wurts SW, Edgar DM. Circadian and homeostatic control of rapid eye movement (REM) sleep: Promotion of REM tendency by the suprachiasmatic nucleus. J Neurosci 2000; 20: 4300-10
74. Zhang S, Lin L, Kaur S, Thankachan S, Blanco-Centurion C, Yanagisawa M, et al. The development of hypocretin (orexin) deficiency in hypocretin/ataxin-3 transgenic rats. Neuroscience 2007a; 148: 34-43
75. Zhang S, Zeitzer JM, Sakurai T, Nishino S, Mignot E. Sleep/wake fragmentation disrupts metabolism in a mouse model of narcolepsy. J Physiol 2007b; 581: 649-63