Influence of vigilance state on physiological consequences of seizures and seizure-induced death in mice

Journal of Neurophysiology

Volumn 115, Issue 5, 2016, Pages 2286-2293

  Hajek, Michael A ^a   Buchanan, Gordon F ^a,b,c  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

Seizure; Sleep; SUDEP

Indexed keywords

ADULT; ALERTNESS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY PLETHYSMOGRAPHY; BREATHING RATE; CAUSE OF DEATH; CLINICAL ASSESSMENT; CONTROLLED STUDY; ELECTRIC SHOCK; ELECTROCARDIOGRAM; ELECTROENCEPHALOGRAM; ELECTROMYOGRAM; MALE; MOUSE; NONHUMAN; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; REM SLEEP; RESPIRATORY FUNCTION; RISK ASSESSMENT; RISK FACTOR; SEIZURE; SLEEP PATTERN; WAKEFULNESS; ANIMAL; BREATHING; C57BL MOUSE; COMPLICATION; ETIOLOGY; PATHOPHYSIOLOGY; SUDDEN DEATH;

ANIMALS; DEATH, SUDDEN; MALE; MICE; MICE, INBRED C57BL; RESPIRATION; SEIZURES; SLEEP, REM; WAKEFULNESS;

EID: 84984666477     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00011.2016     Document Type: Article

References (72)

1. Aiba I, Noebels JL. Spreading depolarization in the brainstem mediates sudden cardiorespiratory arrest in mouse SUDEP models. Sci Transl Med 7: 282ra46, 2015.
2. Anderson RE, Howard RA, Woodbury DM. Correlation between effects of acute acetazolamide administration to mice on electroshock seizure threshold and maximal electroshock seizure pattern, and on carbonic anhydrase activity in subcellular fractions of brain. Epilepsia 27: 504-509, 1986.
3. Auerbach DS, Jones J, Clawson BC, Offord J, Lenk GM, Ogiwara I, Yamakawa K, Meisler MH, Parent JM, Isom LL. Altered cardiac electrophysiology and SUDEP in a model of Dravet syndrome. PLoS One 8: e77843, 2013.
4. Banerjee PN, Filippi D, Allen HW. The descriptive epidemiology of epilepsy- a review. Epilepsy Res 85: 31-45, 2009.
5. Bateman LM, Li CS, Seyal M. Ictal hypoxemia in localization-related epilepsy: analysis of incidence, severity and risk factors. Brain 131: 3239-3245, 2008.
6. Bateman LM, Spitz M, Seyal M. Ictal hypoventilation contributes to cardiac arrhythmia and SUDEP: report on two deaths in video-EEG-monitored patients. Epilepsia 51: 916-920, 2010.
7. Bazil CW, Walczak TS. Effects of sleep and sleep stage on epileptic and nonepileptic seizures. Epilepsia 38: 56-62, 1997.
8. Blum AS. Respiratory physiology of seizures. J Clin Neurophysiol 26: 309-315, 2009.
9. Blumenfeld H. Impaired consciousness in epilepsy. Lancet Neurol 11: 814-826, 2012.
10. Blumenfeld H, McNally KA, Vanderhill SD, Paige AL, Chung R, Davis K, Norden AD, Stokking R, Studholme C, Novotny EJ Jr, Zubal IG, Spencer SS. Positive and negative network correlations in temporal lobe epilepsy. Cereb Cortex 14: 892-902, 2004.
11. Blumenfeld H, Varghese GI, Purcaro MJ, Motelow JE, Enev M, McNally KA, Levin AR, Hirsch LJ, Tikofsky R, Zubal IG, Paige AL, Spencer SS. Cortical and subcortical networks in human secondarily generalized tonicclonic seizures. Brain 132: 999-1012, 2009.
12. Bozorgi A, Lhatoo SD. Seizures, cerebral shutdown, and SUDEP. Epilepsy Curr 13: 236-240, 2013.
13. Buchanan GF. Timing, sleep, and respiration in health and disease. Prog Mol Biol Transl Sci 119: 191-219, 2013.
14. Buchanan GF, Murray NM, Hajek MA, Richerson GB. Serotonin neurones have anti-convulsant effects and reduce seizure-induced mortality. J Physiol 592: 4395-4410, 2014.
15. Buchanan GF, Richerson GB. Central serotonin neurons are required for arousal to CO2. Proc Natl Acad Sci USA 107: 16354-16359, 2010.
16. Bulow K. Respiration and wakefulness in man. Acta Physiol Scand Suppl 59: 1-110, 1963.
17. Cajochen C, Pischke J, Aeschbach D, Borbely AA. Heart rate dynamics during human sleep. Physiol Behav 55: 769-774, 1994.
18. Campen MJ, Tagaito Y, Jenkins TP, Smith PL, Schwartz AR, O’Donnell CP. Phenotypic differences in the hemodynamic response during REM sleep in six strains of inbred mice. Physiol Genomics 11: 227-234, 2002.
19. Darbin O, Casebeer D, Naritoku DK. Effects of seizure severity and seizure repetition on postictal cardiac arrhythmia following maximal electroshock. Exp Neurol 181: 327-331, 2003.
20. Darbin O, Casebeer DJ, Naritoku DK. Cardiac dysrhythmia associated with the immediate postictal state after maximal electroshock in freely moving rat. Epilepsia 43: 336-341, 2002.
21. Degiorgio CM, Miller P, Meymandi S, Chin A, Epps J, Gordon S, Gornbein J, Harper RM. RMSSD, a measure of vagus-mediated heart rate variability, is associated with risk factors for SUDEP: the SUDEP-7 Inventory. Epilepsy Behav 19: 78-81, 2010.
22. Douglas NJ. Control of breathing during sleep. Clin Sci (Lond) 67: 465-471, 1984.
23. Douglas NJ, White DP, Weil JV, Pickett CK, Zwillich CW. Hypercapnic ventilatory response in sleeping adults. Am Rev Respir Dis 126: 758-762, 1982.
24. Drorbaugh JE, Fenn WO. A barometric method for measuring ventilation in newborn infants. Pediatrics 16: 81-87, 1955.
25. Englot DJ, Mishra AM, Mansuripur PK, Herman P, Hyder F, Blumenfeld H. Remote effects of focal hippocampal seizures on the rat neocortex. J Neurosci 28: 9066-9081, 2008.
26. Englot DJ, Modi B, Mishra AM, DeSalvo M, Hyder F, Blumenfeld H. Cortical deactivation induced by subcortical network dysfunction in limbic seizures. J Neurosci 29: 13006-13018, 2009.
27. Faingold CL, Randall M, Tupal S. DBA/1 mice exhibit chronic susceptibility to audiogenic seizures followed by sudden death associated with respiratory arrest. Epilepsy Behav 17: 436-440, 2010.
28. Franken P, Malafosse A, Tafti M. Genetic variation in EEG activity during sleep in inbred mice. Am J Physiol Regul Integr Comp Physiol 275: R1127-R1137, 1998.
29. Friedman L, Haines A, Klann K, Gallaugher L, Salibra L, Han F, Strohl KP. Ventilatory behavior during sleep among A/J and C57BL/6J mouse strains. J Appl Physiol 97: 1787-1795, 2004.
30. Furman M, Zhan Q, McCafferty C, Lerner BA, Motelow JE, Meng J, Ma C, Buchanan GF, Witten IB, Deisseroth K, Cardin JA, Blumenfeld H. Optogenetic stimulation of cholinergic brainstem neurons during focal limbic seizures: Effects on cortical physiology. Epilepsia 56: e198-e202, 2015.
31. Gummadavelli A, Motelow JE, Smith N, Zhan Q, Schiff ND, Blumenfeld H. Thalamic stimulation to improve level of consciousness after seizures: evaluation of electrophysiology and behavior. Epilepsia 56: 114-124, 2015.
32. Hesdorffer DC, Logroscino G, Benn EK, Katri N, Cascino G, Hauser WA. Estimating risk for developing epilepsy: a population-based study in Rochester, Minnesota. Neurology 76: 23-27, 2011a.
33. Hesdorffer DC, Tomson T, Benn E, Sander JW, Nilsson L, Langan Y, Walczak TS, Beghi E, Brodie MJ, Hauser A. Combined analysis of risk factors for SUDEP. Epilepsia 52: 1150-1159, 2011b.
34. Hodges MR, Tattersall GJ, Harris MB, McEvoy SD, Richerson DN, Deneris ES, Johnson RL, Chen ZF, Richerson GB. Defects in breathing and thermoregulation in mice with near-complete absence of central serotonin neurons. J Neurosci 28: 2495-2505, 2008.
35. Kalume F, Oakley JC, Westenbroek RE, Gile J, de la Iglesia HO, Scheuer T, Catterall WA. Sleep impairment and reduced interneuron excitability in a mouse model of Dravet Syndrome. Neurobiol Dis 77: 141-154, 2015.
36. Kalume F, Westenbroek RE, Cheah CS, Yu FH, Oakley JC, Scheuer T, Catterall WA. Sudden unexpected death in a mouse model of Dravet syndrome. J Clin Invest 123: 1798-1808, 2013.
37. Lamberts RJ, Thijs RD, Laffan A, Langan Y, Sander JW. Sudden unexpected death in epilepsy: people with nocturnal seizures may be at highest risk. Epilepsia 53: 253-257, 2012.
38. Langan Y, Nashef L, Sander JW. Sudden unexpected death in epilepsy: a series of witnessed deaths. J Neurol Neurosurg Psychiatry 68: 211-213, 2000.
39. Lhatoo SD, Faulkner HJ, Dembny K, Trippick K, Johnson C, Bird JM. An electroclinical case-control study of sudden unexpected death in epilepsy. Ann Neurol 68: 787-796, 2010.
40. Liebenthal JA, Wu S, Rose S, Ebersole JS, Tao JX. Association of prone position with sudden unexpected death in epilepsy. Neurology 84: 703-709, 2015.
41. + currents to respiratory rhythmogenesis in vivo. J Neurosci 33: 8716-8728, 2013.
42. Motelow JE, Li W, Zhan Q, Mishra AM, Sachdev RN, Liu G, Gummadavelli A, Zayyad Z, Lee HS, Chu V, Andrews JP, Englot DJ, Herman P, Sanganahalli BG, Hyder F, Blumenfeld H. Decreased subcortical cholinergic arousal in focal seizures. Neuron 85: 561-572, 2015.
43. Naritoku DK, Casebeer DJ, Darbin O. Effects of seizure repetition on postictal and interictal neurocardiac regulation in the rat. Epilepsia 44: 912-916, 2003.
44. Nashef L, Garner S, Sander JW, Fish DR, Shorvon SD. Circumstances of death in sudden death in epilepsy: interviews of bereaved relatives. J Neurol Neurosurg Psychiatry 64: 349-352, 1998.
45. Nashef L, Walker F, Allen P, Sander JW, Shorvon SD, Fish DR. Apnoea and bradycardia during epileptic seizures: relation to sudden death in epilepsy. J Neurol Neurosurg Psychiatry 60: 297-300, 1996.
46. Ng M, Pavlova M. Why are seizures rare in rapid eye movement sleep? Review of the frequency of seizures in different sleep stages. Epilepsy Res Treat 2013: 932790, 2013.
47. Nobili L, Proserpio P, Rubboli G, Montano N, Didato G, Tassinari CA. Sudden unexpected death in epilepsy (SUDEP) and sleep. Sleep Med Rev 15: 237-246, 2011.
48. Orem J. Neural mechanisms of respiration in REM sleep. Sleep 3: 251-252, 1980.
49. Orem J, Lovering AT, Dunin-Barkowski W, Vidruk EH. Tonic activity in the respiratory system in wakefulness, NREM and REM sleep. Sleep 25: 488-496, 2002.
50. Orem J, Montplaisir J, Dement WC. Changes in the activity of respiratory neurons during sleep. Brain Res 82: 309-315, 1974.
51. Orem J, Netick A, Dement WC. Increased upper airway resistance to breathing during sleep in the cat. Electroencephalogr Clin Neurophysiol 43: 14-22, 1977.
52. Orem J, Osorio I, Brooks E, Dick T. Activity of respiratory neurons during NREM sleep. J Neurophysiol 54: 1144-1156, 1985.
53. Phillipson EA, Sullivan CE, Read DJ, Murphy E, Kozar LF. Ventilatory and waking responses to hypoxia in sleeping dogs. J Appl Physiol Respir Environ Exercise Physiol 44: 512-520, 1978.
54. Ryvlin P, Nashef L, Lhatoo SD, Bateman LM, Bird J, Bleasel A, Boon P, Crespel A, Dworetzky BA, Hogenhaven H, Lerche H, Maillard L, Malter MP, Marchal C, Murthy JM, Nitsche M, Pataraia E, Rabben T, Rheims S, Sadzot B, Schulze-Bonhage A, Seyal M, So EL, Spitz M, Szucs A, Tan M, Tao JX, Tomson T. Incidence and mechanisms of cardiorespiratory arrests in epilepsy monitoring units (MORTEMUS): a retrospective study. Lancet Neurol 12: 966-977, 2013.
55. Santiago TV, Scardella AT, Edelman NH. Determinants of the ventilatory responses to hypoxia during sleep. Am Rev Respir Dis 130: 179-182, 1984.
56. Schmidt D. Drug treatment of epilepsy: options and limitations. Epilepsy Behav 15: 56-65, 2009.
57. Sedigh-Sarvestani M, Blumenfeld H, Loddenkemper T, Bateman LM. Seizures and brain regulatory systems: consciousness, sleep, and autonomic systems. J Clin Neurophysiol 32: 188-193, 2014a.
58. Sedigh-Sarvestani M, Thuku GI, Sunderam S, Parkar A, Weinstein SL, Schiff SJ, Gluckman BJ. Rapid eye movement sleep and hippocampal theta oscillations precede seizure onset in the tetanus toxin model of temporal lobe epilepsy. J Neurosci 34: 1105-1114, 2014b.
59. Seyal M, Bateman LM, Li CS. Impact of periictal interventions on respiratory dysfunction, postictal EEG suppression, and postictal immobility. Epilepsia 54: 377-382, 2013.
60. Shea SA, Guz A. Personnalite ventilatoire-an overview. Respir Physiol 87: 275-291, 1992.
61. Shea SA, Horner RL, Benchetrit G, Guz A. The persistence of a respiratory ‘personality’ into stage IV sleep in man. Respir Physiol 80: 33-44, 1990.
62. Shouse MN, Scordato JC, Farber PR. Sleep and arousal mechanisms in experimental epilepsy: epileptic components of NREM and antiepileptic components of REM sleep. Ment Retard Dev Disabil Res Rev 10: 117-121, 2004.
63. Smith JC, Ellenberger HH, Ballanyi K, Richter DW, Feldman JL. Pre-Botzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254: 726-729, 1991.
64. Snyder F, Hobson J, Morrison D, Goldfrank F. Changes in respiration, heart rate, and systolic blood pressure in human sleep. J Appl Physiol 19: 417-422, 1964.
65. Sowers LP, Massey CA, Gehlbach BK, Granner MA, Richerson GB. Sudden unexpected death in epilepsy: fatal post-ictal respiratory and arousal mechanisms. Respir Physiol Neurobiol 189: 315-323, 2013.
66. Stein PK, Bosner MS, Kleiger RE, Conger BM. Heart rate variability: a measure of cardiac autonomic tone. Am Heart J 127: 1376-1381, 1994.
67. Tao JX, Qian S, Baldwin M, Chen XJ, Rose S, Ebersole SH, Ebersole JS. SUDEP, suspected positional airway obstruction, and hypoventilation in postictal coma. Epilepsia 51: 2344-2347, 2010.
68. Tao JX, Sandra R, Wu S, Ebersole JS. Should the "Back to Sleep" campaign be advocated for SUDEP prevention? Epilepsy Behav 45: 79-80, 2015.
69. Thurman DJ, Hesdorffer DC, French JA. Sudden unexpected death in epilepsy: assessing the public health burden. Epilepsia 55: 1479-1485, 2014.
70. Tupal S, Faingold CL. Evidence supporting a role of serotonin in modulation of sudden death induced by seizures in DBA/2 mice. Epilepsia 47: 21-26, 2006.
71. Zhan Q, Buchanan GF, Motelow JE, Andrews J, Vitkovskiy P, Chen WC, Serout F, Gummadavelli A, Kundishora A, Furman M, Li W, Bo X, Richerson GB, Blumenfeld H. Impaired serotonergic brainstem function during and following seizures. J Neurosci 36: 2711-2722, 2016.
72. Zhao ZQ, Scott M, Chiechio S, Wang JS, Renner KJ, Gereau RW, Johnson RL, Deneris ES, Chen ZF. Lmx1b is required for maintenance of central serotonergic neurons and mice lacking central serotonergic system exhibit normal locomotor activity. J Neurosci 26: 12781-12788, 2006.