Sympathetic neural responses to 24-hour sleep deprivation in humans: sex differences.

Sleep deprivation has been linked to hypertension, and recent evidence suggests that associations between short sleep duration and hypertension are stronger in women. In the present study we hypothesized that 24 h of total sleep deprivation (TSD) would elicit an augmented pressor and sympathetic neural response in women compared with men. Resting heart rate (HR), blood pressure (BP), and muscle sympathetic nerve activity (MSNA) were measured in 30 healthy subjects (age, 22 ± 1; 15 men and 15 women). Relations between spontaneous fluctuations of diastolic arterial pressure and MSNA were used to assess sympathetic baroreflex function. Subjects were studied twice, once after normal sleep and once after TSD (randomized, crossover design). TSD elicited similar increases in systolic, diastolic, and mean BP in men and women (time, P < 0.05; time × sex, P > 0.05). TSD reduced MSNA in men (25 ± 2 to 16 ± 3 bursts/100 heart beats; P = 0.02), but not women. TSD did not alter spontaneous sympathetic or cardiovagal baroreflex sensitivities in either sex. However, TSD shifted the spontaneous sympathetic baroreflex operating point downward and rightward in men only. TSD reduced testosterone in men, and these changes were correlated to changes in resting MSNA (r = 0.59; P = 0.04). Resting HR, respiratory rate, and estradiol were not altered by TSD in either sex. In conclusion, TSD-induced hypertension occurs in both sexes, but only men demonstrate altered resting MSNA. The sex differences in MSNA are associated with sex differences in sympathetic baroreflex function (i.e., operating point) and testosterone. These findings may help explain why associations between sleep deprivation and hypertension appear to be sex dependent.

[1]  F. Prince,et al.  Sleep deprivation increases blood pressure in healthy normotensive elderly and attenuates the blood pressure response to orthostatic challenge. , 2011, Sleep.

[2]  Claude Gronfier,et al.  Sleep deprivation blunts the night time increase in aldosterone release in humans , 2001, Journal of sleep research.

[3]  N. Montano,et al.  Sympathetic and angiotensinergic responses mediated by paradoxical sleep loss in rats , 2011, Journal of the renin-angiotensin-aldosterone system : JRAAS.

[4]  Y. Hishikawa,et al.  Total sleep deprivation elevates blood pressure through arterial baroreflex resetting: a study with microneurographic technique. , 2003, Sleep.

[5]  P. Raven,et al.  Arterial baroreflex control of muscle sympathetic nerve activity in the transition from rest to steady-state dynamic exercise in humans. , 2007, American journal of physiology. Heart and circulatory physiology.

[6]  B. Wallin,et al.  Possible genetic influence on the strength of human muscle nerve sympathetic activity at rest. , 1993, Hypertension.

[7]  D. Low,et al.  Heat stress enhances arterial baroreflex control of muscle sympathetic nerve activity via increased sensitivity of burst gating, not burst area, in humans , 2006, The Journal of physiology.

[8]  A Pedotti,et al.  Evaluation of baroreceptor reflex by blood pressure monitoring in unanesthetized cats. , 1988, The American journal of physiology.

[9]  C. Spielberger,et al.  Manual for the State-Trait Anxiety Inventory , 1970 .

[10]  Susan Redline,et al.  Association of usual sleep duration with hypertension: the Sleep Heart Health Study. , 2006, Sleep.

[11]  A P Blaber,et al.  Methodology of spontaneous baroreflex relationship assessed by surrogate data analysis. , 1995, The American journal of physiology.

[12]  R. Wu,et al.  Effects of sleep deprivation on serum testosterone concentrations in the rat , 2011, Neuroscience Letters.

[13]  Steven B. Heymsfield,et al.  Short Sleep Duration as a Risk Factor for Hypertension: Analyses of the First National Health and Nutrition Examination Survey , 2006, Hypertension.

[14]  Heikki Kyröläinen,et al.  The effect of 60-h sleep deprivation on cardiovascular regulation and body temperature , 2009, European Journal of Applied Physiology.

[15]  K. Hagbarth,et al.  General characteristics of sympathetic activity in human skin nerves. , 1972, Acta physiologica Scandinavica.

[16]  G. Leftheriotis,et al.  Effect of acute sleep deprivation on vascular function in healthy subjects. , 2010, Journal of applied physiology.

[17]  K. Gräf,et al.  Neuroendocrinological investigations during sleep deprivation in depression I. Early morning levels of thyrotropin, TH, cortisol, prolactin, LH, FSH, estradiol, and testosterone , 1990, Biological Psychiatry.

[18]  B. Wallin,et al.  Sympathetic transients caused by abrupt alterations of carotid baroreceptor activity in humans. , 1982, The American journal of physiology.

[19]  R. Fogari,et al.  Effects of insufficient sleep on blood pressure in hypertensive patients: a 24-h study. , 1999, American journal of hypertension.

[20]  J. Richards,et al.  Effects of sleep deprivation on impulsive behaviors in men and women , 2007, Physiology & Behavior.

[21]  E. Stener-Victorin,et al.  Is polycystic ovary syndrome associated with high sympathetic nerve activity and size at birth? , 2008, American journal of physiology. Endocrinology and metabolism.

[22]  K. Hagbarth,et al.  General characteristics of sympathetic activity in human muscle nerves. , 1972, Acta physiologica Scandinavica.

[23]  B. Wallin,et al.  Sympathetic nervous system and blood pressure in humans: individualized patterns of regulation and their implications. , 2010, Hypertension.

[24]  J. Born,et al.  Acute sleep deprivation reduces energy expenditure in healthy men. , 2011, The American journal of clinical nutrition.

[25]  André Charles,et al.  Effects of sleep deprivation on Color-Word, Emotional, and Specific Stroop interference and on self-reported anxiety , 2006, Brain and Cognition.

[26]  P F Iampietro,et al.  Physiological responses of men during sleep deprivation. , 1968, Journal of applied physiology.

[27]  O. Blin,et al.  Hemodynamic, autonomic and baroreflex changes after one night sleep deprivation in healthy volunteers , 2009, Autonomic Neuroscience.

[28]  C. Kurt,et al.  Sleep deprivation induced anxiety and anaerobic performance. , 2007, Journal of sports science & medicine.

[29]  M Ishii,et al.  Effects of insufficient sleep on blood pressure monitored by a new multibiomedical recorder. , 1996, Hypertension.

[30]  B. Wallin,et al.  Renal noradrenaline spillover correlates with muscle sympathetic activity in humans. , 1996, The Journal of physiology.

[31]  Charles D. Spielberger,et al.  State-Trait Anxiety Inventory for Adults , 2012 .

[32]  Y. Stern,et al.  Increased sympathetic and decreased parasympathetic cardiovascular modulation in normal humans with acute sleep deprivation. , 2005, Journal of applied physiology.

[33]  Ngianga-Bakwin Kandala,et al.  Gender-Specific Associations of Short Sleep Duration With Prevalent and Incident Hypertension: The Whitehall II Study , 2007, Hypertension.

[34]  B. Wallin,et al.  Human muscle nerve sympathetic activity at rest. Relationship to blood pressure and age , 1978, The Journal of physiology.

[35]  J. Palmblad,et al.  Thyroid and adrenomedullary reactions during sleep deprivation. , 1979, Acta endocrinologica.

[36]  J. Carter,et al.  Menstrual cycle alters sympathetic neural responses to orthostatic stress in young, eumenorrheic women. , 2009, American journal of physiology. Endocrinology and metabolism.

[37]  J. Osborn,et al.  A neural set point for the long-term control of arterial pressure: beyond the arterial baroreceptor reflex. , 2005, American journal of physiology. Regulatory, integrative and comparative physiology.

[38]  V. Cortes-gallegos,et al.  Sleep deprivation and adaptive hormonal responses of healthy men. , 1989, Archives of andrology.

[39]  M. Feldner,et al.  A test of the effects of acute sleep deprivation on general and specific self-reported anxiety and depressive symptoms: an experimental extension. , 2010, Journal of behavior therapy and experimental psychiatry.

[40]  G. Sigurdsson,et al.  Effects of sleep deprivation on neural circulatory control. , 2000, Hypertension.