Simultaneous measurements of cardiac noradrenaline spillover and sympathetic outflow to skeletal muscle in humans

Wallin, B G; Esler, M; Dorward, P; Eisenhofer, G; Ferrier, C; Westerman, R; Jennings, G

doi:10.1113/jphysiol.1992.sp019217

Cited by 298Cardiovascular and exercise physiologyHeart Rate Variability and Autonomic ControlBlood Pressure and Hypertension Studies

Simultaneous measurements of cardiac noradrenaline spillover and sympathetic outflow to skeletal muscle in humans

Open access

Wallin, B G, Esler, M, Dorward, P, Eisenhofer, G, Ferrier, C, Westerman, R, Jennings, G·1992·The Journal of Physiology

DOI 10.1113/jphysiol.1992.sp019217PMC PMC1175546

Open this paper in CoChat — free account

Abstract

1. Muscle sympathetic nerve activity (MSA) was recorded in the peroneal nerve at the knee by microneurography in ten healthy subjects and determinations were made simultaneously of intra-arterial blood pressure, and whole-body and cardiac noradrenaline spillover to plasma. Measurements were made at rest, during isometric handgrip at 30% of maximum power and during stress induced by forced mental arithmetic. 2. At rest there were significant positive correlations between spontaneous MSA (expressed as number of sympathetic bursts min-1) and both spillover of noradrenaline from the heart and concentration of noradrenaline in coronary sinus venous plasma. 3. Both isometric handgrip and mental arithmetic led to sustained increases of blood pressure, heart rate and MSA. Plasma concentrations of noradrenaline and spillover of noradrenaline (total body and cardiac) increased. In general the effects were more pronounced during handgrip than during stress. 4. When comparing effects during handgrip and stress the ratio between the fractional increases of MSA and cardiac noradrenaline spillover were significantly greater during handgrip. 5. The data suggest (a) that there are proportional interindividual differences in the strength of resting sympathetic activity to heart and skeletal muscle which are determined by a common mechanism and (b) that handgrip and mental stress are associated with differences in balance between sympathetic outflows to heart and skeletal muscle.

Integrity signals

Registry

Crossref · 10.1113/jphysiol.1992.sp019217

Cites

29 of 29 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Measures of cardiac norepinephrine spillover correlate well with recordings of peripheral sympathetic nerve activity.
“Importantly, however, evidence does suggest that measures of cardiac norepinephrine spillover do correlate well with recordings of peripheral sympathetic nerve activity (41).”
From Hypertensive left ventricular hypertrophy: relation to peripheral sympathetic drive (2001) · cites this paper as [41]

Somatosensory, proprioceptive, and sympathetic activity in human peripheral nerves
Vallbo, A. B., Hagbarth, K. E., Torebjork, H. E., & Wallin, B. G. (1979) · Physiological Reviews · doi:10.1152/physrev.1979.59.4.919 · Cited by 1,507 · see citing works
General Characteristics of Sympathetic Activity in Human Muscle Nerves
Delius, W., Hagbarth, K. ‐., Hongell, A., & Wallin, B. G. (1972) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1972.tb05157.x · Cited by 831 · see citing works
Self-citation
Overflow of catecholamine neurotransmitters to the circulation: source, fate, and functions
Esler, M., Jennings, G., Lambert, G., Meredith, I., Horne, M., & Eisenhofer, G. (1990) · Physiological Reviews · doi:10.1152/physrev.1990.70.4.963 · Cited by 794 · see citing works
Microneurographic studies of the mechanisms of sympathetic nerve responses to static exercise in humans.
Mark, A. L., Victor, R. G., Nerhed, C., & Wallin, B. G. (1985) · Circulation Research · doi:10.1161/01.res.57.3.461 · Cited by 748 · see citing works
Assessment of human sympathetic nervous system activity from measurements of norepinephrine turnover.
Esler, M., Jennings, G., Korner, P., Willett, I., Dudley, F., Hasking, G., Anderson, W., & Lambert, G. (1988) · Hypertension · doi:10.1161/01.hyp.11.1.3 · Cited by 642 · see citing works
The variability of muscle nerve sympathetic activity in resting recumbent man
Sundlöf, G., & Wallin, B. G. (1977) · The Journal of Physiology · doi:10.1113/jphysiol.1977.sp012050 · Cited by 442 · see citing works
Influence of ventilation and hypocapnia on sympathetic nerve responses to hypoxia in normal humans
Somers, V. K., Mark, A. L., Zavala, D. C., & Abboud, F. M. (1989) · Journal of Applied Physiology · doi:10.1152/jappl.1989.67.5.2095 · Cited by 365 · see citing works
Sympathetic nerve discharge is coupled to muscle cell pH during exercise in humans.
Victor, R. G., Bertocci, L. A., Pryor, S. L., & Nunnally, R. L. (1988) · Journal of Clinical Investigation · doi:10.1172/jci113730 · Cited by 343 · see citing works
Effects of partial neuromuscular blockade on sympathetic nerve responses to static exercise in humans.
Victor, R. G., Pryor, S. L., Secher, N. H., & Mitchell, J. H. (1989) · Circulation Research · doi:10.1161/01.res.65.2.468 · Cited by 241 · see citing works
SYMPATHETIC ACTIVITY IN MAN AFTER SPINAL CORD INJURY
Stjernberg, L., Blumberg, H., & Wallin, B. G. (1986) · Brain · doi:10.1093/brain/109.4.695 · Cited by 233 · see citing works
The effects of stimulation of the left atrial receptors on sympathetic efferent nerve activity
Karim, F., Kidd, C., Malpus, C. M., & Penna, P. E. (1972) · The Journal of Physiology · doi:10.1113/jphysiol.1972.sp010030 · Cited by 220 · see citing works
Reciprocal and non-reciprocal action of the vagal and sympathetic nerves innervating the heart
Kollai, M., & Koizumi, K. (1979) · Journal of the Autonomic Nervous System · doi:10.1016/0165-1838(79)90004-3 · Cited by 191 · see citing works
Responses in muscle sympathetic activity to acute hypoxia in humans
Saito, M., Mano, T., Iwase, S., Koga, K., Abe, H., & Yamazaki, Y. (1988) · Journal of Applied Physiology · doi:10.1152/jappl.1988.65.4.1548 · Cited by 183 · see citing works
SYMPATHETIC OUTFLOW IN MAN AFTER ANAESTHESIA OF THE GLOSSOPHARYNGEAL AND VAGUS NERVES
Fagius, J., Wallin, B. G., Sundlöf, G., Nerhed, C., & Englesson, S. (1985) · Brain · doi:10.1093/brain/108.2.423 · Cited by 182 · see citing works
Cardiovascular adjustment to somatomotor activation. The elicitation of increments in heart rate, aortic pressure and venomotor tone with the initiation of muscle contraction.
FREYSCHUSS, U. (1970) · PubMed · Cited by 137 · see citing works
Muscle sympathetic activity and norepinephrine release during mental challenge in humans
Hjemdahl, P., Fagius, J., FREYSCHUSS, U., Wallin, B. G., Daleskog, M., Bohlin, G., & Perski, A. (1989) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1989.257.5.e654 · Cited by 131 · see citing works
Simultaneous determination of plasma noradrenaline and adrenaline kinetics
Os, M., Esler, M., Angus, J. A., Cox, H., & Eisenhofer, G. (1990) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/bf00169730 · Cited by 120 · see citing works
Contribution of individual organs to total noradrenaline release in humans.
Esler, M., Jennings, G., Leonard, P., SACHARIAS, N., Burke, F., Johns, J., & Blombery, P. A. (1984) · PubMed · Cited by 114 · see citing works
Measurement of overall and cardiac norepinephrine release into plasma during cognitive challenge
Esler, M., Jennings, G., & Lambert, G. W. (1989) · Psychoneuroendocrinology · doi:10.1016/0306-4530(89)90047-4 · Cited by 101 · see citing works
Augmented sympathetic nerve activity in response to stressors in young borderline hypertensive men
MATSUKAWA, T., GOTOH, E., UNEDA, S., MIYAJIMA, E., SHIONOIRI, H., TOCHIKUBO, O., & ISHII, M. (1991) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1991.tb09064.x · Cited by 97 · see citing works
Sympathetic activation is associated with increases in EMG during fatiguing exercise
Seals, D. R., & Enoka, R. M. (1989) · Journal of Applied Physiology · doi:10.1152/jappl.1989.66.1.88 · Cited by 95 · see citing works
Evidence for increased renal norepinephrine overflow during sodium restriction in humans.
Friberg, P., Meredith, I. T., Jennings, G., Lambert, G. W., Fazio, V., & Esler, M. D. (1990) · Hypertension · doi:10.1161/01.hyp.16.2.121 · Cited by 91 · see citing works
Arterial baroreflex control of sympathetic nerve activity during elevation of blood pressure in normal man: dominance of aortic baroreflexes.
Sanders, J. S., Ferguson, D. W., & Mark, A. L. (1988) · Circulation · doi:10.1161/01.cir.77.2.279 · Cited by 82 · see citing works
BARORECEPTOR RESETTING AND OTHER DETERMINANTS OF BAROREFLEX PROPERTIES IN HYPERTENSION
Korner, P. I. (1989) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.1989.tb02995.x · Cited by 69 · see citing works
Assessment of norepinephrine secretion and production.
Hoeldtke, R. D., Cilmi, K. M., Reichard, G., Boden, G. H., & Owen, O. E. (1983) · PubMed · Cited by 61 · see citing works
STUDIES UPON THE RELATIONSHIP BETWEEN BARORECEPTOR AND SYMPATHETIC ACTIVITY
Green, J. H., & Heffron, P. F. (1968) · Quarterly Journal of Experimental Physiology and Cognate Medical Sciences · doi:10.1113/expphysiol.1968.sp001942 · Cited by 52 · see citing works
Study of cardiac sympathetic and vagal efferent activity during reflex responses produced by stretch of the atria
Kollai, M., Koizumi, K., Yamashita, H., & Brooks, C. M. (1978) · Brain Research · doi:10.1016/0006-8993(78)90817-x · Cited by 42 · see citing works
Adrenaline infusion in man increases muscle sympathetic nerve activity and noradrenaline overflow to plasma
Persson, B., Andersson, O. K., Hjemdahl, P., Wysocki, M., Agerwall, S., & Wallin, G. (1989) · Journal of Hypertension · doi:10.1097/00004872-198909000-00009 · Cited by 38 · see citing works
Nature of differential sympathetic discharges in chemoreceptor reflexes
Kollai, M., Koizumi, K., & Brooks, C. M. (1978) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.75.10.5239 · Cited by 32 · see citing works

Flagged first, then by citations

Sorted by citations

Heart rate variability: origins, methods, and interpretive caveats
BERNTSON, G. G., THOMAS BIGGER, J., ECKBERG, D. L., GROSSMAN, P., KAUFMANN, P. G., MALIK, M., NAGARAJA, H. N., PORGES, S. W., SAUL, J. P., STONE, P. H., et al. (1997) · Psychophysiology · doi:10.1111/j.1469-8986.1997.tb02140.x · Cited by 3,962 · see citing works
Sympathovagal Balance: A Critical Appraisal
Eckberg, D. L. (1997) · Circulation · doi:10.1161/01.cir.96.9.3224 · Cited by 1,087 · see citing works
The utility of low frequency heart rate variability as an index of sympathetic cardiac tone: A review with emphasis on a reanalysis of previous studies
Reyes del Paso, G. A., Langewitz, W., Mulder, L. J. M., van Roon, A., & Duschek, S. (2013) · Psychophysiology · doi:10.1111/psyp.12027 · Cited by 954 · see citing works
Sympathetic Nervous System Overactivity and Its Role in the Development of Cardiovascular Disease
Malpas, S. C. (2010) · Physiological Reviews · doi:10.1152/physrev.00007.2009 · Cited by 696 · see citing works
Mechanisms Underlying Very-Low-Frequency RR-Interval Oscillations in Humans
Taylor, J. A., Carr, D. L., Myers, C. W., & Eckberg, D. L. (1998) · Circulation · doi:10.1161/01.cir.98.6.547 · Cited by 660 · see citing works
How to assess sympathetic activity in humans
Grassi, G., & Esler, M. (1999) · Journal of Hypertension · doi:10.1097/00004872-199917060-00001 · Cited by 455 · see citing works
Self-citation
The human respiratory gate
Eckberg, D. L. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2002.037192 · Cited by 431 · see citing works
Regional Sympathetic Nervous Activity and Oxygen Consumption in Obese Normotensive Human Subjects
Vaz, M., Jennings, G., Turner, A., Cox, H., Lambert, G., & Esler, M. (1997) · Circulation · doi:10.1161/01.cir.96.10.3423 · Cited by 404 · see citing works
Heart rate spectral analysis, cardiac norepinephrine spillover, and muscle sympathetic nerve activity during human sympathetic nervous activation and failure.
Kingwell, B. A., Thompson, J. M., Kaye, D. M., McPherson, G. A., Jennings, G., & Esler, M. (1994) · Circulation · doi:10.1161/01.cir.90.1.234 · Cited by 401 · see citing works
Body fat and sympathetic nerve activity in healthy subjects.
Scherrer, U., Randin, D., Tappy, L., Vollenweider, P., Jéquier, E., & Nicod, P. (1994) · Circulation · doi:10.1161/01.cir.89.6.2634 · Cited by 383 · see citing works
Clinical aspects of sympathetic activation and parasympathetic withdrawal in heart failure
Floras, J. S. (1993) · Journal of the American College of Cardiology · doi:10.1016/0735-1097(93)90466-e · Cited by 358 · see citing works
Sex Differences in Sympathetic Neural-Hemodynamic Balance: Implications for Human Blood Pressure Regulation
Hart, E. C., Charkoudian, N., Wallin, B. G., Curry, T. B., Eisenach, J. H., & Joyner, M. J. (2009) · Hypertension · doi:10.1161/hypertensionaha.108.126391 · Cited by 349 · see citing works
Exposure to hypoxia produces long-lasting sympathetic activation in humans
Xie, A., Skatrud, J. B., Puleo, D. S., & Morgan, B. J. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.91.4.1555 · Cited by 303 · see citing works
Exercise training restores baroreflex sensitivity in never-treated hypertensive patients
Laterza, M. C., de Matos, L. D. N. J., Trombetta, I. C., Braga, A. M. W., Roveda, F., Alves, M. J. N. N., Krieger, E. M., Negrão, C. E., & Rondon, M. U. P. B. (2007) · Hypertension · doi:10.1161/hypertensionaha.106.085548 · Cited by 299 · see citing works
Autonomic Adjustments to Exercise in Humans
Fisher, J. P., Young, C. N., & Fadel, P. J. (2015) · Comprehensive physiology · doi:10.1002/cphy.c140022 · Cited by 343 · see citing works
Marked Sympathetic Activation in Patients with Chronic Respiratory Failure
Heindl, S., Lehnert, M., Criée, C.-P., Hasenfuss, G. P., & Andreas, S. (2001) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.164.4.2007085 · Cited by 288 · see citing works
Microneurography: how the technique developed and its role in the investigation of the sympathetic nervous system
Vallbo, Å. B., Hagbarth, K. E., & Wallin, B. G. (2004) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00470.2003 · Cited by 273 · see citing works
Sympathetic Neural Mechanisms in Human Cardiovascular Health and Disease
Charkoudian, N., & Rabbitts, J. A. (2009) · Mayo Clinic Proceedings · doi:10.4065/84.9.822 · Cited by 270 · see citing works
Balance between cardiac output and sympathetic nerve activity in resting humans: role in arterial pressure regulation
Charkoudian, N., Joyner, M. J., Johnson, C. P., Eisenach, J. H., Dietz, N. M., & Wallin, B. G. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.090076 · Cited by 254 · see citing works
Self-citation
Sympathetic restraint of respiratory sinus arrhythmia: implications for vagal-cardiac tone assessment in humans
Taylor, J. A., Myers, C. W., Halliwill, J. R., Seidel, H., & Eckberg, D. L. (2001) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2001.280.6.h2804 · Cited by 249 · see citing works
The 2009 Carl Ludwig Lecture: pathophysiology of the human sympathetic nervous system in cardiovascular diseases: the transition from mechanisms to medical management
Esler, M. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00832.2009 · Cited by 242 · see citing works
Gender affects sympathetic and hemodynamic response to postural stress
Shoemaker, J. K., Hogeman, C. S., Khan, M. R., Kimmerly, D. S., & Sinoway, L. I. (2001) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2001.281.5.h2028 · Cited by 243 · see citing works
Decreased heart rate variability is associated with higher levels of inflammation in middle-aged men
Lampert, R., Bremner, J. D., Su, S., Miller, A., Lee, F., Cheema, F., Goldberg, J., & Vaccarino, V. (2008) · American Heart Journal · doi:10.1016/j.ahj.2008.07.009 · Cited by 240 · see citing works
Sympathetic regulation of vascular function in health and disease
Bruno, R. M., Ghiadoni, L., Seravalle, G., Dell’Oro, R., Taddei, S., & Grassi, G. M. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00284 · Cited by 241 · see citing works
Depressed Baroreflex Sensitivity in Patients With Obstructive Sleep Apnea
Carlson, J. T., Hedner, J. A., Sellgren, J., Elam, M., & Wallin, B. G. (1996) · American journal of respiratory and critical care medicine · doi:10.1164/ajrccm.154.5.8912770 · Cited by 239 · see citing works
Ventral medial prefrontal cortex and cardiovagal control in conscious humans
Wong, S. W., Massé, N., Kimmerly, D. S., Menon, R. S., & Shoemaker, J. K. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2006.12.027 · Cited by 233 · see citing works
Sympathetic Neural Activity in Hypertension and Related Diseases
Grassi, G. M. (2010) · American Journal of Hypertension · doi:10.1038/ajh.2010.154 · Cited by 225 · see citing works
Is polycystic ovary syndrome associated with high sympathetic nerve activity and size at birth?
Sverrisdóttir, Y. B., Mogren, T., Kataoka, J., Janson, P. O., & Stener-Victorin, E. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00725.2007 · Cited by 216 · see citing works
Sympathetic Nervous System and Blood Pressure in Humans
Joyner, M. J., Charkoudian, N., & Wallin, B. G. (2010) · Hypertension · doi:10.1161/hypertensionaha.109.140186 · Cited by 221 · see citing works
Sympathetic Activity in Patients With Panic Disorder at Rest, Under Laboratory Mental Stress, and During Panic Attacks
Wilkinson, D. J. C., Thompson, J. M., Lambert, G. W., Jennings, G. L., Schwarz, R. G., Jefferys, D., Turner, A. G., & Esler, M. D. (1998) · Archives of General Psychiatry · doi:10.1001/archpsyc.55.6.511 · Cited by 214 · see citing works
Self-citation
Sympathetic neural control of integrated cardiovascular function: Insights from measurement of human sympathetic nerve activity
Wallin, B. G., & Charkoudian, N. (2007) · Muscle & Nerve · doi:10.1002/mus.20831 · Cited by 206 · see citing works
Central sympathetic overactivity: Maladies and mechanisms
Fisher, J. P., Young, C. N., & Fadel, P. J. (2009) · Autonomic Neuroscience · doi:10.1016/j.autneu.2009.02.003 · Cited by 202 · see citing works
The rhythmicity of sympathetic nerve activity
Malpas, S. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00030-6 · Cited by 192 · see citing works
Low-frequency electroacupuncture and physical exercise decrease high muscle sympathetic nerve activity in polycystic ovary syndrome
Stener-Victorin, E., Jedel, E., Janson, P. O., & Sverrisdottir, Y. B. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00197.2009 · Cited by 194 · see citing works
Sex, ageing and resting blood pressure: gaining insights from the integrated balance of neural and haemodynamic factors
Hart, E. C., Joyner, M. J., Wallin, B. G., & Charkoudian, N. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2011.224642 · Cited by 192 · see citing works
Human autonomic rhythms: vagal cardiac mechanisms in tetraplegic subjects.
Koh, J., Brown, T. E., Beightol, L. A., Ha, C. Y., & Eckberg, D. L. (1994) · The Journal of Physiology · doi:10.1113/jphysiol.1994.sp020039 · Cited by 186 · see citing works
Human muscle sympathetic nerve activity and plasma noradrenaline kinetics in space
Ertl, A. C., Diedrich, A., Biaggioni, I., Levine, B. D., Robertson, R. M., Cox, J. F., Zuckerman, J. H., Pawelczyk, J. A., Ray, C. A., Buckey, J. C., et al. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2001.012576 · Cited by 184 · see citing works
Chronic Exercise Reduces Sympathetic Nerve Activity in Rabbits With Pacing-Induced Heart Failure
Liu, J., Irvine, S. D., Reid, I. A., Patel, K. P., & Zucker, I. H. (2000) · Circulation · doi:10.1161/01.cir.102.15.1854 · Cited by 168 · see citing works
Recording sympathetic nerve activity in conscious humans and other mammals: guidelines and the road to standardization
Hart, E. C., Head, G. A., Carter, J. R., Wallin, B. G., May, C. N., Hamza, S. M., Hall, J. E., Charkoudian, N., & Osborn, J. W. (2017) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00703.2016 · Cited by 166 · see citing works
Renal noradrenaline spillover correlates with muscle sympathetic activity in humans.
Wallin, B. G., Thompson, J. M., Jennings, G., & Esler, M. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021265 · Cited by 160 · see citing works
Slow breathing reduces sympathoexcitation in COPD
Raupach, T., Bahr, F., Herrmann, P., Lüthje, L., Heusser, K., Hasenfuss, G. P., Bernardi, L., & Andreas, S. (2008) · European Respiratory Journal · doi:10.1183/09031936.00109607 · Cited by 166 · see citing works
Bioastronautics: The Influence of Microgravity on Astronaut Health
Blaber, E. A., Marçal, H., & Burns, B. P. (2010) · Astrobiology · doi:10.1089/ast.2009.0415 · Cited by 162 · see citing works
Hypertensive left ventricular hypertrophy: relation to peripheral sympathetic drive
Greenwood, J. P., Scott, E. M., Stoker, J. B., & Mary, D. A. S. G. (2001) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(01)01600-x · Cited by 161 · see citing works
A sympathetic view of the sympathetic nervous system and human blood pressure regulation
Joyner, M. J., Charkoudian, N., & Wallin, B. G. (2008) · Experimental Physiology · doi:10.1113/expphysiol.2007.039545 · Cited by 155 · see citing works
Controlled breathing protocols probe human autonomic cardiovascular rhythms
Cooke, W. H., Cox, J. F., Diedrich, A., Taylor, J. A., Beightol, L. A., Ames, J. E., Hoag, J. B., Seidel, H., & Eckberg, D. L. (1998) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1998.274.2.h709 · Cited by 156 · see citing works
Weight loss improves neurovascular and muscle metaboreflex control in obesity
Trombetta, I. C., Batalha, L. T., Rondon, M. U. P. B., Laterza, M. C., Kuniyoshi, F. H. S., Gowdak, M., Barretto, A. C. P., Halpern, A., Villares, S. M., & Negrão, C. E. (2003) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01090.2002 · Cited by 150 · see citing works
The use of heart rate variability measures to assess autonomic control during exercise
SANDERCOCK, G. R. H., & Brodie, D. A. (2006) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.2006.00556.x · Cited by 150 · see citing works
Vascular adrenergic responsiveness is inversely related to tonic activity of sympathetic vasoconstrictor nerves in humans
Charkoudian, N., Joyner, M. J., Sokolnicki, L. A., Johnson, C. P., Eisenach, J. H., Dietz, N. M., Curry, T. B., & Wallin, B. G. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2005.104075 · Cited by 145 · see citing works
Self-citation
Sympathetic Nervous System
Neukirchen, M., Kienbaum, P., Warner, D. S., & Warner, M. A. A. (2008) · Anesthesiology · doi:10.1097/aln.0b013e31818e435c · Cited by 144 · see citing works
Sympathetic Neural Regulation of Blood Pressure: Influences of Sex and Aging
Hart, E. C., & Charkoudian, N. (2014) · Physiology · doi:10.1152/physiol.00031.2013 · Cited by 146 · see citing works
Low-frequency Spectral Power of Heart Rate Variability Is Not a Specific Marker of Cardiac Sympathetic Modulation
Hopf, H., Skyschally, A., Heusch, G., & Peters, J. (1995) · Anesthesiology · doi:10.1097/00000542-199503000-00002 · Cited by 142 · see citing works
Sympathetic neural responses to mental stress: responders, nonresponders and sex differences
Carter, J. R., & Ray, C. A. (2009) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01234.2008 · Cited by 139 · see citing works
Gender-related differences in the sympathetic vasoconstrictor drive of normal subjects
Hogarth, A. J., Mackintosh, A., & Mary, D. (2007) · Clinical Science · doi:10.1042/cs20060288 · Cited by 136 · see citing works
Neurovascular responses to mental stress
Carter, J. R., Kupiers, N. T., & Ray, C. A. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2004.079665 · Cited by 130 · see citing works
Relationship Between Central Sympathetic Drive and Magnetic Resonance Imaging–Determined Left Ventricular Mass in Essential Hypertension
Burns, J., Sivananthan, M. U., Ball, S. G., Mackintosh, A. F., Mary, D. A. S. G., & Greenwood, J. P. (2007) · Circulation · doi:10.1161/circulationaha.106.668863 · Cited by 122 · see citing works
Neural Control of the Circulation: How Sex and Age Differences Interact in Humans
Joyner, M. J., Barnes, J. N., Hart, E. C., Wallin, B. G., & Charkoudian, N. (2014) · Comprehensive physiology · doi:10.1002/cphy.c140005 · Cited by 143 · see citing works
Sympathetic regulation during thermal stress in human aging and disease
Greaney, J. L., Kenney, W. L., & Alexander, L. M. (2015) · Autonomic Neuroscience · doi:10.1016/j.autneu.2015.11.002 · Cited by 117 · see citing works
Assessment of sympathetic neural activity in chronic insomnia: evidence for elevated cardiovascular risk
Carter, J. R., Grimaldi, D., Fonkoue, I. T., Medalie, L., Mokhlesi, B., & Cauter, E. V. (2018) · SLEEP · doi:10.1093/sleep/zsy048 · Cited by 110 · see citing works
Region-Specific Neuropeptide Y Overflows at Rest and During Sympathetic Activation in Humans
Morris, M. J., Cox, H. S., Lambert, G. W., Kaye, D. M., Jennings, G., Meredith, I. T., & Esler, M. (1997) · Hypertension · doi:10.1161/01.hyp.29.1.137 · Cited by 107 · see citing works
Sympathetic Neural Activity to the Cardiovascular System: Integrator of Systemic Physiology and Interindividual Characteristics
Charkoudian, N., & Wallin, B. G. (2014) · Comprehensive physiology · doi:10.1002/cphy.c130038 · Cited by 107 · see citing works
Elevated Muscle Sympathetic Nerve Activity Contributes to Central Artery Stiffness in Young and Middle-Age/Older Adults
Holwerda, S. W., Luehrs, R. E., DuBose, L. E., Collins, M. T., Wooldridge, N. A., Stroud, A., Fadel, P. J., Abboud, F. M., & Pierce, G. L. (2019) · Hypertension · doi:10.1161/hypertensionaha.118.12462 · Cited by 106 · see citing works
Free plasma catecholamines in spinal cord injured persons with different injury levels at rest and during exercise
Schmid, A., Huonker, M., Stahl, F., Barturen, J.-M., König, D., Heim, M. U., Lehmann, M. J., & Keul, J. (1998) · Journal of the Autonomic Nervous System · doi:10.1016/s0165-1838(97)00127-6 · Cited by 106 · see citing works
Sympathetic activation in human heart failure: diverse mechanisms, therapeutic opportunities
Floras, J. S. (2003) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.2003.01087.x · Cited by 104 · see citing works
Cardiovascular Autonomic Dysfunction in Chronic Kidney Disease: a Comprehensive Review
Salman, I. M. (2015) · Current Hypertension Reports · doi:10.1007/s11906-015-0571-z · Cited by 108 · see citing works
Sympathoneural and Adrenomedullary Responses to Mental Stress
Carter, J. R., & Goldstein, D. S. (2014) · Comprehensive physiology · doi:10.1002/cphy.c140030 · Cited by 115 · see citing works
Impact of Acute Mental Stress on Sympathetic Nerve Activity and Regional Blood Flow in Advanced Heart Failure
Middlekauff, H. R., Nguyen, A. H., Negrão, C. E., Nitzsche, E. U., Hoh, C. K., Natterson-Horowitz, B., Hamilton, M. A., Fonarow, G. C., Hage, A., & Moriguchi, J. D. (1997) · Circulation · doi:10.1161/01.cir.96.6.1835 · Cited by 97 · see citing works
Intense Sympathetic Nerve Activity in Adults with Hypopituitarism and Untreated Growth Hormone Deficiency1
Sverrisdóttir, Y. B., Elam, M., Herlitz, H., Bengtsson, B., & Johannsson, G. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.6.4895 · Cited by 97 · see citing works
Phenotypic Evidence of Faulty Neuronal Norepinephrine Reuptake in Essential Hypertension
Rumantir, M. S., Kaye, D. M., Jennings, G. L., Vaz, M., Hastings, J. A., & Esler, M. D. (2000) · Hypertension · doi:10.1161/01.hyp.36.5.824 · Cited by 95 · see citing works
Regional Sympathetic Nervous Activation after a Large Meal in Humans
Cox, H. S., Kaye, D. M., Thompson, J. M., Turner, A., Jennings, G., Itsiopoulos, C., & Esler, M. (1995) · Clinical Science · doi:10.1042/cs0890145 · Cited by 95 · see citing works
Sympathetic neural adaptations to exercise training in humans
Carter, J. R., & Ray, C. A. (2015) · Autonomic Neuroscience · doi:10.1016/j.autneu.2014.10.020 · Cited by 94 · see citing works
Stress and Its Role in Sympathetic Nervous System Activation in Hypertension and the Metabolic Syndrome
Lambert, É., & Lambert, G. W. (2011) · Current Hypertension Reports · doi:10.1007/s11906-011-0186-y · Cited by 93 · see citing works
Regulation of central angiotensin type 1 receptors and sympathetic outflow in heart failure
Zucker, I. H., Schultz, H. D., Patel, K. P., Wang, W., & Gao, L. (2009) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00073.2009 · Cited by 94 · see citing works
Nitric oxide-independent effects of tempol on sympathetic nerve activity and blood pressure in DOCA-salt rats
Xu, H., Fink, G. D., & Galligan, J. J. (2002) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00134.2002 · Cited by 91 · see citing works
Dissociation between microneurographic and heart rate variability estimates of sympathetic tone in normal subjects and patients with heart failure
Notarius, C. F., Butler, G. C., Ando, S., Pollard, M. J., Senn, B. L., & Floras, J. S. (1999) · Clinical Science · doi:10.1042/cs0960557 · Cited by 89 · see citing works
Postmenopausal Estrogen Administration Suppresses Muscle Sympathetic Nerve Activity<sup>1</sup>
Weitz, G., Elam, M., Born, J., Fehm, H. L., & Dodt, C. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.1.7138 · Cited by 97 · see citing works
Clinical Application of Noradrenaline Spillover Methodology: Delineation of Regional Human Sympathetic Nervous Responses
Esler, M. (1993) · Pharmacology & Toxicology · doi:10.1111/j.1600-0773.1993.tb00579.x · Cited by 82 · see citing works
Therapeutic strategies for targeting excessive central sympathetic activation in human hypertension
Fisher, J. P., & Fadel, P. J. (2010) · Experimental Physiology · doi:10.1113/expphysiol.2009.047332 · Cited by 85 · see citing works
Regulation of Sympathetic Nerve Activity in Heart Failure
Liu, J., & Zucker, I. H. (1999) · Circulation Research · doi:10.1161/01.res.84.4.417 · Cited by 83 · see citing works
Sympathetic responses to vestibular activation in humans
Carter, J. R., & Ray, C. A. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00896.2007 · Cited by 82 · see citing works
Exercise training enhances baroreflex sensitivity by an angiotensin II-dependent mechanism in chronic heart failure
Mousa, T. M., Liu, D., Cornish, K. G., & Zucker, I. H. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00601.2007 · Cited by 82 · see citing works
Increased Sympathetic Nerve Activity in COPD is Associated with Morbidity and Mortality
Andreas, S., Haarmann, H., Klarner, S. F., Hasenfuss, G. P., & Raupach, T. (2013) · Lung · doi:10.1007/s00408-013-9544-7 · Cited by 79 · see citing works
Low birth size and final height predict high sympathetic nerve activity in adulthood
Boguszewski, M. C. D. S., Johannsson, G., Fortes, L. C., & Sverrisdóttir, Y. B. (2004) · Journal of Hypertension · doi:10.1097/00004872-200406000-00017 · Cited by 76 · see citing works
Sympathetic and baroreflex alterations in congestive heart failure with preserved, midrange and reduced ejection fraction
Seravalle, G., Quarti‐Trevano, F., Dell’Oro, R., Gronda, E., Spaziani, D., Facchetti, R., Cuspidi, C., Mancia, G., & Grassi, G. M. (2018) · Journal of Hypertension · doi:10.1097/hjh.0000000000001856 · Cited by 76 · see citing works
Possible genetic influence on the strength of human muscle nerve sympathetic activity at rest.
Wallin, B. G., Kunimoto, M., & Sellgren, J. (1993) · Hypertension · doi:10.1161/01.hyp.22.3.282 · Cited by 76 · see citing works
Blood Pressure Responses to Renal Denervation Precede and Are Independent of the Sympathetic and Baroreflex Effects
Grassi, G. M., Seravalle, G., Brambilla, G., Trabattoni, D., Cuspidi, C., Corso, R., Pieruzzi, F., Genovesi, S., Stella, A., Facchetti, R., et al. (2015) · Hypertension · doi:10.1161/hypertensionaha.114.04823 · Cited by 75 · see citing works
Direct Evidences for Sympathetic Hyperactivity and Baroreflex Impairment in Tako Tsubo Cardiopathy
Vaccaro, A., Despas, F., Delmas, C., Lairez, O., Lambert, É., Lambert, G. W., Labrunée, M., Guiraud, T., Esler, M., Galinier, M., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093278 · Cited by 75 · see citing works
Sympathetic nerve traffic correlates with the release of nitric oxide in humans: implications for blood pressure control
Skarphedinsson, J. O., Elam, M., Jungersten, L., & Wallin, B. G. (1997) · The Journal of Physiology · doi:10.1111/j.1469-7793.1997.671bm.x · Cited by 75 · see citing works
Abnormal Neurovascular Control during Sympathoexcitation in Obesity
Kuniyoshi, F. H. S., Trombetta, I. C., Batalha, L. T., Rondon, M. U. P. B., Laterza, M. C., Gowdak, M. M. G., Barretto, A. C. P., Halpern, A., Villares, S. M. F., Lima, E. G., et al. (2003) · Obesity Research · doi:10.1038/oby.2003.190 · Cited by 74 · see citing works
Sympathetic nervous system and hypertension: New evidences
Seravalle, G., & Grassi, G. M. (2022) · Autonomic Neuroscience · doi:10.1016/j.autneu.2022.102954 · Cited by 73 · see citing works
Effects of the menstrual cycle on sympathetic neural responses to mental stress in humans
Carter, J. R., & Lawrence, J. E. (2007) · The Journal of Physiology · doi:10.1113/jphysiol.2007.141051 · Cited by 71 · see citing works
Baroreflex control of muscle sympathetic nerve activity after 120 days of 6° head-down bed rest
Kamiya, A., Iwase, S., Kitazawa, H., Mano, T., Виноградова, О. Л., & Kharchenko, I. B. (2000) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2000.278.2.r445 · Cited by 71 · see citing works
Relative burst amplitude of muscle sympathetic nerve activity is an indicator of altered sympathetic outflow in chronic anxiety
Holwerda, S. W., Luehrs, R. E., Gremaud, A. L., Wooldridge, N. A., Stroud, A., Fiedorowicz, J. G., Abboud, F. M., & Pierce, G. L. (2018) · Journal of Neurophysiology · doi:10.1152/jn.00064.2018 · Cited by 69 · see citing works
Single‐unit muscle sympathetic nervous activity and its relation to cardiac noradrenaline spillover
Lambert, E. A., Schlaich, M. P., Dawood, T., Sari, C., Chopra, R., Barton, D. A., Kaye, D. M., Elam, M., Esler, M. D., & Lambert, G. W. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.205351 · Cited by 68 · see citing works
Sympathetic nerve traffic and baroreflex function in optimal, normal, and high-normal blood pressure states
Seravalle, G., Lonati, L. M., Buzzi, S., Cairo, M., Trevano, F. Q., Dell’Oro, R., Facchetti, R., Mancia, G., & Grassi, G. M. (2015) · Journal of Hypertension · doi:10.1097/hjh.0000000000000567 · Cited by 68 · see citing works
Leptin interacts with heart rate but not sympathetic nerve traffic in healthy male subjects
Narkiewicz, K., Kato, M., Phillips, B. G., Pesek, C. A., Choe, I., Winnicki, M., Palatini, P., Sivitz, W. I., & Somers, V. K. (2001) · Journal of Hypertension · doi:10.1097/00004872-200106000-00014 · Cited by 68 · see citing works
Nasal Oxygen and Muscle Sympathetic Nerve Activity in Heart Failure*
Andreas, S., Binggeli, C., Mohaçsi, P., Lüscher, T. F., & Noll, G. (2003) · CHEST Journal · doi:10.1378/chest.123.2.366 · Cited by 66 · see citing works
Isometric exercise facilitates attention to salient events in women via the noradrenergic system
Mather, M., Huang, R., Clewett, D., Nielsen, S. E., Velasco, R., Tu, K., Han, S., & Kennedy, B. L. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.116560 · Cited by 61 · see citing works
Neural and cardiovascular responses to emotional stress in humans
Carter, J. R., Durocher, J. J., & Kern, R. P. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90646.2008 · Cited by 65 · see citing works
Relationship between muscle sympathetic nerve activity and systemic hemodynamics during nitric oxide synthase inhibition in humans
Charkoudian, N., Joyner, M. J., Barnes, S. A., Johnson, C. P., Eisenach, J. H., Dietz, N. M., & Wallin, B. G. (2006) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00234.2006 · Cited by 64 · see citing works
Sympathomodulatory Effects of Antihypertensive Drug Treatment
Grassi, G. M. (2016) · American Journal of Hypertension · doi:10.1093/ajh/hpw012 · Cited by 64 · see citing works

Muscle sympathetic activity and venous plasma noradrenaline concentrations during static exercise in normotensive and hypertensive subjects
Wallin, B. G., Mörlin, C., & Hjemdahl, P. (1987) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1987.tb08088.x · Cited by 76 · see citing works
Muscle sympathetic activity and plasma concentrations of noradrenaline.
Bg, W. (1984) · PubMed · Cited by 36 · see citing works
Responses in muscle sympathetic nerve activity to sustained hand-grips of different tensions in humans
Saito, M., Mano, T., Abe, H., & Iwase, S. (1986) · European Journal of Applied Physiology · doi:10.1007/bf00421643 · Cited by 66 · see citing works
Inter‐individual Variability in Muscle Sympathetic Nerve Activity during Static Handgrip in Healthy Young Men
Incognito, A. V., Doherty, C. J., Lee, J. B., Burns, M. J., & Millar, P. J. (2017) · The FASEB Journal · doi:10.1096/fasebj.31.1_supplement.708.8
Muscle sympathetic activity and norepinephrine release during mental challenge in humans
Hjemdahl, P., Fagius, J., FREYSCHUSS, U., Wallin, B. G., Daleskog, M., Bohlin, G., & Perski, A. (1989) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1989.257.5.e654 · Cited by 131 · see citing works

Authors: Wallin, B. G., Esler, M., Dorward, P., Eisenhofer, G., Ferrier, C., Westerman, R., & Jennings, G.
Affiliations: Baker Heart and Diabetes Institute (AU)
ORCID: Esler, M
Jennings, G
Venue: The Journal of Physiology
Publisher: Wiley
Published: 1992-07
Volume: 453
Issue: 1
Pages: 45-58
ISSN: 0022-3751 (ISSN-L)
1469-7793
DOI: 10.1113/jphysiol.1992.sp019217
PMC: PMC1175546
OpenAlex: W2138399442
Cited by: 298
References: 29
Citations by year: 2026: 3 · 2025: 5 · 2024: 2 · 2023: 5 · 2022: 7 · 2021: 8 · 2020: 12 · 2019: 6 · 2018: 11 · 2017: 4 · 2016: 7 · 2015: 16 · 2014: 18 · 2013: 7 · 2012: 14
FWCI: 16.30
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: The Journal of Physiology (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Blood Pressure and Hypertension Studies
Keywords: muscle sympathetic nerve activity, peroneal nerve, isometric handgrip, mental arithmetic stress, blood pressure, heart rate, interindividual variability, sympathetic nervous system
MeSH terms: Adult, Aged, Blood Pressure, Heart, Heart Rate, Humans, Isometric Contraction, Male, Middle Aged, Muscles, Myocardium, Norepinephrine, Stress, Psychological, Sympathetic Nervous System

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Simultaneous measurements of cardiac noradrenaline spillover and sympathetic outflow to skeletal muscle in humans

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks