TY - JOUR
T1 - Asynchronous action potential discharge in human muscle sympathetic nerve activity
AU - Klassen, Stephen A.
AU - Moir, M. Erin
AU - Limberg, Jacqueline K.
AU - Baker, Sarah E.
AU - Nicholson, Wayne T.
AU - Curry, Timothy B.
AU - Joyner, Michael J.
AU - Shoemaker, J. Kevin
N1 - Funding Information:
Part of this study was completed in the National Institutes of Health Center for Clinical and Translational Science at the Mayo Clinic (UL1TR000135). Funding support was provided by American Heart Association Grant 15SDG25080095 and National Heart, Lung, and Blood Institute Grants HL-083947 (to M. J. Joyner), HL-130339 (to J. K. Limberg), and HL-131151 (to S. E. Baker). This work was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant 217916-2013 (to J. K. Shoemaker). S. A. Klassen is supported by a NSERC Doctoral Scholarship and formerly by an Ontario Graduate Doctoral Scholarship (OGS). M. E. Moir is supported by an OGS. J. K. Shoemaker is a Tier 1 Canadian Research Chair for Integrative Physiology of exercise and Health.
Publisher Copyright:
© 2019 the American Physiological Society.
PY - 2019
Y1 - 2019
N2 - What strategies are employed by the sympathetic system to communicate with the circulation? Muscle sympathetic nerve activity (MSNA) occurs in bursts of synchronous action potential (AP) discharge, yet whether between-burst asynchronous AP firing exists remains unknown. Using multiunit microneurography and a continuous wavelet transform to isolate APs, we studied AP synchronicity within human MSNA. Asynchronous APs were defined as those which occurred between bursts. Experiment 1 quantified AP synchronicity in eight individuals at baseline (BSL), -10 mmHg lower body negative pressure (LBNP), -40 mmHg LBNP, and end-expiratory apnea (APN). At BSL, 33 ± 12% of total AP activity was asynchronous. Asynchronous discharge was unchanged from BSL (67 ± 37 AP/min) to -10 mmHg LBNP (69 ± 33 AP/min), -40 mmHg LBNP (83 ± 68 AP/min), or APN (62 ± 39 AP/min). Across all conditions, asynchronous AP probability and frequency decreased with increasing AP size. Experiment 2 examined the impact of the ganglia on AP synchronicity by using nicotinic blockade (trimethaphan). The largest asynchronous APs were derecruited from BSL (11 ± 4 asynchronous AP clusters) to the last minute of the trimethaphan infusion with visible bursts (7 ± 2 asynchronous AP clusters). However, the 6 ± 2 smallest asynchronous AP clusters could not be blocked by trimethaphan and persisted to fire 100 ± 0% asynchronously without forming bursts. Nonnicotinic ganglionic mechanisms affect some, but not all, asynchronous activity. The fundamental behavior of human MSNA contains between- burst asynchronous AP discharge, which accounts for a considerable amount of BSL activity. NEW & NOTEWORTHY Historically, sympathetic nerve activity destined for the blood vessels supplying skeletal muscle (MSNA) has been characterized by spontaneous bursts formed by synchronous action potential (AP) discharge. However, this study found a considerable amount (~30% during baseline) of sympathetic AP discharge to fire asynchronously between bursts of human MSNA. Trimethaphan infusion revealed that nonnicotinic ganglionic mechanisms contribute to some, but not all, asynchronous discharge. Asynchronous sympathetic AP discharge represents a fundamental behavior of MSNA.
AB - What strategies are employed by the sympathetic system to communicate with the circulation? Muscle sympathetic nerve activity (MSNA) occurs in bursts of synchronous action potential (AP) discharge, yet whether between-burst asynchronous AP firing exists remains unknown. Using multiunit microneurography and a continuous wavelet transform to isolate APs, we studied AP synchronicity within human MSNA. Asynchronous APs were defined as those which occurred between bursts. Experiment 1 quantified AP synchronicity in eight individuals at baseline (BSL), -10 mmHg lower body negative pressure (LBNP), -40 mmHg LBNP, and end-expiratory apnea (APN). At BSL, 33 ± 12% of total AP activity was asynchronous. Asynchronous discharge was unchanged from BSL (67 ± 37 AP/min) to -10 mmHg LBNP (69 ± 33 AP/min), -40 mmHg LBNP (83 ± 68 AP/min), or APN (62 ± 39 AP/min). Across all conditions, asynchronous AP probability and frequency decreased with increasing AP size. Experiment 2 examined the impact of the ganglia on AP synchronicity by using nicotinic blockade (trimethaphan). The largest asynchronous APs were derecruited from BSL (11 ± 4 asynchronous AP clusters) to the last minute of the trimethaphan infusion with visible bursts (7 ± 2 asynchronous AP clusters). However, the 6 ± 2 smallest asynchronous AP clusters could not be blocked by trimethaphan and persisted to fire 100 ± 0% asynchronously without forming bursts. Nonnicotinic ganglionic mechanisms affect some, but not all, asynchronous activity. The fundamental behavior of human MSNA contains between- burst asynchronous AP discharge, which accounts for a considerable amount of BSL activity. NEW & NOTEWORTHY Historically, sympathetic nerve activity destined for the blood vessels supplying skeletal muscle (MSNA) has been characterized by spontaneous bursts formed by synchronous action potential (AP) discharge. However, this study found a considerable amount (~30% during baseline) of sympathetic AP discharge to fire asynchronously between bursts of human MSNA. Trimethaphan infusion revealed that nonnicotinic ganglionic mechanisms contribute to some, but not all, asynchronous discharge. Asynchronous sympathetic AP discharge represents a fundamental behavior of MSNA.
KW - Action potential
KW - Asynchronous discharge
KW - Microneurography
KW - Muscle sympathetic nerve activity
KW - Paravertebral ganglia
KW - Sympathetic nervous system
KW - Sympathetic neural recruitment
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U2 - 10.1152/ajpheart.00258.2019
DO - 10.1152/ajpheart.00258.2019
M3 - Article
C2 - 31373511
AN - SCOPUS:85072849343
SN - 0363-6135
VL - 317
SP - H754-H764
JO - American Journal of Physiology
JF - American Journal of Physiology
IS - 4
ER -