Advertisement

Recruitment pattern of sympathetic neurons during breath-holding at different lung volumes in apnea divers and controls

      Abstract

      We tested the hypothesis that breath-hold divers (BHD) attain higher level of sympathetic activation than controls due to the duration of breath-hold rather than a different recruitment strategy. In 6 control subjects and 8 BHD we measured muscle sympathetic neural activity (MSNA) prior to and during functional residual capacity (FRC) and total lung capacity (TLC) breath-holding. On a subset of subjects we applied a new technique for the detection of action potentials (APs) in multiunit MSNA. Compared with controls, BHD group had lower burst AP content (13±7 vs. 6±3 AP/burst; P=0.05) and number of active clusters (5±1 vs. 3±1 clusters/burst; P=0.05) at baseline. However, the overall sympathetic AP/unit-time was comparable between the groups (131±105 vs. 173±152 AP/min; P=0.62) due to increased burst frequency in BHD group (20±4 bursts/min) vs. controls (13±3 bursts/min) (P=0.039). The achieved level in total MSNA during FRC breath-holds was higher in divers (2298±780 vs. 1484±575 a.u./min; P=0.039). Total MSNA at the end of TLC breath-hold was comparable between the groups (157±50 (controls) vs. 214±41 s (BHD); P=0.61). FRC and TLC breath-holds increased AP frequency, burst AP content and active clusters/bursts in both groups but the response magnitude was determined by the type of the breath-hold. The divers used fewer number of APs/burst and active clusters/burst. In both groups breath-holds resulted in similar increases in MSNA which were reached both by an increase in firing frequency and by recruitment of previously silent, larger (faster conducting) sympathetic neurons, and possibly by repeated firing within the same burst.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Autonomic Neuroscience: Basic and Clinical
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Bakovic D.
        • Valic Z.
        • Eterovic D.
        • Vukovic I.
        • Obad A.
        • Marinovic-Terzic I.
        • Dujic Z.
        Spleen volume and blood flow response to repeated breath-hold apneas.
        J. Appl. Physiol. 2003; 95: 1460-1466
        • Barwood M.J.
        • Datta A.K.
        • Thelwell R.C.
        • Tipton M.J.
        Breath-hold time during cold water immersion: effects of habituation with psychological training.
        Aviat. Space Environ. Med. 2007; 78: 1029-1034
        • Breskovic T.
        • Ivancev V.
        • Banic I.
        • Jordan J.
        • Dujic Z.
        Peripheral chemoreflex sensitivity and sympathetic nerve activity are normal in apnea divers during training season.
        Auton. Neurosci. 2010; 154: 42-47
        • Breskovic T.
        • Valic Z.
        • Lipp A.
        • Heusser K.
        • Ivancev V.
        • Tank J.
        • Dzamonja G.
        • Jordan J.
        • Shoemaker J.K.
        • Eterovic D.
        • Dujic Z.
        Peripheral chemoreflex regulation of sympathetic vasomotor tone in apnea divers.
        Clin. Auton. Res. 2010; 20: 57-63
        • Delius W.
        • Hagbarth K.E.
        • Hongell A.
        • Wallin B.G.
        Manoeuvres affecting sympathetic outflow in human muscle nerves.
        Acta Physiol. Scand. 1972; 84: 82-94
        • Dujic Z.
        • Ivancev V.
        • Heusser K.
        • Dzamonja G.
        • Palada I.
        • Valic Z.
        • Tank J.
        • Obad A.
        • Bakovic D.
        • Diedrich A.
        • Joyner M.J.
        • Jordan J.
        Central chemoreflex sensitivity and sympathetic neural outflow in elite breath-hold divers.
        J. Appl. Physiol. 2008; 104: 205-211
        • Elam M.
        • Sverrisdottir Y.B.
        • Rundqvist B.
        • McKenzie D.
        • Wallin B.G.
        • Macefield V.G.
        Pathological sympathoexcitation: how is it achieved?.
        Acta Physiol. Scand. 2003; 177: 405-411
        • Ferrigno M.
        • Hickey D.D.
        • Liner M.H.
        • Lundgren C.E.
        Cardiac performance in humans during breath holding.
        J. Appl. Physiol. 1986; 60: 1871-1877
        • Hagbarth K.E.
        • Vallbo A.B.
        Pulse and respiratory grouping of sympathetic impulses in human muscle-nerves.
        Acta Physiol. Scand. 1968; 74: 96-108
        • Henneman E.
        • Somjen G.
        • Carpenter D.O.
        Functional significance of cell size in spinal motoneurons.
        J. Neurophysiol. 1965; 28: 560-580
        • Hentsch U.
        • Ulmer H.V.
        Trainability of underwater breath-holding time.
        Int. J. Sports Med. 1984; 5: 343-347
        • Heusser K.
        • Dzamonja G.
        • Tank J.
        • Palada I.
        • Valic Z.
        • Bakovic D.
        • Obad A.
        • Ivancev V.
        • Breskovic T.
        • Diedrich A.
        • Joyner M.J.
        • Luft F.C.
        • Jordan J.
        • Dujic Z.
        Cardiovascular regulation during apnea in elite divers.
        Hypertension. 2009; 53: 719-724
        • Jellema W.T.
        • Imholz B.P.
        • Oosting H.
        • Wesseling K.H.
        • van Lieshout J.J.
        Estimation of beat-to-beat changes in stroke volume from arterial pressure: a comparison of two pressure wave analysis techniques during head-up tilt testing in young, healthy men.
        Clin. Auton. Res. 1999; 9: 185-192
        • Kelman G.R.
        • Wann K.T.
        Mechanical and chemical control of breath holding.
        Q. J. Exp. Physiol. Cogn. Med. Sci. 1971; 56: 92-100
        • Lindholm P.
        • Lundgren C.E.
        Alveolar gas composition before and after maximal breath-holds in competitive divers.
        Undersea Hyperb. Med. 2006; 33: 463-467
        • Macefield V.G.
        • Wallin B.G.
        Effects of static lung inflation on sympathetic activity in human muscle nerves at rest and during asphyxia.
        J. Auton. Nerv. Syst. 1995; 53: 148-156
        • Macefield V.G.
        • Wallin B.G.
        Firing properties of single vasoconstrictor neurones in human subjects with high levels of muscle sympathetic activity.
        J. Physiol. 1999; 516: 293-301
        • Macefield V.G.
        • Wallin B.G.
        • Vallbo A.B.
        The discharge behaviour of single vasoconstrictor motoneurones in human muscle nerves.
        J. Physiol. 1994; 481: 799-809
        • Morgan B.J.
        • Denahan T.
        • Ebert T.J.
        Neurocirculatory consequences of negative intrathoracic pressure vs. asphyxia during voluntary apnea.
        J. Appl. Physiol. 1993; 74: 2969-2975
        • Narkiewicz K.
        • van de Borne P.J.
        • Pesek C.A.
        • Dyken M.E.
        • Montano N.
        • Somers V.K.
        Selective potentiation of peripheral chemoreflex sensitivity in obstructive sleep apnea.
        Circulation. 1999; 99: 1183-1189
        • Overgaard K.
        • Friis S.
        • Pedersen R.B.
        • Lykkeboe G.
        Influence of lung volume, glossopharyngeal inhalation and P(ET) O2 and P(ET) CO2 on apnea performance in trained breath-hold divers.
        Eur. J. Appl. Physiol. 2006; 97: 158-164
        • Palada I.
        • Obad A.
        • Bakovic D.
        • Valic Z.
        • Ivancev V.
        • Dujic Z.
        Cerebral and peripheral hemodynamics and oxygenation during maximal dry breath-holds.
        Respir. Physiol. Neurobiol. 2007; 157: 374-381
        • Parkes M.J.
        Breath-holding and its breakpoint.
        Exp. Physiol. 2006; 91: 1-15
        • Salmanpour A.
        • Brown L.J.
        • Shoemaker J.K.
        Spike detection in human muscle sympathetic nerve activity using a matched wavelet approach.
        J. Neurosci. Methods. 2010; 193: 343-355
        • Salmanpour A.
        • Brown L.J.
        • Steinback C.D.
        • Usselman C.W.
        • Goswami R.
        • Shoemaker J.K.
        Relationship between size and latency of action potentials in human muscle sympathetic nerve activity.
        J. Neurophysiol. 2011; 105: 2830-2842
        • Somers V.K.
        • Mark A.L.
        • Zavala D.C.
        • Abboud F.M.
        Contrasting effects of hypoxia and hypercapnia on ventilation and sympathetic activity in humans.
        J. Appl. Physiol. 1989; 67: 2101-2106
        • Steinback C.D.
        • Breskovic T.
        • Banic I.
        • Dujic Z.
        • Shoemaker J.K.
        Autonomic and cardiovascular responses to chemoreflex stress in apnoea divers.
        Auton. Neurosci. 2010; 156: 138-143
        • Steinback C.D.
        • Salmanpour A.
        • Breskovic T.
        • Dujic Z.
        • Shoemaker J.K.
        Sympathetic neural activation: an ordered affair.
        J. Physiol. 2010; 588: 4825-4836