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Autonomic Nervous System Responses Relation to Ventilatory Threshold* Yoshiharu Yoshio Yamanwto, PhD; Richard Nakamura, L. Hughson, Ph.D.; our recent approach to study control of heart rate during means rate ofheart reference (Tvent). The nervous rationale with nomic (HRV) for the (cardiac) system gether variability study was that parasympathetic (PNS the and SNS, underlying analysis to ventilatory markedly reduced HRV respectively) sympathoadrenal and epinephrine enhanced above rine was and SNS the low-dimensional less complex Tvent, that indicators concentrations Tvent, and that indicators were autonomic considered activity. respect with with dynamics DF) to- These appearance that might findings to implication in uring incremental exercise, (VE) begins oxygen uptake to the increase (o) or minute nonlinearly noninvasive using onset on bicarbonate abrupt blood Since these on the specific work lactacidosis buffering early rate (WR) acidosis, evidence has stimulus.12 was However, both such is, dioxide an increase not always in accom- compromise methodologically speaking, parameters it of relating by what question to is called arises; authorsl2 should only may and they be said have physio- response to “V-slope” method.’ exercise, not Then all ofthe reinterpret most performed VE these were not to this question regarded that been the we responded that can AT that AT determined for the subjects was at rose by pattern of counterevidences Dempsey were et provided. develop lactacidemia during The clinically examined given by the by these by VE responses whose ventilatory could be control “appropriately.” However, consid- the responses as such appropriate Tvent,3’4 that responses during subse- an alteration in concomitant could change included recently these factors in heavy forced concept the 2 more was the because original to modify despite of of authors the Dempsey could not marked acidemia. of the anaerobic significance the Department of Kinesiology, University Ontario, Canada (Drs. Yamamoto and of Sports Science, Waseda University, Japan (Dr. Nakamura). of Tvent of shown to intensity. catecholamines,” of potassium.’5 recent review and All of of Cunningham we introduce our recent system control during rate variability spectral (HRV; respiratory As the controller with was directly, the delineate the detailed for Tvent. However, implication has been of the discussed last they ty.’7 not for results for on beat- reference to its investigating ofthese physiologic there was results in the intervals special method and approachesl321 to exercise by means heartbeat analysis to Tvent. HRV Waterloo, Hughson), and Tokorozawa, PARAMETERS TO studies mechanisms at least one clinical cardiology. section. EVALUATE CONTROL The analysis. 2 or more at frequency of are coherent with nervous that might system Nervous System with time series spectral human HRV spectra have harmonic components.” solely system usually blood AUTONOMIC HEART mediated nervous components demonstrated <0. 15 Hz Autonomic major >0. 15 Hz, parasympathetic other OF study of HRV has evolved In the frequency domain, displayed are Waterloo, Department Saitama, in the were to high of in to a lack of hyperventilation than lactacidosis at a moderate temperature, concentration listed basis) could not responsible This a Tvent inability On the contrary, trained athletes body arterial article, nervous of heart the direct report demonstrated despite their exercise the al, other exercise are relationship in LA onset et al18 to modulate feedback control of ventilation, are thought to be related to the sympathoadrenal to-beat blood change both These more the for is necessary. Several factors affect YE during In this autonomic lactate failed exercise the enzyme, myophosphorylase. et al’ reported that highly (AT) to exercise One et al’#{176} in which they with McArdle’s disease evidence blood before that Hagberg patients This leading responsible per se at Tvent potential Tvent.8 the review threshold doubt cast strenuous status could not induce the and that epinephrine infusion hyperventilate of ofTvent. that significantly exercise,56 moderate dysoxia, occurrence preliminary to activation have observations of ventilatory incremental acid-base Tvent,7 a resultant cellular in the mechanisms respect threshold (Tvent). to be due to the studies that the (LA) the many resulted induced to alter quent reports, included concentration lactacidosis and the system.’2 hypothesisl2 metabolic 206S in carbon with Tvent determinations necessarily ering ventilation with exercise intensity, namely the ventilatory This al)rupt increase in VE was considered *From That increase commensurate while problems mechanisms been cardiol- an that YE tracked the increase in Vco2, this is circular logic. To answer this question, therefore, a study on the physiologic D In by this validated ogy. and always presented results because latter method? The answer of have was exchange that to lactacidosis definite the reflect for clinical (Vco,) due to gas Methodologically (DF) of HRV that PNS was the more emphasized logically. auto- of change norepineph- incline panied and SNS indicator) these changes in PNS associated (low recently raise activity, the rate (plasma to they H has been of cerebral and output and sympathetic complexity below activity with threshold system in terms of fractal dimension series. The experimental results showed time and autonomic exercise by spectral to its relationship to reflect shown in Ph.D. We introduce nervous system special to Exercise seen pressure (PNS) at or and Response PNS to Exercise Downloaded From: http://journal.publications.chestnet.org/pdfaccess.ashx?url=/data/journals/chest/21646/ on 05/07/2017 at both The 0. 1 Hz It is levels activity.”” below variability.” the latter components be associated with (SNS) One by changing has and been frequencies sympathetic activities.un (Yamamoto, Hug/non, Nakamura) There are taken in the components to indicate PNS of a nonharmonic and HRV SNS component band spectrom.’ This to be “fractal” in nature signal and can developed graining that monic permits simultaneous components well related as computation The Yamamoto the to and fact that power after whereas, the was used the original and shown the components, nonharmonic (fractal) subtracted Sxx’ form (Ph) and ratio HRV power with magnitude retains its of Eight plus tests the harmonic consideration nonharmonic has been is 13 component plane with of this repre- component. spectral was plotted plot. for the effect (j) vs log frequency slope of the From the value of 3, for 1 <33. For 3>3 1 and infinity (oo), respectively. value of DF or 3 can have the taken DF was and The in spec- meanings. The brain oscillators complex and the dynamics.” reflection ofthe DF number dimensionality correlation consists interactions vs log power work regression was is thought ofthese of human dimension to cerebral (the be lower encephalographic be 8 to -0o in the (EEG) awake, recording, eye-opened, high-dimensional system is also physical evaluated of DF) by “information epileptic As to the implication the producing agent activity that toward the correlation had of this finding, the a stable seizure periodic test to A rich:’ stimuli that cen- dimension a low mean they tended motion. value drive In of of 2.05. speculated to the such PNS to decrease subjects intensity dra- exercised. reached was it increased autonomic detail,” more by observing that male on an 60% statistically significantly nervous system by adopting catecholamines volunteers a ramp and performed electrically of a 5-mm braked warm-up in a ramp analyzed for DF (3) fashion incremental cycle ergometer, 50 W, followed exhaustion. The period for was HRV epinephrine Overall in Figures et al,” rate was Arterialized from an indwelling heated plasma of change so small dorsum in LA during that Tco, of the intensity. Such expected for 1) pressures states, “isocapnic a reduction these buffering” CHEST the very 1). Thus, is I 101 showed clear at in PE’rCO2 an ramps anomaly I 5 I MAY, Downloaded From: http://journal.publications.chestnet.org/pdfaccess.ashx?url=/data/journals/chest/21646/ on 05/07/2017 1992 for and very slow ramp linearly in the determination (Tvent) slow hand are shown Wasserman almost method’s was impossible profile of end-tidal 0, hyperventilation brain venous catheter (NE), increased (Fig The particularly norepinephrine intensity ofY-slope the Fig of of data. periods response analysis. 5 mm on the LA, to exercise ( PE’ICO,, rate slow ramp responses (E) concentrations. responses of the physiologic variables 1 through 3. As was suggested by was Nevertheless, onset of the relation every vein analyses 10-mm heart spectral sampled in a superficial the of by rate at until successive nature important blood in the first report for the dynamics in the field of human seizure data, of increase in WR was 2.0 Wmin’. This very protocol allowed us to observe quasi-steady-state ofTvent demonstrated and increment Babloyantz and Destexhe, existence oflow dimensional during these for 6 healthy Briefly, exercise EEG and exchange, HRV contrary, while studied exercise protocol ters,” it is not surprising to see high DF (3 close to unity) in the resting human HRV#{176}” with high level ofPNS activity.’#{176} physiology, gas the the the on the initial WRs of 20 predetermined indicator when Tvent, for the ofthe From until indicator, recently steady-state reported state.’ and this makes redundant processing of external possible. Considering the fact that there are projections could transmit the cerebral activity to the autonomic to decrease to of HRV of an electro- has been but quiet called very For example, activity, limit the 110% PNS exercise position. constant alveolar rest to to Tvent. sitting increased continuously. were calculated. up to 100% exercise WR physiologic oscillators.”’ was and the the it reached profile, responses relative submaximal in WR with HRV set 17-mm until showed SNS the Tvent. consisting of (nonlinear) VENTILATORY intensity 100%, compared We have as DF generate of the responses. calculated them aging,3’ instability observed tests, 90%, results 110% responses among various susceptibil- challenges,’#{176}’ AND six ventilatory The plots of a number centers. in including measurement fashion 60%, unchanged at we completed It continued fractal following one way, we have SNS responses autonomic electrical with resting while matically as The Tvent the 031, study,’ exercise in a ramp power linear and submaximal mm total HRV by orthostatic HRV were measured and SNS indicators characteristics, Therefore, in a log as the in the reflex albeit observed situations, induced one W, or 30%, in of change power-law frequency 3 (P/Ph), by been stress,’8 subjects and Tvent. component exponent.a 3 estimated power normalized to have in log ft frequency was also RESPONSE load During we arrhythmia. (fractal) the DF=2J(3-1) the sinus reported by expressed where to high of the state has pathologic In an earlier constant time Thus, attractor, THRESHOLD grained) Sxx’ and DF AUTONOMIC spectra 18 recovery process In an analogous increase ofdefensive the in syncope heart.”'” harmonic whereas, indicator of respiratory The trum as of low PNS respectively.182 to and to on a chaotic of a functional physiologic ity remains that impossible However, challenges#{176} and exercise” was associated with close to 2.0 (13-- 1 .0), suggesting that DF of HRV reduction on From the harmonic component, the integrated power 0.0 to 0. 15 Hz (P,) and 0. 15 to 1.0 Hz (Ph) was calculated. PNS and SNS activities were evaluated by high frequency power indicative The based spectra represent Sxx to obtain of HRV psychologic cross-power (coarse to DF was by was brain shown its rescaled version, does not. A standard and rescaled as detailed auto-power (Sxx) Sxx was (fractal) (Sxx’). nonharmonic been component with to estimate series activities,’8 the method Briefly, har- components.2#{176} has nonharmonic time SNS nonharmonic method “ fractal HRV series sented this of the recently be diffIcult. low to orthostatic analysis would extremely the of very by spectral processing be activities, sense is indicative We have recently and it is cross-correlated the harmonic component original between use Hughson. method FFT the of DF from rationale broad- suggested evaluation to PNS information would be characterized in some series.” coarse those consists its has been the fractal dimension (DF) which of the complexity of a given time (CGSA), also by noise , ‘‘#{176} than HRV characterized broad-band a technique, other activities. for all subjects. and CO, (PE’rO,) evidence moderate at Tvent because of the I Supplement of the exercise is to be so-called specific 15 2075 (mmol’ (L- mm) 80 L’) 6i C 0 a) 60 0 C C) (L’ mm’) 2.0 40 > (ngmL’) a 2 -I 20 0 c%J 0 --1’ - 0 C 0 I.. a 0 - 0 1.0 1C a (Torr) C,l z0 (ng-mL1) 0.2 0 .40 w -40 0 -20 delta Work FIGURE 1. VE, VCo2, Wmin’) ramp exercise. 20 Rate from T and PErCO, responses All variables shown - 40 a. (W) during w very in Figures slow (2.0 1 through 0 3 delta exercise. protocol. In Figures been shown to the Tvent as ensemble determined The statistical above Tvent comparison showed that 1 through 3, all variables averages for 6 subjects by the PETO, and PEiCO, of regression only PEi’CO, systematically at Tvent. Figure 2 shows the responses as intensity and Tvent. and E. Each of increase increase in the recent study of Mazzeo and Marshall.” the recent study of Savard et al” suggested that creases progressively The 3. study,” low gradually values over it increased the slopes. reached 2.04 higher was of Tvent, below with (lower for the orthostatic component of heart SNS indicator greater had our recent C/) z in- 0 Tvent, to the graded the fractal less 21- 3 with finding dimensional, w for at Tvent that a change A similar responses 3r C C) C 0 increased value of 1.92) C) a Cl) -40 delta nervous 2085 summary, system responses results during concerning exercise autonomic in 0 -20 20 40 complex dynamics. In 0 40. reaching than mean indicating low I 80 earlier (p<0.05) thereafter. stress,” HRV the rate ramp i!1 (0I z summarized At WR to DF DF) slow Cl) of our a significant (corresponding values are results increased, interestingly, very was muscles as WR The Tvent. steeply More obtained levels at more the during intensity. variables with decreased WR leg exercise of HRV-related indicator concentrations exercising greater In agreement PNS very the with responses in Figure in from responses See text for abbreviations. . suggested of catecholamines E (W) A threshold-like of the However, and 40 T in in response effiux catecholamine NE, 20 Rate from 0.1 1 changed with an greater LA, 0 Work profiles. below Figure NE, gradually apparently exceeded blood in have in relation slopes of LA, LA, NE, and E increased exercise intensity, with an concentration 2. FIGURE text for abbreviations. Wmin’ -20 -40 are ensemble averages for 6 subjects in relation to ventilatory threshold (Tvent) determined by the PETO, and PEi’CO, profiles, and plotted against work rate (WR) relative to WR at Tvent. See relation Work Rate from T to (W) 3. PNS indicator, SNS indicator, and the spectral (13)responses during very slow ramp exercise. FIGURE Autonomic Nervous System Response to Exercise Downloaded From: http://journal.publications.chestnet.org/pdfaccess.ashx?url=/data/journals/chest/21646/ on 05/07/2017 (Yamamoto, exponent Hughson, Nakamura) Tvent showed Tvent, that indicators in that the PNS rate withdrew was enhanced PNS and appearance less Tvent, indicators the and were below autonomic increases anesthetized activity that these changes associated low-dimensional complex completely in sympathoadrenal above SNS of reflect almost of changes with dynamics the the that might ered the to be mechanisms important methodologically. results for ventilatory context, Proper of the the system these and the peripheral beyond the could have by showing that cardiac performance” has been via demia due et several the by their mechanisms impaired originally to decreased oxygen that well-trained could as matched trained runners despite the maximal cardiac output of the patients. show oxidative indicators lactacidemia might Neither such if one and merely Tvent, reflect affects of the reduced skeletal examined the lower to indicate the relationship Tvent physical increase anterior susceptible during the vagotomy arrvthmia using kins,’ HRV or Electrical to increase atropine formation.42 spectral exercise has Recently, analysis had the of HRV dogs and with the other hand, sympathetic neural could threshold, indicators to than activity also and provided that that a protec- DF (3) of HRV above the to increased between system moderate Tvent exercise risk of cardiac the change in cardiac status and a possible cardiac exercise remains to be inves- experimentally Whipp study BJ, respiratory in future was Koyal blood gas lactate, and J Appl Physiol research. supported in part by SN, Beaver RL. muscle Methodologies WL. 1984; GC. during Anaerobic exercise. metabolites in progressive for measurement Physiologist Gass exchange 1983; 54:1032-38 5 Davis HA, before and during The SW, Ivy JL. Lactate anaerobic lactic of the anaerobic 27:304-11 acidosis. threshold as determined J Appl Physiol 1981; Eur 47: 141-49 6 Farrell during exercise. acidosis J Appl Heigenhauser GJF, incremental 7 Kowalchuk per the dogs occlusion approximating complexity, lead and a Holter correlation to 1 .0 (to 3.0) of their J Appl Physiol 1973; 35:236-43 2 Wasserman K, Whipp BJ, Koyal SN, Cleary MG. Effect of carotid body resection on ventilatory and acid-base control during exercise, J AppI Physiol 1975; 39:354-58 3 Green HJ, Hughson RL, Orr GW, Ranney DA. Anaerobic exercise. Hos- dimension generator This K, and 8 Scheen healed to of HRV patient wearing They stated the loss as wellas 1 Wasserman JM, and metabolic shown published arrhythmogenesis relationship clinically threshold. resistant. On nervous during 4 Hughson of spontaischemia,’ been PNS autonomic vulnerability exercise. stimulation ventricular reported that by a coronary lower as innervattone Biliman in nor to recently Considering Tvent The patients cardiac function. the spectral analysis myocardial infarctions, to ventricular fibrillation submaximal a are and due susceptibility dimensionality gradually indicating above between in cardiac to REFERENCES intracellular inactivity ofthe heart. been shown heartbeat (increased) threshold ratio, the activity of cardiac autonomic nerves sinoatrial node.” The cardiac parasympathetic bilateral as efilux, pyruvate can in the and muscle in lactate lactate et al,” their electrical stability vagus nerves has age- redox potential concentrations changes as of lethal observation fibrillation threshold and decrease the incidence neous ventricular fibrillation during myocardial while graded to Vo2max This muscle enzyme disease per se, not the impaired It should be emphasized that evaluated ing the during capacity of the effiux and of muscle Wasserman Thus, dysoxia.#{176} responses disease LA response during exercise.” by Connett et aF’#{176} has convincingly review availability. by endurance of in suggested LA similar capacity shown that lactate interactive functions redox similar as shown In our results, of SNS with grants from the Ministry ofEducation, Japan (02951196), from Meiji Life Foundation of Health and Welfare, Japan, and from the Natural Sciences and Engineering Research Council ofCanada. The authors are grateful to Isao Muraoka, Professor of Waseda University, and Minort, Shinohara, M.Sc. , at University ofTokyo for their help in conducting part of the experiments in this study. Coyle heart been increase to an integer arrythmogenesis. study, has The extrasystole PNS almost completely. that changes in cardiac al” onset ACKNOWLEDGMENT: lactaci- Indeed, ischemic et on the in a cardiac time ofhis death. vulnerability. tigated performie, transport.’” exercise substrate lower clas- effect might Skinner process our 60%. for In instability. decreased intensity concept cardiac proposed, patients determinant the recent in about PNS activity.e the enhancement at Tvent to the from this by observations decreased had the lower Tvent. 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Lipsitz Furey SA autonomic extrasystole III, Levy activity, MN. and threshold The interactions arterial in the and ventricular dog. among fibrillation. heart rate, pressure Am upon the multiple Heart J 1983; 106:1112- 20 AUtOnOmiC Nervous System Response to Exercise Downloaded From: http://journal.publications.chestnet.org/pdfaccess.ashx?url=/data/journals/chest/21646/ on 05/07/2017 (Yamamoto, Hughson, Nakamura)