Ventilatory response to exercise does not evidence electroencephalographical respiratory-related activation of the cortical premotor circuitry in healthy humans

Ventilatory response to exercise does not evidence

electroencephalographical respiratory-related activation of

the cortical premotor circuitry in healthy humans

L. Jutand,1,2 L. Tremoureux,2 A. Pichon,3 N. Delpech,1 A. Denjean,4 M. Raux,2,5

C. Straus2,6,† and T. Similowski7†

1 Universite de Poitiers, Laboratoire des Adaptations Physiologiques aux Activites Physiques, Faculte des Sciences du Sport, UPRES

EA 3813, 4 Allee Jean Monnet, 86000, Poitiers, France

2 UPMC Univ Paris 6, ER10 UPMC, 75013, Paris, France

3 Universite Paris 13, UFR SMBH, STAPS, UPRES EA 2363, Laboratoire Reponses Cellulaires et Fonctionnelles a l’Hypoxie, 74 rue

Marcel Cachin, 93017, Bobigny, France

4 Assistance Publique – Hopitaux de Paris, Hopital Robert Debre, Service de physiologie, Explorations Fonctionnelles, 75019, Paris,

France

5 Assistance Publique – Hopitaux de Paris, Groupe Hospitalier Pitie-Salpetriere, Departement d’Anesthesie-Reanimation, 75013,

Paris, France

6 Assistance Publique – Hopitaux de Paris, Groupe Hospitalier Pitie-Salpetriere, Service Central d’Explorations Fonctionnelles Respi-

ratoires, 75013, Paris, France

7 Assistance Publique – Hopitaux de Paris, Groupe Hospitalier Pitie-Salpetriere, Service de Pneumologie et Reanimation, 75013,

Paris, France.

Received 18 August 2011,

revision requested 10 October

2011,

revision received 9 February

2012,

accepted 12 February 2012

Correspondence: Dr Christian

Straus, Service Central d’Explora-

tions Fonctionnelles Respiratoires,

Groupe Hospitalier Pitie-Salpetri-

ere, 47-83 Bd de l’Hopital, 75651

Paris Cedex 13, France.

E-mail: [email protected]

†Both last authors.

Abstract

Aim: The neural structures responsible for the coupling between ventila-

tory control and pulmonary gas exchange during exercise have not been

fully identified. Suprapontine mechanisms have been hypothesized but not

formally evidenced. Because the involvement of a premotor circuitry in the

compensation of inspiratory mechanical loads has recently been described,

we looked for its implication in exercise-induced hyperpnea.Methods: Electroencephalographical recordings were performed to iden-

tify inspiratory premotor potentials (iPPM) in eight physically fit normal

men during cycling at 40 and 70% of their maximal oxygen consumption

( _VO2max). Relaxed pedalling (0 W) and voluntary sniff manoeuvres were

used as negative and positive controls respectively.Results: Voluntary sniffs were consistently associated with iPPMs. This

was also the case with voluntarily augmented breathing at rest (in three

subjects tested). During the exercise protocol, no respiratory-related

activity was observed whilst performing bouts of relaxed pedalling. Exer-

cise-induced hyperpnea was also not associated with iPPMs, except in one

subject.Conclusion: We conclude that if there are cortical mechanisms involved

in the ventilatory adaptation to exercise in physically fit humans, they are

distinct from the premotor mechanisms activated by inspiratory load com-

pensation.

Keywords cerebral cortex, control of breathing, exercise, humans.

© 2012 The AuthorsActa Physiologica © 2012 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2012.02427.x356

Acta Physiol 2012, 205, 356–362

Mammalian breathing depends on brainstem neurons

that produce the ventilatory rhythm and adjust venti-

lation to meet metabolic demands. In humans, partic-

ularly powerful suprapontine commands can disrupt

metabolic ventilation, for example during speech.

Motor cortical structures engage during volitional

breathing (Macefield & Gandevia 1991, Smejkal et al.

2000) and during certain types of inspiratory load

compensation (Raux et al. 2007a). Whether or not

they are involved in the control of breathing during

exercise is not known.

During physical exercise, ventilation must adapt to

sequential changes in the interior milieu. Early on,

exercise increases the production of carbon dioxide

(CO2): in response, ventilation augments to regulate

the arterial partial pressure of CO2. When exercise

intensifies and the lactate threshold is crossed, meta-

bolic acidosis sets in, requiring additional ventilatory

compensation. A constant work rate exercise results

in an immediate increase in ventilation that rises

exponentially until an isocapnic steady state is

reached (Whipp & Ward 1998). Recent experiments

have identified a subset of neurons within the

mesencephalic locomotor region that sends direct

inputs to neurons in the respiratory generator (Gari-

epy et al. 2012) and thus seems intimately involved in

the coupling between respiration and locomotion

(Gariepy et al. 2012). However, the neural mecha-

nisms responsible for the coupling between ventilatory

control and pulmonary gas exchange during exercise

have not been fully identified (review in Haouzi

2006). This coupling is bound to be complex, insofar

as exercise proceeds from voluntary commands acti-

vating automatic programs. Krogh and Lindhard

(1913) suggested early on that exercise-related hyper-

ventilation can depend on cortical structures, at least

in the early stages of effort. A cortical mechanism has

also been proposed to account for the increase in ven-

tilation that occurs during anticipation of exercise

and at its very onset (Tobin et al. 1986), where venti-

lation exceeds the actual exercise-related ventilatory

demand. Cerebral imaging studies have lent support

to this concept. For example, Fink et al. (1995)

observed increases in regional blood flow during exer-

cise in areas associated with volitional breathing.

During imagined exercise, Thornton et al. (2001) also

described activation in areas of the brain that relate

to voluntary breathing during imagined exercise under

hypnosis. Yet, contradictory to these elements that

support the role of a cortical input to the ventilatory

response to exercise, it has been shown that during

sinusoidal work, the ventilatory response to exercise

is dynamically linked to metabolism through carbon

dioxide production (Casaburi et al. 1977, 1978,

Haouzi et al. 1992). This suggests that the rate at

which CO2 leaves the tissues and is exchanged at the

lungs during exercise is a major determinant of exer-

cise-related hyperpnea (Haouzi et al. 2004) and that,

in contrast, cortical commands play a minor role. In

line with this, in a patient suffering from an Arnold

Chiari malformation who completely lacked a ventila-

tory response to carbon dioxide, Haouzi et al. (2000)

observed that the ventilatory response to exercise was

profoundly abnormal inspite of an apparently normal

voluntary control of breathing. Although this observa-

tion contrasted with the persistence of a ventilatory

response to aerobic exercise observed in patients with

Ondine’s curse also lacking chemosensitivity (Shea

et al. 1993), Haouzi et al. (2000) concluded that the

corticospinal respiratory pathway did not play a

major role in exercise-related ventilatory adaptation.

This case report indicates that cortical mechanisms

may not be mandatory for an appropriate ventilatory

response to exercise, but it is, however, not sufficient

to rule out cooperative mechanisms involving brain-

stem and suprapontine structures. Such cooperative

mechanisms probably account for the active compen-

sation of a mechanical, inspiratory load that occurs in

awake humans but not during sleep, as illustrated by

the presence of cortical respiratory-related premotor

potentials in such circumstances (Raux et al. 2007b,

Tremoureux et al. 2010).

We therefore set out to test the hypothesis that an

exercise-related activation of the cortical premotor

respiratory circuitry exists. To do so, we performed

inspiratory-triggered retro-averagings of the electroen-

cephalogram (Raux et al. 2007a,b) in a population of

physically active, normal volunteers during exercise.

Material and methods

Subjects

Eight physically active, male, healthy subjects (age

27 ± 5 years, _VO2max 55 ± 6 mL min�1 per kg, body

mass index 23 ± 6 kg m�2) were studied. They were

instructed to refrain from sedative intake and alcohol

consumption, to avoid sleep deprivation and to avoid

heavy exercise during the 24 h preceding the tests.

The study was approved by the appropriate ethical

committee, and all subjects gave their written,

informed consent.

Maximal oxygen consumption ( _VO2max)

_VO2max was measured in the subjects exercising on a

braked cycle ergometer (Ergoselect 100P; Ergoline,

Bitz, Germany). After a 5 min warm up at 90 W, the

load was increased by 25 W every minute until the

subject was unable to carry on despite vigorous

© 2012 The AuthorsActa Physiologica © 2012 Scandinavian Physiological Society, doi: 10.1111/j.1748-1716.2012.02427.x 357

Acta Physiol 2012, 205, 356–362 L. Jutand et al. · Cortical respiratory control during exercise

encouragement. The subjects breathed through a face-

mask (Hans Rudolph, Kansas City, MO, USA) con-

nected in series to a low-resistance pneumotachograph

(Sensormedics; VIASYS Healthcare, Palm Springs, CA,

USA). Inspiratory and expiratory gas was analysed,

breath by breath, using an automated system (Vmax

Encore; Viasys Healthcare, Palm Srings, CA, USA).

Three criteria were required to be met before accept-

ing the highest _VO2 recorded: (i) _VO2 stabilization

despite an increase in exercise intensity, (ii) respiratory

exchange ratio >1.1 and (iii) attainment of the age-

predicted maximal heart rate (220 – age).

Electroencephalographical recordings (EEG)

Electroencephalographical activity was recorded with

a sterile single-use subcutaneous needle electrode

inserted into the scalp at Cz (international 10–20 sys-

tem) (12 mm, diameter 0.35 mm, ref. MF3OE1S3512;

Comepa, Bagnolet, France) with two reference elec-

trodes on the mastoids. The impedance of the EEG

electrodes was regularly checked during the experi-

ments and remained between 2 and 5 kOhms. These

electrodes were connected to an EEG preamplifier

(2000-fold gain, band-pass frequency 0.05–500 Hz;

Electronique du Mazet, Le Mazet St Voy, France) out

of which the signals were fed to an analog–digital con-

verter and digitized at a sampling frequency of

2000 Hz (ML 780 PowerLab 8s, 16 bits resolution,

maximum range ± 10 V, recording range set on ±1 V;

Chart v5.2 software; AD Instruments, Castle Hill,

Australia) with a 1000-Hz low-frequency band-pass

anti-aliasing filter, then stored as computer files for sub-

sequent analysis (same as in Tremoureux et al. 2010).

Protocol

During all the experiments, the subjects watched a

movie on a computer screen placed at the centre of

their visual field, to deflect as much as possible their

attention from the physiological recordings. They

wore a facemask connected in series to a pneumotacho-

graph (MLT 1000 L, AD Instrument, dead space

350 mL, flow resistance 0.002 cm H2O L�1 s�1).

Mouth pressure was recorded with a linear differential

transducer (DP-45-18, ±2 cmH20; Validyne, North-

ridge, CA, USA) connected to the mask. End-tidal

CO2 partial pressure (PET, CO2) was measured from

another side port of the mouthpiece, using an infrared

CO2 gas analyser (IR1505; Servomex, Plaine Saint

Denis, France).

First, voluntary sniffs were performed. Then, the

exercise protocol began with a 15-min control run

during which the subjects breathed freely, seated on

the bicycle. They then exercised at an intensity corre-

sponding to 40% of their maximal oxygen uptake

( _VO2max) during 15 min. This was followed by a sec-

ond control run consisting of 15 min cycling at

0 Watts. The final part of the experiment included a

bout of cycling for 15 min at an intensity correspond-

ing to 70% _VO2max. No instruction was given to the

subjects regarding their pedalling rate, to avoid their

focusing on the experiment.

EEG processing

This was performed according to the method previ-

ously described (Raux et al. 2007a,b). In each of the

study conditions, 80 EEG epochs of 4-s duration

(from 2.5 s before to 1.5 s after the onset of mechani-

cal inspiration defined as the point of zero flow) were

created once a steady-state _VO2 had been reached.

Epochs exhibiting obvious artifacts were discarded,

and the rest was ensemble averaged. On the averaged

tracings, an inspiratory premotor activity was sought

in the form of a slow upward shift of the EEG signal

starting between 2 and 0.5 s before inspiration. When

this occurred, a first-order least-square regression

equation was fitted to the corresponding segment. A

premotor potential was considered present if and only

if the slope of this equation was positive and signifi-

cantly different from zero according to the F-test for

equality of variance. Motor potentials, defined as an

increase in negativity synchronous with the onset of

inspiration, were looked for in a similar manner.

Statistical analysis

This was conducted with the Prism 4 (GraphPad Soft-

ware Inc., La Jolla, CA, USA) and Excel (Microsoft

Corporation, Redmond, WA, USA) software. Data

distributions being consistently normal according to a

Shapiro–Wilk, the values are reported in terms of

mean ± SD. The effects of exercise on respiratory pat-

tern data were assessed using a one-way analysis of

variance with a post hoc Newman–Keuls test. The

proportions of the subjects exhibiting a premotor

activity in the various conditions were compared with

Fisher’s exact test. The results were considered signifi-

cant when the risk of a first type error was below 5%

(P < 0.05).

Additional experiments

The absence of respiratory-related premotor potentials

during exercise in our subjects (see Results below)

raised the issue of the sensitivity of the technique. To

address this, we conducted complementary experi-

ments using exactly the same recording technique and

signal processing method in three subjects who were


Cortical respiratory control during exercise · L. Jutand et al. Acta Physiol 2012, 205, 356–362

asked to voluntarily augment their breathing indepen-

dently of any exercise.

Results

Respiratory pattern

Exercise significantly increased minute ventilation,

breathing frequency, tidal volume and mouth pressure.

These increases were in proportion to exercise inten-

sity (Table 1). Inspiratory and expiratory times

decreased with the intensity of exercise (Table 1).

Premotor potentials

Typical inspiratory premotor potentials were present

during sniff manoeuvres (Fig. 1).

No EEG changes suggestive of respiratory-related

premotor activity were found during the two control

sessions in any of the subjects (Fig. 2). Except in one

subject, inspiratory premotor potentials were not iden-

tified during exercise, either at 40% _VO2max or at

70% _VO2max (Fig. 2).

The occurrence of inspiratory premotor potentials

during exercise was therefore not significantly more

frequent than during the relaxed, pedalling control

conditions (P = 0.23).

Voluntarily augmented breathing

In the three subjects tested, voluntarily augmented

breathing was associated with a clear upward depar-

ture of the Cz-EEG trace from baseline that occurred

circa 1.5 s before the start of inspiration and met all

the characteristics of a respiratory-related premotor

potential.

Discussion

In this study, healthy fit volunteers failed to exhibit

inspiratory premotor potentials during exercise-related

hyperpnea.

As in any instance of a negative result, the first

hypothesis to consider is an insufficient statistical

power, related to the small size of the study popula-

tion. However, in other experimental models involv-

ing inspiratory load compensation paradigms (Raux

et al. 2007a,b, Tremoureux et al. 2010), inspiratory

premotor potentials have been evidenced with a statis-

tically significant frequency in populations as small as

the present one. Therefore, we can reasonably con-

sider that exercise is a much less potent stimulus than

inspiratory mechanical loading to activate the respira-

tory premotor circuitry, if at all. Of note, we consis-

tently found premotor potentials during voluntary

sniff manoeuvres in our subjects, in agreement with

previous studies (Macefield & Gandevia 1991, Raux

et al. 2007b), which validates our methodology. We

also found premotor potentials before inspiration dur-

ing voluntarily augmented breathing at rest in the

three subjects who were tested in this manner. This

goes against our technique not being sensitive enough

to detect the signal if present during exercise.

One of our subjects did exhibit EEG evidence of a

respiratory-related premotor activity during exercise.

After the experiments, this subject reported that,

according to his habit, he had concentrated on breath-

ing in synchrony with his running rhythm. This proba-

bly explains why this subject deviated from the general

pattern, all the more so that he did not exhibit a pre-

motor potential during the control conditions. It is

tempting to relate this observation to the study per-

formed by Wuyam et al. (1995), during which it was

Table 1 Ventilatory pattern in the study population

Control‡ 40% _VO2max 70% _VO2max

Ventilation (L min�1) 13.8 ± 3.6 44.4 ± 5.1* 77.1 ± 10.5*†

Breathing frequency (cycle min�1) 14.4 ± 2.8 23.2 ± 2.0* 30.6 ± 3.6*†

Tidal volume (VT) (L) 0.94 ± 0.12 1.94 ± 0.25* 2.54 ± 0.36*†

Inspiratory time (TI) (s) 1.75 ± 0.31 1.18 ± 0.13* 0.92 ± 0.09*†

Expiratory time (s) 2.57 ± 0.99 1.30 ± 0.32* 1.03 ± 0.25*

TI/TT 0.39 ± 0.04 0.44 ± 0.02* 0.46 ± 0.02*

VT/TI 0.57 ± 0.15 1.67 ± 0.24* 2.76 ± 0.37*†

PETCO2 44.0 ± 4.3 48.0 ± 5.3 46.3 ± 5.2

Mouth pressure (cmH2O) �0.24 ± 0.07 �0.81 ± 0.22 �1.75 ± 0.49*

All values expressed as mean ± SD.

TT, breathing period.

*Significantly different from control.

†Significantly different from 40% _VO2max.

‡Average of the two control periods.



shown that imagination of exercise produced signifi-

cant alterations in cardioventilatory variables in ath-

letes, but not in untrained normal subjects. Of note,

the subjects who participated in our study were all fit

and physically active. This necessitates a word of cau-

tion regarding the general validity of our observations:

we cannot exclude the hypothesis that a control group

of sedentary subjects would have behaved differently.

Indeed, training can modify cortical processes both in

general and regarding respiratory muscle control

(Demoule et al. 2008). Comparing athletes and nonath-

letes in terms of their ventilatory response to exercise,

Wuyam et al. (1995) found that only trained individu-

als exhibited breathing pattern changes and hypocap-

nia when imagining efforts. The coupling between

breathing and pedalling, for instance, is also known to

occur differently in athletes vs. nonathletes (Kohl et al.

1981). This could stem from mechanisms resembling,

or related to, ‘classical respiratory conditioning’ as it is

known to occur in humans (Gallego & Perruchet

1991). In view of this, the lack of cortical involvement

in the response to exercise of trained subjects would

not be surprising. In addition, it is known that the cor-

tical activation related to a volitional movement

Figure 1 Results of the inspiratory-triggered back averaging of the electroencephalographical (EEG) signal in one of the study

subjects. In each panel, the top trace is the mouth pressure signal, and the bottom trace is the EEG signal. The top panel

corresponds to a positive control experiment (voluntary sniffing), showing the clear presence of a premotor potential (horizontal

double arrow) starting about 0.9 s before inspiration (vertical line) and followed by a clearly visible motor potential attesting to

a cortical contribution to the inspiratory command. On the middle row, the left panel corresponds to the pre-exercise control

period, whereas the right panel corresponds to exercise at 40% _VO2max. On the bottom row, the left panel corresponds to the

post-exercise control period (following immediately the previous exercise bout), whilst the right one corresponds to exercise at

70% _VO2max. In these four cases, there is no indication of a pre-inspiratory EEG activity and no motor potential.



decreases dramatically when this movement becomes

automatic and is performed without attention directed

towards its detail (Wu et al. 2004, 2008).

The absence of inspiratory-triggered premotor

potentials during exercise in our subjects contributes

to the notion that the involvement of the cerebral cor-

tex is not necessary to explain the exercise-related

hyperpnea (see review in Haouzi 2006), at least dur-

ing the steady-state phase of exercise. Because evi-

dencing an inspiratory premotor potential requires the

averaging of EEG epochs gathered over many respira-

tory cycles (80 in the present series of measurements),

namely several minutes, our results cannot, however,

contribute to the discussion concerning an early and

transitory cortical component to exercise-related

hyperpnea. It has indeed been shown that, in humans,

ventilation augments at the beginning of a spell of

exercise before the increase in metabolism demands

such an augmentation (Tobin et al. 1986). The period

of exercise during which ventilation is ‘anticipated in

excess’ lasts only a few seconds (Tobin et al. 1986),

which is in line with the rapid decrease of the fast

component of exercise-related hyperpnea that has

been described by Koehle and Duffin (1996). Yet the

fast component of exercise-related hyperpnea is

depressed by cotasking an exercise bout with cognitive

work (Bell et al. 2005), which points towards a corti-

cal contribution to its origin. EEG analysis techniques

apt to detect respiratory-related changes in a quasi-

instantaneous manner would be necessary to extend

our observations beyond the steady-state phase of

exercise. To our knowledge, no such technique has

presently been validated.

Our study adds to the observation made by Haouzi

et al. (2000) in a patient suffering from an Arnold

Chiari malformation. This patient was able to mobi-

lize her vital capacity normally and to achieve

expected levels of voluntary hyperventilation but

lacked chemosensitivity (Haouzi et al. 2000). Her ven-

tilatory response to exercise was profoundly abnor-

mal, leading Haouzi et al. (2000) to infer that the

corticospinal pathway to the respiratory muscles was

not adequate to ensure ventilatory adaptation. This

observation is, however, not sufficient to rule out

cooperative mechanisms involving a suprapontine con-

trol. Similarly, the lack of inspiratory premotor poten-

tials in our subjects during exercise only indicates that

steady-state exercise does not engage the supplemen-

tary motor area, where premotor potentials mainly

originate. It does not exclude the contribution of other

cortical circuits, or, as discussed earlier, a cortical con-

tribution to the fast ventilatory response to exercise.

We conclude that the cortical phenomena that have

been described during inspiratory load compensation

in humans (EEG evidence for premotor cortical activ-

ity) do not seem to be involved in the ventilatory

response to exercise observed in physically active

humans, at least during the steady-state phase. Further

studies are needed to determine whether or not this is

also the case in sedentary individuals, whether or not

any other suprapontine mechanisms could be

involved, and what’s more, the exact significance of

the cortical activations seen in respiratory-related

areas during exercise (Fink et al. 1995) remains to be

elucidated.

Conflict of interest

All the authors declare that they have no conflict of

interest relevant to this study.

The authors are grateful to Dr Joanna Wilson-Dorsett for

editing the manuscript. This work was supported by a « Legs

Poix » research grant from the Chancellerie de l’Universite

de Paris, Paris, France.

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Figure 2 Frequency of inspiratory pre-

motor potentials (iPMPs) in the group of

subjects, according to the different study

conditions. The occurrence of iPMPs

was not significantly more frequent dur-

ing exercise than during the relaxed,

pedalling control conditions.



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Ventilatory response to exercise does not evidence electroencephalographical respiratory-related activation of the cortical premotor circuitry in healthy humans