# Physiological changes in response to apnea impact the timing of motor representations: a preliminary study

Franck Di Rienzo, Nady Hoyek, Christian Collet, Aymeric Guillot

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Franck Di Rienzo, Nady Hoyek, Christian Collet, Aymeric Guillot. Physiological changes in response to apnea impact the timing of motor representations: a preliminary study. Behavioral and Brain Functions, 2014. hal-01743947

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# Physiological changes in response to apnea impact the timing of motor representations: a preliminary study

Franck Di Rienzo¹*, Nady Hoyek¹, Christian Collet¹ and Aymeric Guillot¹,²

**Abstract**

**Background:** Reduced physiological arousal in response to breath-holding affects internal clock processes, leading swimmers to underestimate the time spent under apnea. We investigated whether reduced physiological arousal during static apnea was likely to affect the temporal organization of motor imagery (MI).

**Methods:** Fourteen inter-regional to national breath-holding athletes mentally and physically performed two 15 m swimming tasks of identical durations. They performed the two sequences in a counterbalanced order, the first while breathing normally using a scuba, the second under apnea. We assessed MI duration immediately after completion of the corresponding task. Athletes performed MI with and without holding breath.

**Results:** MI durations (26.1 s ± 8.22) were significantly shorter than actual durations (29.7 s ± 7.6) without holding breath. Apnea increased MI durations by 10% (± 5%). Heart rate decrease in response to breath-holding correlated with MI durations increase (p < .01). Under apnea, participants achieved temporal congruence between MI and PP only when performing MI of the apnea swimming task. Self-report data indicated greater ease when MI was performed in a physiological arousal state congruent with that of the corresponding motor task.

**Conclusions:** Physiological arousal affected the durations of MI through its effects on internal clock processes and by impacting the congruency in physiological body states between overt and covert motor performance. Present findings have potential implications with regards to the possibility of preventing underestimation of durations spent under a state of reduced physiological arousal.

**Keywords:** Mental chronometry, Motor imagery, Apnea, Heart rate, Internal clock

**Introduction**

Motor Imagery (MI) is the mental representation of a motor act without engaging in its actual execution. A large body of neuroscience research supports that MI and physical practice (PP) of the same task share overlapping neural substrates [1-4], and involve functionally equivalent neural processes [5-8]. As well, behavioral research provided strong evidence for a temporal congruence between the temporal structure of MI and the temporal parameters of the corresponding motor performance, reflecting the involvement of common planning

and programming strategies [9]. Recently, Guillot et al. [10] reviewed the key-components that may affect the durations of MI, i.e., factors that promote temporal congruence or conversely yield to consistent overestimation or underestimation of PP durations. Interestingly, they specifically highlighted the selective influence of several external factors on MI durations. For instance, the characteristics of the motor skill are likely to alter the temporal congruence between MI and PP durations (i.e., short-lasting motor sequences are usually overestimated, whereas long-lasting and cyclical motor skills tend to be underestimated). Similarly, complex motor sequences require greater time to be mentally rehearsed compared to physically executed [9,11,12]. Finally, a proportional increase in MI durations was found along with the intensity of the mental effort [13-15].

<footnote>* Correspondence: franck.di-rienzo@univ-lyon1.fr
¹Centre de Recherche et d'Innovation sur le Sport, EA 647, Université de Lyon, Université Claude Bernard, Lyon 1, Performance Motrice, Mentale et du Matériel (P3M), 27-29 Boulevard du 11 Novembre 1918, Villeurbanne, Cedex 69622, France</footnote>

<footnote>Full list of author information is available at the end of the article</footnote>
While some intrinsic features of the task might impact
its imagined duration, the sport imagery literature
acknowledges that the construction of the temporal
organization of MI is primarily based on the temporal
parameters of the corresponding motor performance
[10,16,17]. Indeed, actual motor experiences participate
to the central elaboration of forward models [18], i.e., an
internal simulation of the movement derived from the
efferent copy of the motor command, predicting future
body states and stimulating the sensory consequences of
the expected actions [18-21]. Accordingly, central pro-
cessing of MI involves the forward modeling of the cor-
responding action, from which substantial information
about its spatial and temporal features is obtained
[18,21-23]. Albeit primarily showed in chronometric ex-
periments, this claim is also supported by brain imaging
data. For instance, Lorey et al. [24] stated that:

"The functional equivalence of action states is due mostly to internal estimations of the expected sensory feedback in both motor control and motor imagery" (p. 1).

Also, applied experiments provided evidence that cen-
tral integration of sensory input during PP affected MI
durations, due to central updating of the temporal struc-
ture of the motor representation [15,22,25,26]. Di Rienzo
et al. [26] observed that physical fatigue led to underesti-
mation of the durations of imagined turns in swimming
athletes. A tight temporal congruence between MI and
PP was measured before fatigue state, but MI durations
were shorter immediately after an intense swimming ex-
ercise. This was only observed for MI tasks that involved
a strong reference to bodily information (i.e., first-person
visual MI) [27]. Conversely, external visual imagery du-
rations were unaffected by physical fatigue. The authors
interpreted their results as an account of the update of
the forward model due to the repeated integration of
sensory feedbacks under fatigue state ([see also 23]).
However, findings might also account for aversive or
motivational effects related to the experience of physical
fatigue. Finally, scientific data in clinical populations also
support the hypothesis of sensory afferences playing a
crucial role in the shaping of MI durations (e.g., [28]).

While cognitive motor processes participate to the
elaboration of the temporal structure of MI [29,30],
Decety et al. [31] early stated that *"MI involve[s] the
same clock mechanism as the actual motor behavior"*,
with reference to Keele et al. [32]. The authors observed
that overestimation of MI durations in stroke patients
might account for *"an impairment in the central imple-
mentation of the clock"* (i.e., in the sense of the internal
clock) [33,34]. In other words, MI durations might not
only depend on the temporal parameters of forward
models but also from internal clock processes generally

involved in time estimation ability. Since Hoagland [33],
theoretical models for a human internal clock were con-
ceptualized from animal research (for a review, see [35]).
Internal clock models assume that temporal features are
centrally represented on the basis of a physiological
"pacemaker" producing pulses at a given rate (the lick
rate was assumed to play the role of the pacemaker in
rats, see [36]). The amount of pulses within a given time
period would be summed, stored within working mem-
ory, and finally compared with a reference long-term
memory model (for an overview, see [34,37,38]). Applied
to motor control, Treisman et al. [39] provided evidence
that an oscillator controlled temporal estimations in
humans and was involved in the control of movement
timing.

Interestingly, a large body of experimental data sup-
ports that heartbeats may be the physiological pace-
maker of the internal clock in humans [38,40-43].
Namely, humans might non-consciously refer to their
own heartbeats to achieve time estimations. This postu-
late accounts for the reported effects of physiological
arousal on time estimation ability [33,41,44-47]. Albeit it
was recently suggested that physiological arousal, but
not heart rate *per se*, influenced time estimation in
humans, thus putting into debate the concept of "*in-
ternal pacemaker*" [48], physiological arousal and heart
rate remain highly correlated. Past experiments also
demonstrated that physiological arousal affected MI
durations (see [10] for a review). For instance, Louis
et al. [49] observed that reduced body arousal elicited by
relaxation resulted in longer MI durations compared to
both aroused and baseline conditions. In the same vein,
Gueugneau et al. [22] found that the duration of MI
followed the circadian rhythms of arousal, i.e., longer MI
durations were measured early in the morning and late
in the evening (see also [50]). To summarize, findings of
a relationship between physiological arousal and MI
durations are congruent with the working hypothesis of
internal clock processes being involved in the temporal
organization of MI. Nonetheless, the cognitive interplay
between internal clock processes and time parameters of
forward models remains at this point incompletely
understood.

Voluntary breath-holding (i.e., apnea) at rest is known
to decrease heart rate both in air and water environ-
ments [38,43,51,52]. Bradycardia occurs in response to
water immersion due to cardiovascular and metabolic
changes triggered by the mammalian diving reflex
[53-56]. In a pioneering study, Jamin et al. [43] observed
that reduced physiological arousal during breath-holding
caused an underestimation of the durations of static ap-
neas by about 20%. According to the authors, bradycar-
dia disturbed the internal clock and impaired time
estimation ability. These findings are of specific concern
for breath-holders, because accurate control of the time
spent under apnea is crucial to achieve safe practice and
avoid syncope accidents [38].

The present study used the unique model of apnea to
understand the respective contribution of i) time param-
eters of forward models derived from *past* motor experi-
ences and ii) internal clock processes depending on the
 current physiological body state on the temporal features
of MI. We hypothesized that breath-holding might affect
MI durations due to changes in the internal clock, and
that these effects would be selective according to the
arousal body state during PP.

**Methods**

**Participants**

Fourteen breath-holding athletes were requested to
physically and mentally perform a set of two swimming
tasks, the first with, and the second without simultan-
eously holding breath. The experimental group consisted
of 14 breath-holding athletes (males = 11, females = 3;
M = 38.3, SD = 7.7) and included both national (n = 9) and
inter-regional (n = 5) athletes. The experimental design
was approved by the Research Ethics Committee of the
University. Informed written consent was obtained ac-
cording to the principles and statements of the Declar-
ation of Helsinki (1964).

Experimental design and settings

Experiments were individually implemented in a 25 m
public swimming pool (F-69110, Sainte Foy-lès-Lyon).
Water temperature was 27.3°C and participants wore an
apnea suit and were not weighted. Three iron sticks were
initially dived at the bottom of the pool, perpendicularly

to the lane. Iron sticks were respectively separated from
each other by 4.5, 3.0 and 1.5 m (Figure 1). All experimen-
tal sessions were carried out in the same daytime (8 pm),
i.e., when MI performance is the most accurate [22,50].

Swimming tasks

Participants were requested to physically and mentally
perform two swimming tasks of 15 m involving a
sequence of aquatic displacements between 3 iron stick
positions. The first task was a 1-3-1-2-1 sequence and the
second was a 3-1-2-1-3 sequence (Figure 1). The first
swimming task was performed while breathing normally
using a scuba after a 45 s period of rest where partici-
pants breathed normally behind the starting iron stick
(PP<sub>BREATHE</sub>). The second task was performed under
apnea following a 45 s period of static apnea behind the
starting iron stick (PP<sub>APNEA</sub>). Pilot recordings showed
that this duration was sufficient to elicit a sustained
bradycardia without eliciting any discomfort for partici-
pants. The two tasks were of equivalent difficulty and
involved a similar number of turns. During both tasks,
participants were instructed to swim using self-paced
breaststroke actions, and to remain by the surface of the
pool (i.e., a part of their body had to be constantly vis-
ible out of water surface by the experimenter). Concern-
ing the turns, after the head had passed the iron stick,
participants turned themselves and swam in the reverse
direction. PP<sub>BREATHE</sub> and PP<sub>APNEA</sub> were presented in a
randomized order across participants. Four PP trials
were completed before measurements of MI durations.

The timekeeping of PP<sub>BREATHE</sub> and PP<sub>APNEA</sub> was
manually performed by a professional swimming coach
who was not informed of the purpose of the study.

<figure><img src="image_1.png" /></figure>
Timekeeping was triggered when breath-holder's head passed above the starting and ending iron sticks (i.e., 1-3-1-2-1 for PP<sub>BREATHE</sub> and 3-1-2-1-3 for PP<sub>APNEA</sub>) (Figure 1).

## Motor imagery ability assessment

Breath-holding participants completed, before the experiment, a validated MI questionnaire to assess their ability to engage into MI (MIQ-3 questionnaire) [57]. The MIQ-3 consists in 12 items for which participants rate the ease/difficulty encountered during MI on 7-point scales (ranging from 1: *"very hard to see/feel"* to 7: *"very easy to see/feel"*) referring to external visual, internal visual, and kinesthetic MI.

Mental chronometry allows investigation of the time course of information processing within the central nervous system [58]. We measured MI duration immediately after PP of the corresponding motor task. Participants sat comfortably in a chair placed by the side of the swimming pool (Figure 1). Participants were instructed to perform MI of the sequence using first-person visual and kinesthetic MI concurrently. For PP<sub>BREATHE</sub> and PP<sub>APNEA</sub>, they performed MI while breathing normally after a 45 s period of normal breathing (MI<sub>BREATHE</sub>) and while holding breath after a 45 s period of static apnea (MI<sub>APNEA</sub>). The two MI conditions were presented in a randomized order (3 trials each). Participants orally indicated the onset and end of each MI trial.

After completion of MI<sub>BREATHE</sub> and MI<sub>APNEA</sub>, participants reported their level of MI ease/difficulty on a 10-point Lickert scale (ranging from 1: *"very easy"* to 10: *"very hard"*).

## Cardiac activity

We recorded the cardiac activity using a heart rate monitor (Polar® RCX3, France) providing the instantaneous heart rate (IHR) in beats per minute (bpm). HR at rest (HR<sub>REST</sub>) was individually evaluated before the onset of experiments. HR<sub>REST</sub> was considered the average value obtained during 45 s of rest during which participants remained motionless, comfortably seated on the chair by the side of the pool (Figure 1).

Voluntary apnea with face immersion in humans is commonly associated with anticipatory tachycardia. Cardiac activity starts to decrease and stabilizes after approximately 30 s of face immersion (e.g., [59]). We could not monitor cardiac activity during the swimming tasks, which required a *waterproof* heart rate monitor. Yet, bradycardia in response to breath holding is largely documented in the literature, and is particularly marked due to the mammalian diving reflex [51, 53, 56, 60].

We collected the average HR during the 45 s period preceding MI and expressed it in percentage of HR<sub>REST</sub> for normalization across participants. We did not collect

HR data during MI due to solid literature background reporting MI-related changes in cardiac activity (i.e., cardiac responses during MI closely mirror physiological changes elicited by PP of the same task and/or recruitment of attentional resources) [61-64].

## Statistical analyses

All statistical calculations were performed using the R freeware [65], and the alpha threshold for significance was settled at $\alpha = 5\%$.

MIQ-3 scores represent discrete variables derived from ordinal scales. Due to assumption of non-Gaussian distribution, they were compared across internal visual, external visual and kinesthetic MI modalities using Friedman's test. Self-reports of ease/difficulty were compared between MI<sub>BREATHE</sub> and MI<sub>APNEA</sub> using paired Wilcoxon's tests.

Normality of chronometric data was checked through visual inspection of Q-Q plots. PP, MI<sub>BREATHE</sub> and MI<sub>APNEA</sub> durations were compared for both swimming tasks using a repeated measures MANOVA model with the swimming task as group factor (PP<sub>BREATHE</sub> and PP<sub>APNEA</sub>) and the task type as repetition factor (PP, MI<sub>BREATHE</sub> and MI<sub>APNEA</sub>). An independent analysis of PP, MI<sub>BREATHE</sub> and MI<sub>APNEA</sub> durations was conducted for PP<sub>BREATHE</sub> and PP<sub>APNEA</sub> using one-way ANOVAs with repeated measures. We used paired Student's t-tests with Holm's Bonferroni corrections (Holm, 1969) for post-hoc comparisons.

For both swimming tasks, independence between HR and MI duration changes was tested using Pearson's product-moment correlation between the percentage of HR change before MI<sub>BREATHE</sub> and MI<sub>APNEA</sub> and the percentage of change in MI<sub>BREATHE</sub> and MI<sub>APNEA</sub> durations.

## Results

### MIQ-3 scores

Testing the MI modality effect on MIQ-3 scores did not reveal statistically significant differences (Friedman's *Chi-squared* = 1.45, *p* = .48). Namely, breath-holders reported similar degrees of difficulty at performing external visual (*M* = 5.84, *SD* = .69), internal visual (*M* = 6.0, *SD* = .80) and kinesthetic MI (*M* = 5.80, *SD* = .97). Mean MIQ-3 scores (*M* = 5.80, *SD* = .59) also showed that participants experienced MIQ-3 tasks as easy to visualize or perceive.

### Likert ratings

Breath holders self-reported greater MI ease scores during MI<sub>BREATHE</sub> (*M* = 3.21, *SD* = .65) as compared to MI<sub>APNEA</sub> (*M* = 4.93, *SD* = .70) when imagining the PP<sub>BREATHE</sub> task (Wilcoxon's *W* = 3.5, *p* = .005). Conversely, lower ratings were obtained during MI<sub>APNEA</sub> (*M* = 3.58, *SD* = .62) compared to MI<sub>BREATHE</sub> (*M* = 5.15, *SD* = .52) when imagining the PP<sub>APNEA</sub> swimming task (Wilcoxon's *W* = 44, *p* = .01).
Temporal data

MANOVA with repeated measures yielded the main effect of Task ($F_{(2,25)}$ = 10.16, *p* < .001, $\eta^2$ = .44) while there was a trend concerning the interaction between the swimming task and task type ($F_{(2,25)}$ = 2.96, *p* = .06, $\eta^2$ = .12).

ANOVA with repeated measures revealed that the effect of task type was statistically significant for both $PP_{BREATHE}$ and $PP_{APNEA}$ ($F_{(2,26)}$ = 4.19, *p* = .02 and $F_{(2,26)}$ = 20.44, *p* < .001, respectively). For both swimming tasks, post-hoc analyses revealed higher durations during PP compared to $MI_{BREATHE}$ (*p* = .02 and *p* < .001, respectively), as well as during $MI_{APNEA}$ compared to $MI_{BREATHE}$ (*p* = .02) as shown by Figure 2. Post-hoc analyses also revealed shorter durations during $MI_{APNEA}$ ($M$ = 27.71, $SD$ = 8.18) compared to $PP_{BREATHE}$ ($M$ = 31.02, $SD$ = 7.15; *p* < .001), whereas no difference emerged between $MI_{APNEA}$ ($M$ = 29.78, $SD$ = 9.95) and $PP_{APNEA}$ ($M$ = 29.79, $SD$ = 6.73) (*p* = .99). As there was no difference between $PP_{BREATHE}$ and $PP_{APNEA}$ durations (*p* = .72), the patterns of MI vs. PP differences in durations across swimming tasks might account for the trend in the MANOVA model, albeit the difference between the two $MI_{APNEA}$ durations was only marginally significant when corrections for multiple comparisons were applied ($M$ = 2.07 s, $SD$ = 3.47, *p* = .09), see Figure 2. Finally, the difference in durations between $MI_{BREATHE}$ of the $PP_{BREATHE}$ and $PP_{APNEA}$ tasks was far from significance (*p* = .98) as shown by Figure 1.

Cardiac activity

HR data were processed from 13 participants as data from one participant was lost due to a technical failure. Overall, average HR before $MI_{BREATHE}$ was 72.61 bpm ($SD$ = 2.29) while average HR before $MI_{APNEA}$

was 66.81 bpm ($SD$ = 2.24). Significant differences were observed in HR before the onset of the two MI conditions for both $PP_{BREATHE}$ (7.0% of $HR_{REST}$ decrease at onset of $MI_{APNEA}$ as compared to $MI_{BREATHE}$; *t* = 3.91, $\mu$ = 0, *p* = .002) and $PP_{APNEA}$ (9.0% of $HR_{REST}$ decrease at onset of $MI_{APNEA}$ as compared to $MI_{BREATHE}$; *t* = 4.27, $\mu$ = 0, *p* = .001).

A correlation between the percentage of HR decrease between periods preceding $MI_{BREATHE}$ and $MI_{APNEA}$ and the percentages of MI durations increase between $MI_{BREATHE}$ and $MI_{APNEA}$ was found for both $PP_{BREATHE}$ and $PP_{APNEA}$ ($R^2$ = .80, *p* < .001 and $R^2$ = .48, *p* < .01, respectively). The sum square error of the regression was 66% higher for $PP_{BREATHE}$ compared to $PP_{APNEA}$ (Figure 3).

Discussion

The present study was designed to investigate the effect of apnea on MI duration, and understand the respective contribution of the temporal parameters of both forward models and internal clock processes to the elaboration of the temporal structure of MI. We assessed participants ability to engage into MI using a validated MI questionnaire [57]. We recorded the durations of two swimming tasks performed with and without holding breath. For each task, we combined chronometric and physiological recordings of MI performed with and without holding breath.

MIQ-3 scores were similar between external visual, internal visual and kinesthetic imagery modalities. We specifically instructed participants to engage into first-person and kinesthetic MI concurrently as these modalities involve greater reference to one's procedural memory

<figure><img src="image_2.png" /><figcaption>**Figure 2** Physical practice and motor imagery durations during breathing and apnea swimming tasks. Error bars represent mean standard error. Only significant differences were graphically represented. PP: Physical Practice. *t*: *p* < .10, \*: *p* < .05, **: *p* < .01, ***: *p* < .001.</figcaption></figure>
<figure><img src="image_3.png" /><figcaption>**Figure 3** Correlations between variations in heart rate (percentage from basal values) and motor imagery duration changes between normal breathing and apnea conditions, for the apnea (left panel) and breathing (right panel) swimming tasks. MI: Motor imagery, HR: Heart rate.</figcaption></figure>

[26,27]. No significant difference was found between the durations of the two swimming tasks. Both were physically performed using a similar swimming technique, involved the same number of turns and a similar distance. Interestingly, PP<sub>BREATHE</sub> durations were underestimated during MI<sub>BREATHE</sub>. This result might account for the characteristics of the swimming sequence. Indeed, PP of both sequences lasted about 30 s. As recently reviewed by Guillot et al. [10], motor sequences longer than 15-20 s tend to be underestimated (e.g., [17,66-68]). The reasons supporting this effect are not straightforward. Temporal parameters of movements may be quantitatively more complex to reproduce accurately in the case of long motor sequences, particularly for actions requiring an important amount of feedback control with reference to the action/control model by Glover [69]:

"(...) the control of nonballistic actions is achieved by continuously regulating the movement during its execution so that the desired end state is achieved at the desired time. The lack of this information in imagery may be what causes a shortening of the duration of the imagined event" [66], p. 880.

Due to the solid literature background supporting that motor experiences shape the temporal organization of MI [22,23,25,28], similar imagined durations were expected between the two swimming tasks. However, MI<sub>APNEA</sub> exceeded MI<sub>BREATHE</sub> durations regardless the swimming task involved. Performing MI while holding breath overall increased MI durations by 2.7 s (≈ 10%). Importantly, increased MI durations under the condition of breath-holding were correlated to the preceding HR decrease. This relationship was observed for both swimming tasks (Figure 3). These findings support the involvement

of internal clock processes in the shaping of MI duration, as early postulated by Decety et al. [31]. As time perception and movement timing both involve reference to a common physiological oscillator [36,39], it is suggested that bradycardia affected the internal clock "pacemaker" [34,35,38,40-42], thus slowing the processing rate of motor representations. The involvement of the internal clock in the generation of MI durations brings new insights for a unified interpretation of experimental results related to factors affecting MI durations, such as the circadian modulation [22,50] or relaxed/aroused body states [49]. Interestingly, these studies reported increased MI durations under low physiological arousal and shortened MI durations under high physiological arousal. These changes were typically associated with different cardiac activities [26,49].

MI<sub>APNEA</sub> durations remained shorter than that of PP for the swimming task involving normal breathing, whereas isochrony was found when comparing MI<sub>APNEA</sub> and apnea swimming task durations. Longer durations (+2.07 s) were recorded during MI<sub>APNEA</sub> of the apnea swimming tasks vs. MI<sub>APNEA</sub> of the swimming task performed while breathing with a scuba. Yet, this difference was only marginally significant when corrections for multiple comparisons were applied (Figure 2). This unexpected finding suggests that congruence in physiological body states between overt and covert motor performance also contributes to the accuracy of MI durations. A limitation to this interpretation is that we did not record isochrony between MI<sub>BREATHE</sub> and PP<sub>BREATHE</sub>. This mismatch was attributed to the task duration, thought to elicit an incomplete encoding of the temporal parameters [10,66]. The apnea swimming task was of identical duration but, crucially, was performed under a state of reduced physiological arousal. As movement
timing parameters are controlled through reference to
the internal clock [39], retention of movement timing
parameters may be facilitated under the condition of
reduced physiological arousal eliciting a slowing down
of the internal clock [38,43]. While the underestimation
of MIBREATHE durations might account for the task
duration in the case of normal breathing, it may rather
relate to the physiological arousal mismatch during
MIBREATHE of the apnea swimming task. Albeit this in-
terpretation remains an inference, forward models relate
to current body states through integration of proprio-
ceptive afferences [27,70]. For instance, the physiological
body state affects the body representation through subtle
changes in proprioceptive inputs to the central nervous
system (see [71,72] for examples). Therefore, the arousal
state is an intrinsic component of the central processing
of the expected consequences of imagined actions (for-
ward modeling). Overall, while reference to internal clock
affected the processing rate of motor representations,
accurate movement timing processing through forward
modeling presumably required a state of congruence in
physiological body states. The fact that the R-squared of
the regression between changes in HR and the associated
changes in MI durations was higher (66%) for the breath-
ing compared to the non-breathing swimming task partly
supports to this assumption, as in the latter case online
changes in the internal clock accounted to a lesser extent
for the associated changes in MI durations.

Isochrony between MI<sub>APNEA</sub> and PP<sub>APNEA</sub> may thus
result from both efficient storage of timing parameters
of actual movement, facilitated by the changes in the
internal clock in response to apnea, and accurate pro-
cessing of the expected sensory consequences of the
imagined action due to congruence in physiological body
states. Such assumption is congruent with the subjective
reports. Breath holders reported greater MI ease when
the physiological arousal condition before initiation of
MI was similar to that preceding PP of the same task (i.e.,
namely with or without holding breath during the 45 s
preceding initiation of MI or PP). These preliminary
results support the co-contribution of forward modeling
and internal clock processes to the shaping of MI
duration. Yet, this preliminary study must be extended by
future designs involving different levels of arousal (e.g.,
increased heart rate) and retention conditions (e.g., per-
forming MI two days later). Complementary measurement
of physiological arousal are also necessary (e.g., autonomic
nervous system recordings), for instance under the condi-
tions of MI and apnea underwater [73,74]. Another inter-
esting issue would be determining to which extent
changes in cerebral blood flow due to apnea might affect
MI ability. For instance, accurate MI duration was associ-
ated with higher activation intensities within regions of
the brain motor system [75]. As previous work underlined

that apnea led to the underestimation of PP duration
[38,43], future studies should seek to determine whether
correcting the effect of breath holding on MI durations
(i.e., involving biased temporal predictions related to
bradycardia amplitude), for instance by providing feed-
back concerning respect of isochrony with PP after com-
pletion of MI, would improve time estimation accuracy.
Taken together, present findings might contribute to pro-
mote safe apnea practice in the currently developing
context of apnea competitions.

Competing interests

The authors declare no competing interests.

Authors’ contributions

All authors (FDR, NH, CC and AG) participated to the design of the study. FDR and NH supervised the experiments. FDR performed the statistical analyses and drafted the manuscript. All authors read, amended and approved the final manuscript.

Acknowledgements

We gratefully acknowledge the H₂O apnea sporting club (Sainte-Foy-lès-Lyon, F-69110) and the Aquatic Club Fidésien apnea elite team (Sainte-Foy-lès-Lyon, F-69110) for their human and material support.

Author details

¹Centre de Recherche et d'Innovation sur le Sport, EA 647, Université de Lyon, Université Claude Bernard, Lyon 1, Performance Motrice, Mentale et du Matériel (P3M), 27-29 Boulevard du 11 Novembre 1918, Villeurbanne, Cedex 69622, France. ²Institut Universitaire de France, 103 boulevard Saint-Michel, Paris 75005, France.

Received: 7 January 2014 Accepted: 15 April 2014
Published: 28 April 2014

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doi:10.1186/1744-9081-10-15

Cite this article as: Di Rienzo et al. Physiological changes in response to apnea impact the timing of motor representations: a preliminary study. *Behavioral and Brain Functions* 2014 10:15.

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