It is well known that endurance exercise modulates the cardiovascular, pulmonary, and musculoskeletal system. However, knowledge about its effects on brain function and structure is rather sparse. Hence, the present study aimed to investigate exercise-dependent adaptations in neurovascular coupling to different intensity levels in motor-related brain regions. Moreover, expertise effects between trained endurance athletes (EA) and active control participants (ACP) during a cycling test were investigated using multi-distance functional near-infrared spectroscopy (fNIRS). Initially, participants performed an incremental cycling test (ICT) to assess peak values of power output (PPO) and cardiorespiratory parameters such as oxygen consumption volume (VO2max) and heart rate (HRmax). In a second session, participants cycled individual intensity levels of 20, 40, and 60% of PPO while measuring cardiorespiratory responses and neurovascular coupling. Our results revealed exercise-induced decreases of deoxygenated hemoglobin (HHb), indicating an increased activation in motor-related brain areas such as primary motor cortex (M1) and premotor cortex (PMC). However, we could not find any differential effects in brain activation between EA and ACP. Future studies should extend this approach using whole-brain configurations and systemic physiological augmented fNIRS measurements, which seems to be of pivotal interest in studies aiming to assess neural activation in a sports-related context.
It is well known that exercise, which is defined as a planned, structured (repetitive) form of distinct physical activities (Budde et al. 2016; Caspersen et al. 1985; Herold et al. 2018b), stimulates cardiovascular, pulmonary and musculoskeletal systems, and its metabolic effects have also been described (Moghetti et al. 2016; Nystoriak and Bhatnagar 2018; Vuori 1995). Contrarily to the profound knowledge about peripheral adaptations to regular exercise, information about its effects on brain function and structure still remains elusive. Recent studies provided compelling evidence that regular exercise and physical activity, which is defined as any bodily, muscle-produced movement (Budde et al. 2016; Caspersen et al. 1985; Herold et al. 2018b), are associated with functional and structural brain alterations (Bullitt et al. 2009; Colcombe et al. 2006; Erickson et al. 2012; Voss et al. 2010; Wagner et al. 2015). On a functional level, Lulic et al. (2017) observed that the propensity for exercise-induced functional plasticity is different in high versus low physically active individuals. Here, a single session of moderate-intensity aerobic exercise increased the amplitude of corticospinal output in the HIGH (physically active) group, and, in contrast, did not alter corticospinal output in the LOW (physically active) group. Furthermore, authors suggest that a single session of aerobic exercise can transiently reduce inhibition in the motor cortex regardless of physical activity level, potentially priming the system for plasticity induction. Apart from causing volume changes (Dordevic et al. 2018; Meier et al. 2016; Weinstein et al. 2012), structural plasticity is associated with changes in cerebral blood flow (CBF) and metabolism (Ide and Secher 2000). Increased metabolic demands due to exercise are met by redistributing oxygen supply in active brain regions from areas that are not necessarily solicited during exercise (Heinonen et al. 2014). With regards to regular physical activity, several cross-sectional studies found that more hours of weekly physical activity and higher cardiorespiratory fitness levels (Albinet et al. 2014; Dupuy et al. 2015) are associated with higher oxyhemoglobin (Hb) levels and superior cognitive performance. However, since physical-activity-induced neurobiological mechanisms are not completely understood yet, it seems reasonable to apply state-of-the-art neuroimaging methods to foster our understanding of the effects of physical activity, exercise and training on neuroplasticity. In general, neuroplasticity can be seen as a phenomenon where the brain adapts its processing as a consequence of, e.g., a changing environment and/or specific demands in everyday life (Pascual-Leone et al. 2005, 2011). Apart from this existing knowledge, the effects of exercise in sport settings still remain elusive.
In the present study, functional near-infrared spectroscopy (fNIRS) was applied in a sport-specific context. This neuroimaging method has been established as a valuable tool for measuring neurovascular coupling (Liao et al. 2013; Pinti et al. 2018) during physical activity and exercise involving the quantification of chromophore concentrations resolved from the measurement of relative changes in oxygenated (Hb) and deoxygenated hemoglobin (HHb) (Obrig et al. 1996; Obrig and Villringer 2003; Perrey 2008; Strangman et al. 2002). Previous studies have demonstrated that fNIRS is an appropriate and reliable method for measuring neurovascular coupling in adults during both simple motor tasks (see Leff et al. 2011) as well as complex body movements such as walking/running (Harada et al. 2009; Holtzer et al. 2011; Suzuki et al. 2004), rowing (Nielsen et al. 1999), squatting (Kenville et al. 2017), juggling (Carius et al. 2016) or playing table tennis (Balardin et al. 2017). Moreover, cycling on an ergometer has been established in several studies as a standardized and comparable task for measuring brain activation during exercise using fNIRS (Ohyanagi et al. 2018; Radel et al. 2018; Tempest and Parfitt 2016; Tempest and Reiss 2018). Nevertheless, previous investigations were mainly limited to fNIRS measurements focusing on prefrontal brain regions (Giles et al. 2014; Jung et al. 2015; Rupp et al. 2008). Our previous knowledge on this topic concerning brain functioning in motor-related areas during cycling is mainly based on studies using positron emission tomography (PET) and electroencephalography (EEG). For example, previous studies using PET (Christensen et al. 2000) and EEG (Brümmer et al. 2011) found that higher motor centers, including M1 and supplementary motor cortices (SMA) as well as cerebellum, take an active part in the generation and control of rhythmic motor tasks such as cycling. These findings were confirmed in fNIRS studies showing increased oxygenation (Takehara et al. 2017) and deoxygenation (Jung et al. 2015) with elevating exercise intensities. Furthermore, previous studies revealed exercise-induced activations in prefrontal cortex (PFC) showing that Hb and HHb levels respond as a function of both exercise load and duration in both experts (Rupp et al. 2008) and non-experts (Auger et al. 2016; Giles et al. 2014; Jung et al. 2015). However, previous studies focusing on neurovascular coupling at several intensity levels show that there is no consensus concerning the type of exercise (incremental tests with short stages vs. constant-load exercises), duration of exercise (Giles et al. 2014; Tsubaki et al. 2016) and intensity (Auger et al. 2016; Byun et al. 2014; Giles et al. 2014; Takehara et al. 2017; Tsubaki et al. 2018).
According to a systematic review by Rooks et al. (2010), exercise-induced responses in neurovascular coupling varied widely between aerobically trained and untrained individuals relating to exercise intensity. At low and moderate intensities, authors suggest a lower cortical metabolic demand in trained people due to lower Hb level and lower blood volume compared to untrained individuals. Contrarily, during maximal and exhaustive intensities, aerobically trained people attained higher levels of cortical Hb, HHb and total hemoglobin than untrained participants. The authors explain these contrasting results by a downregulation of sensory signaling from muscle and limbs to central nervous system (CNS), particularly at submaximal intensities, as an adaption to exercise training (Rooks et al. 2010). As a result, this would lead to a reduced somatosensory input to subcortical and cortical brain regions (Gandevia 2001), and, thus, to a reduced CBF and oxygenation in highly trained individuals, especially at submaximal intensities (Butler et al. 2003; Taylor and Gandevia 2008).
Hence, the present study aimed at (a) revealing intensity-dependent changes in neurovascular coupling in motor-related brain regions and (b) quantifying expertise effects during a short-term constant-load cycling test using a multimodal approach that combined fNIRS and cardiorespiratory measurements. Since fNIRS signal is known to be confounded by extra-cerebral influences (Tachtsidis and Scholkmann 2016), we used a multi-distance fNIRS measurement including multiple short-distance channels to sufficiently control for this matter. The focus was on the question whether a short time window of cycling is capable of inducing alterations in neurovascular coupling at several intensity levels determined by an incremental cycling test (ICT). In general, as a confirmatory hypothesis based on the literature, we expected endurance athletes (EA) to show superior values in peak power output (PPO) and maximum oxygen consumption volume (VO2max) (Kostić 2017; Rankovic et al. 2010) as assessed by ICT, indicating clear differences in training status as compared to active control participants (ACP). Furthermore, we hypothesized to observe neurovascular coupling alterations (increase in Hb and decrease in HHb) in motor-related brain regions such as M1, SMA and premotor cortex (PMC) in dependence of exercise intensity (Auger et al. 2016; Giles et al. 2014; Kenville et al. 2017) assessed by multi-distance fNIRS measurements during short-term and submaximal constant-load cycling exercises as well as an intensity-dependent increase of cardiorespiratory parameters such as VO2 and heart rate (HR). Additionally, we assumed, in line with the “neural efficiency” hypothesis (Dunst et al. 2014), that EA would show less neurovascular coupling at distinct intensity levels as compared to ACP. Similar findings have been observed by Ludyga et al. (2016), showing lower brain activation levels in cyclists with high aerobic fitness compared to peers with less aerobic fitness, indicating enhanced neural efficiency in subjects with high aerobic power.
Materials and methods
The study was approved by the local ethics committee of the Medical Faculty at the University of Leipzig. All participants gave written informed consent to participate in the experiments according to the Declaration of Helsinki.
In the present study, a total number of 42 healthy, young adults were recruited (Table 1), divided into endurance athletes (EA) and active control participants (ACP). As assessed by the Edinburgh Handedness Inventory (Oldfield 1971), all participants were right-handed. To exclude the presence of any neurological disease and/or contraindications, all participants answered a neurological questionnaire prior to testing phase. Inclusion criteria for EA consisted of an individual training history of at least 2 years and a weekly exercise volume of at least 8 h in their respective sports discipline. ACP were not allowed to do more than 5 h of combined sports activities per week, where no kind of any endurance sports may be included. EA consisted of 17 triathletes, 3 cyclists and 2 cross-country skiers. Additionally, all participants with regular practice of musical instruments were excluded from participation since recent studies have shown that musical training induces functional and structural plasticity in motor-related brain regions (Steele et al. 2013; Vollmann et al. 2014) which in turn might affect the assessment of neurovascular coupling.
We used a quasi-experimental design where each participant was tested in two sessions (Fig. 1a) that were separated by at least 24 h to avoid task-related impacts of cognitive or muscular fatigue. Participants were instructed to avoid alcohol and caffeine 24 h prior to each session due to their influences on motor control and CNS functioning (Pesta et al. 2013). Additionally, participants were asked to report their daily activities 48 h prior to each session, along with their current levels of attention, fatigue and discomfort on a visual analog scale (pre and post), as well as their individual amount of sleep the night before experimental sessions.
The first session consisted of an incremental cycling test (ICT) to assess PPO, VO2max and HRmax of each participant. Using these values, three individual intensity levels of 20, 40, and 60% of PPO were derived. During session 2, participants cycled these levels multiple times while measuring cardiorespiratory responses and neurovascular coupling in motor-related brain regions.
A high-performance stationary bicycle (Cyclus 2, RBM elektronik-automation GmbH, Leipzig, Germany) allowing participants to cycle at a constant load measured in watts (W) was used to determine VO2max and its corresponding load. Before each session, the cycle ergometer was individually adjusted to the participant’s anthropometry.
Session 1: Incremental cycling test (ICT)
After adjusting the cycle ergometer and applying the spirometric system including facemask for VO2 and chest strap for HR, session 1 started with a 5 min warm-up phase using a constant load of 50 W. This load was also the starting point for ICT that started immediately afterwards. Until voluntary exhaustion, participants pedaled continuously with a pedaling frequency of 60–80 revolutions per minute (rpm) during 30-s levels, each level providing an increment of 15 W in resistance (Fig. 1a). Ramp tests like this are commonly used to assess individual PPO and VO2max quickly and efficiently (Barker et al. 2011; Chicharro et al. 1997). PPO for each participant was determined by the power of the last completed level. The exercise was considered to be maximal when the following criteria were obtained: no change in VO2 while increasing resistance, participants signal subjective (maximal) exhaustion, or the inability of participants to maintain pedaling frequency despite maximum effort. After ICT was stopped, resistance was reduced to zero, and participants were asked to continue unloaded pedaling for another 4–5 min until physiological parameters nearly reached warm-up values.
Session 2: Multi-intensity cycling test (MICT)
In preparation for session 2, a fNIRS cap was placed on the participant’s head in addition to the spirometric system. After all devices were calibrated and baseline measurement was completed, participants performed a 5 min warm-up phase using a constant load of 50 W. Subsequently, using a block design, participants cycled five trials of 30 s each at intensities of 20, 40, and 60%, respectively (Fig. 1a). The order of trials was randomized, with the exception of avoiding more than two consecutive trials of one intensity. Similar to session 1, participants were instructed to maintain a cycling rate of 60–80 rpm. Each trial was followed by a 30-s resting phase, where participants were asked to sit completely still on the cycle ergometer. Moreover, participants were asked to avoid upper body and head movements during the whole test to prevent fNIRS signal from artifacts. Further artifacts are due to systemic influences such as an increased blood pressure which has been shown during (static) resistance exercises (MacDougall et al. 1985, 1992) but also during cycling on an ergometer (Kim et al. 2013). Hence, before and after each activity phase, we implemented a 10-s transition phase where participants were supposed to gradually start and stop pedaling, respectively. Using this phase, we avoided a critical systemic influence on the fNIRS signal, especially while initiating the pedaling. Consequently, we measured a pure 30-s phase of activity and rest, respectively.
Functional near-infrared spectroscopy (fNIRS)
Hemodynamic response alterations during MICT were assessed using the portable NIRSport measuring system (NIRx Medical Technologies, Glen Head, NY). For this purpose, a cap with a defined number of optodes, which were placed directly on the scalp, was applied on the participant’s head. The center of the cap was placed according to the international 10–20 system over vertex (Cz), determined over the intersection of the courses nasion to inion and left to right pre-auricular point (Jurcak et al. 2007). The arrangement of the optodes allowed the measurement of brain activity within human motor system using a fNIRS configuration with a total number of 15 optodes (8 sources and 7 detectors, Fig. 1b). The aim of using this distinct cap configuration was motivated by the fact that we intended to disentangle hemodynamic response alterations as a function of applied intensities, specifically within the bilateral sensorimotor system, including cortical motor regions such as M1, PMC, SMA, superior parietal lobe (SPL) and inferior parietal lobe (IPL). Infrared light was emitted by sources with wavelengths of 760 and 850 nm (Pereira et al. 2007) and measured with a recording frequency of 7.81 Hz. Spectroscopically, NIRSport operated via a so-called continuous wave method; i.e., sources emit light at constant frequency and intensity (Scholkmann et al. 2014).
In addition to the 22 long-distance (standard) channels, we used a short-distance detector bundle (NIRx Medical Technologies, Glen Head, NY) to eliminate potential fNIRS confounders, such as extra-cerebral blood flow alterations (Huppert et al. 2009; Tachtsidis and Scholkmann 2016). For this purpose, we used additional short-distance detectors for each source with an inter-optode distance of 8 mm, as opposed to the inter-optode distance for all other (long) channels of our configuration (3 cm). This resulted in eight short-distance channels, which were considered in the analysis of fNIRS signal (see “Analysis”).
Cardiorespiratory parameters were assessed using the Metamax 3B (MM3B) system (Cortex Biophysik GmbH, Leipzig, Germany), which has previously been tested as a stable and reliable gas analysis system (Macfarlane and Wong 2012). MM3B is a portable metabolic system composed of a measurement module and a battery module which can be placed on the participant’s upper chest or back using connecting cords and assisting straps. The breath-by-breath system measures volume of inspired and expired air using a bidirectional digital turbine inserted into the facemask. Parameters of ventilation such as VO2 were calculated using standard metabolic algorithms (Wasserman 2012). Measurements were performed using Metasoft 3 software, version 3.7.0 SR2.
Prior to using, the system was switched on for at least 20 min, and then calibrated prior to each test according to the manufacturer’s recommendations. This involved calibrating the gas analysers using a reference gas (Hong Kong Specialty Gases), and then verifying the calibration against ambient air. Second, volume calibration was performed using a standardized 3 l syringe (5530 series, Hans Rudolph, Inc., MO, USA).
Once all preparations have been completed, the appropriate facemask was selected for each participant. Covering nose and mouth, the facemask was secured via an adjustable nylon harness and placed over the fNIRS cap without any disturbances of optode channels. Additionally, a chest strap (Polar Electro Oy, Kempele, Finnland) was applied to assess HR. Subsequently, participants were asked to sit completely still for ~ 1 min to perform baseline measurements.
fNIRS data analysis was performed in MATLAB (MathWorks, Natick, MA, USA) using functions provided in HOMER2 package (Huppert et al. 2009). Statistical analysis was performed using R 3.4.3 (R Core Team, 2017) and RStudio 1.1.383 (RStudio Team, 2017). As a first step, the signal quality of all individual channels was checked by means of a coefficient of variation (CV, exclusion value: 15%). Subsequently, raw fNIRS recordings were pre-processed to reduce the influence of motion artifacts and physiological noise before estimating changes in concentrations of Hb and HHb. First, raw-intensity signals were converted to changes in optical density (Huppert et al. 2009). Correction for motion artifacts was performed using wavelet filtering, which has been described as a promising approach to reduce the influence of motion artifacts in fNIRS recordings (Brigadoi et al. 2014). We used an algorithm described by Molavi and Dumont (2012), as implemented in HOMER2 hmrMotionCorrectWavelet filtering function. The algorithm applies a probability threshold to remove outlying wavelet coefficients, which were assumed to correspond to motion artifacts. We used a threshold of 1.219 times the inter-quartile range (Wiggins and Hartley 2015). Subsequently, data were band-pass filtered to attenuate low-frequency drift and cardiac oscillations using 0.01 Hz as high and 0.5 Hz as low-pass cutoff frequencies (Huppert et al. 2009). Attenuation changes of both wavelengths (850 nm and 760 nm) were transformed to concentration changes of Hb and HHb using the modified Beer–Lambert approach [partial path length factor: 6.0 (Huppert et al. 2009)]. Reporting both (Hb and HHb) changes instead of only one of them is strongly recommended and allows better physiological interpretation of functional experimental results (Tachtsidis and Scholkmann 2016). In general, HHb is described as the more valid parameter for the investigation of hemodynamic response alterations (Muthalib et al. 2015; Piper et al. 2014). Hb signals are more strongly affected by global processes in both extra-cerebral and intra-cerebral compartments and local scalp blood flow regulation, while HHb signals are less contaminated by extra-cerebral processes (Kirilina et al. 2012). To regress extra-cerebral contaminations (measured by short-distance channels) out of the signal, we used HOMER2 hrmDeconvHRF_DriftSS function as previously applied by (Aasted et al. 2016). As implemented in this function, short separation regression (SSR) is performed with the nearest short separation channel while simultaneously estimating HRF (Gagnon et al. 2011) using ordinary least squares (Ye et al. 2009) and a consecutive sequence of Gaussian functions. This method assumes that the signal measured by short-distance channels represents superficial layers and the signal measured by long-distance channels represents both brain tissue and superficial layers. Thus, the effects of systemic physiology can be captured from superficial layers and can then be used as regressors to filter systemic interference from long-distance channels to provide a more robust estimation of underlying hemodynamic alterations to brain activation (Yücel et al. 2015). Afterwards, single trials were baseline-corrected (regarding last 5 s of previous resting phase) and time courses of Hb and HHb concentration changes in each channel were block-averaged using HOMER2 hmrBlockAvg function. Though the experimental block design included long breaks to prevent overlapping of hemodynamic responses between trials, we directly analyzed the height of amplitude [baseline-corrected average of 30-s temporal window with regard to stimulus onset for activity phase (Herold et al. 2018a)].
In fNIRS studies, assumptions for parametric tests are often violated (e.g., normal distribution), as it was for data assessed in the present study. For this reason, robust statistical methods (Wilcox 2017) are a considerable option for data analysis as suggested by Santosa et al. (2018). Hence, differences in Hb and HHb concentration changes between EA and ACP (group as between-subject factor), respectively, intensity levels of 20, 40 and 60% (condition as within-subject-factor) were tested using a robust two-way factorial ANOVA. Additionally, robust dependent t tests were conducted on a group level in a channel-wise manner to test contrasts of activity phases against zero (Piper et al. 2014). These tests were conducted in R using WRS2 package (Mair and Wilcox 2017). As a measure of effect size, Wilcox and Tian (2011) proposed an explanatory measure of effect size ξ. Values of ξ = 0.10, 0.30, and 0.50 correspond to small, medium, and large effect sizes. To control for multiple comparisons during robust t tests and ANOVA, we applied false discovery rate (FDR) correction (Singh and Dan 2006). For all tests, critical level of significance was set to p < 0.05 and FDR-adjusted for multiple comparisons. The resulting channel-wise t values, respectively, f values were mapped using the Brain Function Mapping Tool (Wang et al. 2016). To assign hemodynamic response alterations during MICT to a specific brain region, we utilized a probabilistic atlas implemented in the software fOLD [fNIRS Optodes’ Location Decider (Zimeo Morais et al. 2018)] using the automated anatomical labeling atlas AAL2 (Rolls et al. 2015).
Similar to fNIRS data, statistical analysis was performed using R 3.4.3 (R Core Team, 2017) and RStudio 1.1.383 (RStudio Team, 2017). Regarding cardiorespiratory measurements during ICT, maximum values of VO2 and HR were output directly from Metasoft 3. First, absolute values of VO2 and PPO were calculated in relation to the participant’s body weight to make them comparable inter-individually. Univariate analyses of variance (uANOVA) with factor group (EA vs. ACP) were conducted to test differences between EA and ACP in PPO, VO2max and HRmax. Partial eta-squares (η 2p ) for uANOVAs are provided as measures of effect size and used to aid in interpretation of inferential statistics. As a rule of thumb, η 2p ≥ 0.01 is considered to be a small, η 2p ≥ 0.06 a medium, and η 2p ≥ 0.14 a large effect (Miles and Shevlin 2000).
Regarding MICT, intensity-dependent changes in VO2 and HR were calculated as differences (Δ) between averaged last 5 s of each activity phase (due to delay of the respiratory system during exercise (Roston et al. 1987; Whipp 1994)) and averaged last 5 s of the corresponding previous resting phase (according to processing of fNIRS data). Similar to fNIRS data, differences in ΔVO2 and ΔHR between EA and ACP (group as between-subject factor), respectively, intensity levels of 20, 40, and 60% (condition as within-subject-factor) were tested using a two-way factorial ANOVA.
Using WRS2 package in R, robust correlation coefficients were calculated to correlate channel-wise intensity-dependent neurovascular coupling changes of Hb and HHb with maximum values from ICT (PPO, VO2max, HRmax) and with intensity-dependent cardiorespiratory responses (ΔVO2 and ΔHR). For all tests, a p value of < 0.05 was considered significant and FDR correction was applied for multiple comparisons.
ICT revealed significant differences between EA and ACP in PPO, VO2max and HRmax. uANOVA revealed significantly higher PPO (EA: 5.21 ± 0.63 W/kg vs. ACP: 4.52 ± 0.40 W/kg; main effect of group: F(1,40) = 17.421, p < 0.000, η 2p = 0.303, 95% CI [0.355, 1.022]) and VO2max (EA: 64.59 ± 10.07 ml/min/kg vs. ACP: 52.20 ± 7.21 ml/min/kg; main effect of group: F(1,40) = 20.658, p < 0.000, η 2p = 0.341, 95% CI [6.881, 17.901]) values in EA as compared to ACP, indicating clear differences in cardiorespiratory fitness level between groups (Fig. 2a). No differences were found in HRmax (EA: 182.36 ± 10.59 bpm vs. ACP: 179.55 ± 6.83 bpm; main effect of group: F(1,40) = 1.024, p = 0.318, η 2p = 0.025, 95% CI [− 2.806, 8.434]).
Intensity-dependent changes in neurovascular coupling
In all channels tested, we did not find any condition x group interaction during MICT neither for Hb (0.014 ≤ F(2,80) ≤ 1.688, 0.444 ≤ padjusted ≤ 0.980, 0.012 ≤ ξ ≤ 0.107) nor HHb (0.014 ≤ F(2,80) ≤ 1.662, 0.462 ≤ padjusted ≤ 0.993, 0.007 ≤ ξ ≤ 0.121). However, in left PMC, we found a significant influence of factor condition on HHb concentration (F(2,80) = 18.049, padjusted = 0.001, ξ = 0.382, 95% CIs [− 0.001, 0.060], [− 0.008, 0.156], [0.235, 0.148]), indicating a larger HHb decrease across all participants at an intensity of 60% as compared to 20% (padjusted < 0.000) (Fig. 3).
In a further analysis step at a group level, we aimed to illustrate hemodynamic response alterations for each intensity level separately. Robust independent t tests revealed significant decreases of Hb and HHb in both groups (Fig. 4a). We found decreased Hb concentrations in precentral areas such as PMC and SMA and left-hemispheric IPL for EA and only in right-hemispheric PMC (at 20%) for ACP. HHb concentrations decreased bilaterally in pre- and postcentral areas as well as in M1 in both groups, except ACP at 20% showing no significant HHb alterations.
Additionally, robust independent t tests were also performed without applying SSR. Figure 4b elucidates deltas between alterations in brain activation before and after SSR, indicating that hrmDeconvHRF_DriftSS function was capable of filtering systemic interferences from long-distance channels.
Intensity-dependent cardiorespiratory responses
During MICT, robust two-way factorial ANOVA revealed significant influences of factors condition (F(2,80) = 63.450, padjusted = 0.001, ξ = 0.401, 95% CIs [− 9.140, − 20.448], [− 16.768, − 0.159], [− 10.572, − 4.954]) and group (F(2,80) = 5.916, padjusted = 0.019, ξ = 0.254, 95% CI [1.077, 11.197]) on VO2, but a non-significant condition x group interaction (F(2,80) = 4.307, padjusted = 0.134, ξ = 0.101, 95% CIs [− 5.592, − 8.994], [− 8.862, 3.389], [0.882, 2.952]) (Fig. 2b). Post-hoc tests revealed significant differences between all intensity levels (20 vs. 40%: padjusted = 0.014; 20 vs. 60%: padjusted < 0.000; 40 vs. 60%: padjusted < 0.000), indicating intensity-dependent increase in VO2.
Concerning intensity-dependent HR changes during MICT, robust two-way factorial ANOVA revealed significant influences of factors condition (F(2,80) = 170.639, padjusted = 0.001, ξ = 0.432, 95% CIs [− 29.599, − 52.907], [− 31.148, − 14.596], [− 35.763, − 13.327]) and group (F(2,80) = 16.944, padjusted = 0.001, ξ = 0.398, 95% CI [8.754, 25.242]), but a non-significant condition x group interaction (F(2,80) = 4.076, padjusted = 0.146, ξ = 0.127, 95% CIs [− 10.774, − 15.458], [− 12.524, 4.229], [1.686, 5.297]) (Fig. 2b). Post-hoc tests revealed significant differences between all intensity levels (20 vs. 40%: padjusted < 0.000; 20 vs. 60%: padjusted < 0.000; 40 vs. 60%: padjusted < 0.000), indicating intensity-dependent increase in HR.
Robust correlation analysis revealed significant negative correlations in two channels (r = − 0.542, padjusted = 0.001 and r = − 0.506, padjusted = 0.004) between HHb concentration changes and ΔVO2 at an intensity of 20% in bilateral SPL (Fig. 5). These findings indicate that larger intensity-dependent increases of VO2 are correlated with larger decreases of HHb at the lowest intensity level. All other correlation analyses concerning intensity-dependent alterations and peak values of measured parameters revealed no further significant results.
The present study aimed to investigate whether a short-term cycling exercise is capable of inducing intensity-dependent hemodynamic response alterations in motor-related brain regions. Using a multimodal approach that combined multi-distance fNIRS and cardiorespiratory measurements, trained endurance athletes (EA) as well as active control participants (ACP) were tested to reveal possible expertise effects. The study focused on the question whether neurovascular coupling depends on exercise intensity and if EA would differ in their exercise-induced brain activation compared to ACP. Our results provide novel evidence concerning the practicability of fNIRS measurements including multiple short-distance channels during a cycling task. We found typical exercise-induced alterations in the more valid parameter HHb as well as a correlation between HHb concentration changes and VO2 at the lowest intensity level. However, our findings suggest that the “neural efficiency” hypothesis (Dunst et al. 2014) seems not to be applicable for highly automated movements such as cycling on an ergometer.
Hemodynamic and cardiorespiratory responses during MICT
We hypothesized to observe an increase in Hb and simultaneously a decrease in HHb in motor-related brain regions in dependence of exercise intensity as well as intensity-dependent increases of cardiorespiratory parameters such as VO2 and HR. This assumption was confirmed by all parameters except Hb. As well known, changes in regional brain activation in response to motor stimulation are associated with higher concentrations of Hb and decreased concentrations of HHb (Obrig et al. 1996; Obrig and Villringer 2003; Perrey 2008; Strangman et al. 2002). Contrarily to this evidence, we found exercise-induced decreases of Hb particularly in precentral brain regions of EA. Such atypical findings were also found in a recent study by Takehara et al. (2017). In this study, participants performed 10 min of exercise at intensities of 30 and 50% of VO2max on a cycle ergometer while Hb concentrations were measured in PFC and M1. Interestingly, they found that Hb concentrations were significantly decreased in the initial phase (first 2–3 min) of exercise in both regions of interest, while they were significantly increased from mid to final phase for both intensities compared with baseline values. Since our activity phase of 30 s coincides with the initial phase of this study, both observations are similar and comparable. According to the authors, the initial phase of complex movements might be a period during which oxygen supply is insufficient for oxygen demands of the brain. As previously shown, neural activity increases in response to increased tissue oxygen consumption and glucose metabolism and thus, leading to an increased blood flow in the brain (Fox et al. 1988). These increases in CBF can be observed approximately 3 s after an increase in neural activity in the brain (Bandettini et al. 1992), whereupon changes are observed at intervals of about 6 s until sufficient increases have occurred (Taoka et al. 1998). During this time, a transient decrease in Hb concentrations can be observed (Takehara et al. 2017). This phenomenon was underlined by a recent study where participants performed 15-min cycling exercises at intensities of 20, 40, and 60% of PPO (Endo et al. 2013). During ergometer exercise, Hb concentrations in PFC initially decreased until 5 min from onset of exercise and increased during later periods. Moreover, initial decreases and later increases of Hb were even dependent on exercise intensity.
To summarize, changes in Hb are considered to be a more sensitive indicator of global processes in both extra-cerebral and intra-cerebral compartments and local scalp blood flow regulation than changes in HHb, while changes in HHb are determined more by venous oxygenation and blood volume than blood flow (Hoshi et al. 2001). These facts resulted in current discussions about reliability and validity of both chromophores with respect to indirect measurement of cortical activity via fNIRS (Obrig and Villringer 2003; Strangman et al. 2002). In general, HHb is described as the more valid parameter (Muthalib et al. 2015; Piper et al. 2014) since it is less contaminated by extra-cerebral processes (Kirilina et al. 2012). Taking this into account, results of the present study must be interpreted carefully since cycling tasks such as MICT are known to enhance systemic influence on fNIRS signal. Therefore, it seems reasonable to focus on the interpretation of HHb results and/or include additional analysis steps (e.g., SSR) to minimize potential confounding influences.
Concerning exercise-induced HHb concentration changes during MICT, our results revealed typical decreases at each intensity level, indicating increased activations in motor-related brain areas such as M1, PMC, SMA, IPL and SPL. A decrease in HHb has previously been reported by Kounalakis and Geladas (2012) during a constant load cycling task at a cycling rate of 80 rpm. Moreover, our findings indicate that HHb alterations might be dependent on exercise intensity. Regarding decreased HHb concentrations, these findings are reasonable and can be explained by previous studies demonstrating that more complex movements are associated with cortical activation increases in SMA and adjacent premotor areas (Orgogozo and Larsen 1979). Even though cortical processing during a rhythmic alternating activity such as cycling has mainly been investigated in prefrontal brain regions by means of fNIRS (Auger et al. 2016; Giles et al. 2014; Rupp et al. 2008), recent studies pointed to the important role of motor-related brain regions in cycling. For example, using PET, Christensen et al. (2000) observed an activation in M1 and SMA during active and passive cycling as two conditions of a rhythmic alternating activity in leg muscles. These findings were strengthened by subsequent fNIRS studies (Jung et al. 2015; Lin et al. 2012; Takehara et al. 2017), providing evidence for the important role of these brain regions in the planning, preparation and execution of complex movements (Leff et al. 2011). Hence, our findings and those of other groups demonstrate that there is a significant cerebral involvement in control of rhythmic locomotor movements in man. Beyond the fact that our results revealed a significant cerebral involvement during MICT, we also observed that HHb concentration changes might be modulated by increasing intensities (resistance) during cycling. This finding is further strengthened by previous studies demonstrating that higher cadences (MacIntosh et al. 2000) and intensities (Macdonald et al. 2008) during a cycling task are associated with a higher leg muscle activation. Hence, it is reasonable to assume that an increased recruitment of muscle fibers requires higher levels of neural resources in motor-related brain areas not only on a regional but also on a network level (Kenville et al. 2017). The fact that we observed intensity-dependent changes during cycling in a single brain region only (left PMC) does certainly not indicate that this area is exclusively responsible for modulating brain areas during increased workload during cycling. Even subcortical and/or cerebellar influences might potentially be involved in changing brain activation patterns during increased physical demands while executing movements (Maudrich et al. 2018; Sehm et al. 2016).
No evidence for “neural efficiency” in athletes during MICT
We further hypothesized to find differential hemodynamic alterations as a response to exercise intensity between EA and ACP in accordance with the “neural efficiency” hypothesis (Dunst et al. 2014). We expected to find less brain activation in EA when compared to ACP at the same intensity level. However, we could not confirm this assumption, which contrasts with the “neural efficiency” hypothesis.
Recent studies have transferred the “neural efficiency” hypothesis into a context of motor tasks and expertise. There is evidence that extensive practice over a long period of time leads expert athletes to develop a focused and efficient organization of task-related neural networks (Milton et al. 2007) and that neural activity is reduced in motor experts (Del Percio et al. 2009). Several previous studies revealed that compared to novices/non-athletes, expert athletes show less brain activation during resting state (Babiloni et al. 2010) or performing cognitive/motor tasks such as strategic planning (Deeny et al. 2009), upright standing (Del Percio et al. 2009), balancing (Seidel et al. 2017), and wrist extension task (Del Percio et al. 2010). In a recent study, table tennis athletes and non-athletes performed a visuo-spatial task while cortical activation was examined using fMRI (Guo et al. 2017). Researchers found that athletes exhibited less brain activation than non-athletes in motor-related brain regions such as SMA and cerebellum, suggesting that long-term training prompts athletes to develop a focused and efficient organization of task-related neural networks. Contrarily, many other studies reported more or partly cortical activation in expert athletes compared to non-athletes, especially while observing sports videos (Aglioti et al. 2008; Orgs et al. 2008). During preparation or execution of a motor task, Del Percio et al. (2011) found higher alpha coherence values in parietal, temporal and occipital areas in elite pistol shooters using EEG. Findings of the present study also tend in this direction, indicating no differential effects in brain activation between EA and ACP. On the one hand, these findings might be due to task complexity of MICT, since cycling is a highly automated motor task not only for EA but also for ACP. Therefore, it seems reasonable to assume that larger effects of neural efficiency in athletes might be more likely to be observed in coordinatively more demanding and less familiar/automated movement patterns (Lyons et al. 2010; Woods et al. 2014). On the other hand, a recent study by Ludyga et al. (2016) suggests that in exercises with low coordinative demands (e.g., cycling) the level of cardiorespiratory fitness is of critical importance concerning neurophysiological correlates of neural efficiency (i.e., EEG signals). Authors showed that EA with higher VO2max values were able to complete submaximal cycling exercise with a lower level of brain cortical activity as compared to participants with a lower VO2max indicating enhanced neural efficiency in participants with high aerobic power. This inconsistency concerning the relation between neural efficiency and task complexity certainly deserves further investigation in future studies and is clearly beyond the scope of the current study.
We used a multi-distance fNIRS approach to observe alterations in neurovascular coupling in motor-related brain areas during a cycling task in EA and ACP. To get a better understanding of neuronal correlates of complex motor tasks and potential effects of expertise, further studies using neurophysiological assessments of brain activation are needed. Our findings indicate that short-term exercise such as MICT seems to be less capable of inducing typical alterations in both chromophores Hb and HHb. Therefore, in future studies, duration of intensity levels as well as a clear distinction (e.g., larger intensities) between those levels need to be considered to observe typical and differential alterations. Additionally, fNIRS findings must be interpreted with caution, because, given our inter-optode distance, the penetration depth of infrared light is only ~ 1.5 cm (Pellicer and Bravo 2011; Perrey 2008). Hence, subcortical alterations obviously cannot be captured with this kind of imaging technique. Finally, we assessed brain activity predominantly over motor-related brain regions and did not use a whole-brain configuration to assess MICT-induced cortical alterations outside the human motor system. This seems particularly important since the vast majority of previous studies investigated exercise-dependent alterations in neurovascular coupling outside the human motor system focusing on prefrontal regions which are associated with cognitive domains but contribute indirectly to motor control (Giles et al. 2014; Rupp et al. 2008). For future studies, it should be mentioned that the validity of fNIRS during complex movements should be addressed in more detail, aiming to find task-dependent fNIRS modulations.
In the present study, we used a multimodal approach that combined cardiorespiratory measurements and a multi-distance fNIRS measurement, including short-distance channels as a promising method to globally correct fNIRS signal during a complex motor task. We provide evidence that cycling at several intensity levels leads to hemodynamic response alterations within the human motor system measured as decreases in HHb. However, we could not find any differential effects in brain activations between EA and ACP, which is contrary to the “neural efficiency” hypothesis. For future studies, more knowledge on neural processing as well as whole-brain and systemic physiological augmented fNIRS measurements are required to get a holistic view, which seems to be of pivotal interest in studies aiming to assess neural activation during execution of complex movements in context of sport.
Aasted CM, Yücel MA, Steele SC, Peng K, Boas DA, Becerra L, Borsook D (2016) Frontal lobe hemodynamic responses to painful stimulation: a potential brain marker of nociception. PLoS One 11:e0165226. https://doi.org/10.1371/journal.pone.0165226
Aglioti SM, Cesari P, Romani M, Urgesi C (2008) Action anticipation and motor resonance in elite basketball players. Nat Neurosci 11:1109–1116. https://doi.org/10.1038/nn.2182
Albinet CT, Mandrick K, Bernard PL, Perrey S, Blain H (2014) Improved cerebral oxygenation response and executive performance as a function of cardiorespiratory fitness in older women: a fNIRS study. Front Aging Neurosci 6:272. https://doi.org/10.3389/fnagi.2014.00272
Auger H, Bherer L, Boucher É, Hoge R, Lesage F, Dehaes M (2016) Quantification of extra-cerebral and cerebral hemoglobin concentrations during physical exercise using time-domain near infrared spectroscopy. Biomed Opt Express 7:3826–3842. https://doi.org/10.1364/BOE.7.003826
Babiloni C, Marzano N, Iacoboni M, Infarinato F, Aschieri P, Buffo P, Cibelli G, Soricelli A, Eusebi F, Del Percio C (2010) Resting state cortical rhythms in athletes: a high-resolution EEG study. Brain Res Bull 81:149–156. https://doi.org/10.1016/j.brainresbull.2009.10.014
Balardin JB, Zimeo Morais GA, Furucho RA, Trambaiolli L, Vanzella P, Biazoli C, Sato JR (2017) Imaging brain function with functional near-infrared spectroscopy in unconstrained environments. Front Hum Neurosci 11:258. https://doi.org/10.3389/fnhum.2017.00258
Bandettini PA, Wong EC, Hinks RS, Tikofsky RS, Hyde JS (1992) Time course EPI of human brain function during task activation. Magn Reson Med 25:390–397
Barker AR, Williams CA, Jones AM, Armstrong N (2011) Establishing maximal oxygen uptake in young people during a ramp cycle test to exhaustion. Br J Sports Med 45:498–503. https://doi.org/10.1136/bjsm.2009.063180
Brigadoi S, Ceccherini L, Cutini S, Scarpa F, Scatturin P, Selb J, Gagnon L, Boas DA, Cooper RJ (2014) Motion artifacts in functional near-infrared spectroscopy: a comparison of motion correction techniques applied to real cognitive data. Neuroimage 85(Pt 1):181–191. https://doi.org/10.1016/j.neuroimage.2013.04.082
Brümmer V, Schneider S, Strüder HK, Askew CD (2011) Primary motor cortex activity is elevated with incremental exercise intensity. Neuroscience 181:150–162. https://doi.org/10.1016/j.neuroscience.2011.02.006
Budde H, Schwarz R, Velasques B, Ribeiro P, Holzweg M, Machado S, Brazaitis M, Staack F, Wegner M (2016) The need for differentiating between exercise, physical activity, and training. Autoimmun Rev 15:110–111. https://doi.org/10.1016/j.autrev.2015.09.004
Bullitt E, Rahman FN, Smith JK, Kim E, Zeng D, Katz LM, Marks BL (2009) The effect of exercise on the cerebral vasculature of healthy aged subjects as visualized by MR angiography. AJNR Am J Neuroradiol 30:1857–1863. https://doi.org/10.3174/ajnr.A1695
Butler JE, Taylor JL, Gandevia SC (2003) Responses of human motoneurons to corticospinal stimulation during maximal voluntary contractions and ischemia. J Neurosci 23:10224–10230
Byun K, Hyodo K, Suwabe K, Kujach S, Kato M, Soya H (2014) Possible influences of exercise-intensity-dependent increases in non-cortical hemodynamic variables on NIRS-based neuroimaging analysis during cognitive tasks: technical note. J Exerc Nutr Biochem 18:327–332. https://doi.org/10.5717/jenb.2014.18.4.327
Carius D, Andrä C, Clauß M, Ragert P, Bunk M, Mehnert J (2016) Hemodynamic response alteration as a function of task complexity and expertise-An fNIRS study in jugglers. Front Hum Neurosci 10:126. https://doi.org/10.3389/fnhum.2016.00126
Caspersen CJ, Powell KE, Christenson GM (1985) Physical activity, exercise, and physical fitness: definitions and distinctions for health-related research. Public Health Rep 100:126–131
Chicharro JL, Pérez M, Vaquero AF, Lucía A, Legido JC (1997) Lactic threshold vs ventilatory threshold during a ramp test on a cycle ergometer. J Sports Med Phys Fitness 37:117–121
Christensen LO, Johannsen P, Sinkjaer T, Petersen N, Pyndt HS, Nielsen JB (2000) Cerebral activation during bicycle movements in man. Exp Brain Res 135:66–72
Colcombe SJ, Erickson KI, Scalf PE, Kim JS, Prakash R, McAuley E, Elavsky S, Marquez DX, Hu L, Kramer AF (2006) Aerobic exercise training increases brain volume in aging humans. J Gerontol A Biol Sci Med Sci 61:1166–1170. https://doi.org/10.1093/gerona/61.11.1166
Deeny SP, Haufler AJ, Saffer M, Hatfield BD (2009) Electroencephalographic coherence during visuomotor performance: a comparison of cortico-cortical communication in experts and novices. J Mot Behav 41:106–116. https://doi.org/10.3200/JMBR.41.2.106-116
Del Percio C, Babiloni C, Bertollo M, Marzano N, Iacoboni M, Infarinato F, Lizio R, Stocchi M, Robazza C, Cibelli G, Comani S, Eusebi F (2009) Visuo-attentional and sensorimotor alpha rhythms are related to visuo-motor performance in athletes. Hum Brain Mapp 30:3527–3540. https://doi.org/10.1002/hbm.20776
Del Percio C, Infarinato F, Iacoboni M, Marzano N, Soricelli A, Aschieri P, Eusebi F, Babiloni C (2010) Movement-related desynchronization of alpha rhythms is lower in athletes than non-athletes: a high-resolution EEG study. Clin Neurophysiol 121:482–491. https://doi.org/10.1016/j.clinph.2009.12.004
Del Percio C, Iacoboni M, Lizio R, Marzano N, Infarinato F, Vecchio F, Bertollo M, Robazza C, Comani S, Limatola C, Babiloni C (2011) Functional coupling of parietal α rhythms is enhanced in athletes before visuomotor performance: a coherence electroencephalographic study. Neuroscience 175:198–211. https://doi.org/10.1016/j.neuroscience.2010.11.031
Dordevic M, Schrader R, Taubert M, Müller P, Hökelmann A, Müller NG (2018) Vestibulo-hippocampal function is enhanced and brain structure altered in professional ballet dancers. Front Integr Neurosci 12:50. https://doi.org/10.3389/fnint.2018.00050
Dunst B, Benedek M, Jauk E, Bergner S, Koschutnig K, Sommer M, Ischebeck A, Spinath B, Arendasy M, Bühner M, Freudenthaler H, Neubauer AC (2014) Neural efficiency as a function of task demands. Intelligence 42:22–30. https://doi.org/10.1016/j.intell.2013.09.005
Dupuy O, Gauthier CJ, Fraser SA, Desjardins-Crèpeau L, Desjardins M, Mekary S, Lesage F, Hoge RD, Pouliot P, Bherer L (2015) Higher levels of cardiovascular fitness are associated with better executive function and prefrontal oxygenation in younger and older women. Front Hum Neurosci 9:66. https://doi.org/10.3389/fnhum.2015.00066
Endo K, Matsukawa K, Liang N, Nakatsuka C, Tsuchimochi H, Okamura H, Hamaoka T (2013) Dynamic exercise improves cognitive function in association with increased prefrontal oxygenation. J Physiol Sci 63:287–298. https://doi.org/10.1007/s12576-013-0267-6
Erickson KI, Weinstein AM, Sutton BP, Prakash RS, Voss MW, Chaddock L, Szabo AN, Mailey EL, White SM, Wojcicki TR, McAuley E, Kramer AF (2012) Beyond vascularization: aerobic fitness is associated with N-acetylaspartate and working memory. Brain Behav 2:32–41. https://doi.org/10.1002/brb3.30
Fox PT, Raichle ME, Mintun MA, Dence C (1988) Nonoxidative glucose consumption during focal physiologic neural activity. Science 241:462–464
Gagnon L, Perdue K, Greve DN, Goldenholz D, Kaskhedikar G, Boas DA (2011) Improved recovery of the hemodynamic response in diffuse optical imaging using short optode separations and state-space modeling. Neuroimage 56:1362–1371. https://doi.org/10.1016/j.neuroimage.2011.03.001
Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725–1789. https://doi.org/10.1152/physrev.2001.81.4.1725
Giles GE, Brunyé TT, Eddy MD, Mahoney CR, Gagnon SA, Taylor HA, Kanarek RB (2014) Acute exercise increases oxygenated and deoxygenated hemoglobin in the prefrontal cortex. NeuroReport 25:1320–1325. https://doi.org/10.1097/WNR.0000000000000266
Guo Z, Li A, Yu L (2017) “Neural efficiency” of athletes’ brain during visuo-spatial task: an fMRI study on table tennis players. Front Behav Neurosci 11:72. https://doi.org/10.3389/fnbeh.2017.00072
Harada T, Miyai I, Suzuki M, Kubota K (2009) Gait capacity affects cortical activation patterns related to speed control in the elderly. Exp Brain Res 193:445–454. https://doi.org/10.1007/s00221-008-1643-y
Heinonen I, Kalliokoski KK, Hannukainen JC, Duncker DJ, Nuutila P, Knuuti J (2014) Organ-specific physiological responses to acute physical exercise and long-term training in humans. Physiology (Bethesda) 29:421–436. https://doi.org/10.1152/physiol.00067.2013
Herold F, Wiegel P, Scholkmann F, Müller NG (2018a) Applications of functional near-infrared spectroscopy (fNIRS) neuroimaging in exercise cognition science: a systematic, methodology-focused review. J Clin Med. https://doi.org/10.3390/jcm7120466
Herold F, Hamacher D, Schega L, Müller NG (2018b) Thinking while moving or moving while thinking—concepts of motor-cognitive training for cognitive performance enhancement. Front Aging Neurosci 10:228. https://doi.org/10.3389/fnagi.2018.00228
Holtzer R, Mahoney JR, Izzetoglu M, Izzetoglu K, Onaral B, Verghese J (2011) fNIRS study of walking and walking while talking in young and old individuals. J Gerontol A Biol Sci Med Sci 66:879–887. https://doi.org/10.1093/gerona/glr068
Hoshi Y, Kobayashi N, Tamura M (2001) Interpretation of near-infrared spectroscopy signals: a study with a newly developed perfused rat brain model. J Appl Physiol 90:1657–1662. https://doi.org/10.1152/jappl.2001.90.5.1657
Huppert TJ, Diamond SG, Franceschini MA, Boas DA (2009) HomER: a review of time-series analysis methods for near-infrared spectroscopy of the brain. Appl Opt 48:D280–D298
Ide K, Secher NH (2000) Cerebral blood flow and metabolism during exercise. Prog Neurobiol 61:397–414
Jung R, Moser M, Baucsek S, Dern S, Schneider S (2015) Activation patterns of different brain areas during incremental exercise measured by near-infrared spectroscopy. Exp Brain Res 233:1175–1180. https://doi.org/10.1007/s00221-015-4201-4
Jurcak V, Tsuzuki D, Dan I (2007) 10/20, 10/10, and 10/5 systems revisited: their validity as relative head-surface-based positioning systems. Neuroimage 34:1600–1611. https://doi.org/10.1016/j.neuroimage.2006.09.024
Kenville R, Maudrich T, Carius D, Ragert P (2017) Hemodynamic response alterations in sensorimotor areas as a function of barbell load levels during squatting: an fNIRS study. Front Hum Neurosci 11:241. https://doi.org/10.3389/fnhum.2017.00241
Kim YJ, Chun H, Kim C-H (2013) Exaggerated response of systolic blood pressure to cycle ergometer. Ann Rehabil Med 37:364–372. https://doi.org/10.5535/arm.2013.37.3.364
Kirilina E, Jelzow A, Heine A, Niessing M, Wabnitz H, Brühl R, Ittermann B, Jacobs AM, Tachtsidis I (2012) The physiological origin of task-evoked systemic artefacts in functional near infrared spectroscopy. Neuroimage 61:70–81. https://doi.org/10.1016/j.neuroimage.2012.02.074
Kostić V (2017) Differences in aerobic capacity and spirometric parameters between athletes and nonathletes. Porto Biomed J 2:184. https://doi.org/10.1016/j.pbj.2017.07.022
Kounalakis SN, Geladas ND (2012) Cardiovascular drift and cerebral and muscle tissue oxygenation during prolonged cycling at different pedalling cadences. Appl Physiol Nutr Metab 37:407–417. https://doi.org/10.1139/h2012-011
Leff DR, Orihuela-Espina F, Elwell CE, Athanasiou T, Delpy DT, Darzi AW, Yang G-Z (2011) Assessment of the cerebral cortex during motor task behaviours in adults: a systematic review of functional near infrared spectroscopy (fNIRS) studies. Neuroimage 54:2922–2936. https://doi.org/10.1016/j.neuroimage.2010.10.058
Liao L-D, Tsytsarev V, Delgado-Martínez I, Li M-L, Erzurumlu R, Vipin A, Orellana J, Lin Y-R, Lai H-Y, Chen Y-Y, Thakor NV (2013) Neurovascular coupling: in vivo optical techniques for functional brain imaging. Biomed Eng Online 12:38. https://doi.org/10.1186/1475-925X-12-38
Lin P-Y, Lin S-I, Chen J-JJ (2012) Functional near infrared spectroscopy study of age-related difference in cortical activation patterns during cycling with speed feedback. IEEE Trans Neural Syst Rehabil Eng 20:78–84. https://doi.org/10.1109/TNSRE.2011.2170181
Ludyga S, Gronwald T, Hottenrott K (2016) The athlete’s brain: cross-sectional evidence for neural efficiency during cycling exercise. Neural Plast 2016:4583674. https://doi.org/10.1155/2016/4583674
Lulic T, El-Sayes J, Fassett HJ, Nelson AJ (2017) Physical activity levels determine exercise-induced changes in brain excitability. PLoS One 12:e0173672. https://doi.org/10.1371/journal.pone.0173672
Lyons IM, Mattarella-Micke A, Cieslak M, Nusbaum HC, Small SL, Beilock SL (2010) The role of personal experience in the neural processing of action-related language. Brain Lang 112:214–222. https://doi.org/10.1016/j.bandl.2009.05.006
Macdonald JH, Farina D, Marcora SM (2008) Response of electromyographic variables during incremental and fatiguing cycling. Med Sci Sports Exerc 40:335–344. https://doi.org/10.1249/mss.0b013e31815b491e
MacDougall JD, Tuxen D, Sale DG, Moroz JR, Sutton JR (1985) Arterial blood pressure response to heavy resistance exercise. J Appl Physiol 58:785–790. https://doi.org/10.1152/jappl.1918.104.22.1685
MacDougall JD, McKelvie RS, Moroz DE, Sale DG, McCartney N, Buick F (1992) Factors affecting blood pressure during heavy weight lifting and static contractions. J Appl Physiol 73:1590–1597. https://doi.org/10.1152/jappl.1922.214.171.1240
Macfarlane DJ, Wong P (2012) Validity, reliability and stability of the portable Cortex Metamax 3B gas analysis system. Eur J Appl Physiol 112:2539–2547. https://doi.org/10.1007/s00421-011-2230-7
MacIntosh BR, Neptune RR, Horton JF (2000) Cadence, power, and muscle activation in cycle ergometry. Med Sci Sports Exerc 32:1281–1287
Mair P, Wilcox R (2017) Robust Statistical Methods Using WRS2. https://cran.r-project.org/web/packages/WRS2/vignettes/WRS2.pdf. Accessed 7 March 2019
Maudrich T, Kenville R, Lepsien J, Villringer A, Ragert P (2018) Structural neural correlates of physiological mirror activity during isometric contractions of non-dominant hand muscles. Sci Rep 8:9178. https://doi.org/10.1038/s41598-018-27471-5
Meier J, Topka MS, Hanggi J (2016) Differences in cortical representation and structural connectivity of hands and feet between professional handball players and ballet dancers. Neural Plast 2016:6817397. https://doi.org/10.1155/2016/6817397
Miles J, Shevlin M (2000) Applying regression and correlation: a guide for students and researchers. Sage publications Ltd, London
Milton J, Solodkin A, Hlustík P, Small SL (2007) The mind of expert motor performance is cool and focused. Neuroimage 35:804–813. https://doi.org/10.1016/j.neuroimage.2007.01.003
Moghetti P, Bacchi E, Brangani C, Donà S, Negri C (2016) Metabolic effects of exercise. Front Horm Res 47:44–57. https://doi.org/10.1159/000445156
Molavi B, Dumont GA (2012) Wavelet-based motion artifact removal for functional near-infrared spectroscopy. Physiol Meas 33:259–270. https://doi.org/10.1088/0967-3334/33/2/259
Muthalib M, Re R, Zucchelli L, Perrey S, Contini D, Caffini M, Spinelli L, Kerr G, Quaresima V, Ferrari M, Torricelli A (2015) Effects of increasing neuromuscular electrical stimulation current intensity on cortical sensorimotor network activation: a time domain fNIRS study. PLoS One 10:e0131951. https://doi.org/10.1371/journal.pone.0131951
Nielsen HB, Boushel R, Madsen P, Secher NH (1999) Cerebral desaturation during exercise reversed by O2 supplementation. Am J Physiol 277:H1045–H1052. https://doi.org/10.1152/ajpheart.1999.277.3.H1045
Nystoriak MA, Bhatnagar A (2018) Cardiovascular effects and benefits of exercise. Front Cardiovasc Med 5:135. https://doi.org/10.3389/fcvm.2018.00135
Obrig H, Villringer A (2003) Beyond the visible—imaging the human brain with light. J Cereb Blood Flow Metab 23:1–18. https://doi.org/10.1097/01.WCB.0000043472.45775.29
Obrig H, Hirth C, Junge-Hülsing JG, Döge C, Wolf T, Dirnagl U, Villringer A (1996) Cerebral oxygenation changes in response to motor stimulation. J Appl Physiol 81:1174–1183
Ohyanagi H, Tsubaki A, Morishita S, Obata H, Qin W, Onishi H (2018) Changes in the prefrontal cortex oxygenation levels during cycling in the supine and upright positions. Adv Exp Med Biol 1072:133–137. https://doi.org/10.1007/978-3-319-91287-5_21
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
Orgogozo JM, Larsen B (1979) Activation of the supplementary motor area during voluntary movement in man suggests it works as a supramotor area. Science 206:847–850
Orgs G, Dombrowski J-H, Heil M, Jansen-Osmann P (2008) Expertise in dance modulates alpha/beta event-related desynchronization during action observation. Eur J Neurosci 27:3380–3384. https://doi.org/10.1111/j.1460-9568.2008.06271.x
Pascual-Leone A, Amedi A, Fregni F, Merabet LB (2005) The plastic human brain cortex. Annu Rev Neurosci 28:377–401. https://doi.org/10.1146/annurev.neuro.27.070203.144216
Pascual-Leone A, Freitas C, Oberman L, Horvath JC, Halko M, Eldaief M, Bashir S, Vernet M, Shafi M, Westover B, Vahabzadeh-Hagh AM, Rotenberg A (2011) Characterizing brain cortical plasticity and network dynamics across the age-span in health and disease with TMS-EEG and TMS-fMRI. Brain Topogr 24:302–315. https://doi.org/10.1007/s10548-011-0196-8
Pellicer A, Bravo MdC (2011) Near-infrared spectroscopy: a methodology-focused review. Semin Fetal Neonatal Med 16:42–49. https://doi.org/10.1016/j.siny.2010.05.003
Pereira VJ, Linden KG, Weinberg HS (2007) Evaluation of UV irradiation for photolytic and oxidative degradation of pharmaceutical compounds in water. Water Res 41:4413–4423. https://doi.org/10.1016/j.watres.2007.05.056
Perrey S (2008) Non-invasive NIR spectroscopy of human brain function during exercise. Methods 45:289–299. https://doi.org/10.1016/j.ymeth.2008.04.005
Pesta DH, Angadi SS, Burtscher M, Roberts CK (2013) The effects of caffeine, nicotine, ethanol, and tetrahydrocannabinol on exercise performance. Nutr Metab 10:71. https://doi.org/10.1186/1743-7075-10-71
Pinti P, Tachtsidis I, Hamilton A, Hirsch J, Aichelburg C, Gilbert S, Burgess PW (2018) The present and future use of functional near-infrared spectroscopy (fNIRS) for cognitive neuroscience. Ann N Y Acad Sci. https://doi.org/10.1111/nyas.13948
Piper SK, Krueger A, Koch SP, Mehnert J, Habermehl C, Steinbrink J, Obrig H, Schmitz CH (2014) A wearable multi-channel fNIRS system for brain imaging in freely moving subjects. Neuroimage 85(Pt 1):64–71. https://doi.org/10.1016/j.neuroimage.2013.06.062
Radel R, Tempest GD, Brisswalter J (2018) The long and winding road: effects of exercise intensity and type upon sustained attention. Physiol Behav 195:82–89. https://doi.org/10.1016/j.physbeh.2018.07.028
Rankovic G, Mutavdzic V, Toskic D, Preljevic A, Kocic M, Nedin Rankovic G, Damjanovic N (2010) Aerobic capacity as an indicator in different kinds of sports. Bosn J Basic Med Sci 10:44–48. https://doi.org/10.17305/bjbms.2010.2734
Rolls ET, Joliot M, Tzourio-Mazoyer N (2015) Implementation of a new parcellation of the orbitofrontal cortex in the automated anatomical labeling atlas. Neuroimage 122:1–5. https://doi.org/10.1016/j.neuroimage.2015.07.075
Rooks CR, Thom NJ, McCully KK, Dishman RK (2010) Effects of incremental exercise on cerebral oxygenation measured by near-infrared spectroscopy: a systematic review. Prog Neurobiol 92:134–150. https://doi.org/10.1016/j.pneurobio.2010.06.002
Roston WL, Whipp BJ, Davis JA, Cunningham DA, Effros RM, Wasserman K (1987) Oxygen uptake kinetics and lactate concentration during exercise in humans. Am Rev Respir Dis 135:1080–1084. https://doi.org/10.1164/arrd.19126.96.36.1990
Rupp T, Thomas R, Perrey S, Stephane P (2008) Prefrontal cortex oxygenation and neuromuscular responses to exhaustive exercise. Eur J Appl Physiol 102:153–163. https://doi.org/10.1007/s00421-007-0568-7
Santosa H, Zhai X, Fishburn F, Huppert T (2018) The NIRS Brain AnalyzIR Toolbox. Algorithms 11:73. https://doi.org/10.3390/a11050073
Scholkmann F, Kleiser S, Metz AJ, Zimmermann R, Mata Pavia J, Wolf U, Wolf M (2014) A review on continuous wave functional near-infrared spectroscopy and imaging instrumentation and methodology. Neuroimage 85(Pt 1):6–27. https://doi.org/10.1016/j.neuroimage.2013.05.004
Sehm B, Steele CJ, Villringer A, Ragert P (2016) Mirror motor activity during right-hand contractions and its relation to white matter in the posterior midbody of the corpus callosum. Cereb Cortex 26:4347–4355. https://doi.org/10.1093/cercor/bhv217
Seidel O, Carius D, Kenville R, Ragert P (2017) Motor learning in a complex balance task and associated neuroplasticity: a comparison between endurance athletes and nonathletes. J Neurophysiol 118:1849–1860. https://doi.org/10.1152/jn.00419.2017
Singh AK, Dan I (2006) Exploring the false discovery rate in multichannel NIRS. Neuroimage 33:542–549. https://doi.org/10.1016/j.neuroimage.2006.06.047
Steele CJ, Bailey JA, Zatorre RJ, Penhune VB (2013) Early musical training and white-matter plasticity in the corpus callosum: evidence for a sensitive period. J Neurosci 33:1282–1290. https://doi.org/10.1523/JNEUROSCI.3578-12.2013
Strangman G, Culver JP, Thompson JH, Boas DA (2002) A quantitative comparison of simultaneous BOLD fMRI and NIRS recordings during functional brain activation. Neuroimage 17:719–731. https://doi.org/10.1006/nimg.2002.1227
Suzuki M, Miyai I, Ono T, Oda I, Konishi I, Kochiyama T, Kubota K (2004) Prefrontal and premotor cortices are involved in adapting walking and running speed on the treadmill: an optical imaging study. Neuroimage 23:1020–1026. https://doi.org/10.1016/j.neuroimage.2004.07.002
Tachtsidis I, Scholkmann F (2016) False positives and false negatives in functional near-infrared spectroscopy: issues, challenges, and the way forward. Neurophotonics 3:30401. https://doi.org/10.1117/1.NPh.3.3.030401
Takehara N, Tsubaki A, Yamazaki Y, Kanaya C, Sato D, Morishita S, Onishi H (2017) Changes in oxyhemoglobin concentration in the prefrontal cortex and primary motor cortex during low- and moderate-intensity exercise on a cycle ergometer. Adv Exp Med Biol 977:241–247. https://doi.org/10.1007/978-3-319-55231-6_33
Taoka T, Iwasaki S, Uchida H, Fukusumi A, Nakagawa H, Kichikawa K, Takayama K, Yoshioka T, Takewa M, Ohishi H (1998) Age correlation of the time lag in signal change on EPI-fMRI. J Comput Assist Tomogr 22:514–517
Taylor JL, Gandevia SC (2008) A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol 104:542–550. https://doi.org/10.1152/japplphysiol.01053.2007
Tempest G, Parfitt G (2016) Self-reported tolerance influences prefrontal cortex hemodynamics and affective responses. Cogn Affect Behav Neurosci 16:63–71. https://doi.org/10.3758/s13415-015-0374-3
Tempest GD, Reiss AL (2018) The utility of fNIRS for measuring cortical activity during cycling-exercise. Med Sci Sports Exerc. https://doi.org/10.1249/MSS.0000000000001875
Tsubaki A, Takai H, Oyanagi K, Kojima S, Tokunaga Y, Miyaguchi S, Sugawara K, Sato D, Tamaki H, Onishi H (2016) Correlation between the cerebral oxyhaemoglobin signal and physiological signals during cycling exercise: a near-infrared spectroscopy study. Adv Exp Med Biol 923:159–166. https://doi.org/10.1007/978-3-319-38810-6_21
Tsubaki A, Morishita S, Tokunaga Y, Sato D, Tamaki H, Yamazaki Y, Qin W, Onishi H (2018) Changes in cerebral oxyhaemoglobin levels during and after a single 20-minute bout of moderate-intensity cycling. Adv Exp Med Biol 1072:127–131. https://doi.org/10.1007/978-3-319-91287-5_20
Vollmann H, Ragert P, Conde V, Villringer A, Classen J, Witte OW, Steele CJ (2014) Instrument specific use-dependent plasticity shapes the anatomical properties of the corpus callosum: a comparison between musicians and non-musicians. Front Behav Neurosci 8:245. https://doi.org/10.3389/fnbeh.2014.00245
Voss MW, Prakash RS, Erickson KI, Basak C, Chaddock L, Kim JS, Alves H, Heo S, Szabo AN, White SM, Wojcicki TR, Mailey EL, Gothe N, Olson EA, McAuley E, Kramer AF (2010) Plasticity of brain networks in a randomized intervention trial of exercise training in older adults. Front Aging Neurosci. https://doi.org/10.3389/fnagi.2010.00032
Vuori I (1995) Exercise and physical health: musculoskeletal health and functional capabilities. Res Q Exerc Sport 66:276–285. https://doi.org/10.1080/02701367.1995.10607912
Wagner G, Herbsleb M, de la Cruz F, Schumann A, Brünner F, Schachtzabel C, Gussew A, Puta C, Smesny S, Gabriel HW, Reichenbach JR, Bär K-J (2015) Hippocampal structure, metabolism, and inflammatory response after a 6-week intense aerobic exercise in healthy young adults: a controlled trial. J Cereb Blood Flow Metab 35:1570–1578. https://doi.org/10.1038/jcbfm.2015.125
Wang Y, Yan J, Wen J, Yu T, Li X (2016) An intracranial electroencephalography (iEEG) brain function mapping tool with an application to epilepsy surgery evaluation. Front Neuroinform 10:15. https://doi.org/10.3389/fninf.2016.00015
Wasserman K (2012) Principles of exercise testing and interpretation: Including pathophysiology and clinical applications, 5th edn. Kluwer/Lippincott Williams & Wilkins, Philadelphia
Weinstein AM, Voss MW, Prakash RS, Chaddock L, Szabo A, White SM, Wojcicki TR, Mailey E, McAuley E, Kramer AF, Erickson KI (2012) The association between aerobic fitness and executive function is mediated by prefrontal cortex volume. Brain Behav Immun 26:811–819. https://doi.org/10.1016/j.bbi.2011.11.008
Whipp BJ (1994) The slow component of O2 uptake kinetics during heavy exercise. Med Sci Sports Exerc 26:1319–1326
Wiggins IM, Hartley DEH (2015) A synchrony-dependent influence of sounds on activity in visual cortex measured using functional near-infrared spectroscopy (fNIRS). PLoS One 10:e0122862. https://doi.org/10.1371/journal.pone.0122862
Wilcox RR (2017) Introduction to robust estimation and hypothesis testing. Statistics, 4th edn. Elsevier, Amsterdam
Wilcox RR, Tian TS (2011) Measuring effect size: a robust heteroscedastic approach for two or more groups. J Appl Stat 38:1359–1368. https://doi.org/10.1080/02664763.2010.498507
Woods EA, Hernandez AE, Wagner VE, Beilock SL (2014) Expert athletes activate somatosensory and motor planning regions of the brain when passively listening to familiar sports sounds. Brain Cogn 87:122–133. https://doi.org/10.1016/j.bandc.2014.03.007
Ye JC, Tak S, Jang KE, Jung J, Jang J (2009) NIRS-SPM: statistical parametric mapping for near-infrared spectroscopy. Neuroimage 44:428–447. https://doi.org/10.1016/j.neuroimage.2008.08.036
Yücel MA, Aasted CM, Petkov MP, Borsook D, Boas DA, Becerra L (2015) Specificity of hemodynamic brain responses to painful stimuli: a functional near-infrared spectroscopy study. Sci Rep 5:9469. https://doi.org/10.1038/srep09469
Zimeo Morais GA, Balardin JB, Sato JR (2018) fNIRS optodes’ location decider (fOLD): a toolbox for probe arrangement guided by brain regions-of-interest. Sci Rep 8:3341. https://doi.org/10.1038/s41598-018-21716-z
We acknowledge all participants of this study for their contribution. We also thank Martina Clauß for her organizational and technical support.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Seidel, O., Carius, D., Roediger, J. et al. Changes in neurovascular coupling during cycling exercise measured by multi-distance fNIRS: a comparison between endurance athletes and physically active controls. Exp Brain Res 237, 2957–2972 (2019). https://doi.org/10.1007/s00221-019-05646-4
- Neurovascular coupling
- Primary motor cortex