Changes in neurovascular coupling during cycling exercise measured by multi-distance fNIRS: a comparison between endurance athletes and physically active controls

Abstract

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.

Keywords: Athletes; Cycling; Neurovascular coupling; Primary motor cortex; fNIRS.

Fig. 1

Study design and experimental setup. a Procedures for session 1 and 2. The first session consisted of an incremental cycling test (ICT) starting with a 5 min warm-up phase using a constant load of 50 W. Until voluntary exhaustion, participants pedaled continuously with a pedaling frequency of 60–80 revolutions per minute (rpm) during 30-s levels, with each level providing an increment of 15 W in resistance. Using peak power output (PPO), three individual intensity levels of 20, 40, and 60% of PPO were derived that were cycled multiple times during session 2 [multi-intensity cycling test (MICT)]. During MICT, participants cycled 5 trials of 30 s each, followed by a 30-s phase of rest after each activity phase. b Illustration of fNIRS configuration used during MICT. Transmitters are shown as red dots and detectors as blue dots. Yellow dots represent the centers of the 22 long (standard) channels. Additionally, eight short-distance detectors (not included in the figure) for each source with an inter-optode distance of 8 mm were used, as opposed to the inter-optode distance for all other (long) channels of our configuration (3 cm)

Fig. 2

ICT and MICT results. a Peak values of power output (PPO), oxygen consumption volume (VO₂max) and heart rate (HRmax) as assessed by incremental cycling test (ICT). Values are mean ± SD; dark gray dots represent endurance athletes (EA), and light gray dots represent active control participants (ACP). *p < 0.5 indicates significantly better PPO and VO₂max values for EA as compared to ACP. b Relative values of VO₂ and HR during multi-intensity cycling test (MICT). Values are mean ± SD; dark gray lines represent EA, and light gray lines represent ACP. All values of VO₂ and HR are normalized to peak values (= 100%) as assessed by ICT. Black frames represent PPO as assessed by ICT and three individual intensity levels of 20, 40, and 60% of PPO that were cycled multiple times during MICT

Fig. 3

Intensity effect on fNIRS signal during MICT after short-separation regression (SSR). Boxplots represent all participants (EA and ACP). Values are median and interquartile range (being the 25th and 75th percentile). Channels (centered between transmitters and detectors) are shown for the topographic image (L left hemisphere, R right hemisphere); colors represent f values. Images are thresholded at p < 0.05 and FDR-corrected for multiple comparisons. *p < 0.5 indicates a significant influence of factor condition on HHb concentration (F_(2,80) = 18.049, p_adjusted = 0.001, ξ = 0.382), indicating a larger HHb decrease across all participants at an intensity of 60% as compared to 20% (p_adjusted < 0.000) in left premotor cortex (PMC)

Fig. 4

Hemodynamic response alterations during MICT. Channels (centered between transmitters and detectors) are shown for each image (L left hemisphere, R right hemisphere). Decreases are illustrated in dark blue and increases in dark red; colors represent t-values. All images are thresholded at p < 0.05 and FDR-corrected for multiple comparisons. Topographic images show significant decreases of both Hb and HHb. a Within-group comparisons for Hb and HHb. Comparisons were performed using robust dependent t tests testing activity phases (20, 40, and 60% of PPO) of endurance athletes (EA) and active control participants (ACP) against zero revealing significant decreases of Hb and HHb in both groups. b Effect of short-separation regression (SSR). Tests were performed before and after SSR to compare the effect of short-distance channels. The image illustrates the deltas between alterations in brain activation before and after SSR, indicating extra-cerebral signals and systemic interferences that were regressed out of the long-distance channels by SSR

Fig. 5

Correlation analysis between intensity-dependent HHb alterations and VO₂ changes at 20% of PPO. Scatter plots for all participants (EA and ACP) show significant negative associations within bilateral superior parietal lobe for HHb in two channels (r = − 0.542, p_adjusted = 0.001 and r = − 0.506, p_adjusted = 0.004). ΔHHb and ΔVO₂ are the differences between activity at 20% of PPO and the previous resting phase. fNIRS configuration on the right shows the channels of the significant negative associations (black circles). Transmitters are shown as red dots and detectors as blue dots. Yellow dots represent the centers of the 22 long (standard) channels