Dissociated coupling between cerebral oxygen metabolism and perfusion in the prefrontal cortex during exercise: a NIRS study

Abstract

Purpose: The present study used near-infrared spectroscopy to investigate the relationships between cerebral oxygen metabolism and perfusion in the prefrontal cortex (PFC) during exercises of different intensities. Methods: A total of 12 recreationally active men (age 24 ± 6 years) were enrolled. They performed 17 min of low-intensity exercise (ExL), followed by 3 min of moderate-intensity exercise (ExM) at constant loads. Exercise intensities for ExL and ExM corresponded to 30% and 45% of the participants' heart rate reserve, respectively. Cardiovascular and respiratory parameters were measured. We used near-infrared time-resolved spectroscopy (TRS) to measure the cerebral hemoglobin oxygen saturation (ScO₂) and total hemoglobin concentration ([HbT]), which can indicate the cerebral blood volume (CBV). As the cerebral metabolic rate for oxygen (CMRO₂) is calculated using cerebral blood flow (CBF) and ScO₂, we assumed a constant power law relationship between CBF and CBV based on investigations by positron emission tomography (PET). We estimated the relative changes in CMRO₂ (rCMRO₂) and CBV (rCBV) from the baseline. During ExL and ExM, the rate of perceived exertion was monitored, and alterations in the subjects' mood induced by exercise were evaluated using the Profile of Moods Scale-Brief. Results: Three minutes after exercise initiation, ScO₂ decreased and rCMRO₂ surpassed rCBV in the left PFC. When ExL changed to ExM, cardiovascular variables and the sense of effort increased concomitantly with an increase in [HbT] but not in ScO₂, and the relationship between rCMRO₂ and rCBV was dissociated in both sides of the PFC. Immediately after ExM, [HbT], and ScO₂ increased, and the disassociation between rCMRO2 and rCBV was prominent in both sides of the PFC. While blood pressure decreased and a negative mood state was less prominent following ExM compared with that at rest, ScO₂ decreased 15 min after exercise and rCMRO₂ surpassed rCBV in the left PFC. Conclusion: Dissociated coupling between cerebral oxidative metabolism and perfusion in the PFC was consistent with the effort required for increased exercise intensity and associated with post-exercise hypotension and altered mood status after exercise. Our result demonstrates the first preliminary results dealing with the coupling between cerebral oxidative metabolism and perfusion in the PFC using TRS.

Keywords: cerebral blood flow; cerebral blood volume; cerebral metabolic rate for oxygen; cerebral oxygenation; exercise intensity; mood status; postexercise hypotension.

FIGURE 1

Experimental protocol used for the acquisition of cerebral oxygenation by NIRS during and after a 20-min constant load cycling protocol, comprising 17 min of low-intensity and 3 min of moderate-intensity exercise. The time of exercise initiation was defined as time 0. HRR: heart rate reserve; NIRS: near-infrared spectroscopy; TRS: near-infrared time-resolved spectroscopy.

FIGURE 2

Typical changes for two participants (left and right) in the heart rate and cerebral oxygenation variables obtained by NIRS for the prefrontal cortex during and after the 20-min constant-load cycling protocol, comprising 17 min of low-intensity and 3 min of moderate-intensity exercise. Data were averaged over 15 s at each time point. Changes in ScO₂ for the left (red) and right (brown) PFC and HbT for the left (green) and right (blue) prefrontal cortex are depicted. The thick bars below the NIRS parameter changes indicate the periods of the exercise session of low (gray) and moderate intensity (black). ScO₂: cerebral hemoglobin oxygen saturation; HbT: total hemoglobin concentration in the brain tissue; NIRS: near-infrared spectroscopy.

FIGURE 3

Respiratory variables (A) and cerebral oxygenation variables obtained by near-infrared spectroscopy for the prefrontal cortex (B) during and after the 20-min constant-load cycling protocol, comprising 17 min of low-intensity and 3 min of moderate-intensity exercise. Data were averaged over 15 s at each time point. $\dot{V}$ O₂: pulmonary oxygen consumption; P_ETCO₂: end-tidal carbon dioxide; ScO₂: cerebral hemoglobin oxygen saturation; HbT: total hemoglobin concentration in the brain tissue; Lt: left; Rt: right. Significant difference compared to the baseline: *p < 0.05. Significant difference compared to the end of light-intensity exercise (17 min); §p < 0.05. Statistical differences between each time point evaluated using one-way analysis of variance for repeated measures and Turkey’s post hoc multiple comparison test.

FIGURE 4

Changes in mood ratings for fatigue and confusion and ScO₂ for the left prefrontal cortex. Data were derived from all of the participants (n = 12) and expressed as the mean ± standard error of the mean. Lt: left; PreEx: before the exercise started; PostEx: after the exercise terminated.

FIGURE 5

Relative changes from the baseline in the right and left prefrontal in the cerebral metabolic rate for oxygen and cerebral blood volume (upper), in the cerebral metabolic rate for oxygen and cerebral blood flow (middle), and in the cerebral blood flow and oxygen extraction fraction (lower) during and after the 20-min constant-load cycling protocol, comprising 17 min of low-intensity and 3 min of moderate-intensity exercise. Data were averaged over 15s at each time point and expressed as the mean ± standard error of the mean. rCMRO₂: relative changes from the baseline in the cerebral metabolic rate for oxygen; rCBV: relative changes from the baseline in the cerebral blood volume; rCBF: the relative changes from the baseline in cerebral blood flow; rOEF: the relative changes from the baseline in the oxygen extract fraction; Lt: left; Rt: right; rest: baseline; Ex3, Ex13, and Ex20: 3, 13, and 20 min after exercise initiation, respectively; Post1, Post2, Post3, and Post15: 1, 2, 3, and 15 min after exercise termination, respectively, difference between rCMRO₂ and rCBV, rCMRO₂ and rCBF, and rCBF and rOEF at each time point; **p < 0.05, ***p < 0.001, and ****p < 0.0001; Sidak’s multiple comparison test.