Regional difference in prefrontal oxygenation before and during overground walking in humans: a wearable multichannel NIRS study.

Using wireless multichannel near-infrared spectroscopy, regional difference in cortical activity over the prefrontal cortex (PFC) was examined before and during overground walking and in response to changes in speed and cognitive demand. Oxygenated-hemoglobin concentration (Oxy-Hb) as index of cortical activity in ventrolateral PFC (VLPFC), dorsolateral PFC (DLPFC), and frontopolar cortex (FPC) was measured in 14 subjects, whereas heart rate was measured as estimation of exercise intensity in six subjects. The impact of mental imagery on prefrontal Oxy-Hb was also explored. On both sides, Oxy-Hb in VLPFC, DLPFC, and lateral FPC was increased before the onset of normal-speed walking, whereas Oxy-Hb in medial FPC did not respond before walking onset. During the walking, Oxy-Hb further increased in bilateral VLPFC, whereas Oxy-Hb was decreased in DLPFC and lateral and medial FPC. Increasing walking speed did not alter the increase in Oxy-Hb in VLPFC but counteracted the decrease in Oxy-Hb in DLPFC (but not in lateral and medial FPC). Treadmill running evoked a greater Oxy-Hb increase in DLPFC (n = 5 subjects). Furthermore, increasing cognitive demand during walking, by deprivation of visual feedback, counteracted the decrease in Oxy-Hb in DLPFC and lateral and medial FPC, but it did not affect the increase in Oxy-Hb in VLPFC. Taken together, the profound and localized Oxy-Hb increase is a unique response for the VLPFC. The regional heterogeneity of the prefrontal Oxy-Hb responses to natural overground walking was accentuated by increasing walking speed or cognitive demand, suggesting functional distinction within the PFC.

Increased prefrontal oxygenation prior to and at the onset of over-ground locomotion in humans.

Our laboratory has reported with near-infrared spectroscopy (NIRS) that prefrontal oxygenated-hemoglobin concentration (Oxy-Hb), measured as index of regional cerebral blood flow, increased before and at the onset of arbitrary (i.e., noncued) ergometer exercise in a laboratory environment. In the current study, we hypothesized that naturally occurring over-ground locomotion, despite "very light" motor effort, as indicated by a Borg scale of 8.0 ± 0.3, likewise causes preexercise activation of the prefrontal cortex. Using wireless NIRS, we examined in this study how early and to what extent prefrontal activity changed before the onset of arbitrary walking in 13 subjects. Prefrontal Oxy-Hb increased 2 s before the onset of arbitrary walking, and the increased Oxy-Hb reached a peak at 5 s from walking onset. The preexercise and initial increase in prefrontal Oxy-Hb was absent when over-ground walking was forced to start by cue. The difference in the Oxy-Hb response between arbitrary and cued start, which was considered to be related to central command, became significant 2 s before walking onset, preceding the difference in the heart rate (HR) response by 8 s. This demonstrated a positive relationship with the HR difference in 69% of subjects. Imagery of arbitrary walking was, likewise, able to increase prefrontal oxygenation to the same extent as actual walking. Thus, it is likely that prefrontal oxygenation increases before the onset of naturally occurring walking in daily life, despite "very light" effort. The increased prefrontal oxygenation may contribute at least partly to cardiac adjustment, synchronized with the beginning of motor performance.NEW & NOTEWORTHY We found using wireless near-infrared spectroscopy that prefrontal oxygenation increased before the onset of arbitrary over-ground walking, whereas the preexercise increase was absent when walking was suddenly started by cue. The difference in prefrontal oxygenation between start modes (considered related to central command) preceded heart rate response variances and demonstrated a positive relationship with the difference in heart rate. The central command-related prefrontal activity may contribute to cardiac adjustment, synchronized with the beginning of over-ground walking.

Increased oxygenation in the non-contracting forearm muscle during contralateral skilful hand movement.

NEW FINDINGS: What is the central question of this study? When performing skilful hand movement, motor command descends especially towards distal arm muscles. Does central command evoke a vascular response selectively in the distal arm muscles during skilful hand movement? What is the main finding and its importance? We found, using near-infrared spectroscopy, that unilateral skilful hand movement evoked a greater increase in oxygenation of the contralateral forearm muscle compared with that of the upper arm muscles. Mental imagery of the hand movement also increased oxygenation of the forearm muscle. These findings suggest that central command might contribute to the vasodilator response in the non-contracting forearm muscle during contralateral skilful hand movement. ABSTRACT: The human hand is a special organ to perform skilful movement in daily life. To meet metabolic demands of the working distal arm muscles, central command might evoke neurogenic vasodilatation in the muscles. Based on our previous demonstration that a centrally generated vasodilator signal is transmitted bilaterally to skeletal muscles during exercise, centrally induced vasodilatation might occur in the non-contracting distal arm muscles during contralateral skilful hand movement. To examine this possibility, we used near-infrared spectroscopy to measure the relative concentrations of oxygenated haemoglobin (Oxy-Hb; as an index of regional blood flow) in the non-contracting arm muscles during skilful hand movement (two-ball rotation) in 22 subjects. Two-ball rotation increased Oxy-Hb of both forearm and upper arm muscles, with little changes in perfusion pressure and cardiac output. The increased Oxy-Hb was greater in the forearm muscle than in the upper arm muscles. The increased Oxy-Hb of the forearm muscle during two-ball rotation was greater than that during one-armed cranking performed with no load. Mental imagery of two-ball rotation increased Oxy-Hb of the forearm and biceps muscles. The increases in Oxy-Hb of both forearm and upper arm muscles during two-ball rotation were reduced by decreasing the level of task difficulty. Intravenous administration of atropine attenuated the increases in Oxy-Hb of the arm muscles during two-ball rotation. It is likely that contralateral skilful hand movement evokes a selective increase in Oxy-Hb of the non-contracting forearm muscle via a sympathetic cholinergic mechanism and that the increase in oxygenation might be mediated, at least in part, by central command.

Central command increases muscular oxygenation of the non-exercising arm at the early period of voluntary one-armed cranking.

This study aimed to examine whether central command increases oxygenation in non-contracting arm muscles during contralateral one-armed cranking and whether the oxygenation response caused by central command differs among skeletal muscles of the non-exercising upper limb. In 13 male subjects, the relative changes in oxygenated-hemoglobin concentration (Oxy-Hb) of the non-contracting arm muscles [the anterior deltoid, triceps brachii, biceps brachii, and extensor carpi radialis (ECR)] were measured during voluntary one-armed cranking (intensity, 35-40% of maximal voluntary effort) and mental imagery of the one-armed exercise for 1 min. Voluntary one-armed cranking increased (P < 0.05) the Oxy-Hb of the triceps, biceps, and ECR muscles to the same extent (15 ± 4% of the baseline level, 17 ± 5%, and 16 ± 4%, respectively). The greatest increase in the Oxy-Hb was observed in the deltoid muscle. Intravenous injection of atropine (10-15 µg/kg) and/or propranolol (0.1 mg/kg) revealed that the increased Oxy-Hb of the arm muscles consisted of the rapid atropine-sensitive and delayed propranolol-sensitive components. Mental imagery of the exercise increased the Oxy-Hb of the arm muscles. Motor-driven passive one-armed cranking had little influence on the Oxy-Hb of the arm muscles. It is likely that central command plays a role in the initial increase in oxygenation in the non-contracting arm muscles via sympathetic cholinergic vasodilatation at the early period of one-armed cranking. The centrally induced increase in oxygenation may not be different among the distal arm muscles but may augment in the deltoid muscle.

The prefrontal oxygenation and ventilatory responses at start of one-legged cycling exercise have relation to central command.

When performing exercise arbitrarily, activation of central command should start before the onset of exercise, but when exercise is forced to start with cue, activation of central command should be delayed. We examined whether the in-advance activation of central command influenced the ventilatory response and reflected in the prefrontal oxygenation, by comparing the responses during exercise with arbitrary and cued start. The breath-by-breath respiratory variables and the prefrontal oxygenated-hemoglobin concentration (Oxy-Hb) were measured during one-legged cycling. Minute ventilation (V̇e) at the onset of arbitrary one-legged cycling was augmented to a greater extent than cued cycling, while end-tidal carbon dioxide tension (ETco2) decreased irrespective of arbitrary or cued start. Symmetric increase in the bilateral prefrontal Oxy-Hb occurred before and at the onset of arbitrary one-legged cycling, whereas such an increase was absent with cued start. The time course and magnitude of the increased prefrontal oxygenation were not influenced by the extent of subjective rating of perceived exertion and were the same as those of the prefrontal oxygenation during two-legged cycling previously reported. Mental imagery or passive performance of the one-legged cycling increased V̇e and decreased ETco2 Neither intervention, however, augmented the prefrontal Oxy-Hb. The changes in ETco2 could not explain the prefrontal oxygenation response during voluntary or passive one-legged cycling. Taken together, it is likely that the in-advance activation of central command influenced the ventilatory response by enhancing minute ventilation at the onset of one-legged cycling exercise and reflected in the preexercise increase in the prefrontal oxygenation.

Differential contribution of ACh-muscarinic and ß-adrenergic receptors to vasodilatation in noncontracting muscle during voluntary one-legged exercise.

We have demonstrated the centrally induced cholinergic vasodilatation in skeletal muscle at the early period of voluntary one-legged exercise and during motor imagery in humans. The purpose of this study was to examine whether central command may also cause ß-adrenergic vasodilatation during the exercise and motor imagery. Relative changes in oxygenated hemoglobin concentration (Oxy-Hb) of bilateral vastus lateralis (VL) muscles, as index of tissue blood flow, and femoral blood flow to nonexercising limb were measured during one-legged cycling and mental imagery of the exercise for 1 min before and after propranolol (0.1 mg/kg iv). The Oxy-Hb of noncontracting muscle increased (P < 0.05) at the early period of exercise and the increase was sustained throughout exercise, whereas the Oxy-Hb of contracting muscle increased at the early period but thereafter decreased. We subtracted the Oxy-Hb response with propranolol from the control response in individual subjects to identify the propranolol-sensitive component of the Oxy-Hb response during exercise. In both noncontracting and contracting VL muscles, the increase in Oxy-Hb at the early period of one-legged exercise did not involve a significant propranolol-sensitive component. However, as the exercise proceeded, the propranolol-sensitive component of the Oxy-Hb response was developed during the later period of exercise. Propranolol also failed to affect the initial increases in femoral blood flow and vascular conductance of nonexercising leg but significantly attenuated (P < 0.05) their later increases during exercise. Subsequent atropine (10-15 µg/kg iv) abolished the initial increases in Oxy-Hb of both VL muscles. Mental imagery of the one-legged exercise caused the bilateral increases in Oxy-Hb, which were not altered by propranolol but abolished by subsequent atropine. It is likely that the rapid cholinergic and delayed ß-adrenergic vasodilator mechanisms cooperate to increase muscle blood flow during exercise.

Evidence for centrally induced cholinergic vasodilatation in skeletal muscle during voluntary one-legged cycling and motor imagery in humans.

We have recently reported that central command contributes to increased blood flow in both noncontracting and contracting vastus lateralis (VL) muscles at the early period of voluntary one-legged cycling. The purpose of this study was to examine whether sympathetic cholinergic vasodilatation mediates the increases in blood flows of both muscles during one-legged exercise. Following intravenous administration of atropine (10 µg/kg), eight subjects performed voluntary 1-min one-legged cycling (at 35% of maximal voluntary effort) and mental imagery of the exercise. The relative concentrations of oxygenated- and deoxygenated-hemoglobin (Oxy- and Deoxy-Hb) in the bilateral VL were measured as an index of muscle tissue blood flow with near-infrared spectroscopy (NIRS). The Oxy-Hb in both noncontracting and contracting VL increased at the early period of one-legged cycling, whereas the Deoxy-Hb did not alter at that period. Atropine blunted (P < 0.05) the Oxy-Hb responses of both VL muscles but did not affect the Deoxy-Hb responses. The time course and magnitude of the atropine-sensitive component in the Oxy-Hb response were quite similar between the noncontracting and contracting VL muscles. With no changes in the Deoxy-Hb and hemodynamics, imagery of one-legged cycling induced the bilateral increases in the Oxy-Hb, which were completely abolished by atropine. In contrast, imagery of a circle (with no relation to exercise) did not alter the NIRS signals, irrespective of the presence or absence of atropine. It is concluded that central command evokes cholinergic vasodilatation equally in bilateral VL muscles during voluntary one-legged cycling and motor imagery.