Feedforward- and motor effort-dependent increase in prefrontal oxygenation during voluntary one-armed cranking

Abstract

Key points: Some cortical areas are believed to transmit a descending signal in association with motor intention and/or effort that regulates the cardiovascular system during exercise (termed central command). However, there was no evidence for the specific cortical area responding prior to arbitrary motor execution and in proportion to the motor effort. Using a multichannel near-infrared spectroscopy system, we found that the oxygenation of the dorsolateral and ventrolateral prefrontal cortices on the right side increases in a feedforward- and motor effort-dependent manner during voluntary one-armed cranking with the right arm. This finding may suggest a role of the dorsolateral and ventrolateral prefrontal cortices in triggering off central command and may help us to understand impaired regulation of the cardiovascular system in association with lesion of the prefrontal cortex.

Abstract: Output from higher brain centres (termed central command) regulates the cardiovascular system during exercise in a feedforward- and motor effort-dependent manner. This study aimed to determine a cortical area responding prior to arbitrarily started exercise and in proportion to the effort during exercise. The oxygenation responses in the frontal and frontoparietal areas during one-armed cranking with the right arm were measured using multichannel near-infrared spectroscopy, as indexes of regional blood flow responses, in 20 subjects. The intensity of voluntary exercise was 30% and 60% of the maximal voluntary effort (MVE). At the start period of both voluntary cranking tasks, the oxygenation increased (P < 0.05) only in the lateral and dorsal part of the dorsolateral prefrontal cortex (DLPFC), ventrolateral prefrontal cortex (VLPFC) and sensorimotor cortices. Then, the oxygenation increased gradually in all cortical areas during cranking at 60% MVE, while oxygenation increased only in the frontoparietal area and some of the frontal area during cranking at 30% MVE. The rating of perceived exertion to the cranking tasks correlated (P < 0.05) with the oxygenation responses on the right side of the lateral-DLPFC (r = 0.46) and VLPFC (r = 0.48) and the frontopolar areas (r = 0.47-0.49). Motor-driven passive one-armed cranking decreased the oxygenation in most cortical areas, except the contralateral frontoparietal areas. Accordingly, the lateral-DLPFC and VLPFC on the right side would respond in a feedforward- and motor effort-dependent manner during voluntary exercise with the right arm. Afferent inputs from mechanosensitive afferents may decrease the cortical oxygenation.

Keywords: central command; dorsolateral and ventrolateral prefrontal cortices; motor effort.

Figure 1. Anatomical probe and channel locations identified by three‐dimensional digitiser and transcranial magnetic stimulation

A, anatomical location of the probes on the normalised brain surface. B, schema for anatomical channel location. The correspondence between colour‐filled channels and the cortical areas is as follows: the frontopolar area (Brodmann area (BA) 10) in blue; the lateral site of the dorsolateral prefrontal cortex (lateral‐DLPFC; BA 46) in red; the ventrolateral prefrontal cortex (i.e. the pars triangularis Broca's area, BA 45) in green; the dorsal site of the dorsolateral prefrontal cortex (dorsal‐DLPFC, BA 9) in yellow; the premotor and supplementary motor areas (PM‐SMA, BA 6) in dark blue; the primary motor cortex (BA 4) in wine red; and the somatosensory cortex (BA 1–3, 5 and 7) in orange. The data of NIRS channels in white were excluded from the data analysis because of low probability of any BA (channel 1, 4, 29 and 38) or low signal quality (channel 10 and 13). In 10 subjects, the anatomical locations of channel 23 and 26 were regarded as the arm area of the primary motor cortex, while those were regarded as the PM‐SMA in the other 10 subjects. C, representative recordings of motor evoked potentials (MEPs) of the extensor carpi radialis muscle caused by transcranial magnetic stimulation (TMS) in a subject. TMS was applied five times per site at the same intensity (×1.2 of the motor threshold) around an estimated primary motor cortex, where the greatest Oxy‐Hb response occurred during voluntary one‐armed cranking at 60% of the maximal voluntary effort. The MEPs were superimposed in each site. The MEPs were recorded at the estimated primary motor cortical site (channel 28) and the surrounding sites (1 cm apart from channel 28).

Figure 2. The developed torque and electromyogram (EMG) activity of the contracting right arm muscles during voluntary one‐armed cranking at 30% (black lines) and 60% MVE (white lines) in 20 subjects

Grey area indicates the cranking period; yellow areas indicate the early (11–20 s) and late (51–60 s) period of voluntary cranking. Each variable was sequentially calculated every 1 s. Values are means ± SD. ^*Significant difference (P < 0.05) from the value at the early period of cranking at 60% MVE. †Significant difference (P < 0.05) from the value at the early period of cranking at 30% MVE. Biceps, biceps brachii muscle; ECR, extensor carpi radialis muscle; FCR, flexor carpi radialis muscle; Triceps, triceps brachii muscle; VOL30%, voluntary one‐armed cranking at 30% MVE; VOL60%, voluntary one‐armed cranking at 60% MVE.

Figure 3. Time courses of the cardiovascular responses to voluntary one‐armed cranking at 30% (black lines) and 60% (white lines) MVE in 20 subjects

Grey area indicates the cranking period; yellow areas indicate the early and late period of voluntary cranking. Each variable was sequentially calculated every 1 s. Values are means ± SD. ^*Significant difference (P < 0.05) from the baseline. †Significant difference (P < 0.05) from the value at the early period of cranking. CO, cardiac output; HR, heart rate; MAP, mean arterial blood pressure; SV, stroke volume; TPR, total peripheral resistance.

Figure 4. Time courses of the oxygenated haemoglobin (Oxy‐Hb) responses in the frontal (A) and frontoparietal areas (B) during voluntary one‐armed cranking at 30% (black lines) and 60% MVE (white lines) in 20 subjects

Grey areas indicate the cranking period. Horizontal scatter lines indicate the baseline level. The Oxy‐Hb was sequentially calculated every 1 s and expressed as mean without SD.

Figure 5. Time courses of the Oxy‐Hb responses in the frontal (A) and frontoparietal areas (B) at the start period of voluntary one‐armed cranking at 30% (black circles) and 60% MVE (white circles) in 20 subjects

Grey areas indicate the cranking period. Horizontal scatter lines indicate the baseline level. The Oxy‐Hb responses from the baseline were analysed at the start period (from −5 to 5 s) of voluntary cranking by a one‐way repeated measures ANOVA and Holm–Sidak post hoc test. The Oxy‐Hb was expressed as mean ± SD within the start period and mean without SD outside the start period. ^*Significant difference (P < 0.05) from the baseline of cranking at 60% MVE. †Significant difference (P < 0.05) from the baseline of cranking at 30% MVE.

Figure 6. The Oxy‐Hb responses in the frontal (A) and frontoparietal areas (B) at the early and late period of voluntary one‐armed cranking at 30% (black circles) and 60% MVE (white circles) in 20 subjects

Values are means ± SD. ^*Significant difference (P < 0.05) from the baseline. †Significant difference (P < 0.05) from the value at the early period of cranking.

Figure 7. Time courses of the Oxy‐Hb responses in the frontal (A) and frontoparietal areas (B) during passive one‐armed cranking in 20 subjects

Grey areas indicate the cranking period. Horizontal scatter lines indicate the baseline level. The Oxy‐Hb was sequentially calculated every 1 s and expressed as mean without SD.

Figure 8. The Oxy‐Hb responses in the frontal (A) and frontoparietal areas (B) at the early and late period of passive one‐armed cranking in 20 subjects

In the frontopolar area and the dorsal‐DLPFC, each part (right, middle and left) of the cortical areas is indicated in white, grey and black triangle, respectively. Values are means ± SD. ^*Significant difference (P < 0.05) from the baseline in the left cortical areas. †Significant difference (P < 0.05) from the baseline in the right cortical areas. #Significant difference (P < 0.05) from the baseline in the middle cortical areas.

Figure 9. Forehead skin blood flow responses during voluntary and passive one‐armed cranking

A, the individual forehead skin blood flow responses on the right side during voluntary and passive one‐armed cranking in 8 subjects. B, the average forehead skin blood flow response at the start period of voluntary one‐armed cranking at 30% (black circles) and 60% MVE (white circles) in 8 subjects. ^*Significant difference (P < 0.05) from the baseline of cranking at 60% MVE. †Significant difference (P < 0.05) from the baseline of cranking at 30% MVE. C, the relationship between the skin blood flow response and the Oxy‐Hb response of the lateral‐DLPFC on the right side or the RPE with a sample size of 16 (8 subjects × 2 exercise intensities (30% and 60% MVE)). N.S., not significant (P > 0.05).

Figure 10. Regional difference of cortical oxygenation responses during voluntary and passive one‐armed cranking

A, time courses of the individual Oxy‐Hb responses of the lateral‐DLPFC on the right side and the left primary motor cortex during voluntary and passive one‐armed cranking in 20 subjects. B, time courses of the average Oxy‐Hb responses in the lateral‐DLPFC and the primary motor and somatosensory cortices during voluntary one‐armed cranking at 30% (white lines) and 60% MVE (red lines) and during passive one‐armed cranking (black lines) in 20 subjects. Grey areas indicate the cranking period. Horizontal scatter lines indicate the baseline level. The Oxy‐Hb responses was sequentially calculated every 1 s. Values are means ± SEM for data visibility.