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Table 4 The design of fMRI task and key findings

From: Characterizing the supraspinal sensorimotor control of walking using MRI-compatible system: a systematic review

Studies

Country

Study population

fMRI test

Task blocks

Key findings for brain activation

(Hao et al., 2013) [20]

China

7 healthy participants aged 23–27(4 M/3F)

Supraspinal activation in response to foot sole stimulation.

Three repetitions of 30s stimulation applied to a circular area 4 cm of the right foot sole.

Significant activation contralaterally within the S1, S2 and M1, and bilaterally within the S2 during single-point sinusoidal stimulation were observed.

(Zhang et al., 2019) [21]

China

9 healthy participants aged 20–29

Supraspinal activation in response to foot sole stimulation.

A block-designed 3.5-min stimulation protocol consisting of alternating blocks of 30 s-Rest and 30s-Stim.

Significant activation within the SMA, supramarginal gyrus, paracingulate gyri, INS, precentral gyrus, middle temporal gyrus, and hippocampus during stimulation that mimic walking were observed.

(Kremneva et al., 2012) [22]

Russia

12 healthy participants aged 22–42(6 M/6F; A = 28.8)

Supraspinal activation during mechanical stimulation of plantar support zones in different modes (i.e., standing simulation and slow walking simulation modes).

Two tasks (simulation of standing or slow walking). Alternating rest and stimulation for 3 times, for a total of 3 min 53s each task.

Significant activation in the S1, PMC, dlPFC and INS during mechanical stimulation of the plantar support zones were observed. The involvement of the PFC during simulation of standing and a broad involvement of the S1 and S2 during simulation of slow walking were found.

(Labriffe et al., 2017) [23]

France

18 healthy participants aged 20–40(11 M/7F; A = 27 ± 4.7)

Supraspinal activation under three conditions: gait imagination task, organized (“gait like”) and chaotic sequences of plantar stimulations.

Three sessions, each with two consecutive conditions (rest and stimulation). Each condition was performed for 19s and repeated nine times, for a total session duration of 5 min 41s.

Mechanical plantar stimulation activated M1 and S2 bilaterally. The common patterns of activation between mental imagery and gait-like plantar stimulation were observed, specifically in SMA-proper bilaterally and right pre-SMA. There was no difference between the organized and chaotic patterns of stimulation.

(Jeanvoine et al., 2022) [24]

France

67 healthy participants aged 20–77(32 M/35F; A = 49.2 ± 18.0)

Supraspinal activation under two conditions: organized (“gait like”) and chaotic sequences of plantar stimulations.

Two sessions, each with two consecutive conditions (rest and stimulation). Each condition was performed for 19s and repeated nine times, for a total session duration of 5 min and 42s.

Brain areas (pre-SMA, mid-DLFPC,V1) involved in age-related changes in somatosensory processing of gait.

(Trinastic et al., 2010) [25]

USA

8 intact adults aged 25–57 (6 M/2F; A = 31.5)

The difference in supraspinal activation between active ankle dorsiflexion and plantarflexion.

Fifteen sets of stimuli, each with two active ankle dorsiflexion and two active plantarflexion, for a duration of 288.1s.

Ankle dorsiflexion and plantarflexion may be controlled by both shared and independent neural circuitry.

(Noble et al., 2014) [26]

British

11 participants with normal vision aged 19–34(4 M /7F)

Supraspinal activation under five conditions: R15-ONLY; L15-ONLY; BILAT15; R30-ONLY; L30-ONLY.

Four conditions in random order with 10-16s rest, each condition plantar flexion 3 times for 5s.

Greater levels of activation during bilateral exertions may arise from interhemispheric inhibition, as well as from the greater need for motor coordination and visual processing.

(Belforte et al., 2010) [27]

Italy

one healthy participant

Supraspinal activation in response to active and passive foot movement.

Alternating plantarflexion/dorsiflexion and rest for 12s each, for a total of 6.6 min.

Both active and passive movement induced activation in S1/M1 and SMA, and active movements uniquely induced activation in thalamic, frontal and cingulated regions, while passive movements induced activation in temporal and parietal areas.

(Belforte et al., 2012) [28]

Italy

around 10 healthy participants

Supraspinal activation in response to active and passive foot movement.

Alternating plantarflexion/dorsiflexion and rest for 12s each, for a total of 6.6 min.

Both active and passive movement induced activation in S1/M1 and SMA, and active movements uniquely induced activation in thalamic, frontal and cingulated regions, while passive movements induced activation in temporal and parietal areas.

(Doolittle et al., 2021) [29]

USA

20 healthy participants aged 21–37 (12 M/8F; A = 26)

Supraspinal activation during unipedal and bipedal movement.

Two repetitions of four blocks of dorsiflexion-plantarflexion (right only, left only, both, and rest), for 20s each.

No significant difference in the BOLD signal between unipedal and bipedal motion in the ROI explored were observed.

(Mehta et al., 2009) [31]

USA

10 healthy participants aged 21–53 (6 M/4F; A = 31)

Supraspinal activation in response to pedaling at a rate of 30 RPM.

A single run consisted of 30s of pedaling and 30s of rest alternated 4 times.

Consistent with previous literature, the medial S1 and M1, PMA, SMA and Cb are involved in pedaling.

(Mehta et al., 2012) [32]

USA

10 healthy participants aged 21–53 (6 M/4F; A = 31)

Supraspinal activation during slow (30 RPM), fast (60 RPM), passive (30 RPM), and variable rate pedaling.

A block design consisted of 3 runs. Each run consisted of 4 repetitions of pedaling for 30s and resting for 30s.

Significant activity in M1, S1, SMA, and Cb during pedaling that increased with increasing pedaling rate and complexity. Similar levels of cortical and Cb activity were present during active and passive pedaling.

(Promjunyakul et al., 2015) [33]

USA

14 stroke (5 M/9F; M = 54.5 ± 12.3) and 12 control participants (6 M/6F; A = 53.4 ± 13.1)

Supraspinal activation in response to pedaling in individuals with stroke and age-matched controls.

A single run consisted of 30s of pedaling and 30s of rest alternated 4 times.

Brain activation volume in BA6 and Cb during pedaling was reduced in people post-stroke, as compared to age-matched controls.

(Newton et al., 2008) [30]

USA

9 healthy participants aged 21–58 (4 M/5F; Median = 39)

Supraspinal activation of three isolated lower limb isometric contractions: ankle dorsiflexion, ankle plantarflexion and knee extension.

Four blocks of cued contractions (each 32s in length), interleaved with five rest periods of 28s duration.

Significant BOLD signal increases were observed in L.SM1 in the paracentral lobule and in M2 for ankle dorsiflexion, ankle plantarflexion and knee extension. Within these areas there was substantial overlap of the motor representations though differential activation was observed in SM1, with greater activation of inferior paracentral lobule during knee extension than for either ankle task.

(Martínez et al., 2014) [34]

Spain

19 participants (10 M/9F; A = 33 ± 5)

Supraspinal activation in response to stepping while selecting subject’s individual comfortable amplitude.

Twelve repetitions of 10-s blocks of voluntary alternating strides of the lower limbs and 30-s blocks of rest with a total duration of 8 min.

Stepping generates extensive bilateral activations in several cortical and subcortical brain regions know to be related to motor execution and motor control.

(Martínez et al., 2016) [35]

Spain

19 healthy participants aged 25–42 (10 M/9F; A = 33.29 ± 5.8)

Supraspinal activation in response to stepping at different paces (0.8, 1.2 or 1.75 steps per second).

Two runs, each run consisted of 18 motor blocks (six repetitions by condition) of 10s duration and the corresponding resting of 30s with a total duration of 12 min.

Brain activity patterns showed similar BOLD responses across pace conditions though significant differences were observed in parietal and cerebellar regions.

(Toyomura et al., 2018) [36]

Japan

20 healthy participants aged 20–23 (14 M/6F; A = 21.9)

Supraspinal activation in response to lower-limb movement in three speed conditions (slow, medium, fast).

Brain activity patterns showed similar BOLD responses across pace conditions though significant differences were observed in parietal and cerebellar regions.

The post/pre-central gyrus and Cb showed significant activity during the movements.

(Hollnagel et al., 2011) [37]

Switzerland

one participant aged 30 (M)

Supraspinal activation of the single subject during all nine tasks (e.g., alternating passive stepping at 0.5 Hz).

Nine movement paradigm, each executed 30 times for 10s (five steps for 0.5 Hz), interleaved by 5s rest.

The more “uncommon” the motor task and the more “active” and “challenged” the subject was, the more activity was elicited within the sensorimotor brain areas.

(Hollnagel et al., 2013) [38]

Switzerland

13 healthy participants aged 22–32 (3 F/10 M)

Supraspinal activation during each training mode (active, passive and assist-as-needed stepping).

Three modes, each with 9 trails. Each trial consisted of 30s moving followed by 10s rest.

Active stepping elicited significant activation in an extensive sensorimotor network including medial M1 and L.PMC as well as activation in the Vermis and R.Cb. Passive stepping elicited activation in medial M1 and PMA in the left cerebral hemisphere but not the Cb. Stepping with assist-as-needed led to significant activations in the L.SM1 and bilaterally in the superior parietal lobe.

(Jaeger et al., 2014) [39]

Switzerland

24 healthy right-handed and-footed participants (16 M/8F; A = 27 ± 4)

Supraspinal activation in response to active and passive, bilateral, periodic, multi-joint, lower limb motor control.

Two runs, each with 15 trials of movement, each trial duration was 10s.

Active and passive stepping engaged several cortical and subcortical areas of the sensorimotor network, with higher relative activation of those areas during active movement.

(Jaeger et al., 2015) [40]

Switzerland

24 healthy right-handed and-footed participants (16 M/8F; A = 27 ± 4)

Supraspinal activation in response to repeated active and passive stepping movements.

Two runs, each with 15 blocks of movement, interleaved with 15 blocks of a control condition. Each block lasted 10s and was followed by 9.075s of image acquisition.

Activations during passive movements are less robust over repeated measurement sessions than those during active movements despite lower variability of motor performance during passive movements.

(Jaeger et al., 2016) [41]

Switzerland

16 healthy participants

Supraspinal activation during active and passive stepping across simulated ground reaction forces (0, 20, and 40% of individual body weight).

A block design consisted of 6 runs in random order. Each run consisted of 15 blocks of movement, and 15 blocks of a control condition. Each block lasted 10s and was followed by 9.075s of image acquisition.

A significant modulation of brain activation in sensorimotor areas by the load level could neither be demonstrated during active nor during passive stepping.

(Takahiro et al., 2011) [42]

Japan

one participant

Supraspinal activation during the subject moved the lower extremities voluntarily with or without wearing LOMS.

Four repetitions of 25s rest and 25s gait-like motion.

Activations in the M1, SMA and Cb during flexion and extension of lower extremities were observed.

(Ikeda et al., 2012) [43]

Japan

10 healthy participants aged 20

Supraspinal activation in response to gait-like movement with or without floor reactive force.

Eight repetitions of 30s rest and 36s task.

Activation with floor reactive force at the motor cortex was different from the activation without floor reactive force and, any region of the brain proper to floor reactive force was observed.

(Takahiro et al., 2013) [44]

Japan

one health participant aged 20

Supraspinal activation during active and passive gait-like movement simulated by LOMS.

Four repetitions of 30s rest and 36s motion.

Brain activation area in sensory area during passive gait-like motion was broader than one during active gait-like motion.

(Ikeda et al., 2015) [45]

Japan

13 healthy participants aged 20

Supraspinal activation in response to gait-like motion.

Four repetitions of 25s rest and 25s gait-like motion.

Activated regions are the medial M1 and the medial S1 which are related to gait motion.

  1. AbbreviationBra.Di.P.O., brain discovery pneumatic orthosis; RPM, Revolutions Per Minute; pseudogait-MRCD, pseudogait-magnetic resonance compatible device; MARCOS, magnetic resonance compatible stepper; LOMS, lower-extremity motion simulator; M, man; F, female; A, average; R15-ONLY, right foot at 15% of maximal voluntary contraction (MVC); L15-ONLY, left foot at 15% of MVC; BILAT15, with both feet simultaneously with each foot at 15% MVC; R30-ONLY, right foot at 30% of MVC; L30-ONLY, left foot at 30% of MVC; RPM, Revolutions Per Minute; A, anterior; L, left; R, right; S1, primary somatosensory cortex; M1, primary motor cortex; S2, secondary somatosensory cortex; SMA, supplementary motor area; INS, insula; PMC, premotor cortex; dlPFC, dorsolateral and prefrontal cortices; V1, primary visual areas; PCUN, precuneus; Cb, cerebellum; ROI, regions of interest; BA6, Brodmann’s area 6; BOLD, blood oxygen level dependent; SM1, primary sensorimotor cortex; M2, secondary motor cortex