Human Brain Activation During Sustained and Intermittent Submaximal Fatigue Muscle Contractions: An fMRI Study

Abstract

During prolonged submaximal muscle contractions, electromyographic (EMG) signals typically increase as a result of increasing motor unit activities to compensate for fatigue-induced force loss in the muscle. It is thought that cortical signals driving the muscle to higher activation levels also increases, but this has never been experimentally demonstrated. The purpose of this study was to quantify brain activation during submaximal fatigue muscle contractions using functional magnetic resonance imaging (fMRI). Twelve volunteers performed a sustained handgrip contraction for 225 s and 320 intermittent handgrip contractions ( approximately 960 s) at 30% maximal level while their brain was imaged. For the sustained contraction, EMG signals of the finger flexor muscles increased linearly while the target force was maintained. The fMRI-measured cortical activities in the contralateral sensorimotor cortex increased sharply during the first 150 s, then plateaued during the last 75 s. For the intermittent contractions, the EMG signals increased during the first 660 s and then began to decline, while the handgrip force also showed a sign of decrease despite maximal effort to maintain the force. The fMRI signal of the contralateral sensorimotor area showed a linear rise for most part of the task and plateaued at the end. For both the tasks, the fMRI signals in the ipsilateral sensorimotor cortex, prefrontal cortex, cingulate gyrus, supplementary motor area, and cerebellum exhibited steady increases. These results showed that the brain increased its output to reinforce the muscle for the continuation of the performance and possibly to process additional sensory information.

Shifting of activation center in the brain during muscle fatigue: An explanation of minimal central fatigue?

“…As the level of activation was amplified in these regions of the participants, the weighted center would shift towards these cortical fields. This explanation is in accord with recent fMRI results that demonstrate acute functional adaptations of the brain during progressive muscle fatigue, in which the right sensorimotor, prefrontal (anterior direction), and cingulate (inferior direction) cortices increased activation level (measured by fMRI) with muscle fatigue in the right arm (Liu et al, 2003). Participation of the ipsilateral sensorimotor cortex in control of limb movements has been widely reported, and it has been speculated that an enhancement in the level of its activation occurs to compensate for fatigue (Liu et al, 2002b(Liu et al, , 2003 or damage of the contralateral sensorimotor region (Newton et al, 2002;Staines et al, 2001;Ward et al, 2003).…”

“…This explanation is in accord with recent fMRI results that demonstrate acute functional adaptations of the brain during progressive muscle fatigue, in which the right sensorimotor, prefrontal (anterior direction), and cingulate (inferior direction) cortices increased activation level (measured by fMRI) with muscle fatigue in the right arm (Liu et al, 2003). Participation of the ipsilateral sensorimotor cortex in control of limb movements has been widely reported, and it has been speculated that an enhancement in the level of its activation occurs to compensate for fatigue (Liu et al, 2002b(Liu et al, , 2003 or damage of the contralateral sensorimotor region (Newton et al, 2002;Staines et al, 2001;Ward et al, 2003). The importance of the prefrontal and cingulate cortices in motor control is well described in text books (e.g., Saper et al, 2000) and increases of activity in these association regions during fatigue were also explained as a way to compensate for fatigue-related reduction of activation in the primary motor regions (Liu et al, 2003).…”

“…Very limited studies have quantified cortical signal changes during muscle fatigue (Belhaj-Saïf et a., 1996;Dettmers et al, 1996;Liu et al, 2003), and only three involved fatigue with MVC tasks (Liu et al, 2002b(Liu et al, , 2005a. Due to technical difficulties, none of these studies, however, were able to determine fatigue-related shifting of the activation source.…”

“…Participation of the ipsilateral sensorimotor cortex in control of limb movements has been widely reported, and it has been speculated that an enhancement in the level of its activation occurs to compensate for fatigue (Liu et al, 2002b(Liu et al, , 2003 or damage of the contralateral sensorimotor region (Newton et al, 2002;Staines et al, 2001;Ward et al, 2003). The importance of the prefrontal and cingulate cortices in motor control is well described in text books (e.g., Saper et al, 2000) and increases of activity in these association regions during fatigue were also explained as a way to compensate for fatigue-related reduction of activation in the primary motor regions (Liu et al, 2003).…”

“…A hypothetic answer is that the brain is a redundant organ that has multiple motor control centers with parallel projections to motoneuron pools in the spinal cord; the availability of multiple cortical centers controlling one motor task or muscle group makes "shifting of activation center" possible among these centers to compensate for fatigue. Numerous studies have shown multiple brain region activation even in controlling non-fatigue, simple motor tasks (e.g., Dai et al, 2001;Liu et al, 2003). The concept of activation shifting as a strategy to prolong a motor task under the condition of muscle fatigue has been presented for a long time with limited evidence showing rotation of motor units (Sogaard, 1995), muscles (Côté et al, 2002) and cortical neurons (Belhaj-Saïf et al, 1996).…”