Severe acute hypoxia impairs recovery of voluntary muscle activation after sustained submaximal elbow flexion

Abstract

The purpose of this study was to determine how severe acute hypoxia alters neural mechanisms during, and following, a sustained fatiguing contraction. Fifteen participants (25 ± 3.2 years, six female) were exposed to a sham condition and a hypoxia condition where they performed a 10 min elbow flexor contraction at 20% of maximal torque. For hypoxia, peripheral blood oxygen saturation (SnormalpO2) was titrated to 80% over a 15 min period and maintained for 2 h. Maximal voluntary contraction torque, EMG root mean square, voluntary activation, rating of perceived muscle fatigue, and corticospinal excitability (motor‐evoked potential) and inhibition (silent period duration) were then assessed before, during and for 6 min after the fatiguing contraction. No hypoxia‐related effects were identified for neuromuscular variables during the fatigue task. However, for recovery, voluntary activation assessed by motor point stimulation of biceps brachii was lower for hypoxia than sham at 4 min (sham: 89% ± 7%; hypoxia: 80% ± 12%; P = 0.023) and 6 min (sham: 90% ± 7%; hypoxia: 78% ± 11%; P = 0.040). Similarly, voluntary activation (P = 0.01) and motor‐evoked potential area (P = 0.002) in response to transcranial magnetic stimulation of the motor cortex were 10% and 11% lower during recovery for hypoxia compared to sham, respectively. Although an SnormalpO2 of 80% did not affect neural activity during the fatiguing task, motor cortical output and corticospinal excitability were reduced during recovery in the hypoxic environment. This was probably due to hypoxia‐related mechanisms involving supraspinal motor circuits. Key points Acute hypoxia has been shown to impair voluntary activation of muscle and alter the excitability of the corticospinal motor pathway during exercise. However, little is known about how hypoxia alters the recovery of the motor system after performing fatiguing exercise. Here we assessed hypoxia‐related responses of motor pathways both during active contractions and during recovery from active contractions, with transcranial magnetic stimulation and motor point stimulation of the biceps brachii. Fatiguing exercise caused reductions in voluntary activation, which was exacerbated during recovery from a 10 min sustained elbow flexion in a hypoxic environment. These results suggest that reductions in blood oxygen concentration impair the ability of motor pathways in the CNS to recover from fatiguing exercise, which is probably due to hypoxia‐induced mechanisms that reduce output from the motor cortex.

Post‐fatigue ability to activate muscle is compromised across a wide range of torques during acute hypoxic exposure

“…During the hypoxia condition, reduced oxygen availability would have exacerbated the impact of muscle ischaemia occurring during the sustained MVC (Fulco et al, 1996; Hogan, Kohin, et al, 1999), resulting in a greater rate of decline in torque production compared to the sham condition. In line with our previous findings and those of others, during a fatigued state, we observed hypoxia‐related reductions in VA assessed by TMS, without a corresponding effect of hypoxia on maximal torque output (Goodall et al, 2012; McKeown et al, 2021, 2020). Maintenance of the torque generating capacity of a muscle has been linked to potential increases in adrenergic activity that leads to widespread modulatory effects on cortical circuits (Chandler et al, 2014), facilitation of persistent inward currents at motoneurone dendrites (Lee & Heckman, 1999, 2000) and increased motoneurone acetylcholine release (Young et al, 1980).…”

“…Participants visited the laboratory on two occasions, where they were exposed to either a sham or hypoxia intervention that titrated SpO 2 to 80% over a 15 min period. Once the target SpO 2 was reached, participants were required to rest under hypoxic conditions for a 2-h duration prior to control contractions being performed (McKeown et al, 2021(McKeown et al, , 2020. Control TMS and MNS measures were obtained from each individual when performing three pairs of a brief MVC, followed by a brief 50% MVC (Figure 1b).…”

“…Reductions in VA have been consistently reported during and following fatiguing exercise in hypoxia (Amann et al, 2013;Goodall et al, 2012Goodall et al, , 2014McKeown et al, 2021;Rasmussen et al, 2010;Ruggiero et al, 2018). However, one hypoxia study has used TMS and MNS concurrently to assess VA during acute hypoxia (Goodall et al, 2012).…”

“…These factors include the duration of hypoxic exposure, where short exposures up to 1 h have minimal effects on performance (Katayama et al, 2007;Rupp et al, 2012Rupp et al, , 2015Soo et al, 2020;Szubski et al, 2006), and the severity of hypoxic stimulus, where <80% peripheral blood oxygen saturation (SpO 2 ) is more likely to affect performance due to cerebral hypoxia and disruptions in neurotransmitter turnover (Amann et al, 2007;Gibson & Duffy, 1981;Koob & Annau, 1974;Olson et al, 1983). As the progressive reduction in exercise performance is a consequence of limited oxygen availability to meet energy demand (Lannergren & Westerblad, 1991), it is not surprising that hypoxiarelated impairments in voluntary activation (VA) are particularly evident during prolonged or exhaustive exercise (Amann et al, 2013;Goodall et al, 2012Goodall et al, , 2010McKeown et al, 2021;O'Keeffe et al, 2021;Rasmussen et al, 2010;Ruggiero et al, 2018).…”

Muscle contraction force conforms to muscle oxygenation during constant‐activation voluntary forearm exercise

“…These two characteristics are strikingly different from cellular disturbance‐mediated compromise to force production in hypoxaemic conditions (Amann et al., 2006; Katayama et al., 2007; McKeown et al., 2021; Pitcher & Miles, 1997; Romer & Dempsey, 2006; Romer et al., 2006; Ruggiero et al., 2020; Szubski et al., 2007; Wright et al., 1999), which occur when the task requires maintaining force production and therefore ATP demand. Specifically, when skeletal muscle is ‘forced’ to achieve a given force production in the face of decreased muscle oxygenation, altered phosphorylation and redox potential to maintain aerobic ATP production are observed (Erecinska & Wilson, 1982; Haseler et al., 1998; Hogan et al., 1992, 1996, 1998; Wilson & Erecinska, 1985; Wilson et al., 1979).…”