Proprioception corresponds to an individual’s ability to integrate sensory signals (1) to detect destabilizing stimuli requiring muscular corrections (feedback), and anticipate muscular actions based on predictable joint segment displacements (feed-forward) (2). However, both afferent and efferent neural drives are affected by hyperthermia as evidenced by decreases in voluntary force production, muscle voluntary activation, as well as electrically evoked potentials amplitude and latency (M-wave and Hoffman (H) reflex) (3–5). Electrically evoked M-wave and H-reflex are commonly used as indices of sarcolemma and spinal properties, respectively (6). However, the consequences of these neural alterations on proprioception remain unclear. Negative effects of heat stress on postural stability and/or movement perception has been reported in some (7,8), but not all (9,10), studies. Given that proprioception is a risk factor for injuries (7) and plays a role in sports injury prevention (11), rehabilitation (12), injury prediction (13), sports performance, and talent identification (14), investigating the potential impact of hyperthermia on proprioception is of paramount importance.
Proprioception also plays an integral role in maintaining balance. Balance corresponds to the process of keeping the center of gravity within the base support of the body (15) and represents an important aspect of performance and safety in sports and rehabilitation. Indeed, the better someone is able to establish a stable base of support, the greater their proprioceptive control and joint range of motion (15). Thus, instability and inefficient balance strategies will result in poor athletic performance and an increased risk of injury.
Therefore, the aim of this study was to determine if the previously reported effects of whole-body hyperthermia on neural function in humans would impair proprioception. Although localized warming of the limbs does not affect sensory perception and postural stability (9,16), and whole body heating has produced conflicting results (7–10), we hypothesized that the neural alterations induced by a controlled whole-body hyperthermia would impair active movement-based proprioceptive acuity and postural stability.
Based on previous studies reporting an effect of passive hyperthermia on motor drive and spinal modulation (3), we estimated the required sample size at 12 participants with alpha of 0.05 and beta of 0.20 (i.e., power of 0.8, G*Power 3.1). Fourteen healthy non–heat-acclimated fitness instructors volunteered for this study (eight men and six women, 32 ± 5 yr, 73 ± 8 kg and 176 ± 7 cm for age, body mass, and height, respectively). No participants suffered from illnesses or injuries at the time of the experiment, and all participants self-reported to be free of any lower-limb injury for at least 2 yr before the study. All participants completed a physical activity readiness questionnaire (Par-Q) and were healthy and not taking any medication. They were instructed to avoid vigorous activity for the 24 h preceding each trial. The project was approved by Aspetar scientific committee (approval number CMO/000073/FS) and by an external ethics committee (ADL-Q, approval number E20140000017). The procedures complied with the Declaration of Helsinki regarding human experimentation. Written informed consent was obtained from all participants before the beginning of testing.
Participants visited the laboratory for two experimental sessions in an environmental chamber (Tescor, Warminster, PA) set to control (CON, 24°C, 40% relative humidity [RH]) and hot (HOT, 44°C–50°C, 40%–50% RH) ambient conditions. The room temperature was adapted during the HOT session to maintain core temperature at approximately 39°C during the testing procedure. The testing procedure included: neuromuscular assessments, active movement discrimination testing, dynamic balance testing, and static balance testing. The order of the tests was counterbalanced between participants but was identical for the two sessions within participants. To minimize any learning effect, trials were performed in a counterbalanced order with 4 to 7 d of recovery between them. In addition, participants undertook the complete testing procedures during a familiarization session 2 to 7 d before the first testing trial. All trials were performed at the same time of day and with participants wearing the same attire (i.e., shorts, t-shirts, and shoes when required).
Preceding each trial, participants rested for 1 h in a 24°C laboratory and drank 500 mL of water while being equipped with skin temperature sensors (iButton; Maxim Integrated Products, Sunnyvale, CA) and a HR monitor (Equivital, UK). Also, participants self-inserted a telemetric thermometer pill (VitalSense, Mini Mitter; Respironics, Herrsching, Germany) in the rectum (the length of a gloved index finger beyond the anal sphincter). Participants were asked to provide urine sample. If the urine specific gravity (URC-NE; Atago, Tokyo, Japan) was >1.020, the trial was postponed to allow the participants to drink more water. Thereafter, the participants entered the environmental chamber, rested in a seated position for 20 min (CON) or until reaching a core (i.e., rectal) temperature of 39°C (HOT: range, 45–60 min) before starting the tests. During the HOT trial, the temperature and RH were initially set at 50°C and 50%, respectively. Once participants reached a rectal temperature of 39°C, the environmental temperature and humidity were respectively adjusted between 44°C and 50°C and 40% and 50% to ensure rectal temperature remained at approximately 39°C for the testing procedure. The testing procedure was the same in both CON and HOT and participants allowed to drink ad libitum.
Participants were seated with the right foot strapped in a dynamometric pedal (Captels, St Mathieu de Treviers, France) and the hip, knee and ankle flexed at 90°. Percutaneous stimulations (400 V, rectangular current pulse of 1 ms) were delivered by a constant current stimulator (Digitimer DS7AH, Digitimer, Hertfordshire, England) to the tibial nerve at rest. The cathode (Ambu Blue sensor T, Ambu A/S, Denmark; diameter 1 cm) was located in the popliteal fossa (with constant pressure supplied by a strap) and the anode (5 × 9 cm) was located slightly distal to the patella. The electrically evoked action potentials were recorded over the soleus (SOL) and the gastrocnemius (GM) muscles using MP35 hardware (Biopac Systems Inc., Santa Barbara, CA) and dedicated software (BSL Pro Version 3.6.7; Biopac Systems Inc.) via bipolar Ag/AgCl electrodes (Ambu Blue sensor T, Ambu A/S, Ballerup, Denmark) with a diameter of 1 cm, an interelectrode distance of 3 cm and a reference electrode on the wrist. Before electrode placement, the skin was lightly abraded and washed to remove surface layers of dead skin, hair, and oil. The myoelectric signal was amplified (gain, 1000×), filtered (30–500 Hz) and recorded with a high sampling frequency (10 kHz). Placement of the electrodes was marked with a permanent marker and kept constant throughout the experiment. The amperage of the percutaneous stimulation was progressively increased until there was no further increase in peak twitch mechanical response (Pt) and concomitant electrophysiological response (M-wave). Thereafter, the current was adjusted in smaller increments to determine the maximal peak-to-peak amplitude of the H-reflex. The complete procedure requires approximately 15 min. Mechanical responses were analyzed for amplitude (Pt), contraction time (CT), and half-relaxation time (HRT). Electrophysiological responses were analyzed for amplitude (Hmax and Mmax) and latency. The ratio Hmax/Mmax was also calculated to isolate the spinal adaptations from the peripheral nervous system changes.
Movement discrimination test
Dorsiflexion discrimination sensitivity (i.e., acuity) was measured using the Active Movement Extent Discrimination Apparatus, a purposely designed device with a high reliability (intraclass correlation coefficient = 0.85) (17). Briefly, participants stood barefoot with the left foot on a fixed platform and the right foot on a mobile platform. The axis of rotation of the mobile platform was perpendicular with the long axis of the participant’s foot and the stopper was automatically set to five different dorsiflexion angles each separated by 0.73° between 11.17° and 14.07°. Participants remained standing upright with equal weight distributed through both feet, with the head straight and looking at a mark positioned 5 m in front of them. Of note, participants dried their foot to remove any sweating with a towel before the test in HOT. Each participant tried the five movement displacement distances, in order, from the smallest (position 1) to the largest (position 5), three times each before data collection was commenced. Participants then undertook 50 trials in a random sequence (i.e., 10 at each of the five different movement displacements). The complete test took typically 7 min. During testing, participants were asked to make an absolute judgment as to the position number (1, 2, 3, 4, or 5) of each movement as soon as they returned to the start position. No feedback from the investigator was given as to the correctness of the judgment they made on each trial. The mean error was computed.
Participants performed the single-leg stance (SLS) test barefoot standing on the right leg while maintaining balance for 15 s. Participants dried their foot to remove any sweating with a towel before the test in HOT. Three trials separated by 10 s were performed. The SLS test was performed on an Emed-x plate (Novel, Munich, Germany) with the right foot precisely positioned on the center of the plate. Participants were instructed to stand as still as possible with their hands on their hips while keeping the left leg bent at a 45° angle at the side. The trials were discarded and repeated if the participant touched the ground with the non-stance foot during the trial. The center of pressure (COP) excursion and the contact area of the stance foot were recorded by a pedographic platform (Emed, Novel, Munich, Germany). Values of the three trials were averaged.
Star Excursion Balance Test
The modified Star Excursion Balance Test (SEBT), introduced by Hertel et al. (18), was performed with participant’s standing barefoot on the right leg. Participants dried their foot to remove any sweating with a towel before the test in HOT. Three labeled lines were extended from the center of the foot in medial (M, at 90°), anteromedial (AM, at 45°) and posteromedial (PM, at 45°) directions. These directions have been shown to be the most effective in clinically testing functional deficits related to chronic ankle instability (18). To perform the SEBT, participants maintained a single-right leg stance in semisquat while reaching with the left leg as far as possible along the three directions. Participants had to touch the furthest point possible on the line with the most distal part of their reach foot as lightly as possible using minimal pressure to ensure that the reach leg did not provide support in the maintenance of upright posture and that stability was achieved through balance. Participants then returned to a bilateral stance while maintaining their equilibrium and the investigator visually read on the labeled lines for the distance reached in centimeters. The same investigator took all reach measurements. Each participant performed two practice trials and three data collection trials in each of the three directions, 10 s of rest were provided between individual reach trials. The order of trials was counterbalanced to minimize the effect of potential local fatigue. The primary instruction was to reach as far as possible without lifting the right heel and participants were free to flex their hip, knee, and ankle to whatever angle they desired. Trials were discarded and repeated if a participant did not touch the line with the reach leg while maintaining their balance on the stance leg (e.g. using the reach leg in a way that it gave support). Three properly executed test distances in each direction were averaged. Balance tests (i.e. SLS and SEBT) were completed within 10 min.
Rectal temperature was monitored using a telemetric thermometer pill (VitalSense, Mini Mitter, Respironics, Herrsching, Germany). Skin temperatures of the arm, thigh, and calf were monitored via iButton temperature sensors/data loggers (Maxim Integrated Products). Chest temperature and HR were monitored via a chest strap (Equivital, UK). Mean skin temperature was calculated as 0.3 × chest + 0.3 × arm + 0.2 × thigh + 0.2 × calf temperatures (19). Likert-type scale, ranging from 1 to 7, was used to record thermal sensation (20) and thermal comfort (21) before and after each test.
Data were coded and analyzed in PASW software v.21.0 (SPSS, Chicago, IL). A one-way repeated measures ANOVA test was used to determine the effect of hyperthermia. A two-way repeated measures ANOVA test was used to determine the effect of hyperthermia and direction on distance reached during SEBT. Bonferroni correction was applied for post hoc analyses. Data distribution normality was verified using the Kolmogorov-Smirnoff test. In case of significant Kolmogorov-Smirnoff P value data were transformed (ln) before statistical analysis. This occurred in three cases (body mass loss, HR, skin temperature). All data were presented as means ± SD along with the mean differences (95% confidence interval). The level of statistical significance was set at P < 0.05. Effect-sizes were described in terms of Cohen d (with d ≥ 0.5 representing a moderate difference and d ≥ 0.8 a large difference).
Environmental, core, and skin temperature were all higher in HOT than CON conditions (all P < 0.001, d ≥ 2.92; Table 1). Individual core temperatures during the HOT trial are represented in Figure 1. Moreover, HR, body mass loss, and both thermal sensation and discomfort were also significantly higher in HOT than CON (all P < 0.05, d ≥ 0.95; Table 1).
Maximal amplitude of H-reflex (Fig. 2) and M-wave (Table 2) was reached at a similar intensity of stimulation in CON and HOT (both muscles, P > 0.173, d ≤ 0.28). The M-wave amplitude was not significantly different between conditions for both SOL (95% confidence interval, −1.9 [−4.1 to +0.3] mV; P = 0.084, d = 0.55) and GM (−1.4 [−4.6 to +1.8] mV; P = 0.364, d = 0.31). However, maximal H-reflex amplitude was significantly lower in HOT than CON for both SOL (−1.8 [−2.6 to −1.0] mV P = 0.000, d = 1.14) and GM (−0.8 [−1.5 to −0.1] mV P = 0.021, d = 0.74). In addition, H/M ratio was also significantly lower in HOT than in CON for the SOL (−0.1 [−0.2 to −0.0] mV, P = 0.008, d = 0.79) but not the GM (0.0 [−0.1 to +0.1] mV, P = 0.349, d = 0.32). The latency of both H-reflex and M-wave as well the latency difference (H-M) decreased significantly with hyperthermia (all P < 0.05, d ≥ 0.44).
Pt was reached at a similar intensity of stimulation in HOT (58.8 ± 36.1 mA) and CON (58.7 ± 28.1 mA) (−0.1 [−26.2 to +26.0] mA, P = 0.995, d = 0.00). There was no significant effect of hyperthermia on Pt amplitude (16.2 ± 4.0 N vs 15.7 ± 4.4 N in HOT and CON respectively; −0.5 [−2.8 to +1.7] N, P = 0.619, d = 0.13). However, CT was significantly shorter in HOT (90.9 ± 9.4 ms) than CON (118.9 ± 14.3 ms) (−28.0 [−33.8 to −22.2] ms, P < 0.001, d = 2.31) and HRT was also shorter in HOT (75.8 ± 10.4 ms) than CON (88.7 ± 18.5 ms) (−12.9 [−23.3 to −2.6] ms, P = 0.018, d = 0.86).
Proprioception acuity was impaired in HOT as compared with CON with a significantly larger mean error (+0.08 [+0.01 to +0.15] degrees, P = 0.049, d = 0.64; Fig. 3).
During the SLS test, the contact area between the plantar surface of the foot and the Emed-x® plate was significantly higher in HOT (125.5 ± 13.7 cm2) compared with CON (122.2 ± 13.1 cm2) (+3.3 [+1.2 to +5.4] cm2, P = 0.005, d = 0.25) and the COP excursion tended to be higher in HOT (63.5 ± 14.4 cm) than in CON (57.4 ± 8.9 cm) (+6.1 [−1.3 to +13.6] cm, P = 0.097, d = 0.51).
Distance reached during SEBT was significantly dependent on direction (P < 0.001) with PM direction being higher than M (+6.4 [+3.6 to +9.3] cm, P < 0.001) and M being higher than AM (+6.6 [+4.2 to +9.2] cm, P < 0.001). In addition, passive hyperthermia significantly decreased the distance reached during the SEBT (P = 0.010, d = 0.33; Fig. 4) with an interaction effect between direction and temperature (P = 0.023). Post hoc analyses showed that only the distance reached in the PM direction was significantly impaired by hyperthermia (−4.2 [−6.8 to −1.6] cm, P = 0.004, d = 0.56; Fig. 4), whereas the difference did not reach significance in the M (−1.3 [−3.0 to +0.4] cm, P = 0.129, d = 0.17; Fig. 4) and AM (−1.5 [−3.7 to +0.6] cm, P = 0.151, d = 0.20; Fig. 4) directions.
The aim of this study was to determine the functional consequences of hyperthermia-induced neural alterations. Along with the previously reported decrease in H-reflex amplitude, the current data show that hyperthermia impairs proprioceptive acuity during a specific movement discrimination task and reduces both dynamic and static postural stability during a SEBT and a SLS, respectively. Acknowledging the specificity of each test taken individually, it is noteworthy that all these tests representing clinical (e.g., SEBT) and research (e.g. Active Movement Extent Discrimination Apparatus) standards showed a similar pattern of variation.
The current data confirmed that H-reflex occurred earlier and with a lower maximum amplitude when participants were hyperthermic (3). Such alterations might be explained by a shortening of the opening time of the voltage-gated sodium channels (22,23), a presynaptic inhibition mediated by group III and IV afferents (24) or a synaptic failure (25,26) when temperature increases. Of note, the significant decrease in the H-reflex/M-wave ratio confirms that hyperthermia alters spinal function irrespective of potential changes in sarcolemmal excitability or recording conditions (Table 2). Given that proprioception partly relies on spinal reflexes (27), we therefore hypothesized that this hyperthermia-induced decrease in spinal reflex amplitude might lead to motor control impairments.
Various techniques have been used in the literature to explore proprioception but their ecological validity, data validity, and applicability differ (28). Among them, active movement discrimination seems to be more suitable in sports science as it aims to examine how proprioception functions under natural conditions incorporating active movements that result in a functional interaction with the environment (29). The current results suggest that hyperthermia impairs proprioception acuity as evidenced by a 17% increase in the mean error of movement discrimination (Fig. 3). To our knowledge, this is the first documentation of whole-body passive hyperthermia modulating proprioception. Using therapeutic applications of heat and cold to the foot and ankle, Ingersoll et al. (9) suggested that hot and cold-water immersion failed to affect sensory perception using a two-point discrimination test and one-legged balance test. However, the hot treatment in their study involved 20 min of immersion of the right foot only, whereas whole-body passive hyperthermia was induced in the current protocol. This suggests that whole-body hyperthermia rather than local heating impairs proprioception.
Muscle afferent input is of paramount importance for ankle proprioception (30). For example, movement discrimination partly relies on the increased firing from muscles and capsular tissue stretched by the movement, as well as from decreased firing from shortened muscles (31). The shorter CT and HRT observed in HOT than CON showed that hyperthermia affects muscle shortening velocity and may therefore affect neural feedback to stretching. In addition, the hyperthermia-induced decrease in H-reflex, an electrophysiological variation of the stretch reflex, suggests a decline in neural drive transmission from Ia afferents to α-motor neurons. H-reflex amplitude can be modulated by groups III and IV afferent-mediated presynaptic inhibition (32–34). The III and IV afferent receptor systems are also involved in conscious proprioception by providing somatosensory input via the spinal cord to adequate areas in the CNS (12). Given that groups III and IV afferent fibers are temperature sensitive (35,36), the decrease in proprioceptive acuity reported in the current study may be partly related to a hyperthermia induced activation of these receptors.
Lastly, it is noteworthy to mention that proprioceptive information processing at the level of the CNS is modulated by the cognitive programming (37). Interestingly, hyperthermia has been shown to represent an emotional and cognitive load, in turn reducing cognitive performance (38) through a decrease in available resources. Thus, the higher discomfort in HOT than CON reported in the current study might affect the cognitive resources dedicated to the proprioceptive task.
The current data showed also that the contact area between the foot sole and the Emed-x® pressure plate during the 15-s SLS was significantly higher in HOT comparing to CON (+2.7%) and that the COP excursion was also higher (+11.1%) in HOT as compared to CON condition. These data suggest that hyperthermia impairs static balance. Moreover, our data showed that the average reach distance in the SEBT decreased when subjects were hyperthermic suggesting an impairment in dynamic balance as well. Our study was the first to investigate the effect of whole-body hyperthermia on balance thus mechanistic information explaining these alterations remain unclear, but based on some previous findings some hypotheses could be made. According to Riemann et al. (2) deficits in postural stability have been largely attributed to disruptions in the integrity of the afferent information from mechanoreceptors. Previous studies have shown that among these mechanoreceptors the fusiform muscle spindle receptor is the primary sensory source of information for balance and proprioception (30,39). Interestingly, the muscle spindle response might be affected by the faster muscle shortening velocity in HOT than CON.
Moreover, muscle spindle sensitivity depends on both γ and α motor neuron innervation via the input arising from mechanoreceptors as well as descending supraspinal commands (2). Indeed, stimulation of γ motor neurons heightens muscle spindle sensitivity whereas alteration of its level of activation might influence the input arising from the muscle spindle (40). The current data showed that despite a similar intensity of stimulation and similar associated M-waves, the H-reflex amplitude was lower in HOT than CON. Thus, in line with other studies in our group (3), these observations suggest that hyperthermia can alter the responsiveness of the Ia-afferent–α-motoneurone pathway. Taking all together, it could be speculated that the hyperthermia-induced peripheral nervous changes affecting the Ia-afferent–α motor neuron system could also affect the γ motor neuron system,
Of note, the SEBT has been used extensively in research and clinical applications. It has been well documented in several studies that the SEBT is able to differentiate healthy participants with a specific level of dynamic postural stability among patients with various lower extremity injuries (18). Interestingly, the decrease in SEBT was mainly due to a decrease in the PM direction (Fig. 4). This is in line with previous studies commonly showing that deficits were only evident on the PM reach direction in participants with chronic ankle instability (41,42). It is well documented that the PM reach direction is best suited to representing the overall SEBT performance (18), in detecting functional performance differences and in identifying dynamic balance deficits (42).
As discussed previously, the results of Ingersoll et al. (9) contrast ours in that therapeutic applications of heat to the foot and ankle did not affect sensory perception during on-legged balance and two-point discrimination tests. Furthermore, Dewhurst et al. (16) reported that local warming of the leg did not affect postural stability during quiet stance, in conditions where maximum muscle temperature reached 37°C only. However, previous studies from our group showed that the passive heating protocol of the current study allowed to reach approximately 39°C for both muscle and core temperature (43). Also, it has previously been reported that ankle and knee cooling does not impair dynamic balance whereas cooling to the hip does, suggesting that localized temperature changes do not account for dynamic balance alteration (44). Thus, as for proprioception, these results suggest that it is the increase in whole-body temperature rather than skin temperature that impairs balance. Considering that proprioception contributes to postural stability (2), impairments in the proprioceptive abilities observed in our study might account for the impairments of dynamic and static balance.
Our results showed that participants became dehydrated by 2.2% (Table 1). Albeit this percentage remains relatively low, it can be argued that dehydration partly explained the impairments in proprioception and balance. The literature on the effect of dehydration on neuromuscular control and postural stability is inconclusive, with some studies (7,45) but not all (10,46), suggesting that dehydration impairs neuromuscular control. Of note, in the study of Distefano et al. (7), participants were on fluid restriction starting 20 to 22 h on the day before the test session, they started the session 1% to 2% dehydrated and they lost an additional 5.7% of their body mass during a 1-h exercise. In our study, participants started the session euhydrated and could drink as much as they wanted. Additionally, with similar dehydration levels to our current study, Patel et al. (46) did not report balance performance deficits. Taking all the above together, we suggest that hyperthermia, rather than dehydration, is the main cause for the impairment of proprioception and balance in the current study.
Of note, hyperthermia has been shown to affect several cortical area including the frontal but also the prefrontal and occipitoparietal regions (38). Hyperthermia has also been shown to specifically affect the somatosensory cortex (47), which is controlling proprioception and postural stability (12,27). Therefore, central processes might be partly involved the impairment of proprioception and balance evidenced in the current study. Future studies are necessary to understand the causes and consequences of the hyperthermia-induced alterations in proprioception.
In summary, besides a decrease in H-reflex amplitude, this study suggests that passive hyperthermia affects proprioception and postural stability as evidenced by (i) a reduced ability to discriminate between different dorsiflexion angles, (ii) an impairment in dynamic balance and (iii) an impairment in static balance. These alterations are concordant between themselves and might be due to heat-induced alterations in efferent and afferent signals to and from the muscle, as well as some central processes.
The authors thank Rodney Whiteley for his valuable input in the study design. The authors thank Mohammed Aziz Farooq for his support with the statistical analysis. The authors thank Julien D. Périard for proofreading the manuscript. The authors thank the participants for their involvement. The results of this study are presented clearly, honestly, and without fabrication, falsification, or inappropriate data manipulation. This study was internally funded by Aspetar Orthopaedic and Sports Medicine Hospital.
The authors have no conflicts of interest that are directly relevant to the content of this manuscript. No professional relationships with companies or manufacturers were entered into in the conduct of this study. We acknowledge that the results of the present study do not constitute endorsement by ACSM.
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