Postural control is an essential requirement in physical and daily activities. Proprioceptive input is of primary importance in the control of postural balance (30). Optimal upright standing requires multisegmental control at the ankles, knees, hips, and spine (1). In challenging postural situations, such as standing on an unstable support surface, ankle proprioception becomes less reliable, and consequently, the CNS is forced to use more proximal proprioceptive signals to provide optimal postural control. This process is known as proprioceptive reweighting (23). However, in the presence of pain, fatigue, or injury, specific proprioceptive signals may lose reliability. For example, when back proprioceptive signals lose reliability because of low back pain, individuals may adopt an ankle-steered strategy, irrespective of the postural demands (8). The ability of individuals with low back pain to adapt their postural strategy to the postural demands is impaired (10). This rigid use of an ankle-steered strategy, rather than multisegmental control, is assumed as suboptimal during postural balance. The underlying mechanisms of the reduced postural variability are still obscure.
Respiration imposes a perturbing influence upon postural control (9,29). Generally, healthy individuals are capable of compensating actively for this perturbation (22). However, postural compensation to respiratory perturbation is challenged when respiratory demand increases, for example, during deep breathing (19,22), voluntary hyperventilation (12,37), and inspiratory resistive loading (IRL) (24). Moreover, IRL induces the use of a suboptimal ankle-steered strategy during postural control (24). The underlying mechanisms for the apparent association between respiratory demanding tasks and postural control remain to be examined systematically.
There is now ample evidence that high levels of inspiratory muscle work induce a generalized increase in sympathetic discharge that has been linked to the exacerbation of muscle fatigue (35). The underlying mechanism for this response is the activation of an inspiratory muscle metaboreflex by accumulating metabolites within the inspiratory muscles. This metaboreflex restricts locomotor muscle blood flow, because of preferential perfusion of the respiratory muscles (31,36). Locomotor muscle blood flow and muscle oxygenation can be recorded in real time by near-infrared spectroscopy (NIRS) (18), thereby assessing vasodilatation/vasoconstriction and oxygen extraction at the level of microcirculation (17). Previous studies demonstrated changes in limb muscle oxygenation and blood flow during inspiratory muscle loading (28,31) and unloading (5). Because there is evidence that postural control is suboptimal when the inspiratory muscles are at risk of fatigue (12,24), we may speculate that the metaboreflex may also impair the muscles involved in spinal control (6), e.g., the back muscles (25,38). However, to the author’s knowledge, no study investigated the effect of increased inspiratory muscle work on back muscle oxygenation and blood flow. It remains unknown whether IRL affects back muscle oxygenation and blood flow that may induce a suboptimal postural strategy.
Therefore, the main objective of this study was to investigate whether IRL affects proprioceptive (re)weighting, back muscle oxygenation, and blood volume during postural control. We hypothesize that IRL will necessitate the activation of the inspiratory muscle metaboreflex leading to reduced back muscle oxygenation and blood volume and consequently to the adoption of a suboptimal ankle-steered postural strategy. Postural control will be determined by standing on an unstable support surface (23) while breathing against an IRL. At the same time, simultaneous ankle and back muscle vibration will be used to evaluate the role of proprioceptive signals because it is a powerful stimulus of muscle spindle Ia afferents (8,11,34), and NIRS will be used to assess dynamic changes in back muscle oxygenation and blood flow (18,26). To examine the contribution of habitual postural strategy, individuals who usually adopt an ankle-steered strategy will be compared with those who use a multisegmental strategy during postural control, presuming habitual performance may be predictive for future pathology.
Twelve healthy individuals (age: 21 ± 2 yr; body mass index: 21 ± 2 kg·m−2) participated voluntarily in this study. Individuals with a history of specific balance problems (e.g., vestibular or neurological disorder), respiratory problems, smoking, spinal surgery, lower limb problems, low back pain, or the use of pain-relieving medication or physical treatment were excluded. None of the subjects showed evidence of respiratory obstruction upon examination of forced expiratory volume in 1 s (3.90 ± 0.72 L) and forced vital capacity (4.72 ± 1.19 L) (2). All individuals showed normal respiratory muscle force, as assessed by maximal inspiratory pressure (PImax: 105 ± 16 cm H2O) and maximal expiratory pressure (PEmax: 158 ± 39 cm H2O) using an electronic pressure transducer (MicroRPM; Micromedical Ltd., Kent, UK). The PImax was measured at residual volume and the PEmax at total lung capacity according to the method of Black and Hyatt (3). All participants gave their written informed consent conforming to the principles of the Declaration of Helsinki (1964). The study was approved by the local Ethics Committee of Biomedical Sciences, KU Leuven, Belgium, and registered at www.clinicaltrials.gov with identification number NCT01541020.
Proprioceptive weighting during postural control.
Postural sway characteristics were assessed by anterior–posterior center of pressure (CoP) displacement using a six-channel force plate (Bertec, Columbus, OH), which recorded the moment of force around the frontal axis (Mx) and the vertical ground reaction force (Fz). Force plate signals were sampled at 500 Hz using a Micro1401 data acquisition system using Spike2 software (Cambridge Electronic Design, Cambridge, UK) and were filtered using a low pass filter with a cutoff frequency of 5 Hz.
Local muscle vibration was used to investigate the role of proprioception in postural control. Muscle vibration is a powerful stimulus of muscle spindle Ia afferents (11,34). It evokes an illusion of muscle lengthening in standing. If the CNS uses proprioceptive signals of the vibrated muscles for postural control, it will cause a directional corrective CoP displacement. When the triceps surae (TS) muscles are vibrated, a postural sway in a backward direction is expected, whereas during lumbar paraspinal (LP) muscle vibration, a forward postural body sway is expected, which has been shown by previous studies (8,10,24,25). The amount of CoP displacement during local vibration may represent the extent to which an individual makes use of the proprioceptive signals of the vibrated muscles to maintain the upright posture. Simultaneous vibration on TS and LP muscles may identify the individual’s ability to gate conflicting proprioceptive signals (ankle vs back) during postural control (7). During simultaneous TS–LP muscle vibration, a dominant backward body sway suggests an ankle-steered postural control, whereas a forward body sway indicates a more multisegmental strategy. Muscle vibrators (Maxon Motors, Sachseln, Switzerland) were applied bilaterally over the TS and LP muscles, and vibration was offered at a high frequency and low amplitude (60 Hz, 0.5 mm) (34). Before the actual measurements, the subjects were presented with a few seconds of vibration to avoid startle effects.
An IRL protocol was conducted using an electronic loading device (MicroRMA, MicroMedical Ltd). The device imposes a constant resistance to inspiratory airflow by manipulating the surface area of the inspiratory airway. A week before the actual experiment, all the participants performed a standard breathing trial with the workload increased by 2 kPa·L−1·s−1 every seven breaths (incremental loading protocol). The participants were instructed to inhale against the IRL at a frequency of 15 breaths per minute, a duty cycle of 0.5, and a target flow of 0.6 L·s−1 until the flow could no longer be maintained. In addition, the participants were asked to perform a breathing trial with a constant preset inspiratory resistance of 70% of the maximum workload reached during the incremental loading protocol. This constant loading protocol was used as the definitive IRL protocol to examine the effect on proprioceptive postural control and back muscle parameters. The breathing trials were performed with the subject wearing a nose clip and breathing through the IRL device for a maximum of 900 s. An adapted Borg scale (0–10) was chosen to evaluate the respiratory effort during IRL (4). Both the incremental loading protocol and the definitive constant loading protocol were repeated twice and on different days to familiarize with the protocol before the actual test was performed.
Back muscle oxygenation and blood volume.
The back muscles are primarily involved in postural control (25,41). Local muscle oxygenation profiles of the left LP muscles were evaluated using NIRS (NIRO 200NX; Hamamatsu Photonics, Hamamatsu City, Japan) at two specific wavelengths (760 and 860 nm). The interoptode spacing (between emitter and detector) was 4 cm. The pathlength was set at 16 cm (4 cm (distance between probe and muscle) × 4 (differential pathlength factor)). Because the optimal differential pathlength factor for the back muscles has not been published, we based the setting on previous reports of calf, forearm, and quadriceps muscles (28,40). The optical probes were firmly attached to the skin at the LP muscles approximately 2 cm lateral to the spinous processes at the level of L3 (26). The NIRO 200NX provides a tissue oxygenation index (TOI) (expressed in percentage) and relative changes in oxyhemoglobin (O2Hb) and deoxyhemoglobin (HHb) (expressed in ΔμM) (18). The sum of O2Hb and HHb indicates the change in total blood volume (combined hemoglobin (cHb)), whereas the TOI value (O2Hb/cHb) is a measure of dynamic balance between oxygen delivery and use. Respectively, a modified Beer–Lambert law and spatially resolved spectroscopy were used in the calculation of these parameters. To improve intersubject comparability, values in TOI and cHb were expressed as the change from baseline. Regarding a possible influence of adipose tissue thickness on the NIRS signal, back muscle skinfold thickness was measured at the site of the NIRS probe application using a Harpenden skinfold caliper. Adipose tissue thickness was calculated as one half of the skinfold thickness (39).
During the entire experiment, the participants were instructed to stand barefoot on a foam pad (Airex balance pad: 49.5 cm long, 40.5 cm wide, and 6.5 cm thick), placed on the force plate, with their arms relaxed along the body. On an unstable support surface, ankle proprioceptive signals become less reliable, which enforces reliance upon proximal proprioceptive signals, thereby highlighting proprioceptive deficits (23). A standardized foot position was used, with the heels placed 10 cm apart and with a free forefoot position. The vision of the subjects was occluded by nontransparent goggles. They were instructed to maintain their balance at all times during the experiment, and an investigator was standing next to the subject to prevent actual falls.
Two experimental trials were implemented: 1) The first trial evaluated the weighting of proprioceptive input for postural control during quiet standing. Muscle vibration was applied bilaterally for 15 s to the TS muscles and LP muscles simultaneously. Before the second trial started, the subjects were asked to move their lower limbs and pelvis briefly to reset muscle spindles. 2) During the second trial, after 60 s of upright stance, the subjects were asked to perform the IRL protocol during simultaneous vibration on TS and LP muscles. The back muscle NIRS was assessed during the whole trial. The end of the trial was reached by failure of the subject to reach a flow of 0.6 L·s−1 despite encouragement of the investigator. For pragmatic reasons, the maximum length of the second trial was set at 900 s. Figure 1 displays the experimental set-up of trial 2.
Data reduction and statistical analysis.
Force plate data and NIRS parameters were calculated using Spike2 software and Microsoft Excel. To investigate the capacity to compensate for IRL, the mean values of CoP, TOI, HHb, O2Hb, and cHB (HHb + O2Hb) were calculated every 30 s. To improve the intersubject comparability, the TOI, HHb, O2Hb, and cHb mean values were normalized to the total amplitude of the response; the maximum (100%) was set as the average value during 60 s of upright standing on the foam without vision before the onset of the muscle vibration and IRL (trial 2), whereas the minimum (0%) was determined as the average value during 10 s of maximal voluntary contraction of the back muscles in prone lying. Positive values indicate an anterior body sway (CoP), increased back muscles oxygenation (TOI), increased deoxyhemoglobin (HHb), increased oxyhemoglobin (O2Hb), and increased blood volume (cHb), whereas negative values indicate a posterior body sway (CoP), decreased back muscles oxygenation (TOI), decreased deoxyhemoglobin (HHb), decreased oxyhemoglobin (O2Hb), and decreased blood volume (cHb) compared with the baseline.
A repeated-measures ANOVA was used to examine the differences between subjects and within-subjects over time (each 30 s of IRL). A post hoc test (Fisher) was performed to further analyze these results in detail. A median split analysis was used to subgroup the individuals on the basis of trial 1, placing the participants with the most anterior body sway into the “multisegmental group” and the participants with the most posterior body sway in the “ankle-steered group.” χ2 statistics were used for nominal data. The statistical analysis was performed with Statistica 9.0 (StatSoft, Tulsa, OK). The level of significance was set at P < 0.05.
Proprioceptive postural control during IRL.
The group of healthy individuals showed a slightly posterior body sway during IRL combined with simultaneous TS–LP vibration (Fig. 2). Moreover, this posterior sway increased progressively, and significantly, at approximately 450 s during the subsequent minutes of IRL. To explore this increased posterior sway, the group was retrospectively subdivided on the basis of the participants’ dominant use of proprioceptive signals (ankle vs back) during postural control. Two subgroups were defined on the basis of the participant’s habitual postural control without IRL (trial 1), placing the participants with the most anterior body sway into the “multisegmental group” (−0.5 ± 1.1 cm) and the participants with the most posterior body sway in the “ankle-steered group” (−6.5 ± 4.4 cm) (F(1,10) = 10.26, P = 0.009). The characteristics of the two subgroups are presented in Table 1.
During IRL combined with simultaneous TS–LP vibration, the ankle-steered group showed a significantly larger posterior sway compared with the multisegmental group (F(1,10) = 2.30, P = 0.000). This significant difference was present at all time points starting from the first 30 s, with the exception at 780 and 810 s. Figure 3 displays the mean CoP displacements each 30 s throughout the IRL protocol in the two subgroups. The duration of the IRL protocol did not significantly differ between the ankle-steered group (630 ± 245 s) and the multisegmental group (750 ± 300 s) (F(1,10) = 0.58, P = 0.465). However, only one participant from the ankle-steered group attained the maximum time of 900 s, compared with four from the multisegmental group (χ = 3.09, P = 0.079). The workload and perceived effort did not differ significantly between the ankle-steered group (13.4 ± 5.7 kPa·L−1·s−1 and 8.8 ± 0.8, respectively) and the multisegmental group (17 ± 5.1 kPa·L−1·s−1 and 6.8 ± 2.7, respectively) (F(1,10) = 1.31, P = 0.279, and F(1,10) = 3.03, P = 0.112, respectively).
Back muscle oxygenation and blood volume during IRL and postural control.
Back muscles oxygenation (TOI) decreased significantly in the ankle-steered group compared with the multisegmental group throughout the IRL protocol (F(1,30) = 19.14, P = 0.001). The back muscles TOI showed no decline in the multisegmental group during the full IRL (P = 0.748), whereas the ankle-steered group showed a significantly progressive decline during the IRL protocol (P = 0.000). After 4.5 min of IRL, a significant difference between the groups was observed until task failure (P < 0.05). Figure 4 displays the back muscles TOI in the two subgroups during the IRL protocol.
Simultaneously, both deoxyhemoglobin (HHb) (F(1,30) = 15.19, P = 0.003) and oxyhemoglobin (O2Hb) (F(1,30) = 73.64, P = 0.000) decreased significantly in the ankle-steered group compared with the multisegmental group. Whereas no decline in HHb (from 100% to 82%, P = 0.561) and O2Hb (from 100% to 129%, P = 0.132) was found in the multisegmental group, HHb (from 100% to −1%, P = 0.000) and O2Hb (from 100% to −45%, P = 0.00) declined progressively in the ankle-steered group during the IRL. Accordingly, blood volume in the back muscles (cHb) decreased significantly in the ankle-steered group compared with the multisegmental group (F(1,30) = 39.62, P = 0.000). Although no decline was observed in the multisegmental group (P = 0.132), back muscle blood volume decreased in the ankle-steered group during IRL (P = 0.000). A significant difference between the groups was observed after 2.5 min of IRL (P < 0.05). Figure 5 displays the back muscles cHb in the two subgroups during the IRL protocol. The adipose tissue thickness calculated from back muscle skinfolds was not significantly different between the ankle-steered group (5.7 ± 2.0 mm) and the multisegmental group (7.3 ± 1.5 mm) (P = 0.163).
IRL forces healthy individuals to switch to a suboptimal postural control strategy with an increased proprioceptive gain at the ankles and a decreased gain at the back muscles after approximately 7 min of IRL. Individuals who showed an increased reliance on ankle proprioceptive signals during postural control in the baseline condition maintained this suboptimal postural strategy during IRL. In addition, during IRL, this ankle-steered group showed a progressive decline in back muscle oxygenation and blood volume. In contrast, individuals who showed a more multisegmental control in baseline upright standing maintained this optimal postural strategy during IRL although back muscle oxygenation and blood volume were not affected. Although two different subgroups have been defined, we expect a continuum of proprioceptive strategies, back muscle oxygenation, and blood volume within the healthy population. Although the effect of inspiratory muscle work has been widely examined on limb muscle oxygenation and blood flow affecting cycling and running performance (5,6,31,35,36), this was the first study examining the effect of inspiratory muscle work on back muscle oxygenation and blood flow during a postural control performance.
Muscle blood volume and oxygenation are determined by the summation of several inputs, some of which exert an influence on 1) the muscle vasculature (vasoconstriction/vasodilation), whereas others 2) affect microvascular oxygen extraction. The inputs on muscle vasculature include efferent sympathetic vasoconstrictor activity and the vasodilator influence of local muscle metabolites (16). IRL is known to elicit a generalized increase in sympathetic outflow, which induces vasoconstriction in locomotor muscles (i.e., metaboreflex) (31,35,36). However, in the presence of muscle activity, this neutrally mediated vasoconstrictor influence may be successfully opposed by local vasodilator influences (16). Our results show a decreased back muscle oxygenation (TOI) and blood volume (cHb) in the ankle-steered group, but not in the multisegmental group. This observation is consistent with a mechanism whereby back muscle blood volume was maintained in the multisegmental group by the vasodilator influence of local back muscle metabolites. This vasodilator influence was absent in the ankle-steered group, presuming decreased back muscle use to maintain postural control (25,38). This latter presumption can be corroborated by the fact that the ankle-steered group showed a decrease in HHb, a parameter that can be considered as a surrogate of microvascular oxygen extraction and thus use of the back muscles (15). Because muscle spindles show a dens capillary system (27), the inability to counteract the vasoconstrictor influence of the metaboreflex will inevitably affect the muscle spindle function (14). The vasoconstriction within the back muscles of the ankle-steered group may induce a decrease in back muscle spindle sensitivity (14). This may necessitate the CNS to downweight back proprioceptive signals for postural control and consequently adopt an even more ankle-steered postural control strategy during IRL (8,10,24). Accordingly, our findings may imply that loading of the inspiratory muscles negatively affects proprioceptive postural control, possibly via the inability to counteract back muscle vasoconstriction imposed by the inspiratory muscle metaboreflex and by the decreased use of the back muscles as observed by the decreased oxygen extraction.
The occurrence of a metaboreflex may explain the abrupt increase in posterior sway in the total group around 450 s of IRL (Fig. 2). However, IRL seemed to force individuals to reweight their proprioceptive signals and change their postural control strategy at the commencement of IRL (Fig. 3). This strategy might be explained by the Central Governor Model, an anticipatory regulatory model that allows feedback from the periphery to influence the feedforward central drive that determines the extent of specific muscle recruitment (32). According to this model, independent systems in the periphery provide sensory feedback that influences central motor drive from the brain to the exercising muscles to ensure that a certain task performance (e.g., postural control) changes before a biological “failure” appears. This model is consistent with our observation that the ankle-steered group adopted a posterior body sway at the start of IRL, although the effects of the metaboreflex would only occur progressively during the exercise. The dual engagement of the inspiratory muscles, both in IRL and postural control (21), might overload the multisegmental control performance and consequently force an alternative suboptimal ankle-steered strategy to be used.
Using proprioceptive reweighting, the CNS increases the proprioceptive gain at the ankle muscles when the back muscle proprioceptive signals lose reliability, e.g., in individuals with low back pain (8,10) or in back muscle fatigue (25,41). Previous studies demonstrated increased ankle muscle activity (12,13) and increased lower limb nerve excitability (37) in postural control during hyperventilation but did not examine more proximal proprioceptive sources like the back muscles, although assumed essential for optimal postural control (1,38). Recent evidence showed that a flexible multisegmental control, and not a rigid strategy, is preferred to compensate for breathing (29). Furthermore, a recent study revealed an increased use of ankle proprioceptive signals in postural control immediately after IRL (24). However, to our knowledge, the present study is the first to examine proprioceptive weighting changes in postural control during IRL. In this respect, simultaneous vibration of TS and LP muscles provides a useful tool to examine dynamic changes in proprioceptive weighting during physiological perturbations such as IRL.
Our findings have potential clinical relevance for respiratory-demanding sports involving high amounts of walking and running, because these sports are likely to reduce postural control (33). The use of an ankle-steered strategy after inspiratory muscle loading may increase the risk of sports injuries, either by a higher fall risk or development of low back pain associated with decreased trunk control (20). Accordingly, interventions such as inspiratory muscle training may have a positive effect on postural balance and warrant further exploration.
Some limitations must be addressed. The adipose tissue thickness was evaluated 4 months after the NIRS measurements. However, we do not expect significant differences in adipose tissue thickness over this period because the individuals’ body weight remained equal. Furthermore, to provide definitive evidence of the inspiratory muscle metaboreflex, we suggest future studies recording blood pressure and heart rate during IRL. In addition, transdiaphragmatic pressures and evoked potential responses to bilateral phrenic nerve magnetic stimulation would reveal the presence, or otherwise, of contractile fatigue of the diaphragm (2).
In conclusion, loading of the inspiratory muscles forced healthy individuals to shift to a suboptimal postural strategy during upright standing, with an increased gain at the ankles and a decreased use of back muscle proprioceptive signals. This downweighting of back proprioceptive signals was associated with a decreased back muscle oxygenation and blood flow. This might suggest a decreased ability to counteract the vasoconstrictor influence of the inspiratory muscle metaboreflex upon back muscle oxygenation and blood volume. The latter may impair the reliability of proprioceptive signals from the back muscles, thereby necessitating the CNS to adopt a suboptimal, ankle-steered postural control strategy. Our findings provide a possible explanation for the reduced postural control and spinal injuries observed in high-intensity sports. Further studies must reveal whether unloading of the inspiratory muscles might have a positive effect on proprioceptive postural control.
This work was supported by The Research Foundation—Flanders (FWO) grants 1.5.104.03 and G.0674.09. Lotte Janssens is a Ph.D. fellow of the FWO and Madelon Pijnenburg is a Ph.D. fellow of the Agency for Innovation by Science and Technology—Flanders (IWT). Alison McConnell acknowledges a beneficial interest in an inspiratory muscle training product in the form of a share of license income to the University of Birmingham and Brunel University. She also acts as a consultant to POWERbreathe International Ltd.
For the remaining authors, no conflicts of interest were declared. The authors state that the results of the present study do not constitute endorsement by the American College of Sports Medicine.
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