In line with our expectations, the analysis of the COP sway confirmed the disruptive effect that proprioceptive vibration of the calves has on the participants’ quiet stance. In fact, in both experimental conditions, the administration of the localized vibratory sequence resulted in an increased COP DIST and MV, which together reveal a decreased ability to maintain balance during Q1 compared to the resting state (BASE)38. Interestingly, no significant difference was observed in the posturographic response between the initial and final phases of the trial (Q1 and Q4). With the exception of a slight but statistically significant increase of DIST during the OE task, the last quartile showed negligible postural variation when compared to Q1. These data, therefore, cannot support the presence of the phenomenon that has been termed ‘habituation’ in previous literature, and describes an adjustment in motor control strategies following the prolonged or repeated exposure to external perturbations or changing of environment 2.
This seems to be further confirmed by the results of cortico-muscular and inter-muscular coherence, where no significant difference emerged in any of the considered metrics between Q1 and Q4.
Cortico-muscular coherence is a technique traditionally used to analyse the cortical drive to the muscles, i.e., the descending neural signal that modulates muscle activation39. Studies on the phase lags of CMC signals showed their consistency with the conduction time between motor cortex and muscles, reinforcing the idea that CMC reflects the drive that cortical processes exert on motor neurons 40,41. Previous literature also established beta and low gamma bands (13–30 Hz and 30-45Hz, respectively) as the primary frequency range where neuromuscular couplings effects can be observed, showing how different kind of muscle movements modulate the speed of cortico-muscular oscillations14,42,43.
The investigation conducted in this study focused on those muscles (GL and SOL) which are mostly involved in the postural stabilization mechanism defined as ‘ankle strategy’, the primary one used to reposition the center of gravity either during quiet stance or in response to external perturbations44,45. Being a dorsiflexor, the TA was also included to fully characterize the muscle response to the vibratory stimulation. The most significant results were observed during the CE trial. As depicted in Fig. 3, the results display a consistent increase in CMC, spread throughout beta band, for the SOL muscles after the administration of the proprioceptive vibration, compared to resting state. A statistically significant difference in CMC, identified by the cluster-based permutation test in the frequency bins around 20Hz, is consistent with what reported in previous literature18. The same pattern can be observed for GL in gamma band (see Fig. 5)42. While beta-band CMC has been traditionally associated with static force output, gamma-band CMC has been reported during strong contractions and dynamic force42. In addition, it has been shown how superficial extensor muscles, such as GL, are characterized by higher contraction frequency than deep extensors such as SOL.46
The results of SOL and GL support the idea that the response to a disruptive proprioceptive vibration evokes an enhanced cortico-muscular coupling, particularly observable in correspondence of more challenging tasks such as the CE trial. The lack of visual input, a key afferent in the postural control system, seems to make a greater degree of high-level control necessary, as reflected by the increased CMC which suggest a lesser extent of automaticity in the execution of the task47.
From a statistical standpoint, the observed results are particularly significant (p < 0.01) in the GL and SOL muscles of the dominant leg (right). On the other hand, the results for the TA muscle in beta (OE and CE) present a higher p-val (p < 0.05) and a criticality in the location of the associated electrode clusters in the scalp topography. Indeed, while the electrode clusters identified in the CMC results of SOL in beta band and GL in gamma band are located in the central area of the scalp topography, which is spatially coherent with the underlying motor cortical area (primary and supplementary motor cortex) where the cortical drive is originated, the TA results show an occipital-region cluster whose electrodes are unlikely to pick up electrical activity from the motor cortex48,49. For these reasons, it is possible that the TA results don’t actually correspond to a cortico-muscular coupling effect but represent instead some other type of not yet fully understood synchronization mechanism.
The results of the IMC analysis provide further insight on the postural mechanisms that take place to counteract the imbalance caused by the proprioceptive vibration. Here, the IMC signals computed between pairs of muscles were decomposed into 5 frequency components, and the sets of weights associated with each component were used as a metric of connectivity in determining the networks of lower leg muscles. By comparing the resting state network topography with that recorded during execution of the postural task, we evaluated how the network reconfigured itself to shape a more effective postural strategy. The network topography highlights the groups of muscles whose activity is synchronized, showing the muscles involvement in common muscle synergies13.
Looking at the results reported in Figs. 6 and 7 it can be noticed that the adjacency matrices associated to the first two frequency components identified by the NNMF, present high (~ 1) and most likely non physiological connectivity values in both baseline and Q124. The distribution over the frequency band of these two components (the first dominated by ~ 0Hz and the second spread all over the band) further points to their artefactual nature.
Consistently with the previous results, significant differences in connectivity values and network metrics emerged among baseline and Q1. In this case, though, significant changes were observed during the OE trial as well as during the CE one (Figs. 6 and 7). In particular, higher connectivity values were observed during the execution of the postural task, as well as increased network metrics. The increased connectivity observed in the third frequency component supports the previously reported CMC-based results by confirming, even from a muscular network perspective, a stronger cortical drive expressed in terms of enhanced muscular synergies, IMC in the 16–40 Hz range is in fact thought to have a cortical origin50. Because IMC does not reflect only cortical drive to the muscles, but also common afferent inputs13, the increased connectivity observed in the 6–15 Hz range (fifth component) and in the 0–5 Hz one (fourth component) could reflect an increased inflow of subcortical inputs too50. The fact that not only cortical, but also afferent inputs are enhanced during the task execution, thus contributing to shape the postural response, is in line with the renowned fact that vibrations applied to the muscle bellies induce a stimulation of the muscle spindles9. Therefore, these proprioceptive structures are likely to be more sensitive immediately after the stimulation, increase the sensory input inflow and provide a larger contribution to the modulation of muscle activation, as suggested by our results.
In addition, the nodewise analysis highlights a strong increase in the clustering coefficient and local efficiency of the tibialis and gastrocnemius muscles in the low frequencies, around 2Hz (third frequency component, see Figs. 8 and 9). CC and LE are related network metrics which characterize the density of the network around a certain node by quantifying, respectively, the tendency of a node to form a cluster and the density of connections within the cluster (inverse of the shortest path length). A strengthening of the network at this low frequency (< 5Hz) is consistent with results reported in previous IMC studies during balance tasks 24,47,51.
A note of caution must be introduced concerning a number of factors which may influence the ability to provide a univocal interpretation of the presented results. From a methodological point of view, both CMC and IMC techniques present some limitations, specifically the arbitrariness in the choice of the number of frequency components to use in the IMC analysis, as well as the intrinsic limitations in NNMF procedures themselves13. These techniques have been traditionally used in motor tasks involving voluntary movements and steady-state contractions such as grip, while not as much in balance or postural control tasks52–54. The literature on the topic also lacks an extensive review of the factors affecting CMC and IMC, which may explain the variability observed across experimental designs, individuals etc. Finally, the current data are based on a limited cohort of young, healthy individuals. It will be of great interest to conduct further investigation on different subpopulations (such as ageing individuals) to compare the cortico-muscular recalibration strategies in the wake of the same postural challenge.