Learned Overweight Internal Model Can Be Activated to Maintain Equilibrium When Tactile Cues Are Uncertain: Evidence From Cortical and Behavioral Approaches

Abstract

Human adaptive behavior in sensorimotor control is aimed to increase the confidence in feedforward mechanisms when sensory afferents are uncertain. It is thought that these feedforward mechanisms rely on predictions from internal models. We investigate whether the brain uses an internal model of physical laws (gravitational and inertial forces) to help estimate body equilibrium when tactile inputs from the foot sole are depressed by carrying extra weight. As direct experimental evidence for such a model is limited, we used Judoka athletes thought to have built up internal models of external loads (i.e., opponent weight management) as compared with Non-Athlete participants and Dancers (highly skilled in balance control). Using electroencephalography, we first (experiment 1) tested the hypothesis that the influence of tactile inputs was amplified by descending cortical efferent signals. We compared the amplitude of P1N1 somatosensory cortical potential evoked by electrical stimulation of the foot sole in participants standing still with their eyes closed. We showed smaller P1N1 amplitudes in the Load compared to No Load conditions in both Non-Athletes and Dancers. This decrease neural response to tactile stimulation was associated with greater postural oscillations. By contrast in the Judoka’s group, the neural early response to tactile stimulation was unregulated in the Load condition. This suggests that the brain can selectively increase the functional gain of sensory inputs, during challenging equilibrium tasks when tactile inputs were mechanically depressed by wearing a weighted vest. In Judokas, the activation of regions such as the right posterior inferior parietal cortex (PPC) as early as the P1N1 is likely the source of the neural responses being maintained similar in both Load and No Load conditions. An overweight internal model stored in the right PPC known to be involved in maintaining a coherent representation of one’s body in space can optimize predictive mechanisms in situations with high balance constraints (Experiment 2). This hypothesis has been confirmed by showing that postural reaction evoked by a translation of the support surface on which participants were standing wearing extra-weight was improved in Judokas.

Balance Adaptation While Standing on a Compliant Base Depends on the Current Sensory Condition in Healthy Young Adults

“…This occurs by enhancing the relative amplitude of the very low frequencies and reducing the higher frequencies over time. Throughout this process, the control of balance would be shifted from the lower to the higher nervous centres, with the aim to functionally incorporate the integrative capacities of the cortex and resolve the sensory ambiguity (Lhomond et al, 2021). In the sagittal plane, the mean level of the spectrum slowly increases in amplitude, regardless of its initial value, more than in the frontal plane, concurrently with a steeper rate of increase of the low-frequency windows.…”

“…We posited that a large amount of sensory barrage during standing on foam (Jeka et al, 2004), the unfamiliar and atypical activation of foot sole skin and intrinsic muscle receptors (Duysens et al, 2008), and the abundance in muscle activation (see Latash, 2012) would be conditions favouring sensory channel reweighting and adaptation over time of body sway with task repetition, ideally leading to enhanced body stability (Lhomond et al, 2021). Therefore, we explored the possibility that balance control adaptation would actually occur, and investigated the process of adaptation under different sensory conditions during the repetition of standing on-foam trials, as a development of a recently published paper on the specific effects of distinct sensory conditions on standing balance (Sozzi et al, 2021).…”

Specific Posture-Stabilising Effects of Vision and Touch Are Revealed by Distinct Changes of Body Oscillation Frequencies

“…The data have been collected here and analysed on the basis of one single trial per subject per condition (i.e., the first trial of a series of eight trials), administered in order to investigate the effect of the sensory conditions in the adaptation to repeated stance performances. Given the inter-individual variability in the stance performance (9,176), particularly when standing on foam, this procedure is certainly a limitation however hardly avoidable because repetition of stance trials produces significant adaptation in the balancing pattern (8,127,(177)(178)(179)(180). Alsubaie et al (181) have recently shown that different measures of postural sway are reliable when recorded at two visits 1 week apart, including measures with unstable BoS and sensory conditions.…”

“…A plethora of studies has been published on this topic, including some from our group ( 4 , 5 ). Body sway when standing upright on a solid base of support is normally almost negligible in healthy subjects, witnessing accurate and precise neural control ( 6 , 7 ) based on the internal model of gravitational and inertial forces ( 8 ) and on multiple inputs from the receptors detecting the body state. The excursions of the centre of foot pressure (CoP) of subjects standing quietly on the firm ground are approximately contained within the size of a dime, even if there is a large variability in sway across different healthy subjects ( 9 ).…”

When mechanical engineering inspired from physiology improves postural-related somatosensory processes

“…iii) Afterwards the shear forces continued to increase in the same direction until a second peak was reached before reversing the forces. This second increase can be considered as a postural reaction (Lhomond et al, 2021;Saradjian et al, 2019). The duration of the postural reaction was defined as the time elapsed between these peaks.…”