Sensory reweighting of proprioceptive information of the left and right leg during human balance control

Abstract

Pasma JH, Boonstra TA, Campfens SF, Schouten AC, Van der Kooij H. Sensory reweighting of proprioceptive information of the left and right leg during human balance control. J Neurophysiol 108: 1138-1148, 2012. First published May 23, 2012 doi:10.1152/jn.01008.2011.-To keep balance, information from different sensory systems is integrated to generate corrective torques. Current literature suggests that this information is combined according to the sensory reweighting hypothesis, i.e., more reliable information is weighted more strongly than less reliable information. In this approach, no distinction has been made between the contributions of both legs. In this study, we investigated how proprioceptive information from both legs is combined to maintain upright stance. Healthy subjects maintained balance with eyes closed while proprioceptive information of each leg was perturbed independently by continuous rotations of the support surfaces (SS) and the human body by platform translation. Two conditions were tested: perturbation amplitude of one SS was increased over trials while the other SS 1) did not move or 2) was perturbed with constant amplitude. With the use of system identification techniques, the response of the ankle torques to the perturbation amplitudes (i.e., the torque sensitivity functions) was determined and how much each leg contributed to stabilize stance (i.e., stabilizing mechanisms) was estimated. Increased amplitude of one SS resulted in a decreased torque sensitivity. The torque sensitivity to the constant perturbed SS showed no significant differences. The properties of the stabilizing mechanisms remained constant during perturbations of each SS. This study demonstrates that proprioceptive information from each leg is weighted independently and that the weight decreases with perturbation amplitude. Weighting of proprioceptive information of one leg has no influence on the weight of the proprioceptive information of the other leg. According to the sensory reweighting hypothesis, vestibular information must be up-weighted, because closing the eyes eliminates visual information. system identification; system identification; posture; asymmetry BALANCE IS DESCRIBED as the ability to maintain upright posture in a gravitational field (Niam et al. 1999) and is involved in many daily life activities, such as bipedal stance, walking, and cycling. For small deviations, the gravitational pull effectively is a negative stiffness; a deviation from a perfect upright position results in a torque that accelerates the body further away from this position. External mechanical disturbances, such as a misstep or a slip, and conflicting information of the sensory systems can disturb the equilibrium of the balance system. The central nervous system (CNS) has to cope with these disturbances to maintain the body in upright position.The CNS receives feedback about the body orientation from three main sensory systems: the visual, proprioceptive, and vestibular systems. The CNS integrates this sensory feedback and subseq...

Quantifying balance control during stance

“…This result was expected according to the sensory reweighting hypothesis, as mentioned before. Our findings are therefore also in line with previous studies investigating sensory reweighting during standing balance using system identification techniques (Peterka, 2002;Pasma et al, 2012). No changes were found in the neuromuscular controller by increasing the disturbance amplitude of the SS rotation.…”

“…As mentioned earlier, various underlying systems interact within this neuromuscular controller, allowing humans to use various balance strategies. CLSIT aims to distinguish between: (1) The contribution of each leg in generating corrective muscle forces to keep the CoM within the base of support (van Asseldonk et al, 2006) (2) The contribution from various joints -such as the ankle and the hip -in generating these forces (Boonstra et al, 2013); (3) The separate contribution from intrinsic properties of the muscle-skeletal system (passive control) and the neural components (active control) in the generation of the forces (de Vlugt et al, 2002Vlugt et al, , 2006Ludvig et al, 2011); (4) The sensitivity of the sensory systems -proprioception, vision and vestibular -and their individual contribution to neuromuscular control (Peterka, 2002;Doumas and Krampe, 2010;Jeka et al, 2010;Pasma et al, 2012); (5) The effect of sensory and motor noise on the reliability of the received information and the accuracy of the generated muscle forces (van der Kooij and Peterka, 2011). To study all the effects within the neuromuscular controller, CLSIT use specifically designed and externally applied disturbances; either mechanical (support surface motion or pushes having impact on the human body) or sensory (providing or abandoning inputs to the sensory systems) (Fitzpatrick et al, 1996;van der Kooij et al, 2005;van Asseldonk et al, 2006;Kiemel et al, 2008Kiemel et al, , 2011.…”

“…They use other strategies to maintain standing balance, which cannot prevent, however, that they are more prone to falls in case the proprioceptive or visual information is unreliable or conflicting. Support surface rotation around the ankle axis has been used to specifically evoke proprioceptive responses (Schouten et al, 2011;Pasma et al, 2012). Using such an approach for each leg individually, asymmetries in sensory reweighting between the legs can be detected .…”

“…Previous research showed that system identification techniques are useful to assess the underlying systems of standing balance, in which the response to well-known disturbances are assessed (Engelhart et al, date unknown;Peterka, 2002;Cenciarini, 2010;Pasma et al, 2012;Boonstra et al, 2013). A clear advantage is that this method takes into account the cause and effect relation and separates the contribution of the underlying systems.…”

Identification of connectivity in human motor control: exciting the afferent pathways

“…The newly developed techniques are based on a concept from the field of system identification: the application of external (mechanical) perturbations to 'open' the closed loop of motor control (Ljung, 1999;Pintelon and Schoukens, 2001). Previously this approach has successfully been applied to identify different types of reflexes in posture control (van der Helm et al, 2002;Schouten et al, 2008;Mugge et al, 2010) and to separate the contribution of the legs and joints involved in upright balance control (van Asseldonk et al, 2006;Pasma et al, 2012;Boonstra et al, 2013).…”