Time-interval for integration of stabilizing haptic and visual information in subjects balancing under static and dynamic conditions

Abstract

Maintaining equilibrium is basically a sensorimotor integration task. The central nervous system (CNS) continually and selectively weights and rapidly integrates sensory inputs from multiple sources, and coordinates multiple outputs. The weighting process is based on the availability and accuracy of afferent signals at a given instant, on the time-period required to process each input, and possibly on the plasticity of the relevant pathways. The likelihood that sensory inflow changes while balancing under static or dynamic conditions is high, because subjects can pass from a dark to a well-lit environment or from a tactile-guided stabilization to loss of haptic inflow. This review article presents recent data on the temporal events accompanying sensory transition, on which basic information is fragmentary. The processing time from sensory shift to reaching a new steady state includes the time to (a) subtract or integrate sensory inputs; (b) move from allocentric to egocentric reference or vice versa; and (c) adjust the calibration of motor activity in time and amplitude to the new sensory set. We present examples of processes of integration of posture-stabilizing information, and of the respective sensorimotor time-intervals while allowing or occluding vision or adding or subtracting tactile information. These intervals are short, in the order of 1-2 s for different postural conditions, modalities and deliberate or passive shift. They are just longer for haptic than visual shift, just shorter on withdrawal than on addition of stabilizing input, and on deliberate than unexpected mode. The delays are the shortest (for haptic shift) in blind subjects. Since automatic balance stabilization may be vulnerable to sensory-integration delays and to interference from concurrent cognitive tasks in patients with sensorimotor problems, insight into the processing time for balance control represents a critical step in the design of new balance- and locomotion training devices.

Keywords: dynamic balance; equilibrium; haptic; quiet stance; sensory integration; sensory reweighting; vision.

Figure 1

Reweighting of visual or haptic information during tandem stance. This figure shows an elaboration of the results obtained by Sozzi et al. (2011) in one subject standing upright under tandem-stance condition. In this experiment, the subjects’ visual sensory information was shifted from vision to no-vision (no touch), while haptic simulation was from touch to no-touch (blindfolded). The sensory shifts occurred at 10 s and were involuntary. The upper panel shows the ellipses of 95% confidence interval of CoP position (mean of 50 trials) during the vision/no-vision shift (A1) and touch/no-touch shift (A2). Vision as well as haptic inflow decrease the area of the ellipse. The lower panel shows the “synchro-squeezed” (Daubechies et al., 2011) wavelet transform using a Morlet wavelet of AP CoP (upper traces) and ML CoP (lower traces) between 0.2 and 6 Hz. (B1) shows the transform during the vision/no-vision shift, (B2) during the touch/no-touch shift. The wavelet transform seen here is the mean of the transforms of 50 trials. The colors in the Figure represent the amplitude of the wavelet coefficient. Dark red represent the highest while dark blue is the lowest wavelets coefficient. Bins of 0.1 s have been chosen in order to better highlight the temporal changes in the coefficients after the sensory shift. Occluding vision or haptic information increases the wavelet coefficients in the frequencies ranging from 0.2 to 3 Hz, which indicates increase in the amplitude of the ML and AP oscillations. Higher frequency components were added up to the spectrum when sensory information was lost. The changes in the wavelets coefficient start increasing after a delay of approx. 1 s, to reach a stationary state in a few more seconds.

Figure 2

Simplified scheme of the reweighting process during quiet stance. Vestibular, proprioceptive, visual and haptic signals are coded by the peripheral receptors and reach the brain after a corresponding delay. The information is first processed in 2nd order neurons. The afferent information then diverges to higher integrating centers and may be then reweighted according to the availability and accuracy of the other sensory inputs and balance constraints. Then information converges again (Σ) in the centers responsible for the control of balance. Following a short delay the information is transferred to the spinal cord interneuronal circuitry that generates the appropriate spatio-temporal pattern of muscle activity. This implies activation of MN activity and relevant muscle force, the effect of which is measured as displacement of the center of pressure (CoP). Most likely, the main part of the interval between the shift in sensory condition and the change in CoP displacement (approx. 1–2 s) conditional to active or passive addition or withdrawal of sensory information) depends on the operation of the central mechanisms generating the adaptive gain changes.