Exp Brain Res (1997) 113:475–483

© Springer-Verlag 1997

R E S E A R C H A RT I C L E

&roles:John J. Jeka · Gregor Schöner · Tjeerd Dijkstra Pedro Ribeiro · James R. Lackner

Coupling of fingertip somatosensory information to head and body sway

&misc:Received: 25 March 1996 / Accepted: 6 August 1996

&p.1:Abstract Light touch contact of a fingertip with a stationary surface can provide orientation information that enhances control of upright stance. Slight changes in contact force at the fingertip provide sensory cues about the direction of body sway, allowing attenuation of sway. In the present study, we asked to which extent somatosensory cues are part of the postural control system, that is, which sensory signal supports this coupling? We investigated postural control not only when the contact surface was stationary, but also when it was moving rhythmically (from 0.1 to 0.5 Hz). In doing so, we brought somatosensory cues from the hand into conflict with other parts of the postural control system. Our focus was the temporal relationship between body sway and the contact surface. Postural sway was highly coherent with contact surface motion. Head and body sway assumed the frequency of the moving contact surface at all test frequencies. To account for these results, a simple model was formulated by approximating the postural control system as a second-order linear dynamical system. The influence of the touch stimulus was captured as the difference between the velocity of the contact surface and the velocity of body sway, multiplied by a coupling constant. Comparison of empirical results (relative phase, coherence, and gain) with model predictions supports the hypothesis of coupling between body sway and touch cues through the velocity of the somatosensory stimulus at the fingertip. One J.J. Jeka (✉) · P. Ribeiro Department of Kinesiology, University of Maryland, College Park, MD 20742–2611, USA; e-mail: [email protected] G. Schöner Laboratoire de Neurosciences Cognitives, Center National de la Recherche Scientifique, Marseille, France J.R. Lackner Ashton Graybiel Spatial Orientation Laboratory, National Center for Complex Systems, Brandeis University, Waltham, MA 02254, USA T. Dijkstra Department of Psychology, University of Pennsylvania, Philadelphia, PA 19104, USA&/fn-block:

subject, who perceived movement of the touch surface, demonstrated weaker coupling than other subjects, suggesting that cognitive mechanisms introduce flexibility into the postural control scheme. &kwd:Key words Posture · Somatosensation · Fingertip · Entrainment · Velocity · Human&bdy:

Introduction Flexible control of upright posture during quiet stance and locomotion requires information about the contact forces and textural properties of support surfaces derived from somatosensory receptors, namely, muscle proprioceptors and cutaneous afferents (Martin 1967; Horak and MacPherson 1995). The importance of somatosensory information becomes apparent when we encounter a slippery surface and immediately adopt a more rigid posture (e.g., “walking on eggs”) to compensate for the decreased friction of the support surface. However, our understanding of somatosensory contributions to upright stance and locomotion is primarily empirical (Dietz 1992), with relatively few theoretical models to conceptualize extensive experimental findings. We have developed a paradigm that separates the mechanical support provided by contact of the hand with a rigid surface and the somatosensory cues provided by such contact. When a standing subject lightly touches a stationary surface with a fingertip, body sway is reduced, even when contact forces are inadequate for mechanical support of the body (Holden et al. 1994; Jeka and Lackner 1994, 1995). The relationship observed between body sway and the pattern of forces at the fingertip indicates that subjects use slight changes in contact force at the fingertip to gain information about the direction of body sway, which allows attenuation of sway through appropriate postural muscle activation (Jeka and Lackner 1995). These results indicate that somatosensory information is a powerful orientation reference in the control of human upright stance.

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It is not clear, however, how somatosensory information acts on posture. In particular, one must ask whether somatosensory information forms part of the control system, so that it couples in “closed loop” into the postural system. In the present study, we address this issue with a method similar to the “moving room” paradigm that has been used to demonstrate the coupling of visual information with whole-body posture (Lee and Lishman 1975; Berthoz et al. 1979; Soechting and Berthoz 1979; van Asten et al. 1988; Dijkstra et al. 1994a, b; Peterka and Benolken 1995). Humans initiate responses that reduce body sway relative to movement of the visual world, and such compensation is thought to be driven by velocity-sensitive visual mechanisms (Schöner 1991). It is not known, however, how dynamic somatosensory information couples to body sway. Experimental results have shown that passive displacements of the arm (Brandt et al. 1977) and passive stimulation of the feet while sitting (Lackner and DiZio 1984) can result in compelling illusions of self-rotation. With a moving contact surface at the feet or hands, changing contact forces can be perceived as body movement, movement of the contact surface, or both (Lackner and DiZio 1992). Is there, however, a coherent relationship between body sway and dynamic somatosensory cues? In preliminary empirical work, we found that contact of the fingertip with an oscillating surface led the center of pressure to assume the frequency of the moving surface (Jeka et al. 1994). Here, we report a detailed account of the temporal relationship between dynamic somatosensory cues at the fingertip and head/body sway that demonstrates strong entrainment of the head and the body with the somatosensory cues. We compare our results with those of a model that predicts coupling of body sway to the velocity of the somatosensory stimulus.

Fig. 1 A schematic diagram of the experimental situation. A subject is pictured in the tandem Romberg posture on the force platform contacting the touch bar with the right index finger. The touch bar either was stationary or moved sinusoidally in the medial-lateral plane at a constant frequency (0.1, 0.2, 0.3, 0.4, and 0.5 Hz) and amplitude (≈ 4 mm). For illustration, the subject is shown exceeding the threshold force of 1 N and the alarm is sounding. In the actual experiment, the threshold was never exceeded. A video camera mounted to the ceiling directly above the subject’s head was used to measure head movements&ig.c:/f and Fz) registered by piezo-electric crystals in the corners of the force platform.

Materials and methods

Head motion

Subjects

Medial-lateral head displacement (Hx) was measured with an ISCAN video system. A rigid, hollow aluminum tube attached to an adjustable headband protruded 5 cm outward from the subject’s forehead in the sagittal plane. A light-emitting diode (LED) was attached to the end of the tube, and an ISCAN camera mounted on the ceiling tracked the movement of the LED to measure Hx displacement. The ISCAN system measures two dimensional movement in a field of view 512×256 pixels. The camera was mounted to the ceiling above the subject’s head. Because of differing subject heights, we normalized the field of view across subjects by measuring the distance between the camera and LED and computing a calibration factor for each subject. The mean resolution across subjects was 0.48 mm (Hx).

Five individuals participated, two women and three men, ranging in age from 20–30 years. All subjects were healthy and physically active, with no known musculoskeletal injuries or neurological disorders that might have affected their ability to maintain balance. All were right-handed. The procedures used in the experiment were approved by the Institutional Review Board at the University of Maryland. Informed written consent was obtained from all participants in the study. Apparatus and measures Figure 1 depicts the test situation, with a subject standing in a tandem Romberg position (heel-to-toe) on a force platform, touching with their right index fingertip a device used to measure the forces applied. Center of foot pressure The force platform (Kistler Model 9261A) measured the ground reaction forces through the feet. Medial-lateral coordinates of foot pressure (CPx) were computed from the force components (Fx, Fy,

Fingertip contact forces The “touch device” that the subject contacted with his or her index finger consisted of a horizontal metal bar (46 cm×1 cm×2 cm) supported by a metal stand. A piece of white tape marked the point of fingertip contact at the midpoint of the bar. The bar was positioned parallel to the sagittal plane of the subject, with the stand resting on a rigid wooden platform (155 cm×70 cm) that overlay the force plate and extended beyond its lateral edges. The touch-device apparatus on one side of the platform was balanced by a comparable

477 mass on the other side (see Fig. 1). If the touch bar rested on the floor independent of the force platform, then center-of-pressure movements could be due to either actual body sway or to forces applied to the touch bar. Placing the touch bar on the wooden platform insured that movements of the center of pressure reflected only movements and accelerations of the center of mass. Two dual-element, temperature-compensated strain gauges [Kulite Semiconductor, Type M(12) DGP-350–500] mounted on the metal bar transduced the lateral (FL) and vertical (FV) forces applied by the finger. The strain-gauge signals were amplified and calibrated in units of force (newtons) and a comparator could trigger an auditory tone when a specified threshold force was reached. A computer-controlled stepper motor (Compumotor SX-5751) was attached to the touch bar to move the bar in the medial-lateral plane with a resolution of 0.0005 mm. One end of the touch bar slid back and forth across a lubricated, smooth metal surface, while the other end was held in place and served as an axis of rotation in the medial-lateral plane. The stepper motor was programmed to move the bar sinusoidally at a constant amplitude (4 mm peak-to-peak at the point of fingertip contact) and at different frequencies. A potentiometer attached to the touch bar generated an analog signal of its movement, which was digitized for analysis. Even though the same amplitude was programmed for all frequencies, the recorded amplitude was 3.32 mm (0.1 Hz), 3.56 mm (0.2 Hz), 3.4 mm (0.3 Hz), 3.14 mm (0.4 Hz), and 2.82 mm (0.5 Hz). Procedure The subject stood with right foot behind left along the center of the anterior-posterior axis of the force platform. Adhesive tape was used to mark the position of the feet on the platform, so that the same foot position could be repeated throughout the entire experiment. The touch bar was then adjusted to a comfortable height (approximately waist level) and distance laterally from the subject, to make contact with the right fingertip. The subject’s task was to maintain the tandem stance with eyes closed while keeping the fingertip force on the touch bar below 1 N. The touch bar was either stationary or moving at one of five frequencies: 0.1, 0.2, 0.3, 0.4, or 0.5 Hz (total of six conditions). The subject was not told that the touch bar could move. All subjects completed every trial without ever exceeding the 1-N threshold. Before each trial, the subject took as much time as desired to assume a comfortable stance, with their fingertip on the stationary touch bar. Once ready, the subject closed their eyes and said “Go!” and the experimenter initiated data acquisition that simultaneously initiated touch-bar movement (i.e., on the moving bar trials). A computer-generated tone signaled the beginning and end of the trial. The subject stepped off the platform and rested for at least 2 min in between trials. The experimental trials were run in three blocks of six (one trial of each condition per block) for a total of 18 trials. Conditions were randomized within a block. Trial duration was 80 s and all signals were collected in real time at 60 Hz. The experiment lasted approximately 1 h. Analysis

Fig. 2 Overlaid time series of center-of-pressure (CPx), head (Hx), and touch-bar (TBx) displacement in: a a stationary-bar condition; and b a 0.5-Hz moving-bar condition&ig.c:/f

ed. The MSC is a measure of the strength of locking of body sway to movements of the touch bar. MSC increases to a maximum of 1 with an increase in coupling strength. All spectra were evaluated only at the driving frequency, as no systematic peaks were observed at other frequencies. All spectra were calculated with a Welch procedure (Marple 1987) in order to obtain consistent estimates. We used 7 segments and factor 3 zero-padding&1fn.1: . Gain was defined as the ratio of the CPx amplitude spectrum to the touch-bar amplitude spectrum at the driving frequency. This is a measure of gain relative to the surround (gain in the “world”), unlike in systems theory where gain refers to the ratio of the output signal over the input signal (gain at the “sensory level”). Time series of relative phase We calculated a discrete time series of relative phase between: CPx displacement and touch-bar displacement (TBx); and Hx displacement and touch-bar displacement. The relative phase be1

The experimental posture, tandem Romberg (heel-to-toe), was chosen to enhance medial-lateral body sway. In previous experiments, we found that the horizontal and vertical forces at the fingertip are uncorrelated with anterior-posterior body sway during heel-to-toe stance (Jeka and Lackner 1994, 1995). Consequently, we report here measures related only to medial-lateral CPx and Hx displacement. Linear systems analysis Spectral analysis was performed on all signals; the magnitudesquared coherence (MSC), the gain, and the phase were calculat-

The Welch procedure reduces the variance of the spectral estimate by breaking the signal into overlapping segments and averaging the spectral estimates of each segment. Each segment had onequarter of the length of the trial and was shifted by one-eighth of the trial length relative to the neighboring segment (i.e., overlapping segments). Factor 3 zero-padding made each segment equal in length to the entire trial so that the sampling resolution of the spectral estimate of each segment was equal to that of the full trial. The choice of 7 segments is a compromise between the maximum number of segments to achieve a good estimate of coherence and the maximum number of cycles of data within a segment to get a good estimate of phase (i.e., more segments mean shorter segments of actual data).&/fn:

478 Fig. 3 Spectral plots of CPx, Hx and TBx in each condition. Note that CPx and Hx displacement frequencies are broadband in the stationarybar condition (0.0 Hz), while prominent peaks at the driving frequencies emerge in all moving-bar conditions. CPx and Hx displacement amplitude increase dramatically from the stationary bar to the movingbar condition&ig.c:/f

tween CPx or Hx and TBx was determined as follows&fn.2:2: Significant extrema of position and velocity traces of each signal were picked. Relative phase was calculated by taking the time difference between an extremum of the target signal (CPx or Hx) and an extremum of the reference signal (TBx) and dividing this by the time difference of two extrema in the reference signal. This value was multiplied by 360° to convert relative phase to degrees. The mean and angular deviation of relative phase were calculated for each trial. 2 A more detailed description of the peak-picking method and the calculation of relative phase and angular deviation of relative phase can be found in Dijkstra et al. 1994b. Dr. Dijkstra has made a Matlab toolbox for relative phase analysis available to download from “cattell20.psych.upenn.edu” in the “/pub/tjeerd/RelPhase.box” directory. (His e-mail address is: [email protected].)&/fn:

Peak-picking was also used to calculate individual cycle-to-cycle periods of CPx and Hx displacement for each trial. Individual cycle periods were averaged as a measure of mean CP x and Hx displacement frequency within each trial. Peak-picking was not used in the stationary-bar trials, because relative phase calculations are not possible with a stationary bar (i.e., no driving signal). Consequently, in the stationary-bar trials, the most prominent peak in the power spectrum was chosen for CPx and Hx displacement frequency. Four of the fifteen stationary-bar trials (five subjects×three trials per condition) were not included in the analysis because the spectrum was not unimodal. Unless otherwise noted, one-way ANOVAs were used to test each subject’s data separately, with frequency as the independent variable at a significance level of 0.05.

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Fig. 4 a Mean CPx displacement frequency; b mean Hx displacement frequency. CPx and Hx frequencies averaged between 0.2 and 0.4 Hz in the stationary-bar condition (0.0 Hz), but then decreased and increased with the frequency of the moving touch-bar. Note that individual subject’s data are artificially offset at each driving frequency so that the error bars are not obscured. Error bars in all figures are the SEM&ig.c:/f

Results A clear entrainment of body sway to the touch bar was observed in the moving-bar trials. The contrast between stationary-bar and moving-bar trials can be seen in Fig. 2, which shows overlaid time series of CPx, Hx and TBx displacement in a stationary-bar trial (Fig. 2a) and a trial in which the bar is moving at 0.5 Hz (Fig. 2b). In the stationary-bar trial, CPx and Hx displacement have no prominent characteristic frequencies. In the moving-bar trial, CPx and Hx displacement assume the same frequency as the touch bar. The strong influence of touch-bar movement on head and body sway is further illustrated in Fig. 3, which shows spectral plots of CPx and Hx displacement from individual trials of one subject for each condition. The pronounced spectral peaks of CPx and Hx displacement occur at the same frequency as the touch bar in each condition. At the higher touch-bar frequencies (e.g., 0.4 Hz and 0.5 Hz), an increase in the low-frequency components of CPx displacement was also observed, but with no consistent peak at any particular low-frequency com-

Fig. 5 a Mean CPx rms (RMS); b mean Hx rms. All subjects displayed a steady increase in displacement amplitude with increasing frequency. At 0.5 Hz, CPx and Hx displacement amplitudes were approximately twice that of the stationary-bar condition&ig.c:/f

ponent. Despite the strong influence of touch-bar movement on body sway, questioning after the experiment indicated that only one of the five subjects ever perceived the touch bar as moving during the experiment&fn.3:3. Mean frequency Figure 4 shows that the mean CPx and Hx frequency, collapsed across trials for each subject, matched the touchbar frequency in each condition, with some drop-off at 0.5 Hz. With a stationary bar, the mean CPx displacement frequency was approximately 0.2–0.4 Hz (broadband spectrum); Hx frequency averaged close to 0.2 Hz. In the moving-bar conditions, both CPx and Hx shifted to the frequency of the touch bar. CPx and Hx mean frequency showed a significant main effect for Frequency for all subjects (P0.2). Lateral force averaged slightly above zero at each frequency and also showed no effect for Frequency for all subjects (P>0.1). These results indicate that subjects applied very small, lateral (rightward) and medial(leftward) forces with a slight lateral bias. The lack of differences in contact forces across different frequencies indicates that subjects maintained comparable contact forces with a stationary or moving contact surface, even though four of the five subjects indicated no conscious perception of touch-bar movement. Root-mean-square values CPx and Hx rms in the stationary-bar condition was similar to that found in previous studies (Jeka and Lackner 1994, 1995), averaging between 0.2 and 0.3 cm, but increased significantly in the moving-bar conditions. RMS values for CPx and Hx in the 0.5 Hz condition were almost double those found with a stationary bar (0.0 Hz). Figure 5 illustrates that CPx and Hx rms increased with

Fig. 7 Mean relative phase for a CPx versus TBx and b Hx versus TBx. Both CPx and Hx led touch-bar movement at 0.1 Hz (positive phase) and lagged behind touch-bar movement at frequencies higher than 0.2 Hz&ig.c:/f

increasing frequency of the touch bar. A significant effect for Frequency on rms was found for all subjects (P