doi:10.1152/jn.00504.2007 99:595-604, 2008. First published 21 November 2007;J NeurophysiolEly Rabin, Paul DiZio, Joel Ventura and James R. LacknerFeedbackFreedom on Postural Control With Light Touch Influences of Arm Proprioception and Degrees of

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Influences of Arm Proprioception and Degrees of Freedom on PosturalControl With Light Touch Feedback

Ely Rabin,1 Paul DiZio,2 Joel Ventura,2 and James R. Lackner2

1New York College of Osteopathic Medicine, New York Institute of Technology, Old Westbury, New York; and 2Ashton Graybiel SpatialOrientation Laboratory, Brandeis University, Waltham, Massachusetts

Submitted 4 May 2007; accepted in final form 10 November 2007

Rabin E, DiZio P, Ventura J, Lackner JR. Influences of armproprioception and degrees of freedom on postural control with lighttouch feedback. J Neurophysiol 99: 595–604, 2008. First publishedNovember 21, 2007; doi:10.1152/jn.00504.2007. Lightly touching astable surface with one fingertip strongly stabilizes standing posture.The three main features of this phenomenon are fingertip contactforces maintained at levels too low to provide mechanical support,attenuation of postural sway relative to conditions without fingertiptouch, and center of pressure (CP) lags changes in fingertip shearforces by �250 ms. In the experiments presented here, we testedwhether accurate arm proprioception and also whether the precisionfingertip contact afforded by the arm’s many degrees of freedom arenecessary for postural stabilization by finger contact. In our firstexperiment, we perturbed arm proprioception and control with bicepsbrachii vibration (120-Hz, 2-mm amplitude). This degraded posturalcontrol, resulting in greater postural sway amplitudes. In a secondstudy, we immobilized the touching arm with a splint. This preventedprecision fingertip contact but had no effect on postural sway ampli-tude. In both experiments, the correlation and latency of fingertipcontact forces to postural sway were unaffected. We conclude thatpostural control is executed based on information about arm orienta-tion as well as tactile feedback from light touch, although precisionfingertip contact is not essential. The consistent correlation and timingof CP movement and fingertip forces across conditions in whichpostural sway amplitude and fingertip contact are differentially dis-rupted suggests posture and the fingertip are controlled in parallel withfeedback from the fingertip in this task.

I N T R O D U C T I O N

Suppression of body sway by sensory feedback from non-supportive fingertip contact is dependent on signals generatedby deformation of the fingertip (Holden et al. 1987, 1994; Jekaand Lackner 1994). Any force applied to the body may havesome mechanical effect on postural sway. However, earlierstudies using this paradigm have shown that subjects sponta-neously adopt fingertip force levels of �40 g. This precisionfingertip contact is analogous to precision grip in which gripforces are maintained at appropriate levels to maintain grasp ofan object through changes in load forces, such as duringmoving or swinging the object (cf. Johansson 1991; Johanssonand Westling 1984, 1987; Johansson et al. 1992). Precisionfingertip contact is similar: although no grip is involved,near-constant contact forces are maintained throughout move-ments of the touched surface relative to the body (i.e., duringpostural drifts and corrections). The �40-g contact force is inthe center of the range of maximal sensitivity of mechanore-

ceptors in the glabrous skin of the fingertip (Westling andJohansson 1987) and are optimal for maintaining the fingertipcontact in a manner similar to finger control during precisiongrip (Jeka and Lackner 1995). The low contact force levelsduring precision touch are inadequate to account mechanicallyfor the magnitude of attenuation of postural sway in compar-ison to sway during standing without fingertip contact (Holdenet al. 1994). This suggests that attenuation of postural swaywhen lightly touching is due to the fingertip providing infor-mation about sway that enables compensatory motor adjust-ments to be made before proprioceptive, visual, or vestibularthresholds are exceeded for triggering compensations. Thestabilizing effect of fingertip contact is especially striking inlabyrinthine-defective individuals who are inherently unstable(Lackner et al. 1999) and in subjects using light touch tooverride the destabilizing effects of vibration of the peroneuslongus and brevis muscles when standing in a heel-to-toestance (Lackner et al. 2000).

Postural sway during precision fingertip contact is charac-terized by a highly stereotypical pattern of center of footpressure (CP) shifts lagging parallel changes in fingertip con-tact forces by �250–300 ms (Jeka and Lackner 1995; Jekaet al. 1996; Lackner et al. 1999; Lackner et al. 2000). Changesin EMG activity in the peroneus longus muscles, the anklemuscles largely responsible for inverted pendulum sway inheel-to-toe posture, follow fingertip shear force changes by�150 ms (Jeka and Lackner 1995). By contrast, when subjectslean on their hand for support, there is no time lag betweenfingertip forces and CP: sway energy is passively absorbedthrough contact with the support surface. Contact force levelsduring leaning on the fingertip are around 10 N (Holden et al.1994; Jeka and Lackner 1994, 1995).

The stabilizing effects of light fingertip contact are enhancedor degraded depending on the orientation of the touching arm(Rabin et al. 1999). Touching a surface with the arm extendedattenuates postural sway in the direction of the extended armmore than sway orthogonal to the extended arm. As the bodysways to maintain the fingertip stationary, the configuration ofthe arm has to undergo greater changes for sway parallel asopposed to orthogonal to the touching arm. This creates asensory advantage in terms of the ratio of proprioceptivefeedback to body sway (Rabin et al. 1999).

The goals of the present experiments are to determine theextent to which precision fingertip contact and proprioceptivefeedback relating fingertip location to the torso each contribute

Address for reprint requests and other correspondence: E. Rabin, New YorkCollege of Osteopathic Medicine of New York Institute of Technology, OldWestbury, NY 11568-8000 (E-mail: erabin@nyit.edu).

The costs of publication of this article were defrayed in part by the paymentof page charges. The article must therefore be hereby marked “advertisement”in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

J Neurophysiol 99: 595–604, 2008.First published November 21, 2007; doi:10.1152/jn.00504.2007.

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to the stabilization of posture. We address these issues in twoexperiments in which subjects stood as still as possible witheyes closed in the tandem stance. In these experiments, wedisrupted arm proprioception and limited the degrees of free-dom of the arm and assessed the effects on precision fingertipcontact (measured by fingertip contact forces), on posturalcontrol (measured by center of pressure sway amplitude), andon the temporal relationship of the two (characterized by peakcross-correlations and associated time lags).

In our first experiment, we perturbed proprioception byvibrating the biceps brachii muscle as subjects lightly toucheda stationary surface. Vibrating the surface of a skeletal muscleat �120 Hz excites primary and secondary spindle receptorswithin the muscle and can cause both reflexive contraction, atonic vibration reflex (TVR), and illusory motion of the limbsegment controlled by the vibrated muscle in the directionassociated with lengthening of the vibrated muscle (cf. Calvin-Figuiere et al. 1999; Cody et al. 1990; Gilhodes et al. 1986;Goodwin et al. 1972a,b). Vibrating the biceps brachii causesthe muscle to contract and the elbow to feel more extendedthan it actually is. It is important not to confuse the motoroutput of the tonic vibration reflex (elbow flexion in our case)as an effect of perturbed proprioception. However, we attributean unawareness of the TVR or lack of correction for the TVRto joint misperception of joint orientation from spindle dis-charge from vibration. Therefore we interpret changes in pos-tural or fingertip control during muscle vibration accompany-ing unawareness of or lack of correction for greater elbowflexion during biceps vibration as proof of proprioceptiveinfluence of the vibrated muscle.

In our second experiment, we reduced the degrees of free-dom of the arm by immobilizing the entire arm, from theshoulder to the fingertip, relative to the trunk. This comple-ments our first experiment by eliminating any motor contribu-tion of the arm and effectively making arm proprioceptionrelatively constant since the arm joints cannot change. Anyeffect of immobilizing the arm on postural control can beattributed to the loss of control the fingertip apart from posture,but not to effects of proprioceptive feedback. A null effect ofarm immobilization would allow us to rule out a contributionof the active control of precision fingertip contact to theefficacy of this postural control system. A null effect ofremoving the degrees of freedom of the arm would also suggestthat any effect of biceps brachii vibration in experiment 1 asdue to altered proprioceptive feedback rather than alteredmotor output.

To evaluate the interaction of these arm control perturba-tions and touch feedback on postural stability in each experi-ment, both experimental designs balanced these conditionswith control conditions of touch and no-touch with unperturbedarm control.

M E T H O D S

Experiment 1. Perturbation of arm control and feedback

SUBJECTS. Eight healthy right-handed students, six males and twofemales, took part after giving informed consent to a protocol ap-proved by the Brandeis Human Subjects Committee. They ranged inage from 19 to 38 yr. All were without neurological or skeletomus-cular disorders that could have influenced their balance.

APPARATUS. The test situation and apparatus are illustrated in Fig. 1A.The subject stood on a Kistler force platform (Model 9261A) thatmeasured the reaction forces generated at the feet. An ISCAN videomonitoring system tracked a light emitting diode attached to a head-band the subject wore. The lateral shear and vertical fingertip contactforces were measured with a touch bar instrumented with straingauges. The entire set-up was surrounded on the back and both sidesby a safety railing. All data were digitally sampled at 60 Hz.

CP. The coordinates of CP were computed by Kistler software fromFx, Fy, and Fz force components detected by piezo-electric crystals inthe corners of the platform.

POSTURAL KINEMATICS. To measure sway of the body, the medial-lateral and anterior-posterior components of head sway were com-puted from the movements of the head-mounted light-emitting diode(LED) detected by the ISCAN video recording system. To character-ize the influence of muscle vibration on arm control, we measured themotion of the touching arm of two of the subjects. Markers on theright shoulder, elbow, wrist, and finger were recorded with anOptotrak system, at 200 Hz, and elbow joint angle was computed.

FINGERTIP CONTACT FORCES. The touch bar device (Holden et al.1994) was positioned laterally in relation to the subject and adjustedto a comfortable height. The vertical and lateral sides of the touch barwere instrumented with semiconductor strain gauges (Kulite ModelDGP-350-500) in a full bridge configuration. It rested on a platformriding on the Kistler force plate and was balanced on the opposite sideof the platform by a comparable mass. The lateral and vertical forcesignals from the touch bar strain gauges were amplified and calibratedin Newtons of applied force. The calibration was accurate within 5%.To assure that fingertip forces would not provide significant mechan-ical support, an auditory signal was triggered to alert the subject if aforce level of 1 N (102 g) on the touch bar was exceeded.

PROCEDURE. The subjects’ task was to stand as still as possible witheyes closed in the heel-to-toe tandem Romberg stance for the durationof each 25-s trial. The four experimental conditions varied precisiontouch of the right index fingertip and vibration of the right bicepsbrachii muscle (no-touch, no-vibration; touch, no-vibration; no-touch,vibration; and touch, vibration). The physiotherapy vibrator (0.45 kg;Sears, Model 793,2250) was held in place on the upper arm by elastictensor bandages with the head positioned over the biceps brachiitendon �4 cm above the elbow joint. This arrangement ensured thatcontact of the vibrator with the upper arm provided no external spatialreference cues to the subject. The vibrator was fastened to the arm inall conditions. When activated it provided 120 pulse/s, �2 mmamplitude. Subjects were instructed to hold their finger just above thetouch bar in the conditions not involving finger touch.

Each trial began with the subject assuming the test posture withright forefinger either above or in contact with the bar as appropriate.The subject said “go” when ready and the trial was initiated. Invibration trials, the vibrator was remotely activated 4 s after thesubject said “go.” Prior to the start of the experiment, the subject wasgiven a couple of practice trials with and without touch so that he orshe could feel how much force could be exerted without setting off thetouch bar alarm. A three-sided safety railing surrounded the subject infront and on the sides at waist height. If subjects touched the safetyrail during the trial or moved their feet, the trial was repeated so thateach subject had four “clean” repetitions of each condition. Theconditions were randomized in blocks of four trials and five blockswere run.

ANALYSIS. A heel-to-toe stance was employed in the present studyto enhance medial-lateral sway. In other studies, we have shown thatanterior-posterior sway is small in this stance and is unrelated tolateral and vertical forces at the fingertip (Jeka and Lackner 1994).Therefore we concentrated our analyses on medial-lateral body sway

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measures. For each trial, the time series of medial-lateral CP and ofhead position was reduced to a mean absolute amplitude, MAA

MAA �1

Nt�i�1

Nt

�xi � x��

where Nt is the number of data points in the time series. The samecomputation was used to summarize the average lateral touch barreaction force of a trial.

To determine whether vibration biased postural sway, the lateraldrift of CP and of the head in each trial was calculated by subtractingthe initial point from the final point of a maximum likelihood linear(fit) estimate of each medial-lateral CP and head time series, and thenaveraging across trials and subjects. This approach minimizes anybiasing effects of high-frequency postural corrections.

To determine the effect of biceps vibration on arm control, wecomputed for the two subjects whose arm motion was measured thedifference between initial and final elbow angles during trials with andwithout vibration.

Cross correlations were calculated between CP and contact forcesat the fingertip at 16.07 ms/step over �1,500 ms to identify when the

maximum correlations occurred. r(l)max was calculated for each trialas the maximum of

r�l� �1

Nl�j�1

Nl

FjCPj�l

where Fj is the normalized fingertip shear force, CPj�l is the normal-ized CP data shifted l steps (16.07 ms/step) relative to F, and Nl is thenumber of overlapping samples of the trial for each l. The time lagassociated with the maximum correlation, lmax, was determined fromthe time lags l at which each r(l) was maximal.

A 2 � 2 repeated-measures MANOVA (Pillai’s trace) evaluated thesignificance of fingertip contact (touch, no touch) and arm proprio-ception (vibration, no vibration) on postural stability measures(MAAs and mean lateral drifts of CP and head). The effect of trialorder was not significant by an initial 2 � 2 � 5 MANOVA, so theresults were averaged across trials for each subject. When vibra-tion-touch interactions were significant, Tukey tests were used toevaluate differences between individual conditions. One-wayANOVAs determined the significance of differences in fingertipcontact forces, and correlations and lags of fingertip contact force

FIG. 1. Experimental setups for experiment 1 (A) and experiment 2 (B). C: 4 conditions of experiment 2. Subjects wore the splint, even when the arm wasnot immobilized by it, to control for any effect of the inertia of the cast on postural control.

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and CP changes between conditions of fingertip contact (touch,touch � vibration).

Experiment 2. Reduction of arm degrees of freedom

SUBJECTS. Four female and seven male subjects, ages 18–46, par-ticipated after giving informed consent. All were right handed andwithout known sensory-motor or vestibular anomalies that could haveinfluenced their performance. They provided informed consent to aprotocol approved by the Brandeis Human Subjects Committee.

APPARATUS. Subjects stood on a force plate (surface area 60 � 40cm, Kistler Model 9286A), which measured lateral and fore-aft shearforces and normal force, from which CP was calculated (see Fig. 1B).An Optotrak 3020 system recorded the ongoing position of LEDsfixed to the head, right shoulder, elbow, wrist, and fingertip of theindex finger. All signals were sampled at 100 Hz by a computer. Thetouch bar device used in experiment 1 was employed to measurelateral and vertical finger contact forces.

CONDITIONS. The experimental conditions balanced two indepen-dent variables: fingertip contact or none and arm free or immobilized(see Fig. 1C). The four conditions were: right arm immobilized, nottouching; right arm immobilized, touching; right arm free, not touch-ing; and right arm free, touching.

IMMOBILIZATION OF THE ARM. The right upper arm, forearm, andhand were immobilized with respect to the trunk with a modified armsplint (“Freedom Gunslinger,” AliMed, Dedham, MA). The rightindex finger was immobilized relative to the hand by inserting thehand into a large paper cup that was then filled with insulating foam(Froth-pak, Foam Products Maryland Heights, MD). The subject worea rubber glove to protect the skin from the foam. A small hole in thebottom of the cup exposed the tip of the index finger. The rubber glovewas cut away from the fingertip to allow contact of the pad ofthe fingertip with the touch plate. To control for a possible influenceof the weight of the splint (1.3 kg), subjects wore the splint strappedto their trunk without their arm in it for the trials with the arm free.

The difficulty in maintaining stable fingertip contact while the armwas splinted rendered the alarm more distracting than helpful tosubjects. Consequently, after initial demonstration of the desired lighttouch force levels, we eliminated the auditory feedback about fingertipcontact, and subjects were simply instructed to touch as lightly aspossible and not to lean on their finger.

ANALYSIS. We employed the tandem stance to enhance mediallateral instability and accordingly restricted our analyses to medial-lateral postural sway and contact forces. MAA of CP, head, shoulder,and fingertip contact forces, and mean maximum correlations and lagsof CP and fingertip contact forces were computed using the sameprocedures as in experiment 1. Ranges of motion of the joints of theright arms were determined using maxima and minima of joint anglescalculated from the wrist, elbow and shoulder marker data. A 2 � 2repeated-measures MANOVA (Pillai’s trace) tested for effects of armimmobilization and fingertip contact. Pairwise comparisons with Bon-ferroni corrections for multiple comparisons evaluated the signifi-cance of differences between conditions.

To determine the maximum extent to which the reduction ofpostural sway during fingertip contact can be accounted for bymechanical forces at the fingertip, we compared differences in powerof postural sway with and without fingertip contact to power offingertip contact forces while touching. Using the method devised byHolden at al. (1994). Power of postural sway is calculated by P �(2�2If 3/n)[msgMAA/(dhmsg � 4�If2)]2 where I is lateral moment ofinertia of the subject’s body about the ankle, f is the frequency of bodysway, n is time, g is the acceleration due to gravity, MAA is the meanabsolute amplitude of the center of pressure, dh is the height of thecenter of gravity above the ankle, and ms is the mass of the subject’s

body. Power absorbed through fingertip contact forces is calculated byP � 4Tf [msgMAA/(dhmsg � 4�If2)], where T is torque, which is theforce at the fingertip times the elevation from the ankles to thefingertip.

R E S U L T S

Experiment 1. Perturbation of arm control and feedback

WHEN TOUCHING, POSTURAL SWAY WAS GREATER DURING BICEPS

MUSCLE VIBRATION. Figure 2 shows for one subject the effectsof biceps vibration on medial-lateral fingertip shear-force, CP,head sway, and elbow angle of the touching arm. Thesepatterns reflect the trends observed in all subjects. ANOVAshowed a significant interaction effect of vibration and touchon CP sway amplitude (F � 15.80, P � 0.008). Amplitudes ofCP and head motion in the touch � vibration condition (�0.6and 1.8 cm, respectively) were significantly greater than in thetouch, no vibration condition (�0.3 and 0.5 cm; Tukey testsP � 0.05; Fig. 3A). Vibration had no effect on postural swaywhen there was no fingertip contact. Without touch, the am-plitude of both CP (�1 cm) and head (�2 cm) were greaterthan with fingertip contact without vibration (P � 0.05).

Arm vibration coupled with touch led to shifts in headposition (see Fig. 3B) toward the side of the touching fingertip(rightward) by �3.0 cm, (1-sample t-test, P � 0.05). A typicalshift can be seen in the top left of Fig. 2. CP also shiftedrightward by �0.7 cm. There were no significant shifts of CPor head position in the other conditions.

When asked for their impressions, subjects either reportedthat they did not intentionally change their elbow angle or thatit was constant throughout the trial. They attributed theirinstability to poor ankle control or balance in general. Themean elbow flexion during touch and vibration, 8.9 � 3.4°,was greater than without vibration, 0.6 � 2.4°.

VIBRATION DID NOT PREVENT PRECISION FINGERTIP CONTACT.

During biceps vibration, all subjects maintained lateral andvertical forces on the fingertip below the 1 N threshold fortriggering the touch plate force alarm (data from individualtrials are shown at the top of Fig. 2; and summary results inFig. 3C). The lateral forces in both conditions with touchaveraged �0.2 N; the vertical forces were �0.7 N. Normalcontact forces were higher within this range during trials withvibration (P � 0.03). This is not likely solely an effect ofvibration per se because an elbow flexion from a tonic vibra-tion reflex in this posture would lift the finger and reducenormal force.

VIBRATION DID NOT AFFECT THE CORRELATION AND TIMING OF

POSTURAL SWAY AND FINGERTIP SHEAR. Lateral shear forces atthe fingertip led changes in CP by �250–300 ms in touchconditions with and without arm vibration. This relationshipcan be seen in the individual trial data in Fig. 2 (top). The meancorrelation between lateral shear forces at the fingertip and CPwas r � �0.55 (significance of correlation P � 0.001; Fig.3D). Vibration had no significant effect on this correlation.

Experiment 2. Reduction of arm degrees of freedom

The splint successfully immobilized the right arm. Theangular motion of the wrist, elbow and shoulder were signifi-cantly reduced in the immobilization conditions: the range of

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“wrist” (i.e., fingertip-wrist-elbow) anglular displacementdropped to �1° from �11° without the splint (F � 24.62, P �0.001); the mean range of elbow angle decreased to �1° from�2.5° (F � 17.78, P � 0.002), the range of shoulder angle alsodiminished with fingertip contact (F � 5.96, P � 0.035).

TOUCHING STABILIZED POSTURE, REGARDLESS OF ARM MOBILITY.

Figure 4 shows time series of one subject’s individual trial datasegments. Sway amplitudes of the CP and shoulder during touchdo not differ whether the arm is immobilized (left) or free (right).Mean amplitudes of CP sway were �0.85 cm without fingertipcontact and �0.35 cm with fingertip contact (F � 66.04, P �

0.001; Fig. 5A). The same effect was observed for head (F �30.74, P � 0.001; Fig. 5A) and shoulder (F � 38.98, P � 0.001;Fig. 5B). Immobilizing the arm had no significant effect on swayamplitudes.

IMMOBILIZING THE ARM PREVENTED STATIONARY FINGERTIP

CONTACT. Casting the arm reduced the spatial stability of thefingertip during touch trials. When the touching arm was free(Fig. 4, right) the fingertip shows minimal displacementsrelative to the touch plate, and contact forces are lower com-pared with when the arm was splinted (Fig. 4, left). Meanamplitudes of fingertip movement were �0.1 cm when the arm

FIG. 2. Time traces for 1 subject’s medial-lateral fingertip shear force magnitude (N), medial-lateral movement of center of foot pressure (CP, cm), head (cm),and elbow angle (°) during trials during trials with touch and vibration (left) and touch without vibration (right). The 1st 3 measures were recorded for all subjects,but the last was only recorded for 2 subjects. Note that during biceps vibration (left), the decreased stability of CP, the positive (rightward) shift of the head andelbow flexion, while fingertip forces occupy a similar range with (left) and without (right) biceps vibration. Note also the temporal lag of CP motion behindsimilar fingertip shear force fluctuations.

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was free and �0.2 cm when immobilized (F � 113.74, P �0.001; Fig. 5B). When the arm was not immobilized, subjectsmaintained mean levels of contact force well below 1 N (Fig.5C). When the arm was immobilized fingertip contact forceswere significantly greater (�3 N for both normal and shearcomponents; paired sample t-test P � 0.001); and the fingercould not be maintained in continuous contact with the surface.

Comparing differences in power of postural sway with andwithout fingertip contact to power of fingertip contact forceswhile touching, we determined that the reduction in postural

sway during fingertip contact cannot be accounted for by theenergy “absorbed” by the fingertip contact forces. Assuming amoment of inertia of 67 m2kg, a mass of 66 kg, a CG-ankledistance of 1 m, and empirical values for postural swayfrequency (centroid of the frequency bandwidth, 0.3 Hz), meanMAA, and fingertip force values from our data, we determinedthat the power absorbed through fingertip contact is much lessthan the difference between power of postural sways with andwithout touch. Fingertip contact forces when the arm issplinted (3.5 N) can account at most for only 0.35 mW of a

FIG. 3. Summary results for experiment 1. Error bars are SD (n � 8).

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2.4-mW reduction in postural sway power or �15% of theactual reduction. Contact forces with the arm free (�1 N)account for a mechanical reduction at most of 0.1 mW of swayenergy, �4%. The rest of the energy reduced by fingertipcontact must come from improved postural muscle controlrelated to sensory feedback from fingertip contact.

ARM IMMOBILIZATION HAD NO EFFECT ON THE CORRELATION AND

TIMING OF POSTURAL SWAY AND FINGERTIP SHEAR. In all con-ditions with fingertip contact, the center of foot pressure“echoed” peaks in fingertip shear forces with a �300-ms delay.This difference is clearly visible when precision fingertipcontact is defeated by splinting the arm (Fig. 4, left) makingforces at the fingertip larger. Fingertip shear force correlatedmaximally to CP (r � �0.5; significance of correlation P �0.001) with CP lagging fingertip shear by �250–300 ms. Armimmobilization did not affect the relative timing of this rela-tionship, but the correlation coefficient was lower when thearm was immobilized (paired sample t-test, P � 0.003).

D I S C U S S I O N

Biceps brachii vibration during light fingertip contact dis-rupted postural stability without affecting precision fingertipcontact. Immobilizing the arm with a splint prevented contin-uous fingertip contact, but the stabilizing effects of fingertipcontact on posture persisted. In all cases with fingertip con-tact—even when the either precision fingertip contact wasprevented by the arm cast and when postural control wasdegraded by biceps brachii vibration—the timing of fingertipcontact forces and feet CP movement was the same, �250 ms.These combined results reveal the overlaying sensory integra-tion and motor control mechanisms that govern this highlyeffective postural control, discussed in the text below.

The presence or absence of the alarm signal when the 1 Nthreshold of fingertip force was exceeded had no influence onthe control of posture in this study. In experiment 1, subjectsmaintained contact forces below the threshold and never trig-gered the alarm. In experiment 2, when the arm was immobi-lized, the alarm was turned off and postural sway was attenu-ated virtually as much as in experiment 1.

The greater average contact force at the fingertip with thearm splinted had no additional benefit in terms of decreasing

postural sway amplitude nor did it disrupt the timing offingertip contact forces and CP. This suggests that the samesensorimotor postural control processes were engaged whenthe touching arm had all or none of its degrees of freedomavailable. Our analysis of power of postural sway and offingertip contact forces estimated that the energy “absorbed”by the fingertip contact forces was much less than the posturalenergy “saved” by fingertip contact, relative to the sway in theno-touch conditions. This supports the notion that the improve-ment in postural control with fingertip contact is due to addi-tional sensory information to drive postural control rather thanmechanical support. The assumptions of our mathematicalanalysis, that the entire body is a rigid inverted pendulum andthat forces applied at the fingertip are in phase with posturaloscillations, are extremely conservative. In reality, the 250- to300-ms temporal lag of postural sway behind fingertip contactforces would only reduce the amount of energy absorbed byfingertip contact. This means that the mechanical benefit offingertip contact, even when the arm is immobilized, is evensmaller than our analysis indicates. Mechanical forces at thefingertip could account maximally for about 15% of the swayattenuation achieved with the arm splinted and 4–5% of thereduction achieved with the arm free.

Fingertip contact forces caused by postural drift can be usedto control posture without precision fingertip contact control

The main effect of arm immobilization, higher finger contactforces, demonstrate that the degrees of freedom of the armprincipally allow fingertip contact forces to be �1 N as thebody sways. The low contact forces during biceps vibrationsuggest that the degrees of freedom distal to the elbow aresufficient to compensate for altered biceps control during vibra-tion. Nevertheless, the unchanged effectiveness of postural controlwith feedback from fingertip forces when the arm is splintedindicates that the precision control of the fingertip with the degreesof freedom of the hand and arm is not necessary for acquiringuseful spatial information to control posture.

Tactile feedback from nonsupportive contact of the shoulder(Rogers et al. 2001) or the head or neck (Krishnamoorthy et al.2002) with a stationary cue will attenuate postural sway aswell. Our arm immobilization condition indicates that the

FIG. 4. Time traces for 1 subject’s medial-lateral fingertip shear force magnitude (N) and medial-lateral movement of center of foot pressure (CP, cm),shoulder (cm), and fingertip (cm), during trials with touch with the arm immobilized arm (left) and touch with the arm free (right). Note that during armimmobilization (left), the large-amplitude fingertip forces and the fingertip movement phase locked with the shoulder, whereas CP and shoulder amplitude occupya similar range with (left) and without (right) arm immobilization. Note also the temporal lag of CP motion behind similar fingertip shear force fluctuations.

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coordination of fingertip and posture can be generalized acrossdifferent degrees of freedom. An analogous spontaneous ad-justment in a different domain is the automatic recruitment ofthe lips to compensate for perturbed jaw movements whensubjects are producing speech sounds (Kelso et al. 1984). If astop consonant sound is being produced and the jaw is me-

chanically prevented from bringing the lips together to producebilabial closure, then the lips are spontaneously adjusted inshape to compensate for the decreased closing of the jaw. Inthe present experiment, with the arm immobilized, the com-pensations introduced by the rest of the body represent a motorequivalent strategy to maintain precision fingertip contact.

FIG. 5. Summary results for experiment 2. Error bars are SD (n � 12).

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The disruption of precision fingertip contact by immobiliz-ing the arm without disturbing postural control of the rest of thebody is a unique finding in this area of postural controlresearch. Touching a moving surface (Jeka et al. 1997, 1998),which one might expect to disturb fingertip contact, does theopposite: subjects maintain light fingertip contact, and insteadpostural sway increases by entraining to the frequency of thesurface oscillation (Jeka et al. 1997). Even biceps vibration inthe present study, which can cause reflexive arm movements,did not disturb precision fingertip contact, but destabilizedposture instead. We previously demonstrated that spatial con-stancy of the fingertip was not essential for postural stabiliza-tion: light contact with a slippery surface on which the fingertipslides attenuated sway as much as contact with a rough surface(Jeka and Lackner 1995).

Proprioceptive information from the arm can resolveambiguities of fingertip force signals

Although it is noteworthy that postural sway was signifi-cantly reduced by finger contact even during biceps vibration,the destabilizing influence of biceps vibration compared withtouch without vibration illustrates the importance of an accu-rate representation of the arm. It is likely that the increase ofpostural sway during vibration and touch is due to a distortionof afferent and efferent information about arm configuration.Fingertip shear forces reflect an ambiguous sum of contribu-tions from many sources, including postural drift and armmovements—a confound that can be reduced with accurateproprioceptive feedback about the arm. Biceps vibration cre-ates false proprioceptive feedback signals and tonic vibrationreflexes that introduce arm movements that contribute to fin-gertip shear. If the ambiguous sum of trunk movement and armmovement is resolved using erroneous elbow proprioception,then fingertip shear forces caused by movements at the elbow(including any tonic vibration reflex-related movement) willnot be discriminated accurately from shear forces caused bypostural sway. The result would be inappropriate posturaladjustments and greater sway amplitudes. The observed grad-ual elbow flexion and rightward postural repositioning of thehead and body toward the location of fingertip contact duringtouch with vibration is consistent with this interpretation.

The elbow flexion during touch and vibration in principlecould be a reflexive motor effect of vibration, a volitionalresponse to biased elbow proprioception, or a combination ofboth. The elbow flexion could be from a tonic vibration reflex.If so, subjects might interpret the force change at the fingertipas owing to leftward drift of the body, rather than elbowflexion, and correct by swaying to the right. Alternatively,subjects may voluntarily flex their elbow in response to illusoryelbow extension arising from biceps vibration (Goodwin et al.1972a–c). This would be coupled with rightward posturalmovements toward the touch plate to maintain fingertip contact(Cordo and Nashner 1982; Marsden et al. 1981). The extent towhich the elbow flexion is reflexive or volitional remainsunclear. Nevertheless, in either case proprioceptive feedback iscritical in contextualizing the fingertip feedback to executeappropriate postural control. The null effect on postural stabil-ity of splinting the touching arm in experiment 2 supports theinterpretation that the results of experiment 1 are due to effects

of proprioceptive feedback about arm movement rather than toarm movement itself.

This finding concerning the integration of tactile and pro-prioceptive feedback is related to previous experiments show-ing effects of arm control on posture. Lackner (1988) showedthat vibration-induced reflexive contraction of the tricepsbrachii muscle can lead to apparent motion of the trunk towardthe forearm if the extension of the forearm is physicallyprevented by strapping it to a wall of the experimental chamberand locking the trunk in place. Quoniam et al. (1990) reportedpostural shifts in standing subjects during triceps brachii mus-cle vibration when they were making hand contact with asurface with the vibrated arm. They considered that tricepsvibration moved the forearm into reflexive extension butcaused the elbow to be perceived as being more flexed than itactually was and that consequently subjects voluntarily com-pensated with a backward shift of the body (cf. Hagbarth andEklund 1966). Our results support their assertion that thebackwards movement is a response to sensory effects ratherthan a “push” caused by a vibration reflex. Our measurementsof contact forces rule out the possibility that the observedpostural shifts during arm vibration and finger contact arecaused by a vibration-related mechanical effect. The forces aretoo small; moreover, in our experiment, a reflexive elbow flexionwould only lift the finger off the touch surface not push against it.

Comparisons of the present results and previous work indi-cate that not all proprioceptive feedback is of equal importancein controlling posture with tactile feedback from fingertipcontact. For example fingertip contact rendered ankle propri-oceptive feedback superfluous to postural control in the tandemstance even though the ankles are the principle effectors incontrolling posture. We disrupted ankle proprioception andcontrol using vibration of the peroneus longus muscle, whichgreatly destabilized posture and elicited falls. Yet ankle vibra-tion had no effect whatsoever on balance when subjects weremaintaining light fingertip contact (Lackner et al. 2000). Theentrainment to the oscillating surface creates a situation wheresubjects feel stationary while swaying to amplitudes that normallywould be above threshold for corrective influences on posture tobe evoked (Jeka et al. 1997, 1998). The shifting priorities ofmodality depend on sensory thresholds and experience and ex-pectations with the cues involved (Rabin and Gordon 2004, 2006).The malign influence of ankle vibration may have been defeatedwith light touch because there was no conflation of fingertipcontact control error with postural control error in the fingertipforce feedback as there is during biceps vibration.

Feedback from fingertip contact drives the control of postureand precision fingertip contact in parallel

The CP followed fingertip forces by �300 ms under all ofour conditions involving finger contact. To date, every posturalstudy of sway attenuation by light fingertip contact has repli-cated this finding. The null effects of arm immobilization onpostural stability and CP-fingertip force timing show thatfeedback from “imprecise” fingertip contact will drive posturaladjustments at the same �300-ms latency as feedback fromprecision contact. The consistent temporal pattern of fingertipcontact forces and postural adjustments indicates a defaultcontrol scheme governing posture and precision fingertip con-tact. However, the selective effects on CP stability and preci-

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sion fingertip contact of biceps vibration and of arm splintingindicate that fingertip contact and postural responses are con-trolled in parallel to minimize fingertip shear.

Johansson et al. (1987, 1992) characterized precision grip as areflex-like mechanism that acts to maintain adequate grip forceswhen subjects are holding and moving objects and that may alsobe engaged in an anticipatory fashion. Johansson et al. foundcompensatory increases in grip forces following load changeswith latencies of �80 ms. In their experiments, the arm is usuallystationary or only makes relatively small movements. It is possi-ble that the posture of the entire body may be similarly controlledto prevent slip of the fingertip on a surface in the case of the freearm and to minimize slip as best as possible in the case of thesplinted arm. The difference between the 150-ms response ofankle muscle activity (Jeka and Lackner 1995) versus 80-msresponse of precision grip (Johansson et al. 1992) may be due toslower muscles and a far greater inertial load in postural controlcompared with control of the fingers in a precision grip task.

Conclusion

Our findings demonstrate that the strategy of stabilizing finger-tip contact “with the body” is a response to the fingertip forcechanges in a larger context of sensory feedback and expectedchanges in those feedbacks. Proprioceptive and motor signalsabout the ongoing configuration of the hand, arm, and torso arealso present when an individual is attempting to balance withoutfingertip contact. It is by interrelating the fingertip signals withproprioceptive and motor signals related to the ongoing configu-ration of the body that the nervous system can detect body swayand initiate appropriate innervations of leg muscles to attenuatesway. The results of our arm-immobilization experiment showthat the degrees of freedom of the arm are effectively optional touse feedback from fingertip contact. However, the degradedpostural control during biceps vibration demonstrates that whendegrees of freedom are involved, feedback is required about eachjoint to resolve ambiguity of the tactile cues at the fingertip. Thesame characteristic �250-ms interval between fingertip forcechanges and foot/CP movement even when each was selectivelydisrupted indicates that precision fingertip contact and posture arecontrolled in parallel to minimize changes in fingertip contact force.

A C K N O W L E D G M E N T S

We thank Dr. Joel Ventura for devising the means by which we immobilizedthe arm.

G R A N T S

This research was supported by National Aeronautics and Space Adminis-tration Grants NAG9-1037 and NAG9-1038 and National Space BiomedicalResearch Institute Grant NA00701.

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