Although most of us take it for granted, walking isactually a complex task that requires intricate neu-ral control. Successful navigation through ourchanging daily environments requires the ability to

adapt locomotor outputs to meet a variety of situations. Forexample, in order to walk around an obstacle or along a curveit is necessary to modify locomotor trajectory. The mecha-nisms at work in controlling locomotor trajectory are not wellunderstood. One approach used to investigate these mecha-nisms is use of the rotating circular treadmill. The purpose ofthis article is to present an overview of this line of research.

Visual, Vestibular, and Somatosensory Controlof Locomotor TrajectoryVision is one important source of information for the controlof locomotor trajectory, but one can accurately walk along apreviously viewed curved path with eyes closed [1]. As such,there must be some other system that is important for regula-tion of trajectory. The vestibular semicircular canal systemprovides information about rotation of the head in space andcould provide information that is useful for directional con-trol. However, the dynamic properties of the semicircular ca-nals are such that they act as a high-pass filter. Thus, when oneis walking at a constant rotational velocity along a curvedpath, the vestibular signal will not accurately detect this turn-ing. There must be yet another source of information, asidefrom visual or vestibular inputs, that allows for control of lo-comotor trajectory. The somatosensory system provides thisimportant source of input.

When walking on solid ground, subjects walk a curvedpath via rotation of the head and trunk over the feet during thestance phase of gait [2]. Since the feet are stationary, the rota-tion of the trunk over the feet is equivalent to the rotation ofthe trunk in space. Thus, a somatosensory signal regarding ro-tation of the trunk relative to the feet provides an appropriatenonvisual and nonvestibular input for trajectory control [3].Unlike the vestibular signal, this somatosensory signal accu-rately reflects trajectory of the trunk in space even at low fre-quencies and constant velocities [4]. It is this somatosensoryregulation that allows one to accurately walk along a curvedtrajectory in the dark. In 1998, Weber et al. [3] introduced theterm “podokinetic” to describe this bottom-up somatosensorycontrol system.

Similar bottom-up somatosensory systems have been pro-posed in models of postural control. For example, Mergnerand Rosemeier [5] suggested that somatosensory informationis used to evaluate motion of the body relative to the supportsurface, and the vestibular system provides information onmotion of the body in space. Together, the bottom-upsomatosensory system and the top-down vestibular systemcan provide knowledge of support surface motion in space. Itis unclear whether similar intersensory integration is used toregulate both orientation of the body for stance posture andthe trajectory of locomotion on stable and moving surfaces.Studies of walking trajectories using a rotating circular tread-mill provide new insight into this issue.

The Treadmill as a ToolThe rotating circular treadmill is a useful tool for examininghow the podokinetic system can be adaptively remodeled inresponse to altered sensory inputs. Walking in-place on therotating circular treadmill (Figure 1), analogous to walkingon a giant record player, provides podokinetic stimulation.During podokinetic stimulation, one’s feet walk along acurved trajectory while the trunk and head remain stationaryrelative to space and visual inputs indicate that one is not ro-tating. Following walking in-place on a rotating circulartreadmill, a subject asked to walk across the floor along astraight line without vision will instead walk along a curvedtrajectory. This rotation relative to space is inadvertent andthe subject has no perception that he is turning. Gordon et al.[6] were the first to describe this phenomenon, and they at-tributed it to an adaptive remodeling of the relation betweentrunk rotation relative to the feet and the perception of trunkrotation relative to space. Weber et al. [3] termed this adap-tive phenomenon podokinetic after-rotation (PKAR). If asubject opens his eyes during PKAR, he will stop rotatingrelative to space, but rotation resumes as soon as vision isonce again occluded.

PKAR: The BasicsA typical PKAR response is illustrated in Figure 2. The sub-ject first stepped in-place for 30 minutes on the surface of thecircular treadmill, which was rotating counterclockwise at45 °/s. PKAR was then measured as the subject, wearing ablindfold and earplugs, stepped in-place on a stationary sur-

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Post

ura

lCo

ntro

l Gaining Insightby Going in CirclesUse of the Rotating Circular Treadmillto Study the Neural Control of Human Walking

GAMMON M. EARHARTAND FAY B. HORAK

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©DIGITAL STOCK

face for 30 minutes. The plot shows the subject’s whole bodyrotational velocity relative to space during this 30-minute pe-riod of PKAR. Note that values are positive, which by conven-tion indicates that the subject turned clockwise during PKARfollowing counterclockwise podokinetic stimulation.

The 30-minute PKAR response has two basic components,a rapid rise during the first 2 minutes (white dots) and a slowerdecay from minutes 2 to 28 (gray dots). The early rapid rise isthought to reflect a vestibular-podokinetic interaction. Theinitial rotation likely stimulates semicircular canals, leadingto early vestibular suppression of PKAR. The vestibular sig-nal then decays over the first 2 minutes, allowing PKAR toreach a maximum velocity after which the response is rela-tively free of vestibular influence [3]. The decaying portion ofthe PKAR response can be fitted with a three-parameter expo-nential decay curve, as shown in Figure 2. This curve fittingyields values for the initial velocity (13.20 °/s), decay timeconstant (1/0.09 = 11.11 min), and final asymptote (2.86 °/s).The initial velocity of PKAR is linearly related to stimulusamplitude up to 45 °/s [3], and it is typically about one-thirdthe value of stimulus amplitude (e.g., for a stimulus amplitudeof 45 °/s the initial velocity would be about 15 °/s). Prior to

stepping on the treadmill, a healthy subject asked to stepin-place will not rotate or will rotate very slowly (= 2 °/s).

PKAR: Centrally Mediated Adaptive Processor Peripheral Phenomenon?From the outset, it was clear that PKAR following stepping ona rotating disk was expressed in the lower, but not the upper,extremities. Subjects who traveled curved paths when askedto walk straight across the floor without vision were able topropel a wheelchair in a straight line without vision [6]. Thisresult suggests that the central spatial navigation referencesystem was not altered by podokinetic stimulation. PKAR isalso not dependent on the sensory conflict that is present dur-ing walking in-place on the treadmill, when visual inputs indi-cate stability in space while somatosensory inputs indicatethat the limbs are rotating in space [7]. Removing visual inputduring the period of podokinetic stimulation has no effect onPKAR, suggesting that the process could occur strictly withinthe somatosensory system. These results led some to questionwhether the changes underlying PKAR are simply a local pe-ripheral phenomenon taking place within the lower limbs orare an adaptive process involving central nervous system inte-

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Fig. 1. Illustration of a subject walking on the rotating circulartreadmill. The disk rotates beneath the subject as he walksin-place on its surface.

Ang

ular

Vel

ocity

(Deg

/s)

Time (Min)

20

15

10

5

0

−50 5 10 15 20 25 30

Y = 2.86 + 13.20e−.09x

Fig. 2. Typical PKAR response following 30 minutes of steppingin-place on the surface of a disk rotating at 45 º/s. The plotshows the subject’s whole body rotational velocity in spacefor a 30-minute period of stepping in-place on a stationarysurface while wearing a blindfold and earplugs. White dotsshow the two-minute rise characteristic of the PKAR response.Gray dots show the portion of the curve fitted with athree-parameter exponential decay function to yield theequation shown.

If PKAR were strictly a peripheral

phenomenon, taking place within the

lower extremities, one would expect

that PKAR could be expressed in one

lower limb independently of the other.

gration of somatosensory information. One means of address-ing this question is to examine how specific the changesunderlying PKAR are to the particular locomotor pattern usedwhile walking on the rotating disk.

Can PKAR Be Obtained Independentlyin One Lower Extremity and Not the Other?If PKAR were strictly a peripheral phenomenon, taking placewithin the lower extremities, one would expect that PKARcould be expressed in one lower limb independently of theother. To examine this issue, Earhart et al. [8] had subjectswalk with one foot on the rotating disk and the other foot on astationary surface. Following this unilateral podokinetic stim-ulation, PKAR was measured by recording the rotation of thepelvis and the times of footfall and liftoff. If the two limbswere independent and PKAR was strictly a peripheral phe-nomenon, one would expect the following result: rotation ofthe pelvis over the foot during stance on the stimulated limband no rotation of the pelvis over the foot during stance on theunstimulated limb. Over the first several strides this is indeedwhat was observed. There was evidence that changes had oc-curred in the stimulated limb but not in the unstimulated limb.However, after several strides there was no difference in rota-tion of the pelvis over the foot during stance on the stimulated

or unstimulated limb. PKAR following unilateral stimulationhad an average initial velocity that was approximately onehalf the amplitude of PKAR initial velocity following bilat-eral podokinetic stimulation (i.e., with both feet stepping onthe rotating disk). This indicates that information from bothlower limbs was used to determine the overall PKAR re-sponse, suggesting some central mechanism for integration ofpodokinetic information from the two sides of the body.

Does PKAR Transfer from Stepping to Hopping?Subjects asked to step in-place on a stationary surface afterhaving stepped in-place on the rotating treadmill will turn incircles rather than maintaining a steady heading. Is this af-ter-rotation specific to the form of locomotion used while onthe rotating disk? If the PKAR phenomenon were a centrallymediated, adaptive process, one would expect the adaptationto transfer from the form of locomotion used while on thedisk to other forms of locomotion that have never been per-formed on the disk. Earhart et al. [9] asked whether subjectswould rotate in space when asked to hop in-place on a sta-tionary surface following stepping on the rotating disk. Sub-jects did demonstrate PKAR during hopping followingstepping in-place on the rotating disk, adding support to thehypothesis that PKAR is a centrally mediated adaptation ofgeneral locomotor trajectory. PKAR during stepping andhopping was not identical, however. Although the two re-sponses had very similar time constants, hopping PKAR hadan initial velocity that was one half of that for steppingPKAR. This indicates an incomplete transfer of the adapta-tion, perhaps because of the differences in interlimb coordi-nation between stepping, where the limbs alternate, andhopping, where the limbs move in unison.

Does PKAR Transfer from Forward toBackward Walking?Subjects also demonstrate PKAR during backward walkingfollowing forward walking on the circular treadmill [10]. Fig-ure 3 shows the trajectories one subject produced when askedto walk forward (a) and backward (b) after walking forwardon the rotating disk. Note that the two paths are quite similar.PKAR during backward walking was very similar to that offorward walking in terms of initial velocity, decay time con-stants, and final asymptote. The transfer of PKAR from for-ward to backward walking appeared to be complete, againsuggesting that PKAR involves centrally mediatedsomatosensory integration.

One interesting result obtained when comparing forwardand backward PKAR following forward walking on the diskwas that subjects turned in the same direction during both

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Forward Walking Backward Walking

0.5 m

0.5

m

L

R

R

LStart Start

(a) (b)

Fig. 3. Walking trajectories for a single subject asked to walkstraight across the floor in the forward (a) and backward (b) di-rection, following forward walking in-place on the rotatingtreadmill (trials collected on two separate days). Each trajec-tory represents the path generated during 2 minutes of contin-uous walking that began 10 minutes after coming off thetreadmill. Note the similarity in the two paths despite the differ-ences in walking direction and the fact that the subject neverwalked backward while on the treadmill. (Adapted from [10].)

Subjects asked to step in-place on

a stationary surface after having

stepped in-place on the rotating

treadmill will turn in circles rather than

maintaining a steady heading.

PKAR responses. After walking forward on the clockwise-ro-tating disk, subjects walked counterclockwise across the floorduring PKAR regardless of walking direction. This indicatesthat during forward PKAR the left foot was innermost with re-spect to the center of rotation, but during backward PKAR theright foot was innermost with respect to the center of rotation.As such, the left leg moved through a shorter distance than theright leg during forward PKAR but through a larger distancethan the right leg during backward PKAR. Despite thischange in relationship of the limbs to the center of rotation,the relative rotation between the feet and the trunk was pre-served for both directions of PKAR (see Summary for moredetails). This suggests that podokinetic stimulation results inadaptation of the relationship between rotation of the feet andthe trunk and not the relative step length between the legs.

Is the Cerebellum Important for PKAR?The evidence described above suggests that PKAR is an adap-tive response that is controlled, at least in part, by structureswithin the central nervous system. Studies of other adaptivephenomena, such as adaptation of throwing and pointingmovements when wearing prisms, indicate that adaptation isreduced or abolished following cerebellar damage [11], [12].Is the cerebellum also important for podokinetic adaptation?

In a study of eight subjects with cerebellar damage, overhalf of these subjects showed impaired podokinetic adapta-tion compared to control subjects [13]. (Impaired PKAR wasdefined as a response with an initialvelocity more than two standard devi-ations below the average initial veloc-ity of the control group.) None of thecontrol subjects exhibited impairedPKAR. Despite the reduction inPKAR velocity, subjects with cere-bellar damage had normal decay timeconstants. This suggests that the cere-bellum may be important for regula-tion of PKAR response amplitude,but it may not be critical for storage ofthe adaptation. The structures that areimportant for this storage have yet tobe identified.

SummaryPKAR appears to be an adaptive phe-nomenon that results from a remodel-ing of the rotational relationshipbetween the trunk and the feet. Figure4 illustrates the basic mechanism of

PKAR. During walking on the rotating disk, the feet aretraveling a curved path while the trunk and head remain stablerelative to space. During podokinetic stimulation on a clock-wise-rotating disk, the feet are walking along a counterclock-wise trajectory. The feet are rotating relative to thespace-stable trunk by virtue of their contact with the movingsurface during stance [Figure 4(a)]. This rotation of the feetunder the trunk is accompanied by visual and vestibular sig-nals that indicate fixity relative to space. When the subjectnow attempts to walk straight across the floor without vision,the relative rotational relationship between the feet and trunkis maintained as the system is newly calibrated to reflect thefact that rotation of the feet relative to the trunk has been nec-essary to maintain a space-stable heading. However, insteadof the feet rotating under the trunk, the trunk now rotates overthe feet, which are stable relative to space during stance byvirtue of their contact with the stationary surface [Figure4(b)]. The result is PKAR in the counterclockwise direction;i.e., the same direction that the feet were traveling when walk-ing on the clockwise-rotating disk. This change in the rota-tional relationship between the feet and the trunk isaccompanied by a change in perception, as subjects have nosensation that they are turning in space during PKAR.

Podokinetic adaptation is mediated, at least in part, bysomatosensory information that is integrated within centralnervous system structures. The cerebellum, in particular, isimportant in regulating the amplitude of this adaptive

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PK Stimulation Overground PKAR

Feet Rotate Below Space-Stable Trunk Trunk Rotates Above Space-Stable Feet(a) (b)

Fig. 4. Overhead views illustrating the basic mechanism of PKAR, a remodeling of therelative rotational relationship between the feet and the trunk. During podokinetic stim-ulation (a) the feet turn relative to the space-stable trunk by virtue of their contact withthe rotating surface. During overground walking on a stationary surface (b), the samerelative rotation is achieved by rotation of the trunk over the space-stable foot, result-ing in a curved locomotor trajectory. (Adapted from [10].)

The evidence described above

suggests that PKAR is an adaptive

response that is controlled, at least

in part, by structures within the

central nervous system.

response. The amplitude of PKAR corresponds to the degreeof path curvature produced, as a higher initial velocity resultsin a more tightly curved trajectory. This adaptable control ofgeneral locomotor trajectory via the podokinetic system islikely essential for successful navigation in everyday environ-ments. The podokinetic system can be used not only to adaptlocomotor trajectory but to gauge how far one has rotated dur-ing active, intentional turning [14]. Many questions remain tobe answered about the nature of the podokinetic system andits interactions with other inputs, especially those from the vi-sual and vestibular systems.

AcknowledgmentsThis work was supported by NIH grants 1F32 N241804-01and R01-DC040082, and by MRC grant MA-5639.

Gammon M. Earhart is a postdoctoralfellow working in Dr. Horak’s laboratory.In 1994, she earned a B.A. in psychobiol-ogy and, in 1996, an M.S. in physical ther-apy, both from Beaver College (nowArcadia University). She earned a Ph.D. inmovement science from Washington Uni-versity in St. Louis in 2000. Her research

interests include the neural control of locomotion,sensorimotor integration and adaptation, and the effects ofneurological disorders on movement control. For her doctoralwork, she studied the roles of the spinal cord and cerebellumin motor control using both animal and human models. In hercurrent research, she uses a rotating circular treadmill to an-swer questions about locomotor adaptation and the control oflocomotor trajectory.

Fay B. Horak is a senior scientist at theNeurological Sciences Institute, inBeaverton, Oregon. She is also a professorin the Departments of Neurology andPhysiology at Oregon Health and ScienceUniversity. In 1973, she earned a B.S. inphysical therapy from the University ofWisconsin, Madison, and in 1977, she

earned an M.S. in neurophysiology from the University ofMinnesota, Minneapolis, where she studied cat muscle spin-dles. In 1982, she earned a Ph.D. in physiology and biophysicsfrom the University of Washington, Seattle, where she studiedthe role of the basal ganglia in primate motor control. Her cur-rent research interests include the neural control of balance

and gait and the effects of aging and neurological disorderssuch as Parkinson’s disease, cerebellar ataxia, vestibular dis-orders, and somatosensory loss. She is an internationally rec-ognized expert on postural control and the implications ofmotor control research for rehabilitation with over 100 publi-cations.

Address for Correspondence: Gammon M. Earhart, Neuro-logical Sciences Institute, OHSU-West Campus, 505 NW185th Ave., Beaverton, OR 97006. Tel.: +1 503 418 2605.Fax: +1 503 418 2501. E-mail: earhartg@ohsu.edu.

References[1] J.J. Rieser, D.H. Ashmead, C.R. Talor, and G.A. Youngquist, “Visual perceptionand guidance of locomotion without vision to previously seen targets,” Perception,vol. 19, pp. 675-689, 1990.

[2] T. Imai, S.T. Moore, T. Raphan, and B. Cohen, “Interaction of the body, head, andeyes during walking and turning,” Exp. Brain Res., vol. 136, pp. 1-18, 2001.

[3] K.D. Weber, W.A. Fletcher, C.R. Gordon, G. Melvill Jones, and E.W. Block,“Motor learning in the ‘podokinetic’ system and its role in spatial orientation duringlocomotion,” Exp. Brain Res., vol. 120, pp. 377-385, 1998.

[4] T. Mergner, F. Hlavacka, and G. Schweigart, “Interaction of vestibular andproprioceptive inputs,” J. Vestib. Res., vol. 3, pp. 41-57, 1993.

[5] T. Mergner, and T. Rosemeier, “Interaction of vestibular, somatosensory and vi-sual signals for postural control and motion perception under terrestrial andmicrogravity conditions—A conceptual model,” Brain Res. Rev., vol. 28, pp.118-135, 1998.

[6] C.R. Gordon, W.A. Fletcher, G. Melvill Jones, and E.W. Block, “Adaptive plas-ticity in the control of locomotor trajectory,” Exp. Brain Res., vol. 102, pp. 40-545,1995.

[7] R. Jürgens, T. Boß, and W. Becker, “Podokinetic after-rotation does not dependon sensory conflict,” Exp. Brain Res., vol. 128, pp. 563-567, 1999.

[8] G.M. Earhart, G. Melvill Jones, F.B. Horak, E.W. Block, K.D. Weber, and W.A.Fletcher, “Podokinetic after-rotation following unilateral and bilateral podokineticstimulation,” J. Neurophysiol., vol. 87, pp. 1138-1141, 2002.

[9] G.M. Earhart, G. Melvill Jones, F.B. Horak, E.W. Block, K.D. Weber, and W.A.Fletcher, “Transfer of podokinetic adaptation from stepping to hopping,” J.Neurophysiol., vol. 87, pp. 1142-1144, 2002.

[10] G.M. Earhart, G. Melvill Jones, F.B. Horak, E.W. Block, K.D. Weber, and W.A.Fletcher, “Forward versus backward walking: transfer of podokinetic adaptation,” J.Neurophysiol., vol. 86, pp. 1666-1670, 2001.

[11] J.S. Baizer, I. Kralj-Hans, and M. Glickstein, “Cerebellar lesions and prism ad-aptation in macaque monkeys,” J. Neurophysiol., vol. 81, pp. 1960-1965, 1999.

[12] T.A. Martin, J.G. Keating, H.P. Goodkin, A.J. Bastian, and W.T. Thach,“Throwing while looking through prisms I. Focal olivocerebellar lesions impair ad-aptation,” Brain, vol. 119, pp. 1183-1198, 1996.

[13] G.M. Earhart, W.A. Fletcher, F.B. Horak, E.W. Block, K.D. Weber, O.Suchowersky, and G. Melvill Jones, “Does the cerebellum play a role in podokineticadaptation?,” Exp. Brain Res., vol. 146, pp. 538-542, 2002.

[14] W. Becker, G. Nasios, S. Raab, and R. Jürgens, “Fusion of vestibular andpodokinesthestic information during self-turning towards instructed targets,” Exp.Brain Res., vol. 144, pp. 458-474, 2002.

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The podokinetic system can be used

not only to adapt locomotor trajectory

but to gauge how far one has rotated

during active, intentional turning.