Review Article Human Locomotion under Reduced Gravity Conditions ... - Semantic Scholar

12 Pages·2014·2.4 MB·English

Hindawi Publishing Corporation
BioMed Research International
Volume 2014, Article ID 547242, 12 pages
http://dx.doi.org/10.1155/2014/547242
Review Article
Human Locomotion under Reduced Gravity Conditions:
Biomechanical and Neurophysiological Considerations
FrancescaSylos-Labini,1,2FrancescoLacquaniti,1,2,3andYuriP.Ivanenko2
1CentreofSpaceBio-Medicine,UniversityofRomeTorVergata,ViaMontpellier1,00133Rome,Italy
2LaboratoryofNeuromotorPhysiology,IRCCSSantaLuciaFoundation,ViaArdeatina306,00179Rome,Italy
3DepartmentofSystemsMedicine,UniversityofRomeTorVergata,ViaMontpellier1,00133Rome,Italy
CorrespondenceshouldbeaddressedtoYuriP.Ivanenko;[email protected]
Received24April2014;Accepted12June2014;Published28August2014
AcademicEditor:MarianoBizzarri
Copyright©2014FrancescaSylos-Labinietal.ThisisanopenaccessarticledistributedundertheCreativeCommonsAttribution
License,whichpermitsunrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalworkisproperly
cited.
Reducedgravityoffersuniqueopportunitiestostudymotorbehavior.Thispaperaimsatprovidingareviewoncurrentissuesof
theknowntoolsandtechniquesusedforhypogravitysimulationandtheireffectsonhumanlocomotion.Walkingandrunning
relyonthelimboscillatorymechanics,andonewaytochangeitsdynamicpropertiesistomodifythelevelofgravity.Gravityhasa
strongeffectontheoptimalrateoflimboscillations,optimalwalkingspeed,andmuscleactivitypatterns,andgaittransitionsoccur
smoothlyandatslowerspeedsatlowergravitylevels.Alteredcenterofmassmovementsandinterplaybetweenstanceandswing
legdynamicsmaychallengenewformsoflocomotioninaheterogravityenvironment.Furthermore,observationsinthelackof
gravityeffectshelptorevealtheintrinsicpropertiesoflocomotorpatterngeneratorsandmakeevidentfacilitationofnonvoluntary
limbstepping.Inviewofthat,spaceneurosciencesresearchhasparticipatedinthedevelopmentofnewtechnologiesthatcanbe
usedasaneffectivetoolforgaitrehabilitation.
1.Introduction Understanding locomotion characteristics is critical for
those working in the area of gait biomechanics and neu-
Lifeevolvedinthepresenceofgravity,whichhastwomajor
rophysiology f pattern generation networks and of exer-
impacts on motor functions: specific body orientation in
cisecountermeasuresforastronauts.Manyresearchershave
space and antigravity muscle tone and specific rules of
investigated the effects of reducing and eliminating gravity
motioninthegravityfield.Gravityplaysanessentialrolein
on locomotive kinematics and kinetics [4–8]. Others have
terrestrial locomotion. The dominant hypothesis regarding
studied locomotion in actual weightlessness or hypogravity
templates for bipedal walking in the gravity field is the
[9,10].Thetechniqueshaveincludedsupineanderectcable
pendularmechanismofwalking,uptointermediatespeeds,
suspension, parabolic aircraft flights, water immersion, and
andthebouncingmechanismofrunning,uptothehighest
centrifugalmethods[6].Increasedknowledgeoflocomotion
speedsattainable[1].Theinvertedpendulum-likemechanism
kinematics,kinetics,muscularactivitypatterns,andsensory
of energy exchange taking place during walking would be
feedback modulation may help to facilitate more effective
optimizedatslowerspeedsinreducedgravity[2,3].Despite
exercise countermeasures, develop innovative technologies
our intuitive appreciation for the influence of gravity, we
do not fully understand how gravity interacts with other for gait rehabilitation, and provide new insights into our
forces,suchasinertia,toaffectmanybiologicalandphysical understandingofthephysiologicaleffectsofgravity.Inthis
processesandwhattypeofgaitand/orlimbsynchronization review, we will consider the known tools and techniques
(trot,gallop,lateralsequencewalk,pace,skipping,etc.)would usedforhypogravitysimulationandtheireffectsonhuman
evolveatothergravitylevels. locomotion.
2 BioMedResearchInternational
2.MethodsandApparatusesfor Reduced onatreadmillinweightlessness,asubjectloaddeviceisused
GravitySimulation to return him or her back to the treadmill belt and to load
thelimbs.Thegravityreplacementloadistransferred,viaa
Spaceflights are the more direct way to assess the effect of harness,tothepelvisand/ortheshoulders.Gravitysimulators
gravity on locomotion, but studying locomotion in actual cansimulateactivetreadmillrunninginweightlessnessand
hypogravityisdemandingandexpensive[6].Thedrawbacks provideamethodoftestingproposedimprovementsinSLD
tospaceflightexperimentsincludedifficultyinusingneces- designandexerciseprotocols[20,21].Insupinesuspension
sarydatacollectionhardwareandperforminganexperiment systems (Figure1(e)), subjects are suspended horizontally
with adequate sample size. Parabolic flight offers a viable attachedtolatexrubbercords.Aclothsleeveandrubbercord
alternative,butperiodsofweightlessnessarelimitedto∼20s, areattachedeachtotheupperandlowerarmsandlegs(eight
whichonlyallowsforacutelocomotioninvestigations[11]. total) [20]. The limitation of this system is a local pressure
There are several apparatuses that have been used in onsomepartsofthebody(e.g.,shoulders)andmodifications
the past to simulate reduced gravity locomotion. One of in the swing phase dynamics due to nonconstant forces
the more used systems is the vertical body weight support of rubber cords and gravity acting in the anterioposterior
(BWS)(Figures1(a)and1(b)).Thesekindsofsimulatorsare directionoflegmovements(Figure1(e)).
usually obtained supporting the subjects in a harness that Basedonthepassivegravitybalancingtechnology,Maet
applies a controlled upward force. For example, the WARD al. [22, 23] proposed a design concept of a passive reduced
[12] mechanism consists of a mechanical gear driven by a gravitysimulatortosimulatehumanwalkingorotheractiv-
pneumaticcylinder(Figure1(b)).Itisheldinacartthatslides itiesinareduced-gravityenvironmentforpotentialapplica-
forward and backward over a track. Low-friction sliding of tionsoftrainingastronautsandspacetravelers(Figure1(f)).
the mechanism ensures that only vertical forces are applied The system consists of a 3-DOF dual parallelogram mech-
to the subject. Vertical BWS systems may also make use of anism, a 2-DOF torso support assembly, and a pair of 3-
asmallincreaseinairpressurearoundtheuser’slowerbody DOF leg exoskeletons. The weight of the body and the legs
to create a lifting force approximately at the person’s center is compensated by the spring-balanced dual-parallelogram
of mass [13]. Other vertical systems [8, 14] use a series of mechanism and torso-support assembly, and the weight of
compliantrubberspringelementsthatarestretchedtocreate each leg is compensated by a leg exoskeleton. The system
the upward (to simulate gravity less than 1g) or downward is capable of simulating human walking and jumping in a
(to simulate gravity greater than 1g) force (Figure1(a)). hypogravity environment [24]. Hardware prototyping and
The main limitationof these reduced gravity simulators (in experimental study of the new system are currently under-
additiontohighlocalskinpressureviaaharness)isthateach way.
supportinglimbexperiencesasimulatedreductionofgravity Inthefollowingsectionwediscussthebasicprinciplesof
proportional to the applied force, while the swinging limb adaptationoflocomotiontodifferentgravityvaluesusingthe
experiences1g. technologiesdescribedhere.
The tilted BWS systems (Figures 1(c) and 1(d)) are con-
structedtosimulatemorerealisticeffectsofgravitychanges
3.BiomechanicalAspectsofLocomotion in
on both the stance and swing legs in the sagittal plane.
ReducedGravity
These simulators, that have been used in the past by both
Roscosmos (Russian Federal Space Agency) and NASA to
Despite some differences, all reduced gravity simulation
train astronauts before space flights [15–17], are based on
approaches show a reasonable approximation of the reduc-
the idea of neutralizing the component of the gravity force
normal to the lying surface [mg⋅cos(𝛼), where 𝛼 is the tion in the gravitational force acting on the center of body
mass (COM) and similar results concerning the speed of
angle of inclination], while the component of the gravity
gaittransitions.Animportantconsequenceofthependulum-
force acting on the body and swinging limbs in the sagittal
plane is reduced in relation to the tilt angle [mg⋅sin(𝛼)]. likebehaviorofthelimbsinthegravityfieldistheprinciple
of dynamic similarity [29], which states that geometrically
A similar concept has been used in the reduced gravity
similar bodies that rely on pendulum-like mechanics of
simulator (Figure1(d)) designed by Ivanenko et al. (Italian
movement have similar gait dynamics at the same Froude
patentnumberRm2007A000489):thesubjectliesontheside
∘ number:
on a tilted couch (up to 40 from the horizontal position)
with both legs suspended in the exoskeleton and steps on
𝑉2
the treadmill, which is tilted to the same angle [7, 18, 19]. Fr ∼ , (1)
𝑔𝐿
Thissimulatorincludedadditionalmassofthetiltedchassis
(∼15kg) and exoskeleton (1.5kg for each leg). Thus the
entire assembly had a mass of ∼18kg that increased both where 𝑉 is the speed of locomotion, 𝑔 is the acceleration
gravitationalandinertialforcesduringwalking. of gravity, and 𝐿 is a characteristic leg length. That is, all
Anotherclassofgravity-relatedmanipulationsis“subject lengths, times, and forces scale by the same factors. In
load device” (SLD) that applies a gravity replacement force order to optimize the recovery of mechanical energy, the
inthedirectiondowntothesurface.ThistypeofSLDcanbe kinetic energy and the potential energy curves must be
usedintheverticalsystemstoincreasethegravity[8]orinthe equalinamplitudeandoppositeinphase,asinapendulum.
lyingposition(Figure1(e)).Whenanastronautwalksorruns Assumingthatthechangeinkineticenergywithineachstep
BioMedResearchInternational 3
M
R
F
B
20 m
R
PL
(a) Verticalsystemforalteredgrav- (b) VerticalBWS
itysimulation
𝛼
(c) TiltedBWS (d) TiltedBWS
q1
G
q2 q5 q6
F q4
q3
B
C E q7,8
D q9,10 q11 q12
A
(e) Supinesuspensionsystem (f) Passivegravitybalancingsystem
Figure1:Reducedgravitysimulatorsforlocomotion.(a)Schemaoftheverticalsystemusedtosimulatedifferentgravityvalues(redrawn
from[8]).R:rubberbands,B:lightmetalbars,M:electricmotortostretchtheelasticbandsystem,PL:pulleystoinvertthedirectionof
thepullonthesubject(dashedlines).(b)Verticalbodyweightsupport(BWS)system:subjectwalksonatreadmillwithdifferentlevelsof
BWSwhilebeingsupportedinaharness,pulledupwardsbyapresetunloadingforce𝐹.(c)TiltedBWSsystemusedbyRoscosmos(Russian
∘
FederalSpaceAgency)totrainastronautsbeforespaceflights[15]:thesubjectwalksonatruncatedcone(60mheight,9.2 inclinationrelative
tothevertical),supportedbyfiveropessustainingthehead,trunk,andlegs(pictureportrayingProfessorGurfinkelreproducedwithhiskind
∘
permission).(d)Tiltedunloadingsystemforsteppingonatreadmill:thesubjectliesonthesideonatiltedcouch(upto40 fromthehorizontal
position)withbothlegssuspendedintheexoskeletonandstepsonthetreadmill,whichistiltedtothesameangle.Thecomponentofthe
gravityforceactingonthestanceandswinglimbsegmentsisproportionaltothetiltingangle𝛼[18].(e)Supinesuspensionsystem(adapted
from[20],courtesyofProfessorPeterCavanagh):thesubjectissuspendedhorizontallyattachedtolatexrubbercords.Aclothsleeveand
rubbercordareattachedeachtotheupperandlowerarmsandlegs(eighttotal).Thesubjectisactivelypulledtowardthetreadmillbya
gravityreplacementloadthroughcablesattachedtoaloadsplitter.(f)Passivereducedgravitywalkingsimulator(courtesyofDr.OuMa).
Thesystemconsistsofa3-DOFdualparallelogrammechanism,a2-DOFtorsosupportassembly,andapairof3-DOFlegexoskeletons.The
weightofthebodyandthelegsiscompensatedbythespring-balanceddual-parallelogrammechanismandtorso-supportassembly,andthe
weightofeachlegiscompensatedbyalegexoskeleton[22–24].
is an increasing function of the walking speed (while the optimalexchangebetweenpotentialandkineticenergiesof
change in the potential energy is proportional to gravity), theCOMoccursatFr∼0.25[2](Figure2(a)).Eventhough
the hypothesis was proposed that the inverted pendulum- specificlimbsegmentproportionsmayplayanessentialrole
like mechanism of energy exchange during walking would in the kinematics and energetics of walking [30], animal
beoptimizedatslowerspeedsinreducedgravity[3,10].An anatomy and individualized limb segment dimensions are
4 BioMedResearchInternational
1 g 0.05 g
Walk-run
transition 60
2 Fr = 0.5 4
W 40
B
m/s) F, % 20 2
d ( 0 0
e
e
g sp a–p m –l
n 1
Walki OpFtirm =a 0l .s2p5e ed 0.5 g
60
40
20
0
0 0.5 1 1.5
0
Gravity (g)
Margaria and Cavagna [3] Cavagna et al. [68];
Griffin et al. [67] Cavagna et al. [10] 1 g 0.25 g
Kram et al. [4] 0.65 g 0.05 g
Ivanenko et al. [18] 0.5 g
(a) (b)
Simulated locomotion on Moon (0.16 g)
F =0.84·mg
vert
F =0.16·mg
p
F
g
mg
𝛼
Gravity replacement load Tilted BWS Vertical BWS
Horiz. foot excursion Max horiz. foot vel.
100 10
80 8
1 g
m) 60 1 g m/h) 6
c
( 40 k 4
(
20 2
0 0
x
Gravity replacement load Vertical BWS system
Tilted BWS system (matched foot excursion)
Vertical BWS system
(c)
Figure2:Biomechanicalfeaturesoflocomotioninreducedgravityconditions.(a)Optimal(blue)andwalk-to-runtransition(green)speeds
asafunctionofgravity.DynamicallysimilarspeedspredictedbyFr=0.25andFr=0.5areindicatedbyblueandgreendashedcurves,
respectively[25].Greencirclesandstarsrefertomeasurementsofoptimalwalk-to-runtransitionspeedsinsimulatedlow-gravityconditions
[5,18].ThegreytriangleindicatesanearlierestimateofoptimalwalkingspeedpredictedfortheMoongravitationalenvironmentbyMargaria
andCavagna[3].Bluetrianglesrefertotheoptimalspeeds(atwhichmostofthemechanicalexchangebetweenpotentialandkineticenergy
ofthebodycenterofmassoccurs)obtainedinasimulationstudyofGriffinetal.[26].Bluecirclesrepresentmeasurementsofoptimalspeed
obtainedduringparabolicflight[10,27].(b)Timecourseofthenetverticalcomponentofin-shoereactionforcesplottedasafunctionof
thespatialcoordinatesofthefootatdifferentreducedgravitylevels.Notechangeinverticalscaleinthe0.05gcondition.Thelowerright
panelshowsthetrajectoriesofthecenterofpressuresuperimposedonafootoutline(adaptedfrom[28]).(c)Maximumlongitudinalfoot
velocityandfootexcursion(𝑥)duringwalkingat2km/hat0.16gusingthreedifferentreducedgravitysimulators(representedschematically
intheupperpanels).Horizontaldashedlinesindicatevaluesforwalkingat1g.Thehatchedbar(rightpanel)correspondstothemaximal
footvelocityfortheverticalBWSsystemapproximatedbymatchingthefootexcursiontothatofthetiltedBWSsystem[7].Notesignificantly
lowerfootvelocitiesduringswingusingtiltedBWSsystems.
BioMedResearchInternational 5
optimizedinsuchawaythattheFroudenumbercanexplain appliedattheforefootonly(Figure2(b)).Duringlowerlimb
optimalwalkingvelocity. loading,avarietyofreceptorscanbeactivated,suchasGolgi
OnEarth,walkingandrunninggaitsareusuallyadopted tendonorgans,cutaneousreceptorsofthefoot,andspindles
fordifferentspeedsoflocomotion,withapreferredtransition from stretched muscles [36]. These sensory signals interact
occurringat∼2m/sforhumanadultsandatslowspeedsfor withcentralrhythm-generatingcentersandhelpinshaping
children(Fr∼0.5),inaccordancewiththedynamicsimilarity the motor patterns, controlling phase-transitions, and rein-
theory [29]. Different studies [4, 18] demonstrated that, at forcing ongoing activity [38, 39]. For instance, loading of
lower levels of gravity, the walk-run transition occurred at thelimbenhancestheactivityinantigravitymusclesduring
progressivelyslowerabsolutespeedsbutatapproximatelythe stance and delays the onset of the next flexion [40]. It is
sameFroudenumber(Figure2(a)). important to understand the mechanisms of sensorimotor
Despite similarities in approximating reduced gravity, adaptation to the biomechanics of locomotion and foot
thereareneverthelessessentialdifferencesbetweendifferent placement/loadinginheterogravity,especiallytolonger-term
simulationapproaches.Thevariablesthatshowedthegreat- changesofload.
est differences between vertical and tilted reduced gravity Akeyfeatureofadaptationtohypogravityisaremarkable
systems (Figure1) were maximal longitudinal foot velocity nonlinear scaling of muscle activity patterns contrary to
and longitudinal foot excursion (Figure2(c)), in agreement monotonic changes in foot loading. The simplest kind of
withsignificantinfluencesofgravityonswinglegdynamics change with simulated reduced gravity [28] was seen in
[7].Eventhoughthemaximallongitudinalfootvelocityfor ankle extensors: the mean amplitude of activity decreased
the tilted BWS condition decreased only slightly relative to systematically with decreasing simulated gravity, consistent
the vertical BWS, however, the actual decrement was much with their antigravity function [35, 41]. By contrast, the
moreobviousifonetakesintoaccountthatitwassignificantly behaviorofothermusclescouldnotbepredictedsimplyon
compensatedforormaskedbyincrementsinthestridelength thebasisofthestaticloadduringstance.Theamplitudeand
[7]. A previous modeling study also predicted differential patternofmuscleactivitygenerallydependedonspeedand
effectsofgravityduringstanceandswingphases[31].Infact, could vary nonmonotonically with body unloading. There
thechangesinthelongitudinalfootexcursionwerebasically wasalsoacomplexreorganizationofthepatternofactivity
oppositefortheverticalandtiltedBWSsystems(Figure2(c)). ofthighmuscleswithdecreasingsimulatedgravity,aswellas
For the former system the amplitude of longitudinal foot noteworthyindividualdifferences[28].Figure3(a)illustrates
motion decreased, while for the latter system it increased anexampleofnonlinearreorganizationofEMGpatternsin
relativetothe1gcondition.Consideringamonotonic(pre- onesubjectwalkingat3km/h.Withbodyweightunloading,
sumably proportional [32]) relationship between the stride gluteus maximus and distal leg extensors decreased their
lengthandthemaximalfootvelocityatagivengravitylevel activity, while other muscles demonstrated a “paradoxical”
(1g), the peak foot velocity would be expected to be ∼1.5 increment of activation (e.g., quadriceps) or considerable
times higher for the vertical than for tilted BWS condition changes in the activation waveforms (hamstring muscles).
ifthestridelengthsweresimilar(Figure2(c)).Theprevious Note also the absence of the typical burst of RF at the
studiesonparabolicflightsinvestigatingtheeffectofgravity beginningoftheswingphaseatlowsimulatedgravitylevels
onwalkingmechanicsdemonstratedincrementsintheswing (Figure3(a)), consistent with other studies on the effect of
phase duration (by 29% at 0.25g [33]; see also [11]), in line body weight unloading [42] and walking speed [43]. It is
withthesubstantialcontributionofgravitytotheswingleg. unlikely that these changes are due to the order of trials or
Overall,thefindingsdemonstratethatgravityactingonboth theconsequenceoflearningthehypogravityconditionsince
stance and swing legs plays an important role in shaping presentationorderofspeedsandBWSwasrandomizedacross
locomotorpatterns. sessionsandexperiments[28].Also,thedurationofeachtrial
was ∼1min, with at least 2 min rest between trials, and a
4.NonlinearReorganizationofEMGPatterns short (∼30s) training period of walking at different speeds
wasallowedforeachsimulatedreducedgravitylevelbefore
Itisknownthatloadplaysacrucialroleinshapingpatterned the actual data collection was begun (the walking patterns
motoroutputduringstepping[34–36],andhumansproduce typically adapt rapidly to simulated reduced gravity [4, 5]).
aspecificheel-to-toerollingpatternduringstanceinnormal This reorganization is presumably related to the multifunc-
gravity conditions. Ground contact forces reflect the net tional (biarticular) action of these muscles and to the need
vertical and shear forces acting on the contact surface and torepartitionthejointtorquecontributionsacrossdifferent
result from the sum of the mass-acceleration products of musclesasafunctionofthechangesinducedbygravity.At
all body segments while the foot is in contact with ground 1g, the main peak of m. biceps femoris activity occurring
[37].Simulatingreducedgravitybetween0.05and1greveals before heel-contact serves to decelerate the swinging limb
drastic changes of kinetic parameters but limited changes [37].However,asgravityisdecreased,itsmainactivityoccurs
of the kinematic coordination [28]. The reported accurate inmid-stanceandlatestance,presumablyinrelationtothe
controloflimb/footkinematics[28]maydependonload-and need to assist vaulting over an inverted pendulum of the
displacement-compensationmechanismsworkingeffectively stancelimbandswinginitiation.
throughoutawiderangeofgroundcontactforces,fromfull There might be various factors accounting for the non-
bodyweightupto<5%ofitsvalue.Thepeakverticalcontact linearreorganizationofmuscleactivitypatternswithgravity.
forcesdecreaseproportionallytogravity,butat0.05gtheyare To start with, nonlinear scaling also occurs during walking
6 BioMedResearchInternational
GM VL RF
0.05 g
0.25 g
0.5 g
20 V𝜇 30 V𝜇 30 V𝜇 1 g0.65 g
BF TA LG
0.05 g
0.25 g
0.5 g
30 V𝜇 50 V𝜇 50 V𝜇 1 g0.65 g
0 20 40 60 80 100 0 20 40 60 80 100 0 20 40 60 80 100
Cycle (%) Cycle (%) Cycle (%)
(a)
GM VL RF
5 10 10
4 8 8
V) 3 V) 6 V) 6
𝜇 2 𝜇 4 𝜇 4
( ( (
1 2 2
0 0 0
BF TA LG
20 40 20
15 30 15
V) 10 V)20 V)10
𝜇 𝜇 𝜇
( ( (
5 10 5
0 0 0
Speed5 (km3/h2) 1.1 0 0.2 0.4 0g.6 0.8 1
Speed
5 km/h 2 km/h
3 km/h 1.1 km/h
(b)
Figure3:Nonlinearreorganizationofmuscleactivitypatterns.(a)Anexampleofensemble-averagedelectromyographic(EMG)activityof
lowerlimbmusclesversusthenormalizedgaitcycleisshownforasubjectwalkingat3km/hatdifferentsimulatedreducedgravitylevels
[28].(b)MeanEMGactivitycomputedoverthegaitcycleandaveragedacrossallcyclesandsubjects(𝑛 = 8).Foreachmuscle,valuesfor
trialsperformedateachspeedareplottedasafunctionofsimulatedreducedgravity(adaptedfrom[28]).GM,gluteusmaximus,VL,vastus
lateralis,RF,rectusfemoris,BF,bicepsfemoris,TA,tibialisanterior,LG,andlateralgastrocnemius.
atdifferentspeedsat1g.Forinstance,VLandRFactivityis occursat∼4km/h,Figure2(a)),sothat“paradoxical”incre-
quite small at low speeds (less than ∼3km/h) but becomes mentsofVLandRFEMGactivityinFigure3(a)mayreflect
prominentathigherspeeds(>4km/h)(Figure3(b)),aspeed higher biomechanical demands on proximal leg muscles at
effect consistent with that reported in the literature [28, 43, higher dimensionless speeds. Nonlinear reorganization of
45,46].Giventhat,itshouldbestressedthatwalkingatlower EMG patterns was also observed when using exoskeleton
gravitylevelsatthesamespeed(Figure3(a))correspondsto robotic devices that provide body weight support [42, 47].
walkingathigherspeedsifoneusestheFroudenumberasa Changes in the body reference configuration during stance
dimensionless parameter(e.g., walk-run transitionat 0.25g (slightlyflexedposture[48,49])maycontributetoagreater
BioMedResearchInternational 7
0.16 g 1 g Pluto Mars Earth
Moon
25 𝜇V 100 𝜇V Left
Δ 10
Right
Left 8 Running FFrr ~~ 00..55
Right1 s 0 100 1 s 0 100
cle (%) 0 Cycle (%35)0 Cycle (%6)00S O𝜇VL Speed (km/h) 46 S m o oth transitio ns Abrupt switch
Cy Walking
100
0 0 2
W-R R-W
h)8 Walking
m/4 speed 0
k0
( 0 50 100 150 0 50 100150200250300 0 0.2 0.4 0.6 0.8 1 1.2
Time (s) Time (s) Simulated gravity,gEarth
(a) (b)
Figure 4: Smoothness/abruptness of gait transitions at different gravity levels. (a) Soleus (SOL) EMG patterns during slow changes in
treadmillbeltspeed(lowerpanels)inonerepresentativesubjectat0.16g(left)and1g(right).Upperpanels:examplesofSOLEMGwaveforms
(left,plottedversustime;right,plottedversusnormalizedcycle)during5consecutivestridesofbothlegsaroundthetransitionfromwalking
(blacklines)torunning(graylines).Dottedcurvesdenotethe(transition)strideoftheleginwhichtheswingphasefirstexceeded50%
gaitcycle.Bottomhorizontalbarsdenotestance(black)andswing(white)phases.Lowerpanels:thecolormapsrepresentasequenceof
discreteactivationwaveforms(verticalslices).𝑥-axisindicatesthenumberofthegaitcycles(correspondingtotheappropriatetimingofthe
trial),𝑦-axisindicatesnormalizedgaitcycle(fromtouchdowntoanothertouchdown),andcolorindicatesEMGamplitude.Thewhiteline
indicateswhentoeoffoccurred.Verticaldashedlinesindicatewalk-to-run(W-R)andrun-to-walk(R-W)transitions.Noteabruptchanges
intherelativestancedurationandmuscleactivationpatternsatgaittransitionsat1gandnoobviousdistinctionintheseparametersatthe
transitionfromwalkingtorunningat0.16g.(b)Schematicrepresentationofthesmoothnessofgaittransitionsasafunctionofgravity.The
orangecurvesymbolizesthedimensionlesswalk-runtransitionspeedconsistentwiththetheoryofdynamicsimilarity(Fr∼0.5)[19,29,44].
Thebluecolorrangeofgravitationallevelsrepresentsadiscontinuousswitchfromwalktorun,whereasthewhiteregionindicatessmooth
transitions.
activity of proximal extensors as well. Finally, there is a effect on the speed at which gait transitions occur (Fr ∼
differential effect of speed on quadriceps muscle activity at 0.5). Surprisingly, however, we found [18, 19] that at lower
reduced gravity levels: VL and RF activity increases at low levelsofsimulatedgravitythetransitionbetweenwalkingand
speeds(<3km/h)whileitdecreasesatahighspeed(5km/h) runningwasgenerallygradual,withoutanynoticeableabrupt
(Figure3(b)). Potential nonlinear scaling of muscle activity changeingaitparametersorEMGbursts(Figure4(a)).This
for most whole body movements in microgravity should was associated with a significant prolongation of the swing
alsobetakenintoaccountforexercisecountermeasuresfor phase,whosedurationbecamevirtuallyequaltothatofstance
astronauts. in the vicinity of the walk-run transition speed, and with
a gradual shift from inverted-pendulum gait (walking) to
5.DifferentGaits bouncinggait(running).Alackofdiscontinuouschangesin
thepatternofspeed-dependentlocomotorcharacteristicsina
Considering complex, high-dimensional, dynamically cou- hypogravityenvironment(Figure4(b))isconsistentwiththe
pled interactions between an organism and gravitational ideaofacontinuousshiftinthestateofagivensetofcentral
environment, in principle, one challenging solution is to patterngenerators,ratherthantheactivationofaseparateset
adoptdifferentcoordinationpatternsandnotonlyanoptimal ofcentralpatterngeneratorsforeachdistinctgait[19].
speed of locomotion. Are different gaits possible on other Interestingly,thesmoothnessofgaittransitionsisaccom-
planets? panied by a gradual shift from inverted-pendulum gait
Oneapproachtostudylocomotoradaptationsistolook to bouncing gait, resulting in a “paradoxical” inverted-
at the effect of gravity on gait transitions. A gait has been pendulumrunninginthevicinityofrun-walkandwalk-run
definedas“apatternoflocomotioncharacteristicofalimited transitions[18].Theswingphasemayhavemoreinfluenceon
rangeofspeedsdescribedbyquantitiesofwhichoneormore gait than it was previously thought. For instance, relatively
change discontinuously at transitions to other gaits” [29]. slower swing and longer foot excursions (tilted BWS con-
An important aspect of gait transitions is a discontinuous dition,Figure2(c))mayraisequestionsaboutoptimalityor
switch that occurs at some point while varying the speed comfortofwalkingandcouldaccountforpotentiallydifferent
of progression (although some exceptions may exist [50– preferred gaits, such as loping on the Moon observed in
52]).Asalreadydiscussed(Figure2(a)),gravityhasastrong Apollo astronauts (though the Lunar suit limits the range
8 BioMedResearchInternational
Enceladus Moon
Europa Io
25
N s) 20 10
e (
mpuls 15 bjects
d available i 10 5 uccessful su
e S
ct
di 5
e
Pr
0 0
10 13 16 19 22 25
Simulated gravity,g (%)
Earth
Predicted available impulse (N s)
Successful subjects
(a) (b)
Figure5:Runningonwateratsimulatedreducedgravity.Thebluecurverepresentsthenetverticalimpulseavailabletorunonwater,as
predictedbythemodelusedbyMinettietal.[53].Barsrepresentthenumberofsubjects,outof6,capableofavoidingsinkingatdifferent
simulatedgravityvalues.Bothvariablesshowthat22%ofEarthgravity(𝑔 )isthemaximumgravityatwhichhumanscanrunonwater,
EARTH
whenassistedbyasmallrigidfin(asillustratedintheleftpanel).
of motion in the leg joints and may also contribute to the species, including humans, this is precluded by body size
loping gait on the Moon [9]). The resulting changes in the andproportions,lackofappropriateappendages,andlimited
intersegmentalandinterlimbcoordinationmayinturnaffect muscle power. However, if gravity is reduced to less than
the COM motion. Overall, the results support the idea of Earth’sgravity,runningonwatershouldrequirelessmuscle
looking for new forms of locomotion (both bipedal and power. Recently, Minetti et al. [53] used this hydrodynamic
quadrupedal)inaheterogravityenvironment[54]basedon modelofGlasheenandMcMahon[61]topredictthegravity
theinterplaybetweenstanceandswinglegdynamics,altered levelsatwhichhumansshouldbeabletorunonwaterand
interlimbcoupling,andalteredcenterofmassmovements. testedthehypothesisinthelaboratoryusingareducedgravity
Othersignificantinfluencesofgravityonshort-termand simulator(Figure5).Theresultsshowedthatahydrodynamic
long-term gait adaptations may be related to its effects on model of Basilisk lizards running on water [61] can also be
the body reference configuration [48, 49] and anticipatory appliedtohumans,despitetheenormousdifferenceinbody
mechanisms of limb and body movements [55, 56]. For sizeandmorphology.Particularly,22%ofEarth’sgravityisthe
instance,thebasisofhabitualhumanpostureisposturaltone maximumatwhichhumanscanrunonwater,whenassisted
of the skeletal muscles and microgravity elicits substantial by a small rigid fin (Figure5) [53]. It is also worth noting
changes in muscle tone and posture [48, 49]. Based on thelimitationsforourmusculoskeletalsystemforproducing
clinical observations, it has been recently argued that any force/power (endurance); for instance, the stride frequency
reflection on the nature and choice of preferred gait (e.g., in humans is limited to about 2Hz, whatever the planet is.
bipedalversusquadrupedal)shouldincludeaconsideration OnEarth,thebiggestanimalthatcanrunonwaterislikely
of the mechanisms determining the choice of unconscious WesternGrebes,andeventhesebirdscanrunonlyforseveral
habitual posture [57]. Also, in analogy with the results seconds since the force production is basically anaerobic
based on upper-limb movements related to time-to-contact (participantsin[53]couldrunatsimulated“Moon”gravity
[55] or movement planning [58], anticipatory postural and onlyfor∼10s).Incontrast,atreducedgravity(Moon),these
locomotor adjustments for lower limb movements (e.g., for birds could run on water in a charming manner for much
thecontrolofheelstrikeoraccuratefootplacement)should longertime.
take gravity into consideration. Therefore, altered gravity
conditions may also affect locomotor-related tasks such as
6.ClinicalImplications
thenegotiationofstationaryandmovingobstructionsduring
walkingorgaitinitiation/termination[56,59,60]. Reducedgravityalsooffersuniqueopportunitiesforadjust-
Finally, the repertoire of known gaits can be expanded ing the basic patterns to altered locomotor conditions for
to a variety of animals. For instance, on Earth only a gaitrehabilitation.Bodyweightsupportsystemscoupledwith
few legged species, such as water strider insects and some robotic devices or pharmacologic treatments are now often
aquatic birds and lizards, can run on water. For most other usedintherehabilitationpracticetoassistphysicaltherapyof
BioMedResearchInternational 9
Hand-walking
300 𝜇V 30 cm Hand
RF
BF 200 𝜇V FCU
TA
BIC
LG
Flex 800 𝜇V DELTa
30∘ Hip
Ext
Knee
30∘
50 cm Foot
15∘ Ankle
100 𝜇V ST
5 s
Delay
BF
ES of peroneal nerve 5 s
(a) (b)
Figure 6: Eliciting nonvoluntary limb stepping movements in simulated weightlessness (gravity neutral) conditions. (a) An example of
nonvoluntaryrhythmicmovementsofthesuspendedlegsinducedbyelectricalstimulation(ES)ofperonealnervefromthestudyofSelionov
etal.[62].Notetheabsenceofanklejointrotationsduringevokedair-stepping.(b)Anexampleofevokedrhythmiclegmovementsduring
handwalkinginonesubjectfromthestudyofSylos-Labinietal.[63].RF,rectusfemoris,BF,bicepsfemoris,TA,tibialisanterior,LG,lateral
gastrocnemius,FCU,flexorcarpiulnaris,BIC,bicepsbrachii,DELTa,anteriordeltoid,ST,andsemitendinosus.Handandfootdenoteanterior-
posteriordisplacementsofthelefthandandfoot.
individuals with neurological disorders. We will not review contribute to the clinical development of central pattern
any detailed analysis of clinical outcomes for ambulation generator-modulating therapies and neuroprosthetic tech-
when using locomotor training with body weight support nologies[65,69].
systems and refer to other reviews [64]. Nevertheless, it is
worthemphasizingafacilitatoryeffectofthelackofgravity 7.ConcludingRemarks
onrhythmogenesisanditspotentialforgaitrecovery.
Novel pharmacological strategies [65] and electromag- This perspective outlines an interdisciplinary approach to
neticstimulationtechniques[62,66–68]arebeingdeveloped extend our knowledge on adaptationofhuman locomotion
aimed at modulating spinal activity and restoring the loco- toahypogravityenvironment,includingbiomechanical,neu-
motorfunction.Thespinalcentralpatterngenerator(CPG) rophysiological, and comparative aspects, effective exercise
circuitrycanbeeasilyactivatedinhealthyhumansinagravity countermeasures for astronauts, and even exobiology of
neutral position by applying tonic central and peripheral new forms of locomotion on different planets. The tools
sensory inputs. To minimize interference with the ongoing and techniques used for hypogravity simulation and their
taskofbodyweightandbalancecontrol,steppingmovements effectsonhumanlocomotionprovidenewinsightsintoour
are elicited during air-stepping in the absence of gravity understanding of the physiological effects of gravity. The
influencesandexternalresistance.Figure6illustratesexam- beneficialeffectofweightlessnessonrhythmogenesiswould
plesofnonvoluntaryrhythmicmovementsofthesuspended furtherenhancetheutilityofthisapproachanddevelopments
legsinducedbyelectricalstimulationofperonealnerve[62] ofinnovativetechnologiesforgaitrehabilitation.
and during hand walking [63]. It has been suggested that
functionalmultisensorystimulationsandafunctionalneural ConflictofInterests
coupling between arm and legs can inspect CPG access by
sensoryandcentralactivationsandentrainlocomotorneural The authors declare that there is no conflict of interests
networksandpromotegaitrecovery.Suchinvestigationsmay regardingthepublicationofthispaper.
10 BioMedResearchInternational
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