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odular functional organisation of the axial locomotor systemn salamanders�
ean-Marie Cabelguen ∗, Vanessa Charrier, Alexia Mathoueurocentre Magendie, INSERM U 862, Bordeaux University, 146 rue Léo Saignat, F-33077 Bordeaux Cedex, France
r t i c l e i n f o
rticle history:eceived 12 August 2013eceived in revised form 10 October 2013ccepted 14 October 2013
a b s t r a c t
Most investigations on tetrapod locomotion have been concerned with limb movements. However, thereis compelling evidence that the axial musculoskeletal system contributes to important functions duringlocomotion. Adult salamanders offer a remarkable opportunity to examine these functions because theseamphibians use axial undulations to propel themselves in both aquatic and terrestrial environments. In
vailable online 1 November 2013
eywords:xial systementral pattern generator
this article, we review the currently available biological data on axial functions during various locomotormodes in salamanders. We also present data showing the modular organisation of the neural networksthat generate axial synergies during locomotion. The functional implication of this modular organisationis discussed.
Tetrapod locomotion involves rhythmic and coordinated move-ents of the limbs and the trunk. The locomotor movements of the
imbs have been extensively studied, whereas those of the trunkave received relatively less attention (reviewed in Cabelguen et al.,010; Schilling, 2011).
Most studies addressing the function of the trunk during loco-otion have targeted the part of the axial musculoskeletal system
trunk) located between the two girdles (reviewed in Falgairollet al., 2006; Cabelguen et al., 2010; Schilling, 2011). However,
gaze stabilisation and orientation during locomotion (cf. Chagnaudet al., 2012). Furthermore, studies in tailed tetrapods, includingsalamanders, have shown that during terrestrial stepping, the tailmotions maintain dynamic balance when walking on narrow orslippery substrates or during perturbed locomotion (Siegel, 1970;Wada et al., 1993; Gillis et al., 2009; Bicanski et al., 2013a). Insalamanders, the tail also provides hydrodynamic thrust duringswimming (Frolich and Biewener, 1992). Taken together, theseobservations suggest that the neural networks underlying themovements of the axial musculoskeletal system during locomotioninclude three distinct functional parts (“functional modularity”).
everal observations suggest that the regions of the axial muscu-oskeletal system located rostral to the pectoral girdle (anteriorrunk) and caudal to the pelvic girdle (posterior trunk or tail)lay specific and complicated roles during locomotion. Indeed, thehythmic movements of the anterior trunk region contribute to
� This article is part of a special issue entitled “Axial systems and their actuation:ew twists on the ancient body of craniates”.∗ Corresponding author. Tel.: +33 5 57 57 40 52.
The present short review attempts to provide evidenceregarding the functional modularity of the axial musculoskele-tal system with examples drawn from studies on the locomotorbehaviour of salamanders.
Among vertebrates, salamanders constitute a group well suitedfor investigating this issue. First, there is an abundance of kinematicand EMG data on the operation of the axial musculoskeletal sys-tem during various locomotor behaviours (Chevallier et al., 2008;
Cabelguen et al., 2010; Schilling, 2011). Second, the trunk and tailplay specific roles during locomotion in salamanders (Charrier et al.,2010). Third, the architecture of the neuronal network producing
xial locomotor movements can be investigated in vitro using iso-ated spinal cords (Ryczko et al., 2010).
In this article, we will first provide an overview of the currentnowledge of the diversity of the axial locomotor patterns in sala-anders (Section 2), followed by a discussion of the neurobiological
ata supporting the modular functional organisation of the axialocomotor networks (Section 3).
. Diversity of the axial locomotor patterns
As amphibians, salamanders display a variety of aquatic and ter-estrial locomotor gaits and are able to rapidly switch betweenhem. Because aquatic and terrestrial environments pose differ-nt challenges to movement, the richness of the locomotor skills ofalamanders suggests a highly dynamic locomotor system.
In water, salamanders typically swim in the water column ortep forward along the bottom (“underwater stepping”). The swim-ing gait, which is the fastest gait of the salamander, is similar
o that of anguilliform fishes with axial undulations correspond-ng to waves of lateral displacement propagating from head toail (Roos, 1964; Daan and Belterman, 1968; Frolich and Biewener,992; Carrier, 1993; D’Août et al., 1996; Gillis, 1997; Deban andchilling, 2009). The amplitude of the axial undulations typicallyncreases as it propagates towards the tip of the tail, and the aver-ge wavelength is shorter than the body length (i.e., more thanne wave travels down the body per swimming cycle) and doesot vary with the frequency of oscillation (Frolich and Biewener,992; D’Août and Aerts, 1997). Interestingly, in contrast to lam-reys (McClellan, 1989; Islam et al., 2006) and eels (D’Août anderts, 1999), salamanders do not exhibit (spontaneous or evoked)pisodes of backward swimming.
The axial musculature of salamanders consists of two principalasses, the epaxial and hypaxial muscles (see Schilling, 2011 for
eview). The main epaxial muscle (m. dorsalis trunci) forms a sin-le large dorsolateral bundle extending from the head to the tipf the tail (Francis, 1934). This bundle is completely segmentednto myomeres, one corresponding to each vertebra. Salamandersave clearly defined hypaxial muscle groups based on their rel-tive position on the trunk (Simons and Brainerd, 1999; O’Reillyt al., 2000). The lateral hypaxial muscles consist of 3–4 layers ofuscles wrapping around the lateral aspect of the trunk.EMG recordings performed in salamanders are consistent with
he hypothesis that the m. dorsalis trunci and the lateral hypax-al muscles act synergistically to produce the travelling waves ofateral bending during swimming (Frolich and Biewener, 1992;arrier, 1993; Delvolve et al., 1997; Bennett et al., 2001; Debannd Schilling, 2009). However, the waves of EMG activity travelown the body faster than the mechanical waves of body curva-ure (Frolich and Biewener, 1992; D’Août et al., 1996). Therefore, theelay between the timing of muscle activity and lateral bending (oruscle strain) increases progressively from head to tail. It has been
uggested that activating muscles earlier in the strain cycle pro-ides a mechanism for increasing power production or stiffeninghe tail to improve the transmission of propulsive forces (Williams,986; D’Août et al., 1996; Altringham and Ellerby, 1999; Ellerbyt al., 2001).
The EMG recordings during swimming further suggest that thexial system of salamanders consists of three distinct functionalegions (“modules”): the anterior trunk, the trunk and the tail.irst, the EMG recordings reveal non-uniformities in the inter-egmental coordination pattern of the epaxial muscle activations
t two longitudinal trunk positions: caudal to the pectoral gir-le and close to the pelvic girdle (Frolich and Biewener, 1992;elvolve et al., 1997). Second, the EMG waves are propagatediscontinuously along the entire length of the animal, with the
gy 117 (2014) 57– 63
anterior trunk displaying a slower speed of propagation than thetrunk and tail, where the speeds are comparable (Delvolve et al.,1997). Third, the intersegmental phase lag is independent of theswimming frequency only in the tail. These functional differ-ences are likely related to the presence of limbs (Delvolve et al.,1997), as they have not been observed in anguilliform swimmers(eel and lamprey), which have a more elongated body withoutpaired appendages (fins) (Grillner and Kashin, 1976; Williams et al.,1989).
Although the EMG waves exhibit a non-uniform propagationspeed along the body, the propagation speed of lateral bending isnearly constant along the entire length of the salamander (Frolichand Biewener, 1992; D’Août and Aerts, 1997). This observationsuggests that the locomotor command is well matched to themechanical properties of the body which varied with longitudi-nal position, especially at the girdle levels. Conversely, the bodydynamics might also contribute significantly to gait generation(Knuesel et al., 2013).
During forward underwater stepping, salamanders use eitherstanding or head-to-tail travelling waves of axial oscillations(Ashley-Ross et al., 2009; Deban and Schilling, 2009; Lamarqueet al., 2009). At the level of the trunk, the oscillation patterns arereflected by similar patterns of activation of the m. dorsalis trunci,while at the level of the tail, the EMG activity is usually weak orcan be absent (Fig. 1A), although the concomitant tail movementsare large (Fig. 1B). This observation suggests that some tail move-ments during underwater stepping primarily result from a passivetransmission of the active trunk movements to the tail, furthersuggesting that the network generating the tail movements canbe functionally decoupled from the network generating the trunkmovements.
Interestingly, the variability in the trunk pattern is lower duringterrestrial stepping than during underwater stepping (Ashley-Rosset al., 2009; Lamarque et al., 2009). The lower variability of themotor pattern during terrestrial stepping likely reflects increasedconstraints on the underlying substratum (increased gravity).Another interesting difference is that the average speed duringunderwater stepping is approximately twice the speed observedduring terrestrial locomotion (Ashley-Ross et al., 2009).
During forward stepping on firm ground, combinations of stand-ing and travelling waves of lateral bending have been reported,depending on the speed of locomotion or the type of steppinggait (i.e., walking or trotting) (Roos, 1964; Daan and Belterman,1968; Edwards, 1977; Ashley-Ross, 1994a; Harischandra et al.,2011; Karakasiliotis et al., 2013). Notably, the trunk and limb move-ments are coordinated in such a way that the lateral undulations ofthe trunk have the positive effect of increasing the stride length(Edwards, 1977; Karakasiliotis and Ijspeert, 2009; Crespi et al.,2013). It has been suggested that the more reduced the limbs are,the slower the speed at which the travelling waves appear, i.e.,salamanders with reduced limbs rely more on travelling groundwaves, while those with stronger limbs primarily use standingwaves (Ashley-Ross, 1994a). Interestingly, elongated salamanderswith reduced forelimbs and no hindlimbs combine the alternat-ing use of the forelimbs with travelling undulatory waves duringaquatic walking (Azizi and Horton, 2004). Large horizontal headmovements, constant dorsoventral bending and twisting of thetrunk have also been observed during land stepping (Frolich andBiewener, 1992; D’Août and Aerts, 1997; Delvolve et al., 1997; Gillis,1997; Karakasiliotis et al., 2013).
The EMG pattern of the m. dorsalis trunci during trottingconforms to the pattern expected for the production of lateral
bending of the trunk, with fixed nodes near the girdles (“stand-ing wave”) (Frolich and Biewener, 1992; Delvolve et al., 1997).Indeed, the myomeres located between the forelimb and hindlimb(trunk myomeres) express single synchronous bursts of activity,
Fig. 1. (A) EMG activities recorded from two trunk and one tail epaxial myomeres on the same side of a single individual during overground stepping (left panel) andunderwater stepping (middle and right panels). In each panel, the shaded area indicates one full cycle of locomotion. The electrode locations are specified as a fraction ofsnout vent length (SVL). Note that the trunk myomeres displayed a burst pattern in all cases, whereas the tail myomere displayed quiescence during underwater stepping(right panel). (B) Plots of the maximal lateral displacement (ordinate) of markers glued over the mid-dorsal line vs. the body length (abscissa) for the same individual during5 grey lt valueo he tai
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strides of overground stepping (black line) and 5 strides of underwater stepping (he location of each marker is specified as a fraction of SVL. The circles indicate meanf the girdles are indicated as grey regions. Note the large lateral displacements of t
ontralateral to the hindlimb support, during each step cycle. Inontrast, the lateral hypaxial musculature often exhibits a doubleurst pattern during stepping, with one burst (main burst) present
n every step cycle and the other burst (facultative burst) showingower intensity and more variability in occurrence (Bennett et al.,001). The timing of the bursts within the locomotor cycle suggestshat the hypaxial musculature plays a dual role during terrestrialocomotion in salamanders: (i) resisting torsional forces translatedo the trunk by the limbs (main burst); and (ii) bending the trunkfacultative burst) (Carrier, 1993; O’Reilly et al., 2000; Bennettt al., 2001; Deban and Schilling, 2009).
Recent kinematic and EMG studies have provided evidencehat the tail of the salamander provides dynamic balance duringtepping and contributes to manoeuvring (e.g., turning) during ter-estrial stepping (Charrier et al., 2010; Charrier and Cabelguen,013; Bicanski et al., 2013a). Correspondingly, the tail muscula-ure displays a complex and variable EMG pattern depending onhe direction of progression and the nature of the surface on whichhe animal moves. Typically, during straightforward stepping on
wet or slippery surface, the tail musculature displays an addi-ional burst of activity in phase with every ipsilateral trunk burst
Delvolve et al., 1997; Charrier et al., 2010; Bicanski et al., 2013a)Fig. 2B). The second burst occurs during the main burst generatedontralaterally, thus providing a co-contraction of the left/right tailuscles. A systematic study of the activation patterns of tail epaxial
ine). The lateral displacements are expressed as a fraction of body length (BL), ands, and the thin lines indicate one standard deviation for mean values. The locations
l during both locomotor modes.
muscles showed waves of EMG activity travelling posteriorly andanteriorly along the tail during stepping on a wet surface (Delvolveet al., 1997). During turning, the tail tonically bends towards thedirection of turning, and correspondingly the tail musculature dis-plays a tonic EMG activity (Fig. 2C). In contrast, independently of thenature of the surface and the direction of progression, the activityof the trunk epaxial musculature consists of left/right alternatingunilateral activity (Fig. 2A–C).
A double burst pattern during each terrestrial stepping cycle hasalso been reported for the epaxial myomeres located in the anteriortrunk region (Delvolve et al., 1997). The additional burst in phasewith the trunk activity is more consistent for myomeres locatedclose to the pectoral girdle. The activation of these myomeres mightdynamically stabilise the region of the trunk located near the pec-toral girdle against limb muscle action during terrestrial stepping(Delvolve et al., 1997; Schilling, 2011).
In addition to the typical swimming and stepping gaits, sala-manders utilise specific forms of locomotion, which have not beensystematically investigated because of difficulties in locomotorelicitation for episodes long enough to perform accurate analyses.Occasionally, salamanders use crawling as a second terrestrial gait,
e.g., when trying to rapidly escape in grass. This crawling gait is sim-ilar to swimming movements on the ground (i.e., with limbs foldedagainst the body) (Edwards, 1977; Ashley-Ross, 1994a,b). How-ever, it is not known whether during these “terrestrial swimming
Fig. 2. Representative EMG patterns recorded from epaxial myomeres and the sequence of snapshots captured during (A) straight walking on a non-slippery surface, (B)straight walking on a slippery surface and (C) lateral turning on a non-slippery surface. In each panel, from top to bottom, the EMG recordings are recorded from one trunkand one tail myomere on the left side and one tail myomere on the right side of the animal. The electrode locations are specified as a fraction of SVL. The sequences ofsnapshots show one complete stride (lasting 1080 ms in A, 1680 ms in B and 1210 ms in C). The sequences progress from left to right. Note that during each step cycle, thet nic ac
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ail myomeres exhibited a single burst in (A), two bursts in (B) and a more or less to
dapted from Bicanski et al. (2013a).
ovements” the animals use waves of axial bending and musclectivity similar to those used during aquatic swimming, as pre-iously reported in the eel (Gillis and Blob, 2001). In the water,alamanders occasionally exhibit low-speed paddling of the limbs,ssociated with small axial rhythmic movements (Frolich andiewener, 1992; Ashley-Ross, 1994a; Delvolve et al., 1997), andhort episodes of backward stepping or steering behaviour in
three-dimensional space. Salamanders spontaneously exhibithort episodes of backward stepping during manoeuvring on landCabelguen et al., 2010). Thereafter, these animals switch to a morefficient forward stepping. Much longer episodes of backwardtepping can be induced through training to walk backward on aotorised treadmill (Ashley-Ross and Lauder, 1997). It would be
nteresting to investigate the bending pattern of the trunk or taili.e., the presence of travelling or standing waves) and the EMGattern of axial muscles underlying these locomotor behaviours to
btain deeper insight into the organisation of the axial networksn salamanders.
In conclusion, kinematics and EMG studies have revealed thathe axial system of salamanders has a high flexibility, which is
tivation in (C). In each case, the trunk myomeres displayed a single burst pattern.
essential for successful adaptations of the locomotor movementsto the surrounding and the goals of the animal (e.g., turning orbackward stepping). Importantly, these studies further demon-strated that part of this flexibility is derived from the combinationof the coordination patterns expressed by three distinct axial mod-ules (i.e., the anterior trunk, trunk and tail). These modules worktogether with the limbs in a task- and context-dependent man-ner, thereby increasing the number of degrees of freedom of thelocomotor system. How these different patterns of coordinationare generated remains unknown, but it seems likely that sensoryfeedback and descending inputs contribute substantially in thisregard.
3. The axial locomotor network
The patterned muscle contractions underlying locomotion invertebrates are produced by neural networks located in the spinalcord (central pattern generators: CPGs) (Grillner, 1981). In limbedanimals, it is convenient to distinguish the networks controlling
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xial motions, i.e., the axial locomotor CPGs, from those controllingimb motions, i.e., the limb CPGs (Ijspeert, 2008).
The axial locomotor CPGs have been extensively investigated inimbless, swimming vertebrates. A combination of neurobiologicalnd modelling work in lampreys (Grillner, 2006) and Xenopus lae-is embryos (Roberts et al., 1997) has demonstrated the segmentaltructure of the axial CPG for swimming, showing a double chainf reciprocally coupled identical oscillators (pools of neurons thatxhibit a rhythmic activity) distributed along the spinal cord andutually coupled through local and long-distance intersegmental
oordinating systems. These data further suggest that each hemi-egmental oscillator is a pool of excitatory (glutamatergic) neuronsenerating recurrent bursting, coupled with a pool of inhibitoryglycinergic) neurons to ensure inhibition of the contralateral hemi-egment and generate left/right alternation (Cangiano and Grillner,005; Roberts et al., 2008).
In salamanders, the neurobiological studies on the axial loco-otor CPG have targeted the network generating the motions
f the trunk (“trunk CPG”) and, more recently, the networkontrolling the motions of the tail (“tail CPG”). Unfortunately, theetwork producing the anterior trunk movements (“anterior trunkPG”) during locomotion has not been investigated.
Experiments on surgically isolated segments or hemi-segmentsrom the trunk spinal cord of salamanders provide direct evidencef a strong similarity of the global architecture and operating modef the trunk CPG of the salamander with that of the swimming CPGf the lamprey (Ryczko et al., 2010). Modelling studies also sup-ort this notion (Bem et al., 2003; Ijspeert et al., 2007; Bicanskit al., 2013b). However, salamanders and lampreys differ as to theechanism for terminating each burst generated by the spinal seg-ents. Indeed, this mechanism does not involve Ca2+-activated K+
hannels in salamanders (Ryczko et al., 2010), whereas it does inampreys (El Manira et al., 1994). Further experiments are needed tonvestigate whether the rhythmogenesis in axial segments relies onimilar cellular mechanisms in salamanders and lampreys (Grillner,006).
Propagated waves of motor activity along the trunk cord haveeen observed during chemically induced locomotor-like activity
n vitro using isolated spinal cords of salamanders (see Falgairollend Cazalets, 2007, for a similar observation in the newborn rat).
A systematic investigation of the different patterns of ven-ral root (VR) activity produced in the isolated spinal cord ofalamanders has revealed a high degree of flexibility in the interseg-ental coordination pattern, i.e., in the operating mode of the axial
etworks (Ryczko et al., 2009). Intersegmental phase lags rangerom positive values (i.e., backward propagating waves) to nega-ive values (i.e., forward propagating waves), including the valuesbserved in vivo. Therefore, the variability in the intersegmentalhase lag has been associated with the diversity of the locomotorehaviours observed in vivo (Ryczko et al., 2009). A similar flexi-ility in the operating mode of the axial networks has previouslyeen shown in the lamprey (Matsushima and Grillner, 1992) ando a lesser extent in the tadpole (Green and Soffe, 1996).
The existence of a tail locomotor CPG in the salamanderas recently been demonstrated using isolated tail spinal cordreparations chemically activated through a superfusion of N-ethyl-d-aspartate (NMDA) (Charrier and Cabelguen, 2013). TheR recordings showed that the tail spinal cord produces wavesf motor activity travelling up or down and alternating betweenhe left and right sides. These waves are consistent with the twoistinct waves of EMG activity travelling in opposite directionslong the tail during each stepping cycle performed on a wet
alking surface by freely moving salamanders (Delvolve et al.,
997). Lesion experiments further revealed that the global archi-ecture of the tail CPG is similar to that of the trunk CPG (Charriernd Cabelguen, 2013). Indeed, (i) surgically isolated tail segments
gy 117 (2014) 57– 63 61
can generate a left/right alternating VR activity when chemicallyactivated with bath-applied NMDA; (ii) there is no significant cor-relation between the burst frequency of a given segment and itslocation along the tail spinal cord; (iii) isolated tail hemi-segmentscan generate a rhythmic motor activity when superfused withNMDA.
However, although this similarity explains left/right alterna-tions and the waves of EMG activity travelling along the tail musclesduring terrestrial stepping (Delvolve et al., 1997), it does not explainthe double burst pattern that selectively occurs in the tail duringstepping in an unstable environment. How these variable tail pat-terns are generated remains unknown. One hypothesis might bethat during locomotion, the tail motoneurons receive excitatoryand inhibitory commands simultaneously from right and left seg-mental oscillators, and the relative strength of the two inputs,influenced through afferent and descending inputs, determines thephasing of the motoneuron activity. Thus, the tail muscles mightdisplay one or two bursts per phase. A similar mechanism has beenproposed for the control of bifunctional limb muscles that mightdisplay extensor- or flexor-related activity (or both) during loco-motion in mammals (Perret and Cabelguen, 1980).
The waves of VR activities propagate more rapidly posteri-orly than anteriorly along the isolated trunk cord (Delvolve et al.,1999; Ryczko et al., 2009). Moreover, the intersegmental phase lagalong the isolated trunk cord is longer during caudorostrally thanrostrocaudally propagated waves (Delvolve et al., 1999; Ryczkoet al., 2009). Altogether these data suggest that the ascending anddescending coupling mechanisms are not functionally equivalent inthe trunk network of salamanders. In contrast, functionally equiv-alent ascending and descending coupling mechanisms have beenobserved in the salamander’s tail network (Charrier and Cabelguen,2013). A similar result has been reported during fictive swimmingexpressed by isolated lamprey spinal cords bathed in an NMDAsolution (Matsushima and Grillner, 1992). Interestingly, our pre-vious EMG study in swimming salamanders suggested that onlythe tail network displays all of the properties of the anguilliformswimming network (Delvolve et al., 1997).
Recent experiments have revealed efficient short-distance (i.e.,spanning only 1–2 segments) coupling between the trunk and tailnetworks during the rhythmic motor activity produced by isolatedspinal cords from salamanders (Charrier and Cabelguen, 2013). Inlamprey, short-distance (spanning only 4–6 segments) couplingappears to be the main factor that generates the intersegmentalcoordination appropriate for fictive swimming, while long-distancecoupling mechanisms play a comparatively minor role (McClellanand Hagevik, 1999; Miller and Sigvardt, 2000). However, the rel-ative contribution of short and long coupling mechanisms to theproduction of intersegmental coordination patterns in freely mov-ing animals remains unknown. Modelling studies should guidefurther biological experimentation to address this issue (see Kozlovet al., 2009; Knuesel et al., 2013).
It is reasonable to postulate that the control of the couplingbetween the trunk and the tail through sensory and/or descendinginputs could be an elegant way to generate the axial flexibilityrequired to perform adapted locomotion. Preliminary experimentsin semi-intact salamander preparations (i.e., decerebrated animalsfrom which the forelimbs were removed; Cabelguen et al., 2003)support this view. Indeed, the rhythmic movements restrictedto the tail could be induced through the electrical stimulationof the dorsal region of the first spinal cord segment near theobex (Bicanski et al., 2013b). Furthermore, the stimulation ofmesencephalic sites induces tonic lateral bending of the whole
body towards the left or the right, as required for turning orrhythmic movements of the body during locomotion (Cabelguenet al., 2003). These preliminary results suggest that the control ofthe degrees of freedom of the axial musculoskeletal system results
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rom the activation of a combination of descending pathways,hich selectively activate the anterior trunk, the trunk or the tailPGs (see Bicanski et al., 2013a for further discussion).
To conclude this section, in vitro experiments suggest a modularrganisation of the axial locomotor CPG with the specific controlf each module through descending inputs (“distributed com-and organisation”). This proposed organisation would increase
he dynamics of the axial locomotor CPG with an increasing num-er of degrees of freedom. Further studies are needed to establishhether these modules can be controlled independently througheripheral inputs. Moreover, the interactions between the limb
ocomotor CPGs and each axial module remain unknown.
. Conclusion
This short review emphasises that the modular functionalrganisation of the axial system in vertebrates importantly con-ributes to the dynamics of locomotion. The axial modules, inombination with the limb CPGs, generate muscle synergies andaits that are appropriate for moving in a continuously varyingnvironment. One important goal for future research is to inves-igate the mechanisms that enable flexibility in the axial motorutput depending on the locomotor task. These mechanisms shoulde evaluated based on the complex interplay between the centralervous system, the sensory receptors, the body dynamics and thenvironment. A promising approach is to combine neurobiologi-al experiments, modelling and robotics, as previously used in thealamander (Ijspeert et al., 2007).
cknowledgment
This work was supported through a grant from the Fondationour la Recherche Médicale (DNC20101021008).
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