A commentary on 'Shared strategies for behavioral switching: understanding how locomotor patterns are turned on and off'

by Mesce, K. A., and Pierce-Shimomura, J. T. (2010). Front. Behav. Neurosci. 4:49

Ian A Hope

Jordan Hylke Boyle

Manlio eTassieri

Netta eCohen

Stefano eBerri

English

PubMed

Boyle, J.H.

Berri, S.

Tassieri, M.

Hope, I.A.

Cohen, N.

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Gait modulation in <i>C. Elegans</i>: it's not a choice, it's a reflex!

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Gait modulation in C. elegans: It's not a choice, it's a reflex!

A commentary on Shared strategies for behavioral switching: understanding how locomotor patterns are turned on and off

Boyle, JH

Berri, S

Tassieri M

Hope, IA

Cohen, N

White Rose Research Online

promoting access to White Rose research papersWhite Rose Research Onlineeprints@whiterose.ac.ukUniversities of Leeds, Sheffield and Yorkhttp://eprints.whiterose.ac.uk/This is the published version of a letter to the editor published in Frontiers inBehavioral Neuroscience, 5 (10)White Rose Research Online URL for this paper:http://eprints.whiterose.ac.uk/id/eprint/7739Published article:Boyle, JH, Berri, S, Tassieri M, , Hope, IA and Cohen, N (2011) Gait modulationin C. elegans: It’s not a choice, it’s a reflex! Frontiers in Behavioral Neuroscience,5 (10). 1 - 3.http://dx.doi.org/10.3389/fnbeh.2011.00010Frontiers in Behavioral Neuroscience www.frontiersin.org March 2011 | Volume 5 | Article 10 | 1BEHAVIORAL NEUROSCIENCEGENERAL COMMENTARYpublished: 07 March 2011doi: 10.3389/fnbeh.2011.00010Gait modulation in C. elegans: It’s not a choice, it’s a reflex!Jordan H. Boyle1, Stefano Berri2, Manlio Tassieri3, Ian A. Hope4 and Netta Cohen1,5*1 Biosystems Group, School of Computing, University of Leeds, Leeds, UK2 Leeds Institute of Molecular Medicine, University of Leeds, Leeds, UK3 Division of Biomedical Engineering, School of Engineering, University of Glasgow, Glasgow, UK4 Institute of Integrative and Comparative Biology, University of Leeds, Leeds, UK5 Institute of Membrane and Systems Biology, University of Leeds, Leeds, UK*Correspondence: n.cohen@leeds.ac.ukA commentary onShared strategies for behavioral switching: understanding how locomotor patterns are turned on and offby Mesce, K. A., and Pierce-Shimomura, J. T. (2010). Front. Behav. Neurosci. 4:49. doi: 10.3389/fnbeh.2010.00049In their perspectives article, Mesce and Pierce-Shimomura (2010) make a case for the existence of two locomotion gaits in C. elegans, and for the ability of this nematode worm to choose between them. Here, we offer a counter-perspective, namely, that the variety of observed behaviors are more appropriately described as a single gait.In what follows we focus on pure forward locomotion, which is generally believed to be controlled by a dedicated circuit, distinct from the circuits that control backward locomotion and head motor behavior. With regard to our question of gaits, we are not aware of any evidence that links head swings with the generation of propulsive (forward/backward) locomotion, so these will not be considered here.Are swimming And crAwling chArActerized by quAlitAtively different pAtterns of body bending?In C. elegans, forward locomotion, whether “swimming” (in liquids) or “crawling” (in or on gels) involves smooth propagation of undulations from head to tail. We argue that while such propagations can vary in kinematic parameters such as frequency, wavelength, and amplitude, these variations are continuous and there is no evidence for more than a single fundamental behavior1. If, as Mesce and Pierce-Shimomura (2010) argue, “bends propagate at uniform veloc-ity for crawling, but “whip” to the back of the body after characteristic pauses when the whole-body of the worm is bent into a C-shaped posture during swimming,” then these characteristic pauses would be evi-dent in plots of bending angle over time: the longer the pauses in extreme maximally bent positions, the squarer the bending wave would appear. In fact, in Pierce-Shimomura et al.’s own data, bending plots over time show proportionately little time spent in the extreme positions (Pierce-Shimomura et al., 2008; Vidal-Gadea et al., 2009). Our own data for worms in liquid buffer solution confirm this (Figure 1C). More generally, Figure 1D clearly shows the equivalence of temporal patterns of dorso-ventral bending for “swimming,” “crawling,” and intermedi-ate behaviors, upon normalization by ampli-tude and undulation period.Furthermore, if, as claimed, swimming worms “whip” their bodies and propagate bends at non-uniform velocity, this would be evidenced by non-linear stripes in the contour plots for swimming worms (Figure 1B of Pierce-Shimomura et al., 2008). Our own data (Figures 1A,B, reproduced with permission from Berri et al., 2009) similarly show uniform bend propagation for worms exhibiting a range of behaviors (correspond-ing to a range of physical conditions). Whether looking at the spacing between the stripes (the period of undulation), the inclination of the stripes (the speed of bend propagation) or the amount of overlap (the wavelength along the body), we find only a gradual change between consecutive plots. Finally, we note that bending along the body directly maps muscle activation. Calcium imaging of muscle activity during locomo-tion of unrestrained worms in water and on agar (Pierce-Shimomura et al., 2008) indicates a clear one-to-one relationship between muscle activity and bending. This strong match holds in both environments and does not break down for fast undula-tions (during swimming). Therefore, it is reasonable to expect that the same one-to-one relationship should hold in intermedi-ate environments (up to a fixed phase lag which of course differs in different condi-tions). Another way of putting it is that body curvature is an equally appropriate (and eas-ier to obtain) metric. In summary, the data strongly suggest that the entire transition from “swimming” to “crawling” corresponds to modulation of a single gait. Indeed, we find no evidence of a qualitative distinction between the undulation patterns.Are swimming And crAwling chArActerized by different frequencies of undulAtion?Mesce and Pierce-Shimomura (2010) state that C. elegans worms “crawl with a persist-ent S-shaped posture on a dry substrate with ∼1 Hz high-amplitude bends, and swim in liquid with ∼2 Hz lower amplitude bends.” Indeed, the existence of two locomotion frequencies might be grounds to define two distinct gaits. However, it is impor-tant to point out the current consensus that the worm modulates its frequency of undulations as a function of the resistivity (viscosity or visco-elasticity) of the physi-cal environment. This was demonstrated in Berri et al. (2009) for gelatin solutions (not methylcellulose as described in Mesce and Pierce-Shimomura, 2010). Similar results were independently reproduced for high molecular weight dextran (Fang-Yen et al., 2010). In fact, while this is not mentioned in Mesce and Pierce-Shimomura (2010), Pierce-Shimomura et al. similarly report a nearly threefold modulation of the bending frequency (0.6–1.5 Hz) in what they dub “swim-like” behavior (Vidal-Gadea et al., 2009), while frequencies of 0.2–0.4 Hz are dubbed “crawl-like,” despite the fact that the peak of the power spectrum for 1Specifically, these three quantitative metrics capture the temporal and spatial properties of the body undulation to a good degree of accuracy (although additional metrics could always be added to capture the complex, non-sinusoidal features of the waveform).Boyle et al. C. elegans locomotion: it’s a reflex!Frontiers in Behavioral Neuroscience www.frontiersin.org March 2011 | Volume 5 | Article 10 | 2are these transitions really spontaneous and internally selected? Here we pro-vide an alternative interpretation, moti-vated in part by our own, possibly related observations. One technical difficulty in working with many polymer solutions (e.g., agar, gelatin, methylcellulose) is obtaining homogeneous environments with different concentrations of the col-loidal particles. Indeed, in characterizing a transition as a function of the environ-ment, any observation of a change of behavior must be explicitly controlled against possible changes in the worm’s local, microscopic environment before such differences can be attributed to an internal decision. We therefore needed an objective metric to quantify the local stiff-ness (or visco- elasticity) of our medium. Using image analysis, and treating the worm as a deformable body governed by Newton’s equations of motion (applied to low Reynolds’ numbers), we numerically estimated the ratio of drag coefficients for each short extract of recorded locomotion. Indeed, plotting the data against this phys-ical metric, the smooth and continuous transition in Figures 1D–F of Berri et al. (2009) is immediately obtained. In the absence of such an objective characteri-zation of the microscopic physical environ-ment, it is impossible to have confidence in any statement about behavioral transi-tions being “spontaneous” and driven by “decision” rather than by some possible response of worms to local changes in the physical environment. In Vidal-Gadea et al. (2009), we might ask whether, e.g., the sudden (small) change in frequency observed for worms in 2–3% methylcel-lulose could be due to the worm moving into or out of contact with the more rigid agar surface underneath.does the existence of A swim-defective mutAnt imply multiple gAits?Mesce and Pierce-Shimomura argue that the identification of “swim-defec-tive” mutants supports the existence of a distinct swimming gait, but we note that the three examples given by Pierce-Shimomura et al. (2008) exhibit some locomotion defect on agar as well. That aside, and even in the extreme case of a mutant with a clear phenotype in liq-uid and none on agar, it is important to which “crawling” and “ swimming” (if they are indeed distinct behaviors) are char-acterized by quite similar frequencies. Specifically the transitions are quantified by a difference of 0.2 Hz or less in the undu-lation frequency. This frequency difference is comparable in value to the variability in frequency (1.2–1.5 Hz) for locomotion in 0.5% methylcellulose (Vidal-Gadea et al., 2009), all of which is dubbed swimming. The small magnitude of the transitions may raise questions, not only about the valid-ity of the classification, but even about the selective advantage worms might gain by such “decisions.”That said, it is clear from the bending plots in Vidal-Gadea et al. (2009) that some small frequency transitions were observed by Pierce-Shimomura et al. But “crawling” appears to fall at about 0.8 Hz (Vidal-Gadea et al., 2009). It is therefore clear that C. elegans locomotion cannot be characterized by discrete sets of kinematic parameters, but rather by a broad and con-tinuous range of such parameters.cAn worms switch spontAneously between the discrete gAits of swimming And crAwling?Transitions between two undulation frequencies in a single environment, if spontaneous, could support the existence of two gaits. However, we note that any observed transitions (in the wild type) were only reported for certain high con-centrations (2.25 and 2.75%) of methyl-cellulose  (Vidal-Gadea et al., 2009), for Figure 1 | (A) Frequency–wavelength relation across a range of gelatin concentrations (filled circles) and agar surfaces (black triangles). Colors represent gelatin concentrations (%) as indicated. The best linear fit to the data is superimposed. Adapted from Figure 1B in Berri et al. (2009). Large black circles indicate which contour plots are shown in (B). (B) Seven contour plots of bending angle (represented by color, with dark red corresponding to extreme dorsal bending and dark blue to extreme ventral bending) over time (horizontal) and along the body (vertical), selected to show the range of observed forward locomotion behaviors, from “swimming” in liquid buffer solution (top) to “crawling” in relatively stiff gelatin (bottom; see methods in Berri et al., 2009 for additional details). Note the linear propagation along the entire body without changes in wave speed. (C) Trace of bending angle versus time for a point near the head of a worm in buffer solution [same data as top plot in (B)]. Note that the worm does not dwell in the maximally bent positions (peaks and troughs of the curve). (D) Bending angle traces as in (C), taken from the 1st, 3rd, 5th, and 7th panels of (B; see color-coded arrow heads) and normalized by undulation period and amplitude. Note the similarity of the waveforms.Boyle et al. C. elegans locomotion: it’s a reflex!Frontiers in Behavioral Neuroscience www.frontiersin.org March 2011 | Volume 5 | Article 10 | 3nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 107, 20323–20328.Mesce, K. A., and Pierce-Shimomura, J. T. (2010). Shared strategies for behavioral switching: understanding how locomotor patterns are turned on and off. Front. Behav. Neurosci. 4:49. doi: 10.3389/fnbeh.2010.00049Pierce-Shimomura, J. T., Chen, B. L., Mun, J. J., Ho, R., Sarkis, R., and McIntire, S. L. (2008). Genetic analysis of crawling and swimming locomotory patterns in C. elegans. Proc. Natl. Acad. Sci. U.S.A. 105, 20982–20987.Vidal-Gadea, A., Topper, S., Young, L., and Pierce-Shimomura, J. T. (2009). Neural Mechanisms for Switching Locomotory Patterns in C. elegans. Neuroscience 366:17. Calabrese Ronald: Faculty of 1000 Biology, 11 November, 2009. Conference 2009 October 16–21. Available at: http://f1000biology.com/article/id/1182956/evaluationReceived: 16 November 2010; accepted: 22 February 2011; published online: 07 March 2011.Citation: Boyle JH, Berri S, Tassieri M, Hope IA and Cohen N (2011) Gait modulation in C. elegans: It’s not a choice, it’s a reflex! Front. Behav. Neurosci. 5:10. doi: 10.3389/fnbeh.2011.00010Copyright © 2011 Boyle, Berri, Tassieri, Hope and Cohen. This is an open-access article subject to an exclusive license agreement between the authors and Frontiers Media SA, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.ask whether this discrepancy between water and agar may be explained by the change in the physical environment. If so, then such data on its own would by no means be inconsistent with the single gait hypothesis. Indeed, Fang-Yen et al. (2010) have shown that “swimming” and “crawl-ing” differ greatly in the relative signifi-cance of internal versus environmental forces (i.e., mechanical load). Thus, the selective manifestation of these “swim- defective” mutations could simply be due to the dominance of body forces in liquid, with strong external forces masking the locomotion defect on agar. Therefore, for swim-defective mutant data to sup-port a two gait hypothesis, either (i) the importance of the physics in generating/masking the phenotype in different envi-ronments would have to be ruled out (e.g., by showing the phenotype is independent of the ratio of external to internal forces), or (ii) a neural mechanism/circuit under-lying the selective manifestation of unco-ordination would need to be identified.In conclusion, we argue that, in the absence of compelling evidence of a qualita-tive difference in the pattern of undulations or wave propagation (or in the underlying neural control circuitry), the conclusion that C. elegans can choose to switch between swimming and crawling, while interesting and possibly appealing, remains a conjec-ture. What is certain is that C. elegans is able to modulate its locomotion over an impres-sively broad range of wavelengths and fre-quencies. Understanding the mechanism behind this modulation is an exciting ques-tion that promises to shed important light on the organization and function of this and other nervous systems and their coupling to the physics of body and environment.referencesBerri, S., Boyle, J. H., Tassieri, M., Hope, I. A., and Cohen, N. (2009). Forward locomotion of the nematode C. elegans is achieved through modulation of a single gait. HFSP J. 3, 186–193.Fang-Yen, C., Wyart, M., Xie, J., Kawai, R., Kodger, T., Chen, S., Wen, Q., and Samuel, A. D. T. (2010). Biomechanical analysis of gait adaptation in the 

Gait modulation in C. elegans: It’s not a choice, it’s a reflex!

Jordan H. Boyle

Stefano Berri

Manlio Tassieri

Ian A. Hope

Netta Cohen

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Gait Modulation in C. Elegans: It's Not a Choice, It's a Reflex!

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Frontiers in Behavioral Neuroscience www.frontiersin.org March 2011 | Volume 5 | Article 10 | 1
BEHAVIORAL NEUROSCIENCE
GENERAL COMMENTARY
published: 07 March 2011
doi: 10.3389/fnbeh.2011.00010
Gait modulation in C. elegans: It’s not a choice, it’s a reflex!
Jordan H. Boyle1, Stefano Berri2, Manlio Tassieri3, Ian A. Hope4 and Netta Cohen1,5*
1 Biosystems Group, School of Computing, University of Leeds, Leeds, UK
2 Leeds Institute of Molecular Medicine, University of Leeds, Leeds, UK
3 Division of Biomedical Engineering, School of Engineering, University of Glasgow, Glasgow, UK
4 Institute of Integrative and Comparative Biology, University of Leeds, Leeds, UK
5 Institute of Membrane and Systems Biology, University of Leeds, Leeds, UK
*Correspondence: n.cohen@leeds.ac.uk
A commentary on
Shared strategies for behavioral switching: 
understanding how locomotor patterns are 
turned on and off
by Mesce, K. A., and Pierce-Shimomura, J. 
T. (2010). Front. Behav. Neurosci. 4:49. doi: 
10.3389/fnbeh.2010.00049
In their perspectives article, Mesce and 
Pierce-Shimomura (2010) make a case for 
the existence of two locomotion gaits in C. 
elegans, and for the ability of this nematode 
worm to choose between them. Here, we 
offer a counter-perspective, namely, that 
the variety of observed behaviors are more 
appropriately described as a single gait.
In what follows we focus on pure forward 
locomotion, which is generally believed to 
be controlled by a dedicated circuit, distinct 
from the circuits that control backward 
locomotion and head motor behavior. With 
regard to our question of gaits, we are not 
aware of any evidence that links head swings 
with the generation of propulsive (forward/
backward) locomotion, so these will not be 
considered here.
Are swimming And crAwling 
chArActerized by quAlitAtively 
different pAtterns of body 
bending?
In C. elegans, forward locomotion, whether 
“swimming” (in liquids) or “crawling” (in 
or on gels) involves smooth propagation 
of undulations from head to tail. We argue 
that while such propagations can vary in 
kinematic parameters such as frequency, 
wavelength, and amplitude, these variations 
are continuous and there is no evidence for 
more than a single fundamental behavior1. 
If, as Mesce and Pierce-Shimomura (2010) 
argue, “bends propagate at uniform veloc-
ity for crawling, but “whip” to the back of 
the body after characteristic pauses when 
the whole-body of the worm is bent into a 
C-shaped posture during swimming,” then 
these characteristic pauses would be evi-
dent in plots of bending angle over time: 
the longer the pauses in extreme maximally 
bent positions, the squarer the bending wave 
would appear. In fact, in Pierce-Shimomura 
et al.’s own data, bending plots over time 
show proportionately little time spent in 
the extreme positions (Pierce-Shimomura 
et al., 2008; Vidal-Gadea et al., 2009). Our 
own data for worms in liquid buffer solution 
confirm this (Figure 1C). More generally, 
Figure 1D clearly shows the equivalence of 
temporal patterns of dorso-ventral bending 
for “swimming,” “crawling,” and intermedi-
ate behaviors, upon normalization by ampli-
tude and undulation period.
Furthermore, if, as claimed, swimming 
worms “whip” their bodies and propagate 
bends at non-uniform velocity, this would 
be evidenced by non-linear stripes in the 
contour plots for swimming worms (Figure 
1B of Pierce-Shimomura et al., 2008). Our 
own data (Figures 1A,B, reproduced with 
permission from Berri et al., 2009) similarly 
show uniform bend propagation for worms 
exhibiting a range of behaviors (correspond-
ing to a range of physical conditions). 
Whether looking at the spacing between 
the stripes (the period of undulation), the 
inclination of the stripes (the speed of bend 
propagation) or the amount of overlap (the 
wavelength along the body), we find only a 
gradual change between consecutive plots. 
Finally, we note that bending along the body 
directly maps muscle activation. Calcium 
imaging of muscle activity during locomo-
tion of unrestrained worms in water and 
on agar (Pierce-Shimomura et al., 2008) 
indicates a clear one-to-one relationship 
between muscle activity and bending. This 
strong match holds in both environments 
and does not break down for fast undula-
tions (during swimming). Therefore, it is 
reasonable to expect that the same one-to-
one relationship should hold in intermedi-
ate environments (up to a fixed phase lag 
which of course differs in different condi-
tions). Another way of putting it is that body 
curvature is an equally appropriate (and eas-
ier to obtain) metric. In summary, the data 
strongly suggest that the entire transition 
from “swimming” to “crawling” corresponds 
to modulation of a single gait. Indeed, we 
find no evidence of a qualitative distinction 
between the undulation patterns.
Are swimming And crAwling 
chArActerized by different 
frequencies of undulAtion?
Mesce and Pierce-Shimomura (2010) state 
that C. elegans worms “crawl with a persist-
ent S-shaped posture on a dry substrate with 
∼1 Hz high-amplitude bends, and swim in 
liquid with ∼2 Hz lower amplitude bends.” 
Indeed, the existence of two locomotion 
frequencies might be grounds to define 
two distinct gaits. However, it is impor-
tant to point out the current consensus 
that the worm modulates its frequency of 
undulations as a function of the resistivity 
(viscosity or visco-elasticity) of the physi-
cal environment. This was demonstrated in 
Berri et al. (2009) for gelatin solutions (not 
methylcellulose as described in Mesce and 
Pierce-Shimomura, 2010). Similar results 
were independently reproduced for high 
molecular weight dextran (Fang-Yen et al., 
2010). In fact, while this is not mentioned 
in Mesce and Pierce-Shimomura (2010), 
Pierce-Shimomura et al. similarly report a 
nearly threefold modulation of the bending 
frequency (0.6–1.5 Hz) in what they dub 
“swim-like” behavior (Vidal-Gadea et al., 
2009), while frequencies of 0.2–0.4 Hz 
are dubbed “crawl-like,” despite the fact 
that the peak of the power spectrum for 
1Specifically, these three quantitative metrics capture 
the temporal and spatial properties of the body 
undulation to a good degree of accuracy (although 
additional metrics could always be added to capture 
the complex, non-sinusoidal features of the waveform).
Boyle et al. C. elegans locomotion: it’s a reflex!
Frontiers in Behavioral Neuroscience www.frontiersin.org March 2011 | Volume 5 | Article 10 | 2
are these transitions really spontaneous 
and internally selected? Here we pro-
vide an alternative interpretation, moti-
vated in part by our own, possibly related 
observations. One technical difficulty in 
working with many polymer solutions 
(e.g., agar, gelatin, methylcellulose) is 
obtaining homogeneous environments 
with different concentrations of the col-
loidal particles. Indeed, in characterizing 
a transition as a function of the environ-
ment, any observation of a change of 
behavior must be explicitly controlled 
against possible changes in the worm’s 
local, microscopic environment before 
such differences can be attributed to an 
internal decision. We therefore needed an 
objective metric to quantify the local stiff-
ness (or visco- elasticity) of our medium. 
Using image analysis, and treating the 
worm as a deformable body governed by 
Newton’s equations of motion (applied to 
low Reynolds’ numbers), we numerically 
estimated the ratio of drag coefficients for 
each short extract of recorded locomotion. 
Indeed, plotting the data against this phys-
ical metric, the smooth and continuous 
transition in Figures 1D–F of Berri et al. 
(2009) is immediately obtained. In the 
absence of such an objective characteri-
zation of the microscopic physical environ-
ment, it is impossible to have confidence 
in any statement about behavioral transi-
tions being “spontaneous” and driven by 
“decision” rather than by some possible 
response of worms to local changes in 
the physical environment. In Vidal-Gadea 
et al. (2009), we might ask whether, e.g., 
the sudden (small) change in frequency 
observed for worms in 2–3% methylcel-
lulose could be due to the worm moving 
into or out of contact with the more rigid 
agar surface underneath.
does the existence of A swim-
defective mutAnt imply multiple 
gAits?
Mesce and Pierce-Shimomura argue 
that the identification of “swim-defec-
tive” mutants supports the existence of 
a distinct swimming gait, but we note 
that the three examples given by Pierce-
Shimomura et al. (2008) exhibit some 
locomotion defect on agar as well. That 
aside, and even in the extreme case of a 
mutant with a clear phenotype in liq-
uid and none on agar, it is important to 
which “crawling” and “ swimming” (if they 
are indeed distinct behaviors) are char-
acterized by quite similar frequencies. 
Specifically the transitions are quantified 
by a difference of 0.2 Hz or less in the undu-
lation frequency. This frequency difference 
is comparable in value to the variability in 
frequency (1.2–1.5 Hz) for locomotion in 
0.5% methylcellulose (Vidal-Gadea et al., 
2009), all of which is dubbed swimming. 
The small magnitude of the transitions may 
raise questions, not only about the valid-
ity of the classification, but even about the 
selective advantage worms might gain by 
such “decisions.”
That said, it is clear from the bending 
plots in Vidal-Gadea et al. (2009) that 
some small frequency transitions were 
observed by Pierce-Shimomura et al. But 
“crawling” appears to fall at about 0.8 Hz 
(Vidal-Gadea et al., 2009). It is therefore 
clear that C. elegans locomotion cannot be 
characterized by discrete sets of kinematic 
parameters, but rather by a broad and con-
tinuous range of such parameters.
cAn worms switch 
spontAneously between the 
discrete gAits of swimming And 
crAwling?
Transitions between two undulation 
frequencies in a single environment, if 
spontaneous, could support the existence 
of two gaits. However, we note that any 
observed transitions (in the wild type) 
were only reported for certain high con-
centrations (2.25 and 2.75%) of methyl-
cellulose  (Vidal-Gadea et al., 2009), for 
Figure 1 | (A) Frequency–wavelength relation across a range of gelatin concentrations (filled circles) and 
agar surfaces (black triangles). Colors represent gelatin concentrations (%) as indicated. The best linear fit 
to the data is superimposed. Adapted from Figure 1B in Berri et al. (2009). Large black circles indicate 
which contour plots are shown in (B). (B) Seven contour plots of bending angle (represented by color, with 
dark red corresponding to extreme dorsal bending and dark blue to extreme ventral bending) over time 
(horizontal) and along the body (vertical), selected to show the range of observed forward locomotion 
behaviors, from “swimming” in liquid buffer solution (top) to “crawling” in relatively stiff gelatin (bottom; 
see methods in Berri et al., 2009 for additional details). Note the linear propagation along the entire body 
without changes in wave speed. (C) Trace of bending angle versus time for a point near the head of a worm 
in buffer solution [same data as top plot in (B)]. Note that the worm does not dwell in the maximally bent 
positions (peaks and troughs of the curve). (D) Bending angle traces as in (C), taken from the 1st, 3rd, 5th, 
and 7th panels of (B; see color-coded arrow heads) and normalized by undulation period and amplitude. 
Note the similarity of the waveforms.
Boyle et al. C. elegans locomotion: it’s a reflex!
Frontiers in Behavioral Neuroscience www.frontiersin.org March 2011 | Volume 5 | Article 10 | 3
nematode Caenorhabditis elegans. Proc. Natl. Acad. 
Sci. U.S.A. 107, 20323–20328.
Mesce, K. A., and Pierce-Shimomura, J. T. (2010). Shared 
strategies for behavioral switching: understanding 
how locomotor patterns are turned on and off. Front. 
Behav. Neurosci. 4:49. doi: 10.3389/fnbeh.2010.00049
Pierce-Shimomura, J. T., Chen, B. L., Mun, J. J., Ho, 
R., Sarkis, R., and McIntire, S. L. (2008). Genetic 
analysis of crawling and swimming locomotory 
patterns in C. elegans. Proc. Natl. Acad. Sci. U.S.A. 
105, 20982–20987.
Vidal-Gadea, A., Topper, S., Young, L., and Pierce-
Shimomura, J. T. (2009). Neural Mechanisms 
for Switching Locomotory Patterns in C. elegans. 
Neuroscience 366:17. Calabrese Ronald: Faculty of 
1000 Biology, 11 November, 2009. Conference 2009 
October 16–21. Available at: http://f1000biology.com/
article/id/1182956/evaluation
Received: 16 November 2010; accepted: 22 February 2011; 
published online: 07 March 2011.
Citation: Boyle JH, Berri S, Tassieri M, Hope IA and Cohen 
N (2011) Gait modulation in C. elegans: It’s not a choice, 
it’s a reflex! Front. Behav. Neurosci. 5:10. doi: 10.3389/
fnbeh.2011.00010
Copyright © 2011 Boyle, Berri, Tassieri, Hope and Cohen. 
This is an open-access article subject to an exclusive license 
agreement between the authors and Frontiers Media SA, which 
permits unrestricted use, distribution, and reproduction in any 
medium, provided the original authors and source are credited.
ask whether this discrepancy between 
water and agar may be explained by the 
change in the physical environment. If so, 
then such data on its own would by no 
means be inconsistent with the single gait 
hypothesis. Indeed, Fang-Yen et al. (2010) 
have shown that “swimming” and “crawl-
ing” differ greatly in the relative signifi-
cance of internal versus environmental 
forces (i.e., mechanical load). Thus, the 
selective manifestation of these “swim- 
defective” mutations could simply be due 
to the dominance of body forces in liquid, 
with strong external forces masking the 
locomotion defect on agar. Therefore, 
for swim-defective mutant data to sup-
port a two gait hypothesis, either (i) the 
importance of the physics in generating/
masking the phenotype in different envi-
ronments would have to be ruled out (e.g., 
by showing the phenotype is independent 
of the ratio of external to internal forces), 
or (ii) a neural mechanism/circuit under-
lying the selective manifestation of unco-
ordination would need to be identified.
In conclusion, we argue that, in the 
absence of compelling evidence of a qualita-
tive difference in the pattern of undulations 
or wave propagation (or in the underlying 
neural control circuitry), the conclusion 
that C. elegans can choose to switch between 
swimming and crawling, while interesting 
and possibly appealing, remains a conjec-
ture. What is certain is that C. elegans is able 
to modulate its locomotion over an impres-
sively broad range of wavelengths and fre-
quencies. Understanding the mechanism 
behind this modulation is an exciting ques-
tion that promises to shed important light 
on the organization and function of this and 
other nervous systems and their coupling to 
the physics of body and environment.
references
Berri, S., Boyle, J. H., Tassieri, M., Hope, I. A., and Cohen, 
N. (2009). Forward locomotion of the nematode C. 
elegans is achieved through modulation of a single 
gait. HFSP J. 3, 186–193.
Fang-Yen, C., Wyart, M., Xie, J., Kawai, R., Kodger, 
T., Chen, S., Wen, Q., and Samuel, A. D. T. (2010). 
Biomechanical analysis of gait adaptation in the 


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Enlighten – Research publications by members of the University of Glasgow http://eprints.gla.ac.uk        Boyle, J.H., Berri, S., Tassieri, M., Hope, I.A., and Cohen, N. (2011) Gait modulation in C. Elegans: it's not a choice, it's a reflex! Frontiers in Behavioral Neuroscience, 5. p. 10. ISSN 1662-5153  http://eprints.gla.ac.uk/66326/  Deposited on: 25 June 2012   Frontiers in Behavioral Neuroscience www.frontiersin.org March 2011 | Volume 5 | Article 10 | 1BEHAVIORAL NEUROSCIENCEGENERAL COMMENTARYpublished: 07 March 2011doi: 10.3389/fnbeh.2011.00010Gait modulation in C. elegans: It’s not a choice, it’s a reflex!Jordan H. Boyle1, Stefano Berri2, Manlio Tassieri3, Ian A. Hope4 and Netta Cohen1,5*1 Biosystems Group, School of Computing, University of Leeds, Leeds, UK2 Leeds Institute of Molecular Medicine, University of Leeds, Leeds, UK3 Division of Biomedical Engineering, School of Engineering, University of Glasgow, Glasgow, UK4 Institute of Integrative and Comparative Biology, University of Leeds, Leeds, UK5 Institute of Membrane and Systems Biology, University of Leeds, Leeds, UK*Correspondence: n.cohen@leeds.ac.ukA commentary onShared strategies for behavioral switching: understanding how locomotor patterns are turned on and offby Mesce, K. A., and Pierce-Shimomura, J. T. (2010). Front. Behav. Neurosci. 4:49. doi: 10.3389/fnbeh.2010.00049In their perspectives article, Mesce and Pierce-Shimomura (2010) make a case for the existence of two locomotion gaits in C. elegans, and for the ability of this nematode worm to choose between them. Here, we offer a counter-perspective, namely, that the variety of observed behaviors are more appropriately described as a single gait.In what follows we focus on pure forward locomotion, which is generally believed to be controlled by a dedicated circuit, distinct from the circuits that control backward locomotion and head motor behavior. With regard to our question of gaits, we are not aware of any evidence that links head swings with the generation of propulsive (forward/backward) locomotion, so these will not be considered here.Are swimming And crAwling chArActerized by quAlitAtively different pAtterns of body bending?In C. elegans, forward locomotion, whether “swimming” (in liquids) or “crawling” (in or on gels) involves smooth propagation of undulations from head to tail. We argue that while such propagations can vary in kinematic parameters such as frequency, wavelength, and amplitude, these variations are continuous and there is no evidence for more than a single fundamental behavior1. If, as Mesce and Pierce-Shimomura (2010) argue, “bends propagate at uniform veloc-ity for crawling, but “whip” to the back of the body after characteristic pauses when the whole-body of the worm is bent into a C-shaped posture during swimming,” then these characteristic pauses would be evi-dent in plots of bending angle over time: the longer the pauses in extreme maximally bent positions, the squarer the bending wave would appear. In fact, in Pierce-Shimomura et al.’s own data, bending plots over time show proportionately little time spent in the extreme positions (Pierce-Shimomura et al., 2008; Vidal-Gadea et al., 2009). Our own data for worms in liquid buffer solution confirm this (Figure 1C). More generally, Figure 1D clearly shows the equivalence of temporal patterns of dorso-ventral bending for “swimming,” “crawling,” and intermedi-ate behaviors, upon normalization by ampli-tude and undulation period.Furthermore, if, as claimed, swimming worms “whip” their bodies and propagate bends at non-uniform velocity, this would be evidenced by non-linear stripes in the contour plots for swimming worms (Figure 1B of Pierce-Shimomura et al., 2008). Our own data (Figures 1A,B, reproduced with permission from Berri et al., 2009) similarly show uniform bend propagation for worms exhibiting a range of behaviors (correspond-ing to a range of physical conditions). Whether looking at the spacing between the stripes (the period of undulation), the inclination of the stripes (the speed of bend propagation) or the amount of overlap (the wavelength along the body), we find only a gradual change between consecutive plots. Finally, we note that bending along the body directly maps muscle activation. Calcium imaging of muscle activity during locomo-tion of unrestrained worms in water and on agar (Pierce-Shimomura et al., 2008) indicates a clear one-to-one relationship between muscle activity and bending. This strong match holds in both environments and does not break down for fast undula-tions (during swimming). Therefore, it is reasonable to expect that the same one-to-one relationship should hold in intermedi-ate environments (up to a fixed phase lag which of course differs in different condi-tions). Another way of putting it is that body curvature is an equally appropriate (and eas-ier to obtain) metric. In summary, the data strongly suggest that the entire transition from “swimming” to “crawling” corresponds to modulation of a single gait. Indeed, we find no evidence of a qualitative distinction between the undulation patterns.Are swimming And crAwling chArActerized by different frequencies of undulAtion?Mesce and Pierce-Shimomura (2010) state that C. elegans worms “crawl with a persist-ent S-shaped posture on a dry substrate with ∼1 Hz high-amplitude bends, and swim in liquid with ∼2 Hz lower amplitude bends.” Indeed, the existence of two locomotion frequencies might be grounds to define two distinct gaits. However, it is impor-tant to point out the current consensus that the worm modulates its frequency of undulations as a function of the resistivity (viscosity or visco-elasticity) of the physi-cal environment. This was demonstrated in Berri et al. (2009) for gelatin solutions (not methylcellulose as described in Mesce and Pierce-Shimomura, 2010). Similar results were independently reproduced for high molecular weight dextran (Fang-Yen et al., 2010). In fact, while this is not mentioned in Mesce and Pierce-Shimomura (2010), Pierce-Shimomura et al. similarly report a nearly threefold modulation of the bending frequency (0.6–1.5 Hz) in what they dub “swim-like” behavior (Vidal-Gadea et al., 2009), while frequencies of 0.2–0.4 Hz are dubbed “crawl-like,” despite the fact that the peak of the power spectrum for 1Specifically, these three quantitative metrics capture the temporal and spatial properties of the body undulation to a good degree of accuracy (although additional metrics could always be added to capture the complex, non-sinusoidal features of the waveform).Boyle et al. C. elegans locomotion: it’s a reflex!Frontiers in Behavioral Neuroscience www.frontiersin.org March 2011 | Volume 5 | Article 10 | 2are these transitions really spontaneous and internally selected? Here we pro-vide an alternative interpretation, moti-vated in part by our own, possibly related observations. One technical difficulty in working with many polymer solutions (e.g., agar, gelatin, methylcellulose) is obtaining homogeneous environments with different concentrations of the col-loidal particles. Indeed, in characterizing a transition as a function of the environ-ment, any observation of a change of behavior must be explicitly controlled against possible changes in the worm’s local, microscopic environment before such differences can be attributed to an internal decision. We therefore needed an objective metric to quantify the local stiff-ness (or visco- elasticity) of our medium. Using image analysis, and treating the worm as a deformable body governed by Newton’s equations of motion (applied to low Reynolds’ numbers), we numerically estimated the ratio of drag coefficients for each short extract of recorded locomotion. Indeed, plotting the data against this phys-ical metric, the smooth and continuous transition in Figures 1D–F of Berri et al. (2009) is immediately obtained. In the absence of such an objective characteri-zation of the microscopic physical environ-ment, it is impossible to have confidence in any statement about behavioral transi-tions being “spontaneous” and driven by “decision” rather than by some possible response of worms to local changes in the physical environment. In Vidal-Gadea et al. (2009), we might ask whether, e.g., the sudden (small) change in frequency observed for worms in 2–3% methylcel-lulose could be due to the worm moving into or out of contact with the more rigid agar surface underneath.does the existence of A swim-defective mutAnt imply multiple gAits?Mesce and Pierce-Shimomura argue that the identification of “swim-defec-tive” mutants supports the existence of a distinct swimming gait, but we note that the three examples given by Pierce-Shimomura et al. (2008) exhibit some locomotion defect on agar as well. That aside, and even in the extreme case of a mutant with a clear phenotype in liq-uid and none on agar, it is important to which “crawling” and “ swimming” (if they are indeed distinct behaviors) are char-acterized by quite similar frequencies. Specifically the transitions are quantified by a difference of 0.2 Hz or less in the undu-lation frequency. This frequency difference is comparable in value to the variability in frequency (1.2–1.5 Hz) for locomotion in 0.5% methylcellulose (Vidal-Gadea et al., 2009), all of which is dubbed swimming. The small magnitude of the transitions may raise questions, not only about the valid-ity of the classification, but even about the selective advantage worms might gain by such “decisions.”That said, it is clear from the bending plots in Vidal-Gadea et al. (2009) that some small frequency transitions were observed by Pierce-Shimomura et al. But “crawling” appears to fall at about 0.8 Hz (Vidal-Gadea et al., 2009). It is therefore clear that C. elegans locomotion cannot be characterized by discrete sets of kinematic parameters, but rather by a broad and con-tinuous range of such parameters.cAn worms switch spontAneously between the discrete gAits of swimming And crAwling?Transitions between two undulation frequencies in a single environment, if spontaneous, could support the existence of two gaits. However, we note that any observed transitions (in the wild type) were only reported for certain high con-centrations (2.25 and 2.75%) of methyl-cellulose  (Vidal-Gadea et al., 2009), for Figure 1 | (A) Frequency–wavelength relation across a range of gelatin concentrations (filled circles) and agar surfaces (black triangles). Colors represent gelatin concentrations (%) as indicated. The best linear fit to the data is superimposed. Adapted from Figure 1B in Berri et al. (2009). Large black circles indicate which contour plots are shown in (B). (B) Seven contour plots of bending angle (represented by color, with dark red corresponding to extreme dorsal bending and dark blue to extreme ventral bending) over time (horizontal) and along the body (vertical), selected to show the range of observed forward locomotion behaviors, from “swimming” in liquid buffer solution (top) to “crawling” in relatively stiff gelatin (bottom; see methods in Berri et al., 2009 for additional details). Note the linear propagation along the entire body without changes in wave speed. (C) Trace of bending angle versus time for a point near the head of a worm in buffer solution [same data as top plot in (B)]. Note that the worm does not dwell in the maximally bent positions (peaks and troughs of the curve). (D) Bending angle traces as in (C), taken from the 1st, 3rd, 5th, and 7th panels of (B; see color-coded arrow heads) and normalized by undulation period and amplitude. Note the similarity of the waveforms.Boyle et al. C. elegans locomotion: it’s a reflex!Frontiers in Behavioral Neuroscience www.frontiersin.org March 2011 | Volume 5 | Article 10 | 3nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 107, 20323–20328.Mesce, K. A., and Pierce-Shimomura, J. T. (2010). Shared strategies for behavioral switching: understanding how locomotor patterns are turned on and off. Front. Behav. Neurosci. 4:49. doi: 10.3389/fnbeh.2010.00049Pierce-Shimomura, J. T., Chen, B. L., Mun, J. J., Ho, R., Sarkis, R., and McIntire, S. L. (2008). Genetic analysis of crawling and swimming locomotory patterns in C. elegans. Proc. Natl. Acad. Sci. U.S.A. 105, 20982–20987.Vidal-Gadea, A., Topper, S., Young, L., and Pierce-Shimomura, J. T. (2009). Neural Mechanisms for Switching Locomotory Patterns in C. elegans. Neuroscience 366:17. Calabrese Ronald: Faculty of 1000 Biology, 11 November, 2009. Conference 2009 October 16–21. Available at: http://f1000biology.com/article/id/1182956/evaluationReceived: 16 November 2010; accepted: 22 February 2011; published online: 07 March 2011.Citation: Boyle JH, Berri S, Tassieri M, Hope IA and Cohen N (2011) Gait modulation in C. elegans: It’s not a choice, it’s a reflex! Front. Behav. Neurosci. 5:10. doi: 10.3389/fnbeh.2011.00010Copyright © 2011 Boyle, Berri, Tassieri, Hope and Cohen. This is an open-access article subject to an exclusive license agreement between the authors and Frontiers Media SA, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.ask whether this discrepancy between water and agar may be explained by the change in the physical environment. If so, then such data on its own would by no means be inconsistent with the single gait hypothesis. Indeed, Fang-Yen et al. (2010) have shown that “swimming” and “crawl-ing” differ greatly in the relative signifi-cance of internal versus environmental forces (i.e., mechanical load). Thus, the selective manifestation of these “swim- defective” mutations could simply be due to the dominance of body forces in liquid, with strong external forces masking the locomotion defect on agar. Therefore, for swim-defective mutant data to sup-port a two gait hypothesis, either (i) the importance of the physics in generating/masking the phenotype in different envi-ronments would have to be ruled out (e.g., by showing the phenotype is independent of the ratio of external to internal forces), or (ii) a neural mechanism/circuit under-lying the selective manifestation of unco-ordination would need to be identified.In conclusion, we argue that, in the absence of compelling evidence of a qualita-tive difference in the pattern of undulations or wave propagation (or in the underlying neural control circuitry), the conclusion that C. elegans can choose to switch between swimming and crawling, while interesting and possibly appealing, remains a conjec-ture. What is certain is that C. elegans is able to modulate its locomotion over an impres-sively broad range of wavelengths and fre-quencies. Understanding the mechanism behind this modulation is an exciting ques-tion that promises to shed important light on the organization and function of this and other nervous systems and their coupling to the physics of body and environment.referencesBerri, S., Boyle, J. H., Tassieri, M., Hope, I. A., and Cohen, N. (2009). Forward locomotion of the nematode C. elegans is achieved through modulation of a single gait. HFSP J. 3, 186–193.Fang-Yen, C., Wyart, M., Xie, J., Kawai, R., Kodger, T., Chen, S., Wen, Q., and Samuel, A. D. T. (2010). Biomechanical analysis of gait adaptation in the 

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Gait modulation in <i>C. Elegans</i>: it's not a choice, it's a reflex!

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