for example , while reading this article you might shift your attention to a knock on your office door or glance at your clock in anticipation of an important appointment .
in fact , behavioral switches are an adaptive feature across a broad range of animal species and can maximize an organism 's viability and differential reproductive success .
ultimately , switching between behaviors helps an animal to cope with its changing environment or internal states , and appropriate responses to these stimuli can be critical for survival .
although behavioral switching and choice are inextricably linked , defining what constitutes behavioral choice and understanding how decisions are made remain topics of intense discussion and research ( kristan and shaw , 1997 ; krding , 2007 ; kristan , 2008 ; kiani and shadlen , 2009 ) . in this
 perspectives  article we highlight some of the elegant and conserved neural strategies that have been found to contribute to the selection of one form of locomotor behavior vs. another .
these biologically crafted strategies exemplify ways in which the environment and internal state of an animal can generate behavioral switching .
we will also argue that these mechanisms are found consistently across animal groups separated by millions of years of evolution .
our aim is to describe a collection of neurobiological control mechanisms that switch locomotor behaviors on or off .
we will emphasize the importance of context for appropriate behavioral switching and will provide examples of sensorimotor strategies that are similar across taxa .
individual animals can change their form of locomotion or gait quickly . for instance , an animal may switch from walking to running or switch from crawling to swimming depending on the environmental conditions present . what external and internal events shape the switching from one form of locomotion to another ?
these generally include : ( 1 ) behavioral states related to searching for food or a mate ; escaping from predators ; interacting during agonistic encounters , and ( 2 ) environmental sub - niches , such as rough vs. smooth terrain ; water vs. land or air . during the course of a species evolutionary route , rapid behavioral switching
may have evolved to prevent inefficient movements during escape behaviors and/or in conjunction with changes in terrain .
once a neural mechanism evolved to switch the locomotor form , this trait potentially would be favored due to its efficiency in escape - related survival or the maximization of resource acquisition within differing niches .
although it may be potentially adaptive for an animal to use a variety of forms or gaits under different circumstances , it might be maladaptive to get  stuck  when switching between forms / gaits if the transition were inefficient .
therefore , we propose that during the evolution of a given transition , there must be selective pressure to favor effective behavioral switching to ensure that competing motor patterns are switched on and off in a precise manner . throughout the remainder of this article
, we will focus on two distantly related organisms and the common biological mechanisms they use to switch efficiently between different forms of locomotion .
the medicinal leech , hirudo species , is a well - studied annelid model of neural circuits underlying locomotion and other behaviors ( reviewed in kristan et al . , 2005 ) .
successful electrophysiological analysis of neural circuits involved in quantifiable behaviors has been driven largely by the leech 's simple body plan and size ( 10  cm ) , which allows convenient dissection of its uniquely identifiable neurons .
the considerably smaller nematode worm ( 1  mm ) , caenorhabditis elegans , is an established genetic model of behavior ( de bono and maricq , 2005 ) and has afforded scientists the ability to manipulate neural circuits via genetic tools still unavailable for the leech .
modern molecular phylogenies ( dunn et al . , 2008 ) show that these two species are members of two widely divergent clades of bilaterally symmetric animals .
in fact , they are almost as distant from one another as either is from vertebrates . despite their physiological and morphological differences ( e.g. , the leech is segmented and contains over 10,000 neurons as compared to the 302 neurons in c. elegans ) , a surprising number of shared control strategies for locomotion is now emerging .
the leech has two basic forms of locomotion , swimming and crawling , and each is easily distinguished from the other .
swimming consists of a rostrocaudal sinusoidal wave of body movements involving antiphasic contractions of dorsal and ventral muscles .
crawling entails the co - contractions of dorsal and ventral muscles , which enable the whole - body to elongate and contract .
swimming has a relatively short period between repeated cycles ( 0.31  s ) , whereas crawling has a much longer one ( 720  s ) ( kristan et al . , 2005 ; puhl and mesce , 2008 ) .
understanding the neural bases for these behaviors has benefited from two powerful preparations : the  nearly - intact preparation  , in which overt locomotion can be monitored while the activity of identified neurons is recorded in selected ganglia , and the  isolated nerve cord preparation 
wherein fictive crawling and swimming behaviors are measured based on established patterns of neuronal output ( kristan et al . , 2005 ) .
in both preparations , the leech 's relatively large neurons ( 25100 m diameter ) can be recorded simultaneously over extended periods ( > 3  h ) with electrophysiological methods .
voltage - sensitive dyes have permitted the optical recording of hundreds of identified neurons simultaneously and are providing new insights into the cellular mechanisms of decision - making and multi - functional circuits ( briggman and kristan , 2006 , 2008 ) .
the nearly intact preparation is particularly useful because the goal of matching locomotor kinematics with the activity of identified neurons can be met . in nearly intact leech preparations individual cephalic neurons were identified that either activated locomotion or were rhythmically active during locomotion ( esch et al . , 2002 ; mesce et al . ,
electrical excitation of a single neuron , named r3b-1 ( bilaterally paired ) , was sufficient to elicit sustained locomotor activity ( esch et al .
the form of locomotion induced , however , was entirely dependent on whether the body of the leech was suspended in fluid or allowed to lie upon a dryer surface ( esch et al . , 2002 ) .
thus depolarization of a single r3b-1 neuron resulted in a context - dependent response that was gated by sensory input from either an aquatic or terrestrial environment .
additional studies of overt crawling and swimming confirmed that leeches will quickly switch to a crawling mode when encountering shallow water ( esch et al .
furthermore , when fluid levels were ambiguous , a swim - crawl hybrid locomotor pattern emerged in both fully- and nearly intact animals ( esch et al . , 2002 ) .
thus the decision to locomote is hierarchical , made at the level of a single higher - order descending interneuron , but the switching ( and selection in this case ) of various forms of locomotion is based on the integration of contextual somatosensory cues . if descending signals from the cephalic ganglion are removed reversibly , the leech looses its ability to initiate crawling even in the presence of relevant sensory stimulation ( puhl and mesce , 2010 ) . thus the decision to crawl is entirely dependent on cephalic descending input .
for example , tactile body stimulation can reliably induce swimming when the cephalic ganglion is removed reversibly ( puhl and mesce , 2010 ) . although the cephalic ganglion contains a variety of neurons that can gate or trigger swimming ( brodfuehrer and friesen , 1986 ) , downstream swim - gating neurons are also competent to activate the swim oscillators ( kristan et al .
last , the biomechanics of an animal clearly must constrain which locomotor behaviors are available for selection or the time of transition between forms ; for example , such constraints may help to explain why leech swimming and crawling are always initiated with an elongation of the body and the excitation of similar ( circular ) muscles ( esch et al .
the results above provide a striking example of how sensory information from the environment is fundamentally important for behavioral switching , but what about the internal state of the animal ? are there conditions under which the leech will be strongly biased to crawl or swim because of its internal state ?
recent studies indicate that specific biogenic amines significantly bias the mode of locomotion available to an animal .
for example , dopamine has been shown to turn on the underlying neural circuits generating leech crawling behavior ( puhl and mesce , 2008 , 2010 ) .
in addition , dopamine prevents swimming from becoming activated ( crisp and mesce , 2004 ) . in preparations in which fictive locomotion was recorded , dopamine blocked swimming even when the cns was electrically stimulated in attempts to produce swimming ( crisp and mesce , 2004 ) . in the presence of dopamine , stimulation of cell r3b-1 was found to induce crawling but never swimming , regardless of the swim - specific contextual cues present ( puhl and mesce , personal observations ) .
thus dopamine not only activates crawling , it prevents swimming as well , providing a clear example of a chemical switch for locomotor behavior .
although it is unknown how the levels of dopamine fluctuate normally within the leech , we can speculate that they might significantly rise when the leech comes in contact with its host .
typically , the leech switches to crawling at this time and some evidence suggests that dopamine is linked to feeding ( biting ) behavior ( o'gara et al . , 1991 ) . because swimming often requires detachment of both its front and rear suckers , it makes sense that this form of locomotion needs to be suppressed to prevent loss of contact with the host .
the answer to this question has been long known , and solid evidence indicates that serotonin is the key modulator for activating swimming ( willard , 1981 ; friesen and kristan , 2007 ) . during active feeding behavior ,
however , serotonin was elegantly shown to serve as a direct and powerful inhibitor of the sensory gating for swimming , crawling , and other body movements ( gaudry and kristan , 2009 ) .
it is noteworthy that the central activation of swimming was not inhibited . because serotonin is known to activate the central swim oscillators
paradoxically , focal delivery of serotonin to the cephalic ganglion , but not the nerve cord , was found to suppress swimming by influencing the decision to swim ( crisp and mesce , 2003 ) .
bath application of serotonin was deemed a physiologically appropriate delivery protocol because it matched the anatomically based paracrine - like release of serotonin within the cns ( crisp and mesce , 2003 ) .
furthermore , preliminary data support the idea that dopamine trumps serotonin : a mixture of serotonin and dopamine results in no swimming ( puhl and mesce , personal observation ) .
thus as long as dopamine is present at high enough concentrations during feeding , serotonin 's actions on the swim central pattern generator are observably blocked .
perhaps , when the levels of dopamine drop after a feeding session and serotonin levels are low enough to prevent sensory neuron pre - synaptic inhibition ( gaudry and kristan , 2009 ) , the leech is once again able to switch on its swimming behavior .
what parallels exist for the regulation of locomotion in c. elegans ? in the leech , the dorsal 
ventral undulations used in swimming are unambiguously distinct from the whole - body elongations and contractions made during vermiform crawling ( kristan et al . ,
only recently have several labs considered whether c. elegans also exhibits distinct crawling and swimming forms of motion ( korta et al .
, 2007 ; pierce - shimomura et al . , 2008 ; berri et al . , 2009 ) .
similar to swimming in the leech , both forms of motion in c. elegans appear to depend on thrust generated by bends passed along the body .
kinematic analysis revealed that animals crawl with a persistent s - shaped posture on a dry substrate with 1 hz high - amplitude bends , and swim in liquid with 2  hz lower amplitude bends ( pierce - shimomura et al . ,
the two forms of motion also differ in the pattern of bend propagation : bends propagate at uniform velocity 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 ( pierce - shimomura et al . , 2008 ) .
in c. elegans and the leech , crawling and swimming are further distinguished by the selective overlay of searching - related motor patterns while crawling .
ventral crawl bends , c. elegans wiggles its  nose  at 10  hz in all three dimensions . this behavior has been termed  foraging  because the worm seems to use it as a way to search for food or the detection of substrate properties .
an analogous behavior , although considerably slower , is displayed during crawling in the leech ( gray et al .
these exploratory - type behaviors are turned off during swimming in both the leech ( kristan et al . , 2005 ) and worm ( pierce - shimomura et al . , 2009 ; vidal - gadea et al . , 2009 ) .
the genetic tractability of c. elegans has allowed crawling and swimming to be distinguished with transgenic tools and mutation . by imaging calcium transients in muscles of freely moving animals , with the genetically encodable calcium - indicator chameleon , the two forms of motion were shown to be subserved by distinct patterns of muscle activity ( pierce - shimomura et al . , 2008 ) . in the future , newer imaging techniques may enable the activity patterns of identified neurons to be revealed in freely moving animals ( faumont et al .
crawl and swim are also distinguished genetically in the worm because some mutations have a more severe effect on swimming than crawling ( miller et al . , 1996 ; pierce - shimomura et al . , 2008 )
the specific effects rendered by mutation may be thought of as being analogous to how a pharmacological agent may preferentially affect one form of locomotion over another form in other animals .
although c. elegans crawls and swims with distinct kinematics , it remains controversial whether crawling and swimming represent distinct gait - like forms of motion or simply altered versions of a single form ( korta et al . , 2007 ; pierce - shimomura et al .
this issue is usually addressed in animals with limbs by studying how kinematics vary as an animal moves at different speeds on a treadmill .
gaits are indicated if the animal shows a discontinuous transition in kinematics with a continuous increase in speed just as humans show a sudden switch from walking to running at 4  m / s ( alexander , 1989 ) . in place of a treadmill , c. elegans researchers control speed by immersing the worm in different concentrations of viscous methylcellulose ( korta et al .
two studies have found that bend frequency decreases gradually with increased viscosity ( korta et al .
( 2007 ) reported that that the worm unexpectedly and inexplicably maintained the same swim - like wavelength ( c - shaped waveform ) in both low and high viscosities , but this result has not been reproduced ( fang - yen and samuel , personal communication ) .
a second study instead found that wavelength decreases gradually with increased viscosity ( berri et al . , 2009 ) .
these studies suggest that crawling and swimming may represent a single form of motion in c. elegans .
however , recent unpublished findings show that the worm spontaneously alternates between bouts of crawling and swimming in intermediate viscosity solutions ( pierce - shimomura et al . , 2009 ; vidal - gadea et al . , 2009 ) .
mutations that specifically perturb the development and function of all sensory cilia cause a peculiar defect in swimming  these mutants switch spontaneously between crawl and swim forms of motion in liquid ( pierce - shimomura et al . , 2008 ) .
together , these data suggest that the switch between crawling and swimming reflects a  decision  made by the worm based on sensory input just as it does in the leech . while the neural basis for crawling and swimming has been studied for decades in the leech , how c. elegans switches between crawl and swim is just beginning to be investigated . taking a hint from the leech , the pierce - shimomura lab is investigating whether dopamine plays a role in locomotor switching .
preliminary results suggest that dopamine is necessary and sufficient to facilitate a gait - like switch from swim to crawl in c. elegans ( pierce - shimomura et al . , 2009 ; vidal - gadea et al . ,
interestingly , dopamine does not appear to be necessary to maintain the gross kinematics for either form of motion .
knock - out of the dopamine transporter gene , however , results in a gradual paralysis during swimming that depends on endogenous dopamine synthesis and a d2-type dopamine receptor ( mcdonald et al . , 2007 ) . based on these results ,
this swim - induced paralysis might be explained by dopamine levels rising above a concentration that permits swimming . c. elegans has eight dopamine neurons that appear to act as mechanoreceptors sensitive to substrate texture ( sulston et al .
1975 ; sawin et al . , 2000 ) . with potential parallels to the leech , dopamine neurons in c. elegans
may become activated upon firm contact of the body with the substrate to trigger a switch from swimming to crawling .
how does c. elegans switch from crawl to swim ? while serotonin has a known role in slowing the crawling speed of starved animals after finding food ( sawin et al . , 2000 ) , the pierce - shimomura lab has only begun to study whether serotonin has a role in swimming ( vidal - gadea and pierce - shimomura , unpublished observations ) .
an unbiased genetic screen for mutations that disrupt the crawl to swim transition revealed a key role for the newly described sodium - leak channel pathway ( pierce - shimomura et al . , 2008 ) .
these mutants are capable of crawling , but become frozen in posture within a fraction of a second upon entering liquid .
the sodium - leak channels are widely expressed in the nervous system , so it remains unclear whether they facilitate the crawl to swim switch through neuromodulatory signaling , independent mechanisms , or both ( pierce - shimomura et al . , 2008 ) .
( 2009 ) has determined that the mammalian sodium - leak channel is the major molecular target of substance p which is a potent activator of locomotion in lamprey and mouse ( smith et al . , 1988 ; svensson et al . , 2001 ) .
neuromodulatory switches are also used to switch off specific locomotory subcircuits in c. elegans . in an agar - filled petri dish
, the worm spends most of its time crawling forward , but will occasionally crawl backward either spontaneously or as an escape .
the foraging behavior described previously occurs during forward locomotion but is switched off during backward locomotion ( alkema et al . , 2005 ) .
a recent genetic screen for mutants that forage while moving backward revealed a critical role for the neurotransmitter tyramine . through an elegant combination of laser ablation of identified neurons and muscles , quantitative behavioral analysis , and electrophysiology
 rmd  and  smd  motorneurons and neck muscles involved in foraging through a novel tyramine - gated chloride channel ( alkema et al . , 2005 ; pirri et al .
additional members of this novel class of chloride channels were found to be gated by serotonin , dopamine , acetylcholine , and choline ( ringstad et al .
these channels might serve as neuromodulatory switches to turn off specific motor programs in c. elegans .
throughout the remainder of this article , we will focus on two distantly related organisms and the common biological mechanisms they use to switch efficiently between different forms of locomotion .
the medicinal leech , hirudo species , is a well - studied annelid model of neural circuits underlying locomotion and other behaviors ( reviewed in kristan et al . , 2005 ) .
successful electrophysiological analysis of neural circuits involved in quantifiable behaviors has been driven largely by the leech 's simple body plan and size ( 10  cm ) , which allows convenient dissection of its uniquely identifiable neurons .
the considerably smaller nematode worm ( 1  mm ) , caenorhabditis elegans , is an established genetic model of behavior ( de bono and maricq , 2005 ) and has afforded scientists the ability to manipulate neural circuits via genetic tools still unavailable for the leech .
modern molecular phylogenies ( dunn et al . , 2008 ) show that these two species are members of two widely divergent clades of bilaterally symmetric animals .
in fact , they are almost as distant from one another as either is from vertebrates . despite their physiological and morphological differences ( e.g. ,
the leech is segmented and contains over 10,000 neurons as compared to the 302 neurons in c. elegans ) , a surprising number of shared control strategies for locomotion is now emerging .
the leech has two basic forms of locomotion , swimming and crawling , and each is easily distinguished from the other .
swimming consists of a rostrocaudal sinusoidal wave of body movements involving antiphasic contractions of dorsal and ventral muscles .
crawling entails the co - contractions of dorsal and ventral muscles , which enable the whole - body to elongate and contract .
swimming has a relatively short period between repeated cycles ( 0.31  s ) , whereas crawling has a much longer one ( 720  s ) ( kristan et al .
, 2005 ; puhl and mesce , 2008 ) . understanding the neural bases for these behaviors has benefited from two powerful preparations : the  nearly - intact preparation  , in which overt locomotion can be monitored while the activity of identified neurons is recorded in selected ganglia , and the  isolated nerve cord preparation 
wherein fictive crawling and swimming behaviors are measured based on established patterns of neuronal output ( kristan et al . , 2005 ) .
in both preparations , the leech 's relatively large neurons ( 25100 m diameter ) can be recorded simultaneously over extended periods ( > 3  h ) with electrophysiological methods .
voltage - sensitive dyes have permitted the optical recording of hundreds of identified neurons simultaneously and are providing new insights into the cellular mechanisms of decision - making and multi - functional circuits ( briggman and kristan , 2006 , 2008 ) .
the nearly intact preparation is particularly useful because the goal of matching locomotor kinematics with the activity of identified neurons can be met . in nearly intact leech preparations individual cephalic neurons
were identified that either activated locomotion or were rhythmically active during locomotion ( esch et al . , 2002 ; mesce et al . ,
electrical excitation of a single neuron , named r3b-1 ( bilaterally paired ) , was sufficient to elicit sustained locomotor activity ( esch et al . , 2002 ) .
the form of locomotion induced , however , was entirely dependent on whether the body of the leech was suspended in fluid or allowed to lie upon a dryer surface ( esch et al . , 2002 ) .
thus depolarization of a single r3b-1 neuron resulted in a context - dependent response that was gated by sensory input from either an aquatic or terrestrial environment .
additional studies of overt crawling and swimming confirmed that leeches will quickly switch to a crawling mode when encountering shallow water ( esch et al .
furthermore , when fluid levels were ambiguous , a swim - crawl hybrid locomotor pattern emerged in both fully- and nearly intact animals ( esch et al . , 2002 ) .
thus the decision to locomote is hierarchical , made at the level of a single higher - order descending interneuron , but the switching ( and selection in this case ) of various forms of locomotion is based on the integration of contextual somatosensory cues . if descending signals from the cephalic ganglion are removed reversibly , the leech looses its ability to initiate crawling even in the presence of relevant sensory stimulation ( puhl and mesce , 2010 ) . thus the decision to crawl is entirely dependent on cephalic descending input .
for example , tactile body stimulation can reliably induce swimming when the cephalic ganglion is removed reversibly ( puhl and mesce , 2010 ) . although the cephalic ganglion contains a variety of neurons that can gate or trigger swimming ( brodfuehrer and friesen , 1986 ) , downstream swim - gating neurons are also competent to activate the swim oscillators ( kristan et al . , 2005 ) .
last , the biomechanics of an animal clearly must constrain which locomotor behaviors are available for selection or the time of transition between forms ; for example , such constraints may help to explain why leech swimming and crawling are always initiated with an elongation of the body and the excitation of similar ( circular ) muscles ( esch et al .
the results above provide a striking example of how sensory information from the environment is fundamentally important for behavioral switching , but what about the internal state of the animal ? are there conditions under which the leech will be strongly biased to crawl or swim because of its internal state ?
recent studies indicate that specific biogenic amines significantly bias the mode of locomotion available to an animal .
for example , dopamine has been shown to turn on the underlying neural circuits generating leech crawling behavior ( puhl and mesce , 2008 , 2010 ) .
in addition , dopamine prevents swimming from becoming activated ( crisp and mesce , 2004 ) . in preparations
in which fictive locomotion was recorded , dopamine blocked swimming even when the cns was electrically stimulated in attempts to produce swimming ( crisp and mesce , 2004 ) . in the presence of dopamine , stimulation of cell r3b-1
was found to induce crawling but never swimming , regardless of the swim - specific contextual cues present ( puhl and mesce , personal observations ) .
thus dopamine not only activates crawling , it prevents swimming as well , providing a clear example of a chemical switch for locomotor behavior .
although it is unknown how the levels of dopamine fluctuate normally within the leech , we can speculate that they might significantly rise when the leech comes in contact with its host .
typically , the leech switches to crawling at this time and some evidence suggests that dopamine is linked to feeding ( biting ) behavior ( o'gara et al . , 1991 ) . because swimming often requires detachment of both its front and rear suckers , it makes sense that this form of locomotion needs to be suppressed to prevent loss of contact with the host .
the answer to this question has been long known , and solid evidence indicates that serotonin is the key modulator for activating swimming ( willard , 1981 ; friesen and kristan , 2007 ) . during active feeding behavior ,
however , serotonin was elegantly shown to serve as a direct and powerful inhibitor of the sensory gating for swimming , crawling , and other body movements ( gaudry and kristan , 2009 ) .
it is noteworthy that the central activation of swimming was not inhibited . because serotonin is known to activate the central swim oscillators
paradoxically , focal delivery of serotonin to the cephalic ganglion , but not the nerve cord , was found to suppress swimming by influencing the decision to swim ( crisp and mesce , 2003 ) .
bath application of serotonin was deemed a physiologically appropriate delivery protocol because it matched the anatomically based paracrine - like release of serotonin within the cns ( crisp and mesce , 2003 ) .
furthermore , preliminary data support the idea that dopamine trumps serotonin : a mixture of serotonin and dopamine results in no swimming ( puhl and mesce , personal observation ) .
thus as long as dopamine is present at high enough concentrations during feeding , serotonin 's actions on the swim central pattern generator are observably blocked .
perhaps , when the levels of dopamine drop after a feeding session and serotonin levels are low enough to prevent sensory neuron pre - synaptic inhibition ( gaudry and kristan , 2009 ) , the leech is once again able to switch on its swimming behavior . what parallels exist for the regulation of locomotion in c. elegans ? in the leech , the dorsal 
ventral undulations used in swimming are unambiguously distinct from the whole - body elongations and contractions made during vermiform crawling ( kristan et al . , 2005 ; puhl and mesce , 2008 ) .
only recently have several labs considered whether c. elegans also exhibits distinct crawling and swimming forms of motion ( korta et al . , 2007 ; pierce - shimomura et al . , 2008
similar to swimming in the leech , both forms of motion in c. elegans appear to depend on thrust generated by bends passed along the body .
kinematic analysis revealed that animals crawl with a persistent s - shaped posture on a dry substrate with 1 hz high - amplitude bends , and swim in liquid with 2  hz lower amplitude bends ( pierce - shimomura et al . , 2008 ) .
the two forms of motion also differ in the pattern of bend propagation : bends propagate at uniform velocity 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 ( pierce - shimomura et al . , 2008 ) .
in c. elegans and the leech , crawling and swimming are further distinguished by the selective overlay of searching - related motor patterns while crawling .
ventral crawl bends , c. elegans wiggles its  nose  at 10  hz in all three dimensions . this behavior has been termed  foraging  because the worm seems to use it as a way to search for food or the detection of substrate properties .
an analogous behavior , although considerably slower , is displayed during crawling in the leech ( gray et al .
these exploratory - type behaviors are turned off during swimming in both the leech ( kristan et al . , 2005 ) and worm ( pierce - shimomura et al . , 2009 ; vidal - gadea et al . , 2009 ) .
the genetic tractability of c. elegans has allowed crawling and swimming to be distinguished with transgenic tools and mutation . by imaging calcium transients in muscles of freely moving animals , with the genetically encodable calcium - indicator chameleon , the two forms of motion were shown to be subserved by distinct patterns of muscle activity ( pierce - shimomura et al . , 2008 ) .
in the future , newer imaging techniques may enable the activity patterns of identified neurons to be revealed in freely moving animals ( faumont et al .
crawl and swim are also distinguished genetically in the worm because some mutations have a more severe effect on swimming than crawling ( miller et al . , 1996 ; pierce - shimomura et al . , 2008 )
the specific effects rendered by mutation may be thought of as being analogous to how a pharmacological agent may preferentially affect one form of locomotion over another form in other animals .
although c. elegans crawls and swims with distinct kinematics , it remains controversial whether crawling and swimming represent distinct gait - like forms of motion or simply altered versions of a single form ( korta et al . , 2007 ; pierce - shimomura et al . , 2008
this issue is usually addressed in animals with limbs by studying how kinematics vary as an animal moves at different speeds on a treadmill .
gaits are indicated if the animal shows a discontinuous transition in kinematics with a continuous increase in speed just as humans show a sudden switch from walking to running at 4  m / s ( alexander , 1989 ) . in place of a treadmill , c. elegans researchers control speed by immersing the worm in different concentrations of viscous methylcellulose ( korta et al . , 2007 ; berri et al . , 2009 ) .
two studies have found that bend frequency decreases gradually with increased viscosity ( korta et al .
an initial study by korta et al . ( 2007 ) reported that that the worm unexpectedly and inexplicably maintained the same swim - like wavelength ( c - shaped waveform ) in both low and high viscosities , but this result has not been reproduced ( fang - yen and samuel , personal communication ) .
a second study instead found that wavelength decreases gradually with increased viscosity ( berri et al .
these studies suggest that crawling and swimming may represent a single form of motion in c. elegans .
however , recent unpublished findings show that the worm spontaneously alternates between bouts of crawling and swimming in intermediate viscosity solutions ( pierce - shimomura et al . , 2009 ; vidal - gadea et al . , 2009 ) .
mutations that specifically perturb the development and function of all sensory cilia cause a peculiar defect in swimming  these mutants switch spontaneously between crawl and swim forms of motion in liquid ( pierce - shimomura et al . , 2008 ) .
together , these data suggest that the switch between crawling and swimming reflects a  decision  made by the worm based on sensory input just as it does in the leech .
while the neural basis for crawling and swimming has been studied for decades in the leech , how c. elegans switches between crawl and swim is just beginning to be investigated . taking a hint from the leech , the pierce - shimomura lab is investigating whether dopamine plays a role in locomotor switching .
preliminary results suggest that dopamine is necessary and sufficient to facilitate a gait - like switch from swim to crawl in c. elegans ( pierce - shimomura et al . , 2009 ;
interestingly , dopamine does not appear to be necessary to maintain the gross kinematics for either form of motion .
knock - out of the dopamine transporter gene , however , results in a gradual paralysis during swimming that depends on endogenous dopamine synthesis and a d2-type dopamine receptor ( mcdonald et al . , 2007 ) . based on these results ,
this swim - induced paralysis might be explained by dopamine levels rising above a concentration that permits swimming . c. elegans has eight dopamine neurons that appear to act as mechanoreceptors sensitive to substrate texture ( sulston et al .
may become activated upon firm contact of the body with the substrate to trigger a switch from swimming to crawling .
how does c. elegans switch from crawl to swim ? while serotonin has a known role in slowing the crawling speed of starved animals after finding food ( sawin et al . , 2000 ) , the pierce - shimomura lab has only begun to study whether serotonin has a role in swimming ( vidal - gadea and pierce - shimomura , unpublished observations ) .
an unbiased genetic screen for mutations that disrupt the crawl to swim transition revealed a key role for the newly described sodium - leak channel pathway ( pierce - shimomura et al . , 2008 ) .
these mutants are capable of crawling , but become frozen in posture within a fraction of a second upon entering liquid .
the sodium - leak channels are widely expressed in the nervous system , so it remains unclear whether they facilitate the crawl to swim switch through neuromodulatory signaling , independent mechanisms , or both ( pierce - shimomura et al . , 2008 ) .
( 2009 ) has determined that the mammalian sodium - leak channel is the major molecular target of substance p which is a potent activator of locomotion in lamprey and mouse ( smith et al . , 1988 ; svensson et al . , 2001 ) .
neuromodulatory switches are also used to switch off specific locomotory subcircuits in c. elegans . in an agar - filled petri dish
, the worm spends most of its time crawling forward , but will occasionally crawl backward either spontaneously or as an escape .
the foraging behavior described previously occurs during forward locomotion but is switched off during backward locomotion ( alkema et al . , 2005 ) .
a recent genetic screen for mutants that forage while moving backward revealed a critical role for the neurotransmitter tyramine . through an elegant combination of laser ablation of identified neurons and muscles , quantitative behavioral analysis , and electrophysiology
 rmd  and  smd  motorneurons and neck muscles involved in foraging through a novel tyramine - gated chloride channel ( alkema et al . , 2005 ; pirri et al . 2009 ) . in c. elegans ,
additional members of this novel class of chloride channels were found to be gated by serotonin , dopamine , acetylcholine , and choline ( ringstad et al . , 2009 ) .
these channels might serve as neuromodulatory switches to turn off specific motor programs in c. elegans .
over the course of evolution , modern gene orthologs within different animal species have been found to control behaviors that have only slightly or moderately changed from their presumed original form ( e.g. , circadian rhythms , as well as diverse types of serotonin - dependent learning ) ( kandel , 2001 ; sitaraman et al . , 2008 ; zheng and sehgal , 2008 )
. this surprising degree of conservation , not only of gene sequence but also gene function may , in part , be because such genes shared similar expression patterns in fundamentally conserved neural circuits for behavior , regardless of whether the extant behaviors are now similar or not .
for example , it has been shown that homologous serotonergic neurons across species have the potential to become co - opted for the production of divergent locomotor behaviors ( newcomb and katz , 2007 ) .
an important question that can not be adequately addressed within the scope of this article is how forms of locomotion may have evolved within and between animal species .
regardless , for c. elegans , it is apparent that the sensory - gating of locomotion and the amines are intimately connected , especially as many of the mechanosensory neurons are themselves aminergic . in the leech , the aminergic networks
are centrally located ; however , it has been shown that activation of specific mechanosensory neurons important for the normal activation of swimming can excite specific serotonergic and octopaminergic neurons in the cns ( gilchrist and mesce 1997 ; crisp and mesce , 2006 ) .
although we have yet to identify sensory neurons that excite centrally - located dopaminergic neurons in the leech , it is known that specific dopaminergic neurons are electrically coupled to cephalic neurons that can terminate swimming ( crisp and mesce , 2004 ) .
because these same descending neurons also receive sensory information from the body 's mechanoreceptors ( brodfuehrer and friesen , 1986 ) , it could be argued that the dopaminergic network also processes sensory information . in invertebrates and vertebrates the biogenic amines , especially serotonin , play vital roles for facilitating switching between different behaviors and for selecting specific forms of locomotory outputs ( harris - warrick and marder , 1991 ; faulkes , 2005 ; gillette , 2006 ; guertin and steuer , 2009 ) .
it is also compelling that the dopaminergic innervation of the striatum and its similar types of afferent inputs are conserved throughout evolution from the cyclostomes ( e.g. , lamprey ) to primates ( smeets et al . , 2000 ;
thus it is not too surprising to learn that the neuromodulators released directly and indirectly by sensory neurons to adjust motor behaviors in c. elegans and the leech ( e.g. , serotonin , dopamine , octopamine  the analog of norepinephrine ) are among the best characterized neuroactive substances known to bias higher - order decision - making processes in mammals , including humans ( aragona and wang , 2009 ; crockett , 2009 ) .
human locomotor disorders , such as parkinson 's disease , often involve difficulty in movement initiation and switching between various motor activities ; switching moods is central to our understanding and treatment of bipolar disorders and switching our attention too frequently is at the core of attention deficit hyperactive disorders .
understanding common neural strategies for locomotor decision - making among diverse animal systems may provide new ways of switching our own thinking about behavioral choice and the decisions we make  or that are made for us .
the authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest .
 animals frequently switch from one behavior to another , often to meet the demands of their changing environment or internal state . what factors control these behavioral switches and the selection of what to do or what not to do ? 
 to address these issues , we will focus on the locomotor behaviors of two distantly related  
 worms ,  the medicinal leech hirudo verbana ( clade lophotrochozoa ) and the nematode caenorhabditis elegans ( clade ecdysozoa ) . 
 although the neural architecture and body morphology of these organisms are quite distinct , they appear to switch between different forms of locomotion by using similar strategies of decision - making . for example , information that distinguishes between liquid and more solid environments dictates whether an animal swims or crawls . in the leech , 
 dopamine biases locomotor neural networks so that crawling is turned on and swimming is turned off . in c. elegans , dopamine may also promote crawling , a form of locomotion that has gained new attention . 
Introduction
Behavioral Switches: Selecting Different Forms of Locomotion
A tale of two worms
The Biogenic Amines: Mechanisms of Behavioral Switching Shared Across Animal Species
Conflict of Interest Statement