J Phys Fitness Sports Med, 4(1): 107-110 (2015)

DOI: 10.7600/jpfsm.4.107

JPFSM: Short Review Article

Locomotor adaptation: Significance and underlying neural mechanisms

Tetsuya Ogawa1,2*, Noritaka Kawashima3 and Kimitaka Nakazawa4
1
Faculty of Sports Sciences, Waseda University, 2-579-15 Mikajima, Tokorozawa, Saitama 359-1192, Japan
2
Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda, Tokyo 102-0083, Japan
3
Department of Rehabilitation for Movement Functions, Research Institute, National Rehabilitation Center for Persons with
Disabilities, 4-1 Namiki, Tokorozawa, Saitama 359-8555, Japan
4
Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro, Tokyo 153-8902, Japan

Received: December 18, 2014 / Accepted: December 26, 2014

Abstract Human locomotion is flexible in meeting the requirements of given environmental

or task demands. Hence, in everyday life, we can walk, run, and skip in environmental sur-
roundings that vary from hour to hour and even from second to second. In making such flexible
adjustments, a sense of “adaptability” attained by the central nervous system plays an important
role. In the literature, adaptation studies focusing on locomotion have attracted a great deal of
attention in recent years for their potential application to the designing of gait training pro-
grams, and as a useful method for revealing the specific mechanisms underlying human loco-
motion. In this review article, to address how locomotor adaptation is related to social locomo-
tion, the authors introduce knowledge accumulated in recent decades, particularly that related
to two different types of locomotor adaptation studies: first, studies that address the general
features of locomotor adaptation including underlying neural mechanisms, and second, those
that use experimental paradigms of locomotor adaptation to reveal the context-dependency
of locomotion. It should be noted that, although knowledge of locomotor adaptation has been
increasing, the field is still largely unexplored, and further intensive research in the future is
necessary.
Keywords : locomotion, walking, running, adaptation, specificity

stereotypical movements present in the basic aspects of

Introduction
In everyday life, humans use locomotion (walking,
running, skipping, and so on) to move through space. It
has been well documented that locomotion is not simply
an accumulation of either voluntary- or reflex-induced
movements. Instead, a specialized functional network in
the spinal cord (known as central pattern generators, or
CPGs) (for review, see Ref. 1) is known to exist and play
a significant role in the generation of patterned motor
outputs. The patterned motor outputs, in turn, result in
movement of the limbs. Because of characteristic features
of the functional network, locomotive movements are
often regarded as stereotypical. An example illustrating
such stereotype can be found in a unique behavior of hu-
man infants. In an upright standing posture with external
support, they exhibit patterned stepping-like lower-limb
movements upon their center of mass moved forward;
this is indirect evidence demonstrating the existence of
CPGs. Similar aspects have been demonstrated in cats
that have undergone spinalization2), that is, cats without
any descending input from the higher centers. Despite the
*Correspondence: t.ogawa@aoni.waseda.jp
locomotion, when utilizing locomotion in our daily lives
we always have to adjust to changing environmental and
task demands. For example, road surfaces are not always
flat and smooth; there are variable constraints such as
unevenness, gradient, slipperiness, and many others. We
often wear different types of apparel and shoes, and carry
items with different weights and shapes from day to day.
Regarding the task demands, we not only walk, but also
run and skip and perform any number of other locomo-
tive tasks, and we do so at a variety of speeds. Regardless
of the changing environmental surroundings and task
demands, however, we as adult humans can achieve con-
stant locomotion in any number of situations. Locomotion
is, therefore, not only a stereotypical behavior, but is also
flexible enough to accommodate widely varying situa-
tions. In this review article, the authors present an over-
view of the neural mechanisms through which humans
exercise flexible control of locomotion.
Significance of adaptation in social locomotion
The fact that we can execute smooth and skilled move-
ments in a variety of situations is largely dependent on
108 JPFSM : Ogawa T, et al.
our past experience. That is, the generation of motor pat-
terns to attain such movements occurs through repetitive
practices on the basis of “trial and error” processes. In
other words, any movements without a past precedent (for
example, upon the first exposure to particular environ-
mental surroundings or motor tasks) cannot be executed
smoothly. An example of this “trial and error”-based ac-
cumulation of skilled movement is given in the following
story reflecting an everyday situation.
A boy began his locomotion by crawling at eight
months, and he started walking at around 12 months old.
Now, at two years of age, he has more than 12 months of
walking experience and shows smooth and skillful walk-
ing movement. He can walk even under varied physical
constraints such as uneven road surfaces, slopes, stairs,
and other constraints in his everyday surroundings. One
day, he went shopping with his parents at a nearby super-
market, and was attracted to an escalator that he saw for
the first time in his life. As he saw people stepping onto
the “moving stairs”, he also wanted to get on; and so he
walked over to the escalator and stepped on it. Upon con-
tacting the surface of the moving escalator, his leg was
pulled forward, his center of body mass moved backward,
and he fell.
As stated above, he had enough experience to walk nor-
mally. That is, he already had the motor strategies in the
central nervous system (CNS) that made him capable of
walking in a variety of possible contexts in everyday life.
Lack of a motor strategy for a context to which he was
newly exposed (stepping onto the moving platform of the
escalator, therefore, a trial) could have been responsible
for the fall (error). In later attempts to step onto an escala-
tor, he would perform better; and through practice (further
trials), he would acquire more sophisticated motor strate-
gies and better ways to step on it (thereby minimizing the
error). This acquisition of motor strategies by the CNS
is referred to as “motor adaptation” or “motor learning”.
Below, an overview of the mechanisms underlying motor
adaptation is provided on the basis of studies executed
mostly in the last decade.
Experimental findings related to locomotor adaptation
This review deals with locomotor adaptation, a notion
that may appear strange to many readers. This is because
locomotion such as walking and running are motor tasks
that are frequently practiced in a variety of different
contexts in everyday life beginning in childhood (unlike
those requiring practice such as juggling and playing
musical instruments). To study locomotor adaptation and
therefore to enhance adaptation in adult humans, exposure
to a novel environment that is not available in everyday
life is necessary. Furthermore, to quantitatively analyze
the adaptive phenomena, the subject has to be exposed
to the novel environment both systematically and with
reproducibility. In recent studies focusing on locomotor
adaptation, it was typical to use an experimental appara-
tus such as the following: 1) Robotically-controlled gait
orthosis either to enhance or to interfere with joint move-
ments at particular phases of locomotion3), 2) Specialized
treadmill (split-belt treadmill) with two belts (one under-
neath each foot) operated at independent velocities4-10),
and 3) Application of a force field during the swing phase
of locomotion through the use of a weight load or elastic
rubber band11,12). In any of these cases, the subjects’ nor-
mal gait patterns are transiently interfered with through
the imposition of novel physical constraints. In the min-
utes after this imposition, they acquire motor patterns that
are appropriate under the respective constraints.
Basic knowledge of locomotor adaptation
Studies focusing on motor adaptation, as opposed to lo-
comotor adaptation, have been well established in simple
motor tasks and particularly among simple reaching
movements of the upper extremity13,14). When a person
reaches a hand toward a target in front of him or her, the
hand generally creates a nearly straight trajectory toward
the target. With the repetition of such a movement, a sud-
den and unknown imposition of force fields results in
a deviation of the trajectory toward the direction of the
force field. Through repetitive practice of the movement
in the force field, however, the nearly-straight trajectories
are restored. At this point, a sudden and unknown re-
moval of the force field causes the deviation of the trajec-
tory, this time in the direction opposite to the previously
imposed force field. The neural mechanisms underlying
these phenomena are described below.
In the CNS, a dynamic model of the musculoskeletal
system (known as the “internal model”) is developed on
the basis of past experience. We can, therefore, easily
reach our hand to a given target under normal conditions
without constraints. The deviation of the trajectory (the
difference between the target trajectory and the actual
trajectory) upon exposure to the force field is detected as
an error. Based on the error, the CNS updates the internal
model (that is, it recalibrates the motor output) to mini-
mize the error on a trial-to-trial basis. The subsequent
deviation of the trajectory in the direction opposite to the
force field is therefore regarded as occurring due to the
emergence of motor output necessary to achieve the de-
sired trajectory under the force field.
In the adjustment of motor output seen in these phe-
nomena, the CNS is engaged in two different ways de-
pending on the speed of the movement, namely feedback
and feedforward control. In slow movements, the CNS
continuously monitors the movement error and makes on-
line (or real-time) corrections of the motor output (feed-
back control). Adjustment of the motor output through the
feedback control involves a time delay due to limitations
in the conduction speeds of the nerves and of transmis-
sion between them, and is therefore inappropriate for con-
 JPFSM : Locomotor adaptation in humans
trolling fast movements. Feedforward control is therefore
necessary. In feedforward control, the CNS refers to the
movement error in the previous trials (the feedback error)
and predictively adjusts the motor output that is necessary
to achieve the desired movement trajectory in forthcom-
ing trials. The relative contributions of feedback and
feedforward control can be modified by variable factors
such as the movement speed and the subjects’ proficiency
in the motor task. Regarding locomotor adaptation, it
is possible that the neural mechanisms, as in the above-
mentioned arm reaching movement, are shared partially
or at a certain level. For the most part, however, the
mechanism remains unclear since the notion of locomo-
tor adaptation was only recently recognized and requires
further elucidation. Here we provide a description of what
is known about locomotor adaptation at present.
Reisman and colleagues developed an experimental
paradigm utilizing a split-belt treadmill, and revealed
the general features of locomotor adaptation from the
perspective of both the temporal and spatial aspects of
human walking4). Lam et al. and Blanchette and Bouyer,
by applying a force field during particular phases of
walking, revealed phase-specific contributions of both
feedback and feedforward control3,11). With regard to the
emergence of adaptive phenomena in locomotion, sev-
eral studies have suggested possible neural mechanisms.
For example, it was demonstrated that adaptation takes
place in human infants15). This potentially agrees with the
findings of Hodgson and colleagues who demonstrated a
similar adaptive nature in spinalized cats16). These studies
therefore showed that locomotor adaptation may occur
as a reflection of the neural mechanisms inherent in the
spinal cord. On the other hand, other studies showed that
the cerebellum plays a significant role in locomotor adap-
tation5,17). In patients with cerebellar lesions5) and cats that
underwent experimental deprivation of cerebellar-induced
long-term depression (LTD)17), an aspect of locomotor
adaptation that is present in healthy individuals was im-
paired. These results, despite the difference in their view-
points, suggest the possibility that locomotor adaptation
can occur as long as a particular site in the CNS is intact.
Context-dependency of locomotion revealed by locomo-
tor adaptation paradigms
The study of locomotor adaptation not only provides
us with knowledge useful in the construction (or recon-
struction) of locomotion after particular CNS lesions, but
also has revealed the context-dependency of locomotion,
which implies the existence of independent neural mecha-
nisms that are capable of managing different tasks and
environmental constraints. This context-dependency is
the reason that, as we stated earlier, movements without
past experience (for example, first exposure to particular
environmental surroundings or motor tasks) cannot be
executed smoothly. We therefore have to train in the re-
109
spective contexts and acquire motor programs capable of
movements under each context. Here we describe some
examples of the context-dependency underlying particular
locomotion movements.
The first example of context-dependency in locomotion
was provided by Choi and colleagues in 2007 by utiliz-
ing a locomotor adaptation task on a split-belt treadmill6).
They revealed the existence of independent neural mecha-
nisms for walking forward and backward6). They also
demonstrated that adaptation is dependent on the limb
(left or right). Even when walking in the same direction
(forward), it was subsequently demonstrated that there
were independent neural mechanisms that corresponded
to different walking speeds8). Locomotor adaptations that
took place at particular walking speeds were valid only
at those specific speeds and did not transfer to others8).
Further, the authors demonstrated that even for locomo-
tion at a single speed, the neural mechanisms underlying
walking and running independently represented different
modes of locomotion9). In the experiment, after subjects
adapted to walking on a split-belt treadmill (with a 2:1
ratio between speeds) for 10 minutes, the movement pat-
terns when subsequently walking under a normal belt
condition (two belts at the same speed) showed prominent
asymmetry. Adapting to running on the split-belt tread-
mill also resulted in asymmetric movement when running
afterward under a normal belt condition. However, the
acquired (asymmetric) movement patterns in the respec-
tive gaits (walking or running) were not shared between
the two gaits. That is, the subjects could walk normally
(nearly symmetrically) after adapting to running asym-
metrically, and could also run normally after adapting to
walking asymmetrically. In the same study, further analy-
ses showed interesting results. As stated above, although
the subjects could walk normally after adapting to run-
ning asymmetrically, their movement resulted in promi-
nent asymmetry when they started to walk subsequently
(after running normally). A similar tendency was detected
after adapting to walking asymmetrically. The acquired
movement patterns in the respective gaits were therefore
maintained independently of each other. In the results,
since the use of joints and muscles may be largely shared
between the two gaits, the limited share of the acquired
movement patterns was surprising. Although the specific
mechanisms cannot be directly addressed in a behavioral
study, possible candidates will be considered based on
the results obtained in animal studies. In the supraspinal
mechanism, for example, the mesencephalic locomotor
region (MLR) plays a significant role in determining dif-
ferent gaits. Electrical stimulation of a particular site in
the MLR determined the initiation of different gait modes
in decerebrated cats18) and different swimming behaviors
in salamanders19) that were both dependent on stimulus
intensity. Regarding the spinal cord, McLean and col-
leagues demonstrated in larval zebrafish that particular
sets of swimming-related spinal interneurons were re-
110 JPFSM : Ogawa T, et al.
cruited depending on the swimming frequency20). A group
of interneurons that was active under one movement
frequency was strongly inhibited under others20). More
recently, in mice, experimental lesions in particular sub-
types of locomotion-related spinal interneurons resulted
in the impairment of normal alternate (left-right) locomo-
tion, and the impairment occurred depending on stepping
frequency21). Other results have shown mode-dependency
in the propriospinal neurons during scratching movement
of a turtle hind limb22).
In locomotor adaptation studies attempting to elucidate
the context-dependency of the underlying neural mecha-
nisms, the interpretation of the results is somewhat specu-
lative, and the detailed mechanisms therefore remain un-
clear. These studies are, however, very important from the
perspective of designing training regimens in that there
was certain specificity at the behavioral level, i.e., the
final output of the motor systems. Moreover, these behav-
ioral results provide further motivation for revealing the
more specific mechanisms underlying them.
Summary
In spite of the stereotypic quality of the basic mecha-
nism of human locomotion, locomotion is also flexible
enough to accommodate a variety of environmental and
task demands. The notion of locomotor adaptation has
been recognized only recently in the scientific literature,
and more studies are necessary to elucidate further de-
tails. However, the adaptation concept is closely linked to
what we experience in our everyday life, and any practice
of locomotive movements can be regarded as an example
of locomotor adaptation. Further studies on locomotor
adaptation therefore can function to provide an objective,
scientific understanding of our experience and may lead
to the establishment of locomotion training protocols in a
variety of situations such as sports training and those after
particular CNS lesions.
Conflict of Interests
The authors declare that there is no conflict of interests
regarding the publication of this article.
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