1. Ann. N.Y. Acad. Sci. ISSN 0077-8923
ANNALS OF THE NEW YORK ACADEMY OF SCIENCES
Issue: Neurons, Circuitry, and Plasticity in the Spinal Cord and Brainstem
A dual spinal cord lesion paradigm to study spinal
locomotor plasticity in the cat
Marina Martinez and Serge Rossignol
Department of Physiology, Universit´e de Montr´eal, Montr´eal, Qu´ebec, Canada
Address for correspondence: Dr. Serge Rossignol, Department of Physiology, Groupe de Recherche sur le Syst`eme Nerveux
Central, Faculty of Medicine, Universit´e de Montr´eal, P.O. Box 6128, Station Centre-Ville, Montr´eal, Qu´ebec, Canada H3C 3J7.
serge.rossignol@umontreal.ca
After a complete spinal cord injury (SCI) at the lowest thoracic level (T13), adult cats trained to walk on a treadmill
can recover hindlimb locomotion within 2–3 weeks, resulting from the activity of a spinal circuitry termed the central
pattern generator (CPG). The role of this spinal circuitry in the recovery of locomotion after partial SCIs, when part
of descending pathways can still access the CPG, is not yet fully understood. Using a dual spinal lesion paradigm (first
hemisection at T10 followed three weeks after by a complete spinalization at T13), we showed that major changes
occurred in this locomotor spinal circuitry. These plastic changes at the spinal cord level could participate in the
recovery of locomotion after partial SCI. This short review describes the main findings of this paradigm in adult cats.
Keywords: central pattern generator; plasticity; training; spinal cord injury; locomotion
Introduction
Hindlimb locomotion is controlled by a tripar-
tite system that involves dynamic interactions
among a spinal neuronal network, supraspinal
structures, and peripheral sensory inputs.1–5
Fol-
lowing incomplete spinal cord injury (SCI), this
tripartite interaction is perturbed, but animals can
recover a surprising degree of locomotor perfor-
mance, which probably involves widespread plastic
changes within remaining ascending and descend-
ing pathways,6–9
segmental spinal reflexes,10
and the
spinal cord itself.11,12
While many studies empha-
size the compensatory role of supraspinal structures
in functional recovery after partial SCI, there is little
evidence indicating how plastic changes within the
spinal circuitry itself can account for some of the
locomotor recovery after SCI. This review focuses
on locomotor recovery and plasticity after partial
SCI by describing some fundamental concepts that
emerged from complete SCIs in cats. Adaptation
within the spinal locomotor circuitry after partial
SCI is then discussed.
Complete spinal lesions and the role
of the CPG
In many species, some recovery of hindlimb lo-
comotion can be observed after a complete spinal
cord section.1,2
Since locomotion can be expressed
in kittens spinalized 7–14 days after birth, that
is, before they gain their optimal walking capac-
ities, one can suggest that this behavior is ge-
netically programmed.13–15
After a complete SCI
at the level of the last thoracic segment (T13),
cats can recover hindlimb locomotion that closely
resembles a normal locomotor pattern by using
electrical stimulation,16,17
locomotor training,18,19
pharmacological agents,20–24
or a combination of
the above.25
This, per se, confirms the concept
of spinal generation of locomotion by an intrin-
sic spinal circuitry at the lombosacral level, the
central pattern generator (CPG). Since descend-
ing and ascending pathways are completely de-
stroyed after a complete SCI, some intrinsic changes
must have occurred in the CPG to allow the re-
expression of hindlimb locomotion. After a com-
plete SCI, the excitability of motoneurons,26,27
doi: 10.1111/j.1749-6632.2012.06823.x
Ann. N.Y. Acad. Sci. 1279 (2013) 127–134 c 2013 New York Academy of Sciences. 127

2. Intraspinal plasticity after incomplete SCI Martinez & Rossignol
Figure 1. General methodology for the study of locomotion in cats. The animal is placed on the treadmill (arrows within the
belt indicate the direction of movement) and is allowed to walk with all four limbs. Pairs of EMG wires are implanted into various
muscles (only one pair is represented here) and soldered to a multipin connector cemented to the skull. The EMG signal was filtered
and digitized and was then displayed on a computer. The left panel illustrates the EMG trace of the sartorius (hip flexor and knee
extensor). Reflective markers are placed at various points on the limb, and the angle measurements are taken in the indicated
orientations. For each video field (16.7 milliseconds between fields), the coordinates of the reflective markers are obtained and the
hindlimb movement is reconstructed as indicated in the kinematic model (MTP = metatarsophalangeal joint). A seventh point is
put on the right hindpaw to obtain kinematic data for this limb and information relative to coordination between hindlimbs. From
such data, the swing and stance phases of each cycle can be reconstructed as shown in stick figures and duty cycles. The foot contact
and lift are also measured to determine cycle length and duration and also to synchronize EMG events when needed. A digital time
code (SMPTE) is used to synchronize video and EMG recordings.
cutaneous reflexes,28
and receptors of various neu-
rotransmitter systems29
are changed.
Recovery from partial spinal lesions
Considering that incomplete SCIs are more fre-
quent than complete SCIs in humans, we asked
whether the spinal mechanisms observed after com-
plete SCIs also apply to hindlimb locomotion gen-
erated after partial SCI. To accurately evaluate the
locomotor pattern after spinal lesions, the most
objective method consists of using chronic elec-
tromyographic recordings combined with synchro-
nized video recordings of movements (Fig. 1). This
method permits a powerful quantitative compar-
ison of locomotor performances before and after
spinal lesions, as well as its evolution over time. To
evaluate the role of descending pathways in loco-
motor control, studies have investigated the con-
sequences of lesions targeting specific tracts at the
spinal level.
Dorsal/dorsolateral spinal tracts. After the dor-
sal/dorsolateral SCI’s bilateral effect on the cortico-
and rubrospinal fibers, cats can recover voluntary
quadrupedal locomotion while maintaining their
weight and equilibrium after a 3- to 10-day period.
They, however, have some long-lasting deficits such
as foot drag (resulting from impaired coupling be-
tween hip and knee flexors) and they lose the capac-
ity for anticipatory modifications when negotiating
obstaclesplacedonthetreadmill.30
Despitethesede-
fects, the cats do walk remarkably well with all four
limbs on the treadmill, suggesting that the cortico-
and rubrospinal tracts do not appear critical for the
control of treadmill locomotion but are important
for skilled locomotion.
Ventral/ventrolateralspinaltracts. Vestibulo-and
reticulospinal pathways traveling in the ventral part
of the cord are known to be, respectively, involved
in postural control and initiation of locomotion.
After small ventral/ventrolateral lesions, cats can
walk voluntarily at speeds of up to 0.7 m/s with all
four limbs one to three days after the lesion.31
With
larger lesions, sparing only part of dorsal columns,
cats behave initially as complete spinal cats. How-
ever, with regular treadmill training, all cats could
128 Ann. N.Y. Acad. Sci. 1279 (2013) 127–134 c 2013 New York Academy of Sciences.

3. Martinez & Rossignol Intraspinal plasticity after incomplete SCI
regain voluntary quadrupedal locomotion but, with
the largest lesions, the animals could not walk faster
than 0.4 m/s even after several weeks of training.
The important observation here is that, even with
extensive bilateral lesions to ventral pathways, cats
could initiate and maintain voluntary quadrupedal
locomotion, suggesting that the ventral tracts
do not appear essential for triggering hindlimb
locomotion.
Hemisections. In contrast to bilateral dorsal or
ventral lesions of the cord, unilateral hemisections
damage the dorsal end ventral tracts on one side,
while the other side remains intact. The functional
consequences of such lesions mainly depend on the
extent of the lesion. Indeed, we showed in cats hemi-
sected at thoracic level 10 that the smaller the lesion
the faster the locomotor recovery.11,32
During the
first two to three days after a nearly complete hemi-
section on one side, the hindlimb ipsilateral to the
lesion shows flaccid paresis and animals adopt a tri-
pod gait, such that they require help for body sup-
port and stabilization. One week after hemisection,
voluntary quadrupedal locomotion reappeared de-
spite limping of the hindlimb and inconsistent plan-
tar foot contact on the side of the lesion. Stepping
activity greatly improves during the first three weeks
posthemisection, but some deficits were shown to
persist at this postoperative time. To minimize the
time spent on the effected hindlimb, the support
time was reduced on the side of the lesion while
the swing phase was increased. Concomitantly, the
burst duration of extensors decreased while that of
the flexors increased on the side of the lesion.12
By plotting the relationships between the cycle and
its subphases (stance and swing) at various tread-
mill speeds, we showed that the hemisection had
induced profound changes in the intrinsic struc-
ture of the cycle on both sides and had thus altered
the neural control of locomotion.33
Moreover, fore-
limb/hindlimb coordination on the side of the le-
sion and left/right hindlimb coupling was altered
and cats exhibited an asymmetrical gait.12
The ipsi-
lateral descending reflexes (scratch, vestibular drop
reflex) were lost after hemisection and skilled loco-
motion such as ladder walking was also impaired
durably on the side of the lesion.34–36
Altogether,
although a gradual recovery of walking occurs after
a spinal hemisection, some deficits associated with
dorsal (postural deficits and altered coordination)
and ventral lesions (impaired skilled locomotion)
persist.
From the studies on partial spinal lesions de-
scribed previously, we can conclude that although
there are some deficits due to the interruption of
specific tracts, animals can in most cases regain
a functional locomotor pattern. Several nonexclu-
sive mechanisms occurring at different levels of the
neuraxis probably participate in locomotor recov-
ery after a partial SCI such as physiological and/or
anatomical reorganizations within remnant path-
ways could somehow take over the functions of the
damaged spinal cord.37–43
However, an alternative
interpretation is that after a partial SCI, the CPG
below the lesion assumes a greater role in generat-
ing the hindlimb locomotor pattern. In this case, the
plastic changes in descending pathways would serve
to reorganize functionally the spinal cord and mod-
ify new input–output characteristics of the spinal
CPG. This interpretation requires demonstrating
that changes occur within the CPG after a partial
lesion, which is discussed next.
Role of the CPG after partial spinal lesions:
the dual lesion paradigm
A dual lesion paradigm has been developed11
to
study the changes occurring within the lumbar
spinal locomotor circuitry (CPG) after a partial
spinal lesion. In this paradigm, a unilateral hemi-
section of the cord is first performed at T10–11,
well above the CPG located in the lumbo-sacral
segments, and is followed, several weeks later, by
a second complete spinal lesion two spinal seg-
ments below the first one at T13 (Fig. 2) (i.e., at the
level where the complete spinal lesions were usu-
ally made18,25,44
) to isolate the spinal CPG from
its supraspinal influences. The main idea of this
paradigm is that if intrinsic changes occurred within
thespinalcorditselfduringlocomotorrecoveryafter
the initial hemisection, these changes could prob-
ably be retained and expressed very early after a
second and complete spinalization a few segments
below. In the first study with this paradigm, cats
were trained to walk on the treadmill during the
interim between the two lesions and the second
complete lesion was performed only when the loco-
motor performances of the cats reached a plateau of
locomotor performance. The first major finding was
that within 24 h (i.e., the first testing session) fol-
lowing complete spinalization, cats could reexpress
Ann. N.Y. Acad. Sci. 1279 (2013) 127–134 c 2013 New York Academy of Sciences. 129

4. Intraspinal plasticity after incomplete SCI Martinez & Rossignol
Figure 2. The dual lesion paradigm. (A) In intact cats, locomotion is controlled and modulated by descending inputs (red arrows)
from supraspinal structures that interact with the spinal CPG (in gray) to coordinate the left (lHL, in red) and right (rHL, in
green) hindlimb activity. (B) After a unilateral hemisection targeting the left part of the spinal cord at T10, descending inputs are
disconnected from the CPG on the left side (red dotted arrows). While the right hindlimb remained actively controlled by the
remnant supraspinal fibers, the left hindlimb is mainly under the control of the partially deafferented CPG. (C) Three weeks after
the hemisection, a complete spinal section is performed at T13, removing all the supraspinal inputs to the CPG, such that the left
and right hindlimbs are mainly under the control of the CPG completely devoid of supraspinal inputs.
hindlimb locomotion with plantar foot placement
at high speeds (up to 1.0 m/s) without any pharma-
cologicalstimulation.11,32
Itshouldagainberecalled
that under normal circumstances the expression of
spinal locomotion requires two to three weeks of in-
tense treadmill training in spinal cats.18
This result
indicates that the hemisection had induced changes
within the spinal circuitry below the lesion, such
that it was already primed to reexpress locomotion
after the complete SCI. As these cats were trained to
walk during the interim between the two lesions and
that this interim period varied among cats, it was
important to standardize the conditions required
to induce plastic changes in the spinal locomotor
circuitry after hemisection.
Could such intraspinal changes occur sponta-
neously after the first partial lesion—that is, in the
absence of training and within a short period of
time between the two lesions? To address this ques-
tion, the interim period between the two lesions was
limited to a short period of three weeks in a cohort
of 11 cats.12
To limit self-training that could in-
fluence locomotor recovery after hemisection, cats
were kept in individual cages and their locomotor
performances were recorded only once a week on
the treadmill. Such housing condition limits sen-
sorimotor experience and contrasts with the daily
treadmill training procedure used in previous stud-
ies.11,32
Interestingly, 24 h after spinalization, 6/11
cats (55%) expressed a bilateral hindlimb locomo-
tion, 3/11 expressed a unilateral pattern on the side
of the previous hemisection, and 2/11 were not able
to walk. These results indicate that the spinal cir-
cuitry below the hemisection can reorganize spon-
taneously and within a relatively short period of
time after hemisection.
This result raised the question of the type of reor-
ganizations occurring within the spinal locomotor
circuitry after hemisection. To determine how the
spinal circuits reorganize after hemisection, we in-
vestigated, over the entire dual lesion paradigm, the
evolution of specific locomotor parameters mainly
controlled by the spinal locomotor circuitry.33
We
measured the various subcomponents of the step
cycle (swing, stance) (see, for instance, Fig. 3A) and
plotted the relationships between the cycle and its
subphases at various treadmill speeds. First, the re-
sults showed that after a hemisection, the intrinsic
structure of the cycle is altered in both hindlimbs,
such that the cycle period can change by adapt-
ing the duration of each subphase according to the
speed. Second, removing all supraspinal inputs by
spinalization revealed that the changes observed af-
ter hemisection were retained for a long time but
130 Ann. N.Y. Acad. Sci. 1279 (2013) 127–134 c 2013 New York Academy of Sciences.

5. Martinez & Rossignol Intraspinal plasticity after incomplete SCI
Figure 3. Effect of locomotor training on hindlimb kinematics in completely spinalized cats previously submitted to a spinal
hemisection on the left side. (A) Illustrations of the kinematic measures. Step cycle duration is the time between two successive
contacts of the same foot on the treadmill, whereas the stance duration refers to the time between foot contact and toe off that
initiates the swing phase. Step length is the distance traveled during the stance and swing phase of a complete step cycle. Toe position
relative to the hip at contact was determined by calculating the mean position (in mm) of the toe relative to the vertical projection of
the hip joint on the ground at contact. As the first spinal lesion (the hemisection on the left side) is known to induce an asymmetrical
walking pattern, the locomotor parameters described previously were compared between hindlimbs by calculating an asymmetry
index (AI). An AI of 0 indicates a perfect symmetry, and in normal conditions, the AIs obtained in all parameters are equal to 0 ±
0.05. The AI gives information on the direction of asymmetry. When a parameter is greater on the left than on the right side, the
AI will be positive and vice versa. For example, in the case of a step length AI < 0, the step of the right hindlimb will be longer
than the left. (B) Evolution of the asymmetry indices calculated for cycle duration, step length, stance duration, and toe position at
contact in cats trained to locomote after spinalization and untrained cats over the entire dual lesion paradigm. In the intact state,
the two groups of cats exhibited a symmetrical walking pattern (AIs = 0 ± 0.05). Twenty-one days after a hemisection on the left
side of the cord, both groups displayed an asymmetrical walking pattern due to the deficits of the left hindlimb (side of the lesion).
Note that both groups were comparable before the spinalization and the beginning of training. Twenty-one days after spinalization,
the asymmetrical walking pattern displayed by all cats after hemisection was retained in untrained cats, while it reversed in trained
cats. Statistical differences between delays are indicated by the symbol (∗
). Statistical differences between groups are indicated by
the symbol (#). L, left; R, right.
Ann. N.Y. Acad. Sci. 1279 (2013) 127–134 c 2013 New York Academy of Sciences. 131

6. Intraspinal plasticity after incomplete SCI Martinez & Rossignol
only on the side of the previous hemisection, thus
demonstrating a durable asymmetrical reorganiza-
tion at the spinal level resulting from the previous
partial spinal lesion. In addition, the asymmetrical
walking pattern observed after hemisection was also
retained by cats after the complete SCI45
(Fig. 3B),
such that the hindlimb on the side of the previ-
ous hemisection kept its deficits after spinalization.
Moreover, some changes that occurred in simple
cutaneous reflexes after the partial lesion were also
retained following spinalization.46
These carry-over
of changes that result from the previous partial SCI
indicated that the spinal cord has an intrinsic capac-
ity to be imprinted by past experiences.
However, can a spinal cord previously modi-
fied by past experience (such as a hemisection)
again adapt to new demands, or are these changes
immutable? To address this question, the perfor-
mance of cats subjected to treadmill training af-
ter the complete SCI were compared with that
of untrained cats during the entire dual lesion
paradigm.45
While without training the asymmet-
rical locomotion induced by the previous unilat-
eral hemisection was retained for three weeks af-
ter the subsequent spinalization, training cats after
spinalization reversed the asymmetrical locomotor
pattern induced, suggesting that new plastic changes
occurred within the spinal cord in response to train-
ing (Fig. 3B). Moreover, training cats after spinal-
ization was shown to improve the locomotor per-
formance of the hindlimb previously affected by
the hemisection. These results demonstrated that a
spinal cord previously modified by past experience
(such as after a hemisection) can remarkably adapt
tonewdemandsimposedbylocomotortrainingand
suggest that locomotor training can be beneficial in
the spinal state regardless of the previous experience
of the spinal cord.
Considering the role of locomotor training in
shaping intraspinal plasticity in cats previously sub-
mitted to spinal hemisection, can the locomo-
tor deficits and asymmetrical intraspinal changes
observed after hemisection be compensated by
locomotor training? In the most recent study, we
evaluated the effect of treadmill training on loco-
motorplasticityafterhemisection.Wecomparedthe
functional locomotor outcome of eight cats trained
to locomote for three weeks after hemisection, and
eight untrained cats that served as control. The
activity-induced intraspinal plasticity was then as-
sessedbycomparingthelocomotorperformancesof
both groups of cats 24 h after the subsequent spinal-
ization. We confirmed that a three-week period of
locomotor training after hemisection had a benefi-
cial role in the recovery of voluntary quadrupedal
locomotion. Furthermore, locomotor training en-
hanced plasticity in the spinal cord below the lesion
because 100% of the trained cats reexpressed a high
level of bilateral hindlimb locomotion immediately
after spinalization compared to 60% of untrained
cats. This study highlighted the beneficial role of
locomotor training on facilitating adaptive plastic
changes within the spinal circuitry and in promot-
ing locomotor recovery after hemisection.
From these studies using a dual spinal lesion
paradigm, we demonstrated that (1) the spinal loco-
motor circuitry has an intrinsic potential of plastic-
ity; (2) this plasticity most likely participates in the
recovery of locomotion after partial SCIs; (3) the
spinal cord is a flexible integration center capable
of adapting and shaping its motor circuits in order
to optimize function with available inputs (i.e., de-
scending and sensory); and (4) locomotor training
has a powerful effect on spinal plasticity and acts
positively on spinal circuits by reestablishing kine-
matic parameters approaching the normal state.
Clinical implications
For years, several concepts relative to the notion of
a spinal locomotor CPG have been obtained from
cat models of SCI. This review highlights the notion
that the spinal locomotor CPG plays a prominent
roleintherecoveryoflocomotionaftercompletebut
also after incomplete SCIs. The question of whether
such notions apply to humans, especially when such
a strong role is considered for a spinal cord CPG,
has been debated. Although the existence of a spinal
CPG in humans cannot be directly and stringently
demonstrated as in animal models, there are a num-
ber of indications that the isolated spinal cord of hu-
mans also contains rhythmogenic capabilities.47–50
Consequently, targeting intrinsic spinal circuits to-
getherwithremainingdescendingandsensorypath-
ways should be a prime approach for rehabilitative
strategies in humans with incomplete SCI, which is
the concept of locomotor training.22
Acknowledgments
This work was funded by a Canada Research Chair
ontheSpinalCord,theSensoriMotorRehabilitation
132 Ann. N.Y. Acad. Sci. 1279 (2013) 127–134 c 2013 New York Academy of Sciences.

7. Martinez & Rossignol Intraspinal plasticity after incomplete SCI
Research Team (ERRSM) as part of the Regenerative
Medicine, and the Nanomedicine Strategic Initia-
tive of the Canadian Institute for Health Research
(CIHR), as well as by an individual grant from the
CIHR to S.R. M.M was funded by postdoctoral fel-
lowships from ERRSM, FQRNT, and CIHR.
Conflicts of interest
The authors declare no conflicts of interest.
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