Post on 27-Apr-2023
ORIGINAL ARTICLE
Short-term plasticity of human spinal inhibitory circuitsafter isometric and isotonic ankle training
Traci Jessop • Alyssa DePaola • Lauren Casaletto •
Chaya Englard • Maria Knikou
Received: 15 February 2012 / Accepted: 29 May 2012 / Published online: 9 June 2012
� Springer-Verlag 2012
Abstract The purpose of this study was to determine to
what extent one session of isotonic and isometric ankle
dorsi and plantar flexion training induces changes in the
frequency-dependent depression of the soleus H-reflex.
Further, adaptation of reciprocal Ia inhibition exerted from
tibialis anterior flexor group I afferents on soleus moto-
neurons, and presynaptic inhibition of Ia afferent terminals
induced by a conditioning afferent volley following stim-
ulation of the antagonist nerve were established with sub-
jects seated before and after training. The soleus H-reflexes
evoked at the inter-stimulus intervals of 1, 2, 3, 5, and 8 s
were normalized to the mean amplitude of the H-reflex
evoked every 10 s. Conditioned H-reflexes were normal-
ized to the associated control H-reflex evoked with subjects
seated before and after training. Twenty-six subjects were
randomly assigned to one or more of the 4 exercise groups.
Isometric ankle dorsi flexion training decreased the reci-
procal and presynaptic inhibition, while isotonic ankle
dorsi flexion had no significant effects. Isotonic plantar
flexion training decreased only the reciprocal inhibition,
whilst isometric plantar flexion had no significant effects
on the reciprocal or presynaptic inhibition. None of the
training exercise protocols affected the amount of homo-
synaptic depression of the soleus H-reflex. Our findings
support the notion that plastic changes of reciprocal and
presynaptic inhibition due to exercise are transferrable to a
resting state, and that homosynaptic depression remains
unaltered after a single session of ankle training. Further
research is needed to outline the time-course of plastic
changes of spinal inhibitory mechanisms in humans.
Keywords H-reflex � Human � Homosynaptic
depression � Neural plasticity � Randomized exercise �Reciprocal inhibition � Presynaptic inhibition � Ankletraining
Introduction
Activity-dependent neural plasticity accounts for the
development or preservation of motor behavior and
improvement of motor performance (Wolpaw 2007, 2010).
Neural circuits have the ability to alter their structure and
function in response to motor training (Adkins et al. 2006),
and reorganize simultaneously at multiple sites of the
central nervous system (Wolpaw and Tennissen 2001).
Various training protocols in humans induce reorgani-
zation of spinal neural excitability. For example, 30-min
ankle co-contraction training decreased the ratio of maxi-
mal H-reflex versus maximal M-wave (Hmax/Mmax), and
Communicated by Fausto Baldissera.
T. Jessop � A. DePaola � L. Casaletto � C. Englard �M. Knikou (&)
Department of Physical Therapy, Graduate Center,
College of Staten Island, City University of New York,
2800 Victory Blvd, Bldg 5N-207, Staten Island, NY 10314, USA
e-mail: Maria.Knikou@csi.cuny.edu;
m-knikou@northwestern.edu
URL: http://www.smpp.northwestern.edu/research/eagp/
M. Knikou
Sensory Motor Performance Program,
Rehabilitation Institute of Chicago, Chicago, IL, USA
M. Knikou
Physical Medicine and Rehabilitation, Feinberg School
of Medicine, Northwestern University, Chicago, IL, USA
M. Knikou
Electrophysiological Analysis of Gait and Posture Laboratory,
345 East Superior Street, Suite 1406, Chicago, IL 60611, USA
123
Eur J Appl Physiol (2013) 113:273–284
DOI 10.1007/s00421-012-2438-1
improved motor performance defined as the difference
between the maximum and minimum torque displacements
within 1 min (Perez et al. 2007). Three-week maximal
isometric plantar flexion training enhanced the soleus
H-reflex amplitude measured at 20 and 60 % of maximal
voluntary contraction (MVC) (Holterman et al. 2007),
while no changes were observed when reflexes were
measured with subjects at rest (Holterman et al. 2007).
Similar results were reported after 14-week resistance
training that involved heavy weight-lifting exercises for the
leg muscles with reflexes measured during maximal iso-
metric ramp contractions (Aagaard et al. 2002), whilst 18
sessions eccentric strength training for 7-week increased
the Hmax/Mmax ratio during eccentric MVC but not during
isometric or concentric contractions (Duclay et al. 2008).
In the aforementioned studies, changes in H-reflex ampli-
tude after training were measured during voluntary con-
traction which affects the excitability of spinal cord
circuitries (Nielsen and Kagamihara 1992, 1993). Changes
in H-reflex amplitude after training can result from modi-
fications of interneurons interposed in the spinal pathway
(Knikou 2008). Thus, it is logical to ask whether neural
adaptation in response to motor training is evident in spinal
interneuronal circuits and if this adaptation is transferred to
a resting state.
The disynaptic reciprocal Ia inhibition and presynaptic
inhibition of Ia afferents constitute major spinal interneu-
ronal circuits that contribute significantly to the neural
control of movement. Reciprocal Ia inhibition has been
described in detail through intracellular recordings (Eccles
et al. 1956) and involves one interneuron (Ia inhibitory
interneuron) that is under descending control (Hongo et al.
1969; Lundberg and Voorhoeve 1962). In addition, reci-
procal Ia inhibition is influenced by other spinal inhibitory
interneurons (Hultborn et al. 1971) and segmental afferents
of multimodal origin (Crone and Nielsen 1994; Jankowska
1992). Presynaptic inhibition of Ia afferents is accompa-
nied by primary afferent depolarization (PAD) and caused
by axo-axonal gamma-aminobutyric synapses that reduces
the size of the presynaptic impulse leading to decreased
liberation of excitatory transmitters and consequently a
decrease in monosynaptic transmission of Ia afferents
(Rudomin and Schmidt 1999). Presynaptic inhibition is
also prone to descending influences (Jankowska 1992;
Meunier and Pierrot-Deseilligny 1998). Repetitive activa-
tion of Ia afferents induces a neuronal phenomenon known
as homosynaptic or post-activation depression, ascribed to
a presynaptic inhibitory mechanism (Hultborn et al. 1996).
Sources of this depression include decrease in the amount
of released neurotransmitters (Kuno 1964), depletion of
releasable vesicles, failure of action potential conduction at
axonal branches (Brody and Yue 2000), decrease of pre-
synaptic quantal size (Chen et al. 2004), and adaptation of
exocytosis machinery (Hsu et al. 1996). The frequency-
related depression of the Ia excitatory postsynaptic poten-
tials (EPSPs) in humans has been attributed to similar
mechanisms as those documented in animals (Crone and
Nielsen 1989; Hultborn et al. 1996; Kohn et al. 1997).
Nonetheless, recent evidence suggests that the source or
mechanisms underlying the frequency-dependent depres-
sion of Ia EPSPs in humans are in question (Raoul et al.
2012).
Limited evidence exists on the reorganization of reci-
procal Ia inhibition and presynaptic inhibition with motor
training in humans. Reciprocal inhibition was potentiated
after 12 sessions of ankle dorsi flexion strength training
when measured at the onset of ankle dorsi flexion but
remained unchanged when measured with subjects at rest
(Geertsen et al. 2008), and after 30-min of patterned tonic
stimulation of the common peroneal nerve (Perez et al.
2003). Following a visuo-motor skill task training that
involved a series of ankle dorsi and plantar flexion move-
ments, reciprocal inhibition remained unchanged while
presynaptic inhibition of Ia afferents was increased (Perez
et al. 2005).
Accordingly, the objectives of this study were to
determine to what extent one session of ankle training
induces changes in the homosynaptic depression of the
soleus H-reflex, reciprocal Ia inhibition exerted from flexor
group I afferents on soleus motoneurons, and presynaptic
inhibition of Ia afferent terminals. Electrophysiological
measurements were taken with subjects seated in order to
determine whether neural adaptation is transferrable to a
resting state. Subjects were assigned randomly to one of
four training protocols that involved bilateral isotonic and
isometric ankle dorsi and plantar flexion. We hypothesized
that spinal inhibition is potentiated after isotonic or iso-
metric dorsi flexion training and decreased after isotonic or
isometric plantar flexion.
Methods
Subjects
The experimental protocol was approved by the Graduate
Center/CUNY Institutional Review Board (IRB) commit-
tee (IRB 10-09-203-0135) and was conducted in compli-
ance with the 1964 Declaration of Helsinki. Each subject
signed an informed consent form before participating to the
study. Thirty-one experiments were performed in 26 sub-
jects free of any neuromuscular or orthopedic disorders
who were randomly assigned in one or more of the 4
training exercises. Subjects’ characteristics for each train-
ing protocol are summarized in Table 1. For subjects that
participated in more than one training protocol, the second
274 Eur J Appl Physiol (2013) 113:273–284
123
test was conducted 2 weeks after the first test. Subjects’
daily activity ranged from moderate to intense cardio,
dancing, weight lifting, and anaerobic or aerobic sports.
Surface electromyographic (EMG) recordings
Following standard skin preparation, bipolar surface EMG
electrodes (Bagnoli 8 system, Delsys Inc., MA, USA) with a
fixed inter-electrode distance were placed on the right soleus
(SOL), medial gastrocnemius (MG), tibialis anterior (TA),
and peroneus longus (PL) muscles. EMG surface electrodes
were secured with 3M Tegaderm transparent film. All EMG
signals were sampled at 2,000 Hz andwere filteredwith a cut-
off frequency of 20–1,000 Hz (1401 plus running Spike 2
software, Cambridge Electronic Design Ltd., UK).
Training protocol
Isotonic ankle training was conducted with subjects
standing and involved 50 continuous repetitions for each
set followed by 3-min rest period. Five sets were completed
(250 ankle movements in total). Subjects were asked while
standing to either dorsi flex (stand on their heels) or plantar
flex (stand on their metatarsals). In order to counteract
weight shift to the contralateral leg and thus asymmetrical
body posture as well as the effects of body instability on
the soleus H-reflex (Llewellyn et al. 1990), isotonic ankle
movements were performed in synchrony bilaterally.
Isometric training involved 20 repetitions with 5 s hold
time at each repetition. Each set was followed by a 2-min rest
and 5 sets were completed (100 isometric contractions in
total). Isometric ankle dorsi and plantar flexion were con-
ducted with subjects supine since isometric plantar flexion
during standing is not optimal. Subjects were asked to maxi-
mally push against the foot board or tomaximally pull against
a non-elastic band that was secured around the foot board.
Isometric contractions were conducted in synchrony bilateral
in order to be similar to isotonic protocols. Because isometric
contractions needed more time to be completed, the total
number of isotonic contractions was increased so that all
training protocols have a similar duration of time (Table 1).
Duration and number of repetitions for isometric and isotonic
contractions did not result in muscle fatigue (Kolosova and
Slivko 2006).
Electrophysiological tests and experimental protocol
All electrophysiological tests described below were con-
ducted before and after training with subjects seated (hip
angle 120�, knee angle 160�, ankle angle 110�), and both
feet supported by footrests.
A stainless steel electrode of 4 cm diameter (anode) was
placed proximal to the patella for selective stimulation of
the nerve trunk, while a stainless steel handheld monopolar
electrode (cathode) was used as a probe to determine the
most optimal stimulation site. The right posterior tibial
nerve at the popliteal fossa was stimulated with square
pulse stimuli of 1 ms duration delivered by a constant
current stimulator (DS7A, Digitimer Ltd., Hertfordshire,
UK). Site of stimulation was defined as the one during
which at low stimulation intensities Ia afferents could
selectively be excited without an M-wave being present in
the soleus muscle. When the stimulation site was identified,
the monopolar electrode was replaced by a permanent
electrode (N-10-A; Medicotest, Ølstykee, Denmark), and
soleus H-reflexes were evoked at low stimulation intensi-
ties to ensure a similar reflex expression compared to that
observed with the monopolar handheld electrode. Then, the
stimulating electrode was stabilized and held under con-
stant pressure throughout the experiment. The Mmax was
evoked and measured online. The stimulus intensity was
adjusted to evoke an H-reflex on the ascending part of the
soleus H-reflex recruitment curve that ranged from 20 to
40 % of the Mmax across subjects. Twenty soleus
H-reflexes were evoked at this stimulation intensity ran-
domly at the inter-stimulus intervals of 1, 2, 3, 5, 8, and
10 s.
The right common peroneal nerve was stimulated
according to methods previously utilized in humans (Kni-
kou 2011; Knikou and Mummidisetty 2011; Knikou and
Taglianetti 2006). A single shock of 1 ms duration, gen-
erated by a constant current stimulator (DS7A, Digitimer
Ltd., UK), was delivered with a bipolar stainless steel
electrode placed distal to the head of the fibula. The opti-
mal stimulation site was selected based on that the TA
motor threshold (MT) was lower than that of the peroneal
muscles, and at increased levels of stimulation intensities
ankle eversion and PL muscle activity were absent (Knikou
2005; Knikou and Taglianetti 2006). When the stimulation
Table 1 Participant characteristics
Isotonic dorsi flexion Isotonic plantar flexion Isometric dorsi flexion Isometric plantar flexion
Age ± SD 25.7 ± 2.68 26.5 ± 5.78 25.0 ± 1.54 24.6 ± 2.06
Gender and number of subjects 6 female 7 female 4 female 6 female
3 male 1 male 2 male 2 male
Duration of training (min; mean ± SD) 19.22 ± 2.68 22.35 ± 4.3 26.5 ± 4.96 26.6 ± 1.99
Eur J Appl Physiol (2013) 113:273–284 275
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site for the common peroneal nerve was identified, the
bipolar electrode was stabilized and secured with athletic
wrap. Single pulses were delivered at 0.2 Hz to determine
the TA MT and type of contraction (selective dorsi flexion)
at increased stimulation intensities.
Subsequently, the soleus Mmax was evoked, measured
online, and saved for offline analysis. Then, the stimulation
intensity to the posterior tibial nerve was adjusted in order
to evoke a control H-reflex on the ascending part of the
soleus H-reflex recruitment curve that ranged from 20 to
35 % of the Mmax while the associated M-wave ranged
from 2 to 6 % of the Mmax across subjects. Control and
conditioned H-reflexes were randomly evoked at 0.2 Hz.
For the conditioned H-reflexes, common peroneal nerve
stimulation was delivered at short (2, 3, and 4 ms) and long
(10, 20, 60, and 80 ms) C-T intervals. The soleus H-reflex
depression at these short and long C-T intervals is attrib-
uted to reciprocal Ia inhibition and presynaptic inhibition
of Ia afferent terminals by the conditioning afferent volley,
respectively (Crone et al. 1987; Faist et al. 1996; Capaday
et al. 1995). Across subjects, conditioning stimulation was
delivered at 1–1.3 TA MT. The TA and soleus M-waves
were monitored throughout the experiment to ensure con-
stancy of stimulation during control and conditioning reflex
recordings.
Surface EMG and stimulating electrodes were main-
tained in the same position during training. The same
experimental protocol outlined before for unconditioned
and conditioned H-reflexes was repeated after training,
while homosynaptic depression, reciprocal and presynaptic
inhibition were randomly recorded within and across sub-
jects. In order to compare the amount of reciprocal and
presynaptic inhibition after training to that observed before
training, for each subject, the stimulation intensity to the
posterior tibial and common peroneal nerves was adjusted
so that the unconditioned soleus H-reflexes and TA
M-wave after training is of similar amplitude to those
evoked before training.
Statistical analyses
The area under the full-wave rectified waveform (Spike 2,
CED Ltd., UK) was measured for each control H-reflex,
conditioned H-reflex, and M-wave (Knikou and Taglia-
netti 2006). For each subject, the soleus H-reflexes
(n = 20) evoked at the inter-stimulus intervals of 1, 2, 3,
5 and 8 s were expressed as a percentage of the H-reflex
evoked every 10 s before and after training because there
is no or little homosynaptic depression when the H-reflex
is elicited every 10 s. For each training protocol, the mean
amplitude of the normalized soleus H-reflex from each
subject was grouped based on the time (pre and post-
training) and inter-stimulus interval, and a one-way
ANOVA along with post hoc Bonferroni tests and an
ANOVA for repeated measures at 2 9 5 levels (2, time; 5,
inter-stimulus intervals) was conducted to establish sta-
tistically significant differences across inter-stimulus
intervals and changes in homosynaptic depression before
and after training, respectively.
For each subject, the conditioned soleus H-reflexes
(n = 20) recorded at short and long C-T intervals were
expressed as a percentage of the associated control
H-reflex. For each training protocol, the mean amplitude of
the normalized soleus H-reflex from each subject was
grouped based on the time (pre- and post-training) and
conditioning–test interval, and an ANOVA for repeated
measures at 2 9 3 levels (2, time; 3, C-T intervals) or at
2 9 4 levels (2, time; 4, C-T intervals) was conducted to
establish statistically significant differences before and
after training in reciprocal and presynaptic inhibition,
respectively. The same analysis was also conducted for the
M-waves, which were expressed as a percentage of the
Mmax. For each subject, the unconditioned (or control)
H-reflexes (n = 20) recorded before and after training were
expressed as a percentage of the Mmax. The mean nor-
malized unconditioned H-reflex from each subject was
grouped based on the time of training and a paired t test
was conducted between the normalized unconditioned
H-reflexes recorded before and after training. All statistical
tests were conducted at 95 % of confidence interval. Mean
amplitudes are reported along with the SEM.
Results
Adaptation of soleus H-reflex homosynaptic depression
by ankle training
In Fig. 1a, representative non-rectified waveform averages
(n = 20) of the soleus H-reflex evoked at all inter-stimulus
intervals tested are indicated for one subject (S26) before
and after training (isometric plantar flexion). The soleus
H-reflex amplitude was significantly decreased at short
inter-stimulus intervals when compared to that recorded at
long inter-stimulus intervals, but the H-reflex amplitudes
before training were not different to those recorded after
training. The normalized soleus H-reflex amplitude varied
significantly across the inter-stimulus intervals tested
(p\ 0.05) before and after training, supporting the pres-
ence of homosynaptic depression in the soleus H-reflex.
Soleus H-reflexes from all subjects in each training pro-
tocol at the inter-stimulus interval of 1 s were not statisti-
cally significant different from those evoked every 2 s
(p[ 0.05). This was the case for all protocols before and
after training but not for the isotonic plantar flexion in
which post hoc Bonferroni tests showed that the H-reflex
276 Eur J Appl Physiol (2013) 113:273–284
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evoked every 5 s was not significantly different from that
evoked every 8 s (p[ 0.05).
The overall (all subjects tested) amplitude of the soleus
H-reflex evoked at the inter-stimulus intervals of 1, 2, 3, 5
and 8 s as a percentage of the soleus H-reflex evoked every
10 s for all 4 protocols before and after training is shown in
Fig. 1b–e. No statistically significant difference in the
amount of soleus H-reflex depression at different stimula-
tion frequencies after isotonic dorsi flexion (Fig. 1b;
p = 0.87), isometric dorsi flexion (Fig. 1c; p = 0.43),
isotonic plantar flexion (Fig. 1d; p = 0.25), and isometric
plantar flexion (Fig. 1e; p = 0.43) training was found
compared to that observed before training.
Adaptation of reciprocal and presynaptic inhibition
by isotonic ankle dorsi flexion training
The adaptation of disynaptic reciprocal inhibition exer-
ted from TA group I afferents to soleus motoneurons and
presynaptic inhibition of soleus Ia afferents is indicated
for two subjects (subjects 16 and 6) in Fig. 2a. The
soleus H-reflexes recorded after training (solid lines) at
the C-T intervals of 3 and 10 ms were increased in
subject 16 and decreased in subject 6 when compared to
those observed before training (dashed lines). The con-
ditioned H-reflexes from all subjects tested at short C-T
intervals were not statistically significant different after
training compared to those observed before training
(Fig. 2b; p = 0.48). A similar result was found for the
conditioned H-reflexes recorded at the C-T intervals
that ranged from 10 to 80 ms (p = 0.21). The overall
amplitude of the control soleus H-reflex and M-wave as a
percentage of the Mmax is shown in Fig. 2c and d,
respectively. The control H-reflexes were not statistically
significant different before and after training (paired test,
p[ 0.05), a phenomenon that was apparent also on the
M-waves at short (p = 0.62) and long C-T intervals
tested (p = 0.57).
Fig. 1 Homosynaptic depression of soleus H-reflex after ankle
training. a Non-rectified waveform averages (n = 20) of soleus
H-reflexes evoked at different inters-stimulus intervals before and
after training from one subject. The overall (from all subjects of each
group) amplitude of the soleus H-reflexes evoked at the inter-stimulus
intervals of 1, 2, 3, 5, and 8 s is indicated before (dashed lines) and
after (solid lines) isotonic dorsi flexion (b), isometric dorsi flexion (c),isotonic plantar flexion (d), and isometric plantar flexion (e) training.On the abscissa the inter-stimulus interval is indicated for each
training protocol while the ordinate indicates the amplitude of the
H-reflexes as a percentage of the H-reflex evoked every 10 s. Errorbars represent the SEM
Eur J Appl Physiol (2013) 113:273–284 277
123
Adaptation of reciprocal and presynaptic inhibition
by isometric ankle dorsi flexion training
In Fig. 3a, non-rectified waveform averages (n = 20) of
the conditioned soleus H-reflexes recorded before (dashed
lines) and after (solid lines) training for one subject (S4)
are indicated for the C-T intervals of 2, 3, 60, and 80 ms. In
this subject, the conditioned H-reflexes after training were
increased compared to those observed before training. This
adaptation was not due to changes in the recruitment reflex
gain because the average control H-reflex after training
(32.5 ± 1.2 % of Mmax) was not significantly different
from the control H-reflex recorded before training
(29.4 ± 0.7 % Mmax) (p = 0.12) with the subject seated.
The overall amplitude of the conditioned soleus
H-reflexes from all subjects tested as a percentage of the
associated unconditioned (or control) soleus H-reflex
before and after isometric dorsi flexion training is shown in
Fig. 3b. A statistically significant difference was found
between the conditioned H-reflexes at short C-T intervals
after training compared to those observed before training
(p = 0.027). A similar result was found for the conditioned
H-reflexes recorded at long C-T intervals (p = 0.008). The
changes in the conditioned H-reflexes occurred with stable
Fig. 2 Reciprocal and presynaptic inhibition after isotonic ankle
dorsi flexion training. a Non-rectified waveform averages (n = 20) of
the conditioned H-reflexes recorded at the C-T intervals of 3 and
10 ms before (dashed lines) and after (solid lines) isotonic dorsi
flexion training for two subjects. The conditioned H-reflexes after
training were enhanced in subject 16 compared to that observed
before training, and were decreased in subject 6. b The overall
amplitude of the conditioned soleus H-reflex as a percentage of the
control H-reflex recorded before and after training is plotted against
the C-T interval tested indicated on the abscissa. c Overall (all
subjects tested in this group) mean amplitude of the control H-reflex,
as a percentage of the maximal M-wave, recorded before and after
training and utilized to normalize the associated conditioned
H-reflexes. d Overall amplitude of the M-wave, corresponding to
the conditioned H-reflexes shown in b, as a percentage of the maximal
M-wave for before and after training is plotted against the C-T
interval tested indicated on the abscissa. f indicates statistically
significant differences between the conditioned and the control
H-reflex recorded before training. Error bars indicate the SEM
278 Eur J Appl Physiol (2013) 113:273–284
123
M-waves before and after training at short (p = 0.39) and
long C-T intervals tested (p = 0.29) (Fig. 3c). The
unconditioned soleus H-reflexes, which were recorded with
subjects seated and used to normalize the conditioned
H-reflexes, reached an overall amplitude of 33.84 ± 3.3
and 26.9 ± 5.5 % of the Mmax before and after training,
respectively (Fig. 3d; paired t test, p = 0.15).
Adaptation of reciprocal and presynaptic inhibition
by isotonic ankle plantar flexion training
In Fig. 4a, non-rectified waveform averages (n = 20) of
soleus H-reflexes recorded before and after isotonic plantar
flexion training for two subjects (S3 and S11) are indicated
for short and long C-T intervals. The conditioned
H-reflexes were decreased in S3 and increased in S11 after
training when compared to those recorded before training.
The conditioned H-reflexes from all subjects at short C-T
intervals were statistically significant increased after
training compared to those observed before training
(p = 0.01) (Fig. 4b). In contrast, there was no statistically
significant difference in the conditioned H-reflexes recor-
ded at long C-T intervals after training compared to those
observed before training (p = 0.67) (Fig. 4b). The associ-
ated control soleus H-reflexes, which were recorded before
and after training and used to normalize the conditioned
H-reflexes, reached overall amplitude of 27.6 ± 2 and
24.7 ± 1.9 % (paired t test; p = 0.21) of the Mmax,
respectively (Fig. 4c). Lastly, the M-waves of the condi-
tioned H-reflexes were not statistically significant different
before and after training for the short (p = 0.39) and long
(p = 0.71) C-T intervals tested.
Adaptation of reciprocal and presynaptic inhibition
by isometric ankle plantar flexion training
In Fig. 5a, non-rectified waveform averages of the condi-
tioned soleus H-reflexes from one subject (S10) recorded at
the C-T intervals of 2, 3, 60, and 80 ms before (dashed
lines) and after (solid lines) isometric plantar flexion
training are indicated. The conditioned soleus H-reflex at
the C-T intervals of 2 and 3 ms reached overall amplitude
of 72.5 ± 4.5 and 71.6 ± 3.3 % of the control H-reflex
before training and 51.4 ± 4.9 and 59.4 ± 2.4 % of the
control H-reflex after training, suggesting potentiation of
reciprocal inhibition. In contrast, the conditioned soleus
H-reflex at the C-T intervals of 60 and 80 ms reached
overall amplitude of 52.1 ± 5.1 and 27.18 ± 1.07 % of the
control H-reflex before training and 71.4 ± 5.5 and
27.14 ± 2.7 % of the control H-reflex after training, sug-
gesting decreased or unaltered presynaptic inhibition. In
this subject, the control H-reflex before and after training
reached overall amplitude of 23.16 ± 1.07 and 19.3 ±
2.1 % of the Mmax.
Fig. 3 Reciprocal and presynaptic inhibition after isometric ankle
dorsi flexion training. a Non-rectified waveform average (n = 20) of
the conditioned H-reflex recorded at the C-T intervals of 2, 3, 60, and
80 ms before (dashed lines) and after (solid lines) isometric dorsi
flexion training from one subject. In this subject, the conditioned
H-reflexes were significantly enhanced after training compared to
those recorded before training (see text for more details). b The
overall amplitude of the conditioned soleus H-reflex as a percentage
of the control H-reflex recorded before and after training is plotted
against the C-T interval tested indicated on the abscissa. c Overall
amplitude of the M-wave, corresponding to the conditioned
H-reflexes shown in b, as a percentage of the maximal M-wave for
before and after training is plotted against the C-T interval tested
indicated on the abscissa. d Overall (all subjects tested in this group)
mean amplitude of the control H-reflex recorded before and after
training and utilized to normalize the associated conditioned
H-reflexes as a percentage of the maximal M-wave. Asterisks indicatestatistically significant differences between the conditioned H-reflexes
recorded before and after training, while f indicates statistically
significant differences between the conditioned and the control
H-reflex recorded before training. Error bars indicate the SEM
Eur J Appl Physiol (2013) 113:273–284 279
123
The overall amplitude of the conditioned soleus
H-reflexes from all subjects tested as a percentage of the
unconditioned (or control) soleus H-reflex before and after
isometric plantar flexion training is indicated in Fig. 5b. No
statistically significant difference in the conditioned
H-reflexes at short (p = 0.13) and long (p = 0.2) C-T
intervals was found after training. The control H-reflexes,
which were recorded before and after training and used to
normalize the conditioned H-reflexes, were not signifi-
cantly different (before training, 25.8 ± 2.3 % of the
Mmax; after training, 22.01 ± 2.89 % of the Mmax). Fur-
thermore, the conditioned H-reflexes were recorded at
constant M-wave amplitudes at short and long C-T inter-
vals (short C-T: p = 0.69 and long C-T: p = 0.4)
(Fig. 5d).
Discussion
This study investigated short-term plastic changes in the
homosynaptic depression of the soleus H-reflex, reciprocal
Ia inhibition, and presynaptic inhibition of soleus Ia
afferent terminals after isotonic and isometric ankle dorsi
and plantar flexion training. Subjects did not have to learn
to perform the ankle movements as the exercises utilized in
this study were simple and existed within the repertoire of
movements. None of the exercise training protocols
affected the amount of homosynaptic depression of the
soleus H-reflex (Fig. 1). After one cycling session the
homosynaptic depression increases and the soleus H-reflex
amplitude decreases (Mazzocchio et al. 2006; Meunier
et al. 2007). During cycling, subjects had to establish a
constant cycling speed on a recumbent bicycle despite
frequent changes in pedal resistance that required cali-
brated locomotor compensatory actions (Mazzocchio et al.
2006; Meunier et al. 2007). These along with our findings
support the notion that difficulty of the trained motor task
and likely the duration of training are critical for potenti-
ation of homosynaptic depression. Thus, these factors
should be taken into consideration when the aim is to
restore decreased homosynaptic depression, as is the case
in neurological disorders.
Reciprocal inhibition was decreased after one session of
isometric ankle dorsi flexion and isotonic plantar flexion
training, and remained unchanged after isometric plantar
flexion and isotonic dorsi flexion training, in contrast to our
hypothesis. Reciprocal inhibition is increased or decreased
during tonic voluntary ankle dorsi flexion and is decreased
Fig. 4 Reciprocal and presynaptic inhibition after isotonic ankle
plantar flexion training. a Non-rectified waveform averages (n = 20)
of the conditioned H-reflexes recorded at the C-T intervals of 2, 3, 60,
and 80 ms before (dashed lines) and after (solid lines) isotonic plantarflexion training from two representative subjects. In subject 3, the
conditioned H-reflex at short and long C-T intervals was more
depressed compared to that observed before training, while in subject
11 an opposite effect was observed. b Overall amplitude of the
conditioned soleus H-reflex as a percentage of the control H-reflex
recorded before and after training. The C-T interval tested is indicated
on the abscissa. c Overall amplitude of the control soleus H-reflex as a
percentage of the maximal M-wave before and after training.
d Overall amplitude of the M-wave as a percentage of the maximal
M-wave at each C-T interval tested before and after training.
Asterisks indicate statistically significant differences between the
conditioned H-reflexes recorded before and after training, while
f indicates statistically significant differences between the conditionedand the control H-reflex recorded before training. Error bars indicatethe SEM
280 Eur J Appl Physiol (2013) 113:273–284
123
during tonic plantar flexion or as plantar flexion increases
(Crone et al. 1987; Nielsen et al. 1992; Petersen et al. 1998)
while the amount of reciprocal inhibition depends on the
prior physical activity of the participants with more reci-
procal inhibition to be present in physically active subjects
(Crone et al. 1985).
Activity-dependent plasticity of reciprocal inhibition in
humans remains largely unknown. Reciprocal inhibition
increases after 12 sessions of ankle dorsi flexion isometric
training when measured at the onset of ankle dorsi flexion
but remained unchanged when measured with subjects at
rest (Geertsen et al. 2008). In addition, reciprocal inhibition
remained unchanged after 8 sessions of visuo-motor skill
training (Perez et al. 2005). These findings suggest that
short-term training does not affect the amount of reciprocal
inhibition. Nonetheless, the amount of reciprocal inhibition
was adjusted after one session of ankle training, a phe-
nomenon that was observed with subjects at rest and not
during ankle tonic contraction. Reciprocal inhibition was
decreased after isometric dorsi flexion and isotonic plantar
flexion training, while in some individuals potentiation of
reciprocal inhibition was also evident (Figs. 2a, 4a, 5a).
The differential effect may be related to the participants’
weekly physical activity, which significantly affects the
baseline reciprocal Ia inhibition (Crone et al. 1985). This
implies that plastic changes of reciprocal inhibition due to
motor training may be different based on the amount and
type of physical activity that a participant is engaged.
The observed decreased reciprocal Ia inhibition cannot
be attributed to changes in the recruitment gain of the
soleus motoneurons because the control H-reflex recorded
after training was not significantly different from the con-
trol H-reflex recorded before training (Figs. 2c, 3d, 4c, 5c),
both elicited on the ascending part of the H-reflex
recruitment curve and with subjects seated. Further, a
constant number of soleus Ia afferents were excited as
evident by the stable M-waves recorded before and after
training (Figs. 2d, 3c, 4d, 5d) (Boorman et al. 1996). We
thus theorize that the observed adaptation may reflect the
initial stage of activity-dependent plasticity of the
Fig. 5 Reciprocal and
presynaptic inhibition after
isometric ankle plantar flexion
training. a Non-rectified
waveform averages (n = 20) of
the conditioned H-reflexes
recorded at the C-T intervals of
2, 3, 60 and 80 ms before
(dashed lines) and after (solidlines) training from one subject.
The conditioned H-reflexes after
training were significantly
decreased compared to that
observed before training.
b Overall amplitude of the
conditioned soleus H-reflex as a
percentage of the control
H-reflex before and after
training. The C-T intervals
tested are indicated on the
abscissa. c Overall amplitude of
the control soleus H-reflex as a
percentage of the maximal
M-wave before and after
training. d Overall amplitude of
the M-wave as a percentage of
the maximal M-wave at each
C-T interval tested before and
after training. f indicatesstatistically significant
differences between the
conditioned and the control
H-reflex recorded before
training. Error bars indicate the
SEM
Eur J Appl Physiol (2013) 113:273–284 281
123
reciprocal inhibitory pathway and further research is nee-
ded to outline its time-course.
At this point we should consider the possibility that
reciprocal Ia inhibition was affected by contralateral seg-
mental afferent fibers. It has been shown that contralateral
arm movements increase the reciprocal Ia inhibition in
humans (Delwaide et al. 1988; Baldissera et al. 1987),
while contralateral primary afferents and flexion reflex
afferents facilitate actions of Ia inhibitory interneurons in
humans and low-spinal cat (Delwaide and Pepin 1991;
Harrison and Zytnicki 1984; Hultborn et al. 1976a, b).
Thus, Ia inhibitory interneurons may have received facili-
tatory or inhibitory inputs from the contralateral leg during
training. It remains to be determined whether a similar
adaptation of the reciprocal Ia inhibition is evident when
motor training involves only the ipsilateral leg.
Modulation in the amount of presynaptic inhibition
acting on the synapses between Ia afferents and a moto-
neurons is evident in a plethora of motor tasks and
movement patterns including but not limited to ipsilateral
or bilateral rhythmical active or passive leg movements
(Knikou 2011; Knikou and Rymer 2002), passive ankle
dorsi flexion (Morita et al. 2001), standing (Katz et al.
1988), and walking (Capaday and Stein 1987; Morin et al.
1982). Further, presynaptic inhibition of Ia terminals
directed to the contracting motoneuron pool is decreased
approximately 50 ms before muscle contraction attributed
to descending drive (Nielsen and Kagamihara 1993).
Limited evidence exists on the activity-dependent plasticity
of presynaptic inhibition. Presynaptic inhibition increased
after 8 sessions of voluntary ankle dorsi and plantar flexion
movements that required subjects to follow a cursor on a
computer screen while subjects were performing these
movements (Perez et al. 2005). The soleus H-reflex facil-
itation during the mid-swing phase of backward walking
was decreased after daily backward walking training
(Schneider and Capaday 2003), a phenomenon ascribed to
progressive increase of presynaptic inhibition (Ung et al.
2005). These findings suggest that action of presynaptic
inhibitory interneurons, which decreases monosynaptic
excitation of a motoneurons by Ia afferent inputs, is
magnified when movement requires accuracy. This is
consistent with the reduced soleus H-reflex after one ses-
sion of repeated short bouts of balance maintenance on an
unstable platform (Trimble and Koceja 1994) and reduced
Hmax/Mmax ratio in ballet dancers (Nielsen et al. 1993),
reflecting an increase in presynaptic inhibition of Ia affer-
ents as a result of reciprocal inhibition mechanisms asso-
ciated with co-contraction of the ankle antagonistic
muscles.
In this study, presynaptic inhibition was decreased
immediately after one session of isometric ankle dorsi
flexion training (Fig. 3b), and remained unchanged after
isotonic dorsi-plantar flexion (Figs. 2b, 4b) and isometric
plantar flexion (Fig. 5b) training. The V-wave and H-reflex
amplitudes were increased during maximal isometric ramp
contractions after resistance training, attributed to potenti-
ation of cortical motor drive and altered cortical control of
presynaptic inhibition (Aagaard et al. 2002). Decreased
presynaptic inhibition accounts for the increased soleus
H-reflexes observed after hopping training (Voigt et al.
1998). Thus, we theorize that the effects observed here
might have been driven by potentiation of corticospinal
drive because PAD interneurons in human lumbar spinal
cord are under descending inhibition (Iles 1996; Meunier
and Pierrot-Deseilligny 1998). However, repetitive execu-
tion of a simple movement in absence of motor skill
acquisition in monkeys and humans resulted in nonsub-
stantial changes in primary motor cortex (M1) movement
representations (Plautz et al. 2000; Carroll et al. 2002) and
changes in cortical representation after repetitive-unskilled
movements returned to baseline within a few minutes after
training stopped (Classen et al. 1998). Thus, simple
movements without environmental constraints or motor
skill learning may not be sufficient to alter corticospinal
drive and thus cortical control of presynaptic inhibition.
However, we cannot rule out the possibility that the
reduced reciprocal and presynaptic inhibition was mediated
by released tonic descending inhibitory action of Ia and
PAD interneurons as a result of training.
Functional significance of findings
Isometric ankle dorsi flexion training decreased the reci-
procal and presynaptic inhibition, while isotonic ankle
dorsi flexion did not have any significant effects. Further-
more, isotonic plantar flexion decreased the reciprocal
inhibition, while isometric plantar flexion had no signifi-
cant effects in spinal inhibitory mechanisms. Although the
source of this neural adaptation cannot be defined based on
the current experimental methods, the decreased reciprocal
and presynaptic inhibition we observed here immediately
after training may reflect the initial stage of activity-
dependent plasticity of these spinal interneuronal circuits
(Wolpaw and O’Keefe 1984). The amount of homosy-
naptic depression of the soleus H-reflex was not affected by
any of the training exercise protocols, suggesting that
adaptation of homosynaptic depression may depend on the
duration, type, and amount of training. These factors need
to be defined so appropriate training protocols can be uti-
lized for cases that homosynaptic depression is impaired.
Acknowledgments Authors thank all participants for their volun-
tary participation to the study. This work was supported in part by
the New York State Department of Health (NYSDOH)/Contract
No. C023690, Wadsworth Center, NY, USA. The funding source
282 Eur J Appl Physiol (2013) 113:273–284
123
had no involvement in study design, collection, analysis, or data
interpretation.
Conflict of interest The authors have no conflicts of interest to
report.
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