Short-term plasticity of human spinal inhibitory circuits after isometric and isotonic ankle...

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: [email protected];

[email protected]

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


123

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


123


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


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).


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.


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


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


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


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


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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Short-term plasticity of human spinal inhibitory circuits after isometric and isotonic ankle...

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