Vol.:(0123456789) 1 3
Experimental Brain Research
https://doi.org/10.1007/s00221-019-05520-3
RESEARCH ARTICLE
Contribution of corticospinal drive to ankle plantar flexor muscle
activation during gait in adults with cerebral palsy
Rasmus Feld Frisk
1,2,3
· Jakob Lorentzen
1,3
· Jens Bo Nielsen
1,3
Received: 27 August 2018 / Accepted: 13 March 2019
© Springer-Verlag GmbH Germany, part of Springer Nature 2019
Abstract
Impaired plantar flexor muscle activation during push-off in late stance contributes importantly to reduced gait ability in
adults with cerebral palsy (CP). Here we used low-intensity transcranial magnetic stimulation (TMS) to suppress soleus
EMG activity during push-off as an estimate of corticospinal drive in CP adults and neurologically intact (NI) adults. Ten CP
adults (age 34 years, SD 14.6, GMFCS I–II) and ten NI adults (age 33 years, SD 9.8) walked on a treadmill at their preferred
walking speed. TMS of the leg motor cortex was elicited just prior to push-off during gait at intensities below threshold for
motor-evoked potentials. Soleus EMG from steps with and without TMS were averaged and compared. Control experiments
were performed while standing and in NI adults during gait at slow speed. TMS induced a suppression at a latency of about
40 ms. This suppression was similar in the two populations when differences in control EMG and gait speed were taken into
account (CP 18%, NI 16%). The threshold of the suppression was higher in CP adults. The findings suggest that corticospinal
drive to ankle plantar flexors at push-off is comparable in CP and NI adults. The higher threshold of the suppression in CP
adults may reflect downregulation of cortical inhibition to facilitate corticospinal drive. Interventions aiming to facilitate
excitability in cortical networks may contribute to maintain or even improve efficient gait in CP adults.
Keywords Cerebral palsy · Corticospinal drive · Plantar flexor muscles · Push-off
Introduction
Cerebral palsy (CP) is caused by a non-progressive lesion of
the developing brain primarily characterized by disordered
movement and posture (Graham et al. 2016). Gait impair-
ment has a crucial impact on physical independence, social
participation and quality of life in adults with CP (Anders-
son and Mattsson 2001; Jahnsen et al. 2004; Morgan and
McGinley 2014; Verschuren et al. 2018).
Common gait characteristics in persons with CP are
reduced gait speed, reduced and asymmetrical step length
with increased energy expenditure (Winters et al. 1987;
Roche et al. 2014; Morgan et al. 2016). Weak plantar flexor
muscles have been found to be associated with impaired
propulsive force and reduced gait speed in both children
(Olney et al. 1990; Barber et al. 2017) and adults with CP
(Riad et al. 2012; Roche et al. 2014). Propulsion is gen-
erated during the push-off phase in late stance of the gait
cycle, where force generated by plantar flexor muscles is
transferred to the ground propelling the body upward and
forward (Winters et al. 1987; Neptune et al. 2001; Honeine
et al. 2014). The neural drive to the plantar flexors is the
result of integration of the input to spinal motor neurons
from a number of different sources all of which may poten-
tially be affected in CP. Transmission in specific spinal
pathways contributes to the coordination of muscle activity
during movement, including gait, and have been shown to be
impaired in adults with CP (Achache et al. 2010). Sensory
feedback mechanisms, which contribute to the activation of
the motor neurons during gait, have also been found to be
impaired in persons with CP (Willerslev-Olsen et al. 2014;
Frisk et al. 2017). This likely reflects that sensory feedback
is not sufficiently integrated with central motor commands to
generate an efficient muscle activation at push-off (Nielsen
2002, 2003). Among the descending pathways, the corti-
cospinal tract has received the most interest because of its
* Rasmus Feld Frisk
frisk@sund.ku.dk
1
Institute of Neuroscience, University of Copenhagen,
Blegdamsvej 3, 2200 Copenhagen N, Denmark
2
Professionshøjskolen Absalon, Roskilde, Denmark
3
Elsass Institute, Charlottenlund, Denmark