1 3
Exp Brain Res
DOI 10.1007/s00221-015-4281-1
RESEARCH ARTICLE
More gain less pain: balance control learning shifts the activation
patterns of leg and neck muscles and increases muscular
parsimony
Pierpaolo Iodice
1
· Stefano Cesinaro
2
· Gian Luca Romani
2
· Giovanni Pezzulo
1
Received: 20 October 2014 / Accepted: 6 April 2015
© Springer-Verlag Berlin Heidelberg 2015
deploy postural adjustments just-in-time and to transfer at
least part of the control of posture from anticipatory to less-
demanding feedback-based strategies. In turn, this strat-
egy shift increases the cost-efficiency of muscular activity,
which is a key signature of skilled performance.
Keywords Anticipatory control · Feedback control ·
Skill learning · Expertise · Balance
Introduction
Maintaining stable upright posture in spite of various dis-
turbances, such as those faced by skaters or surfers, is a
hard task that requires the precise coordination of multiple
muscles and the integration of various information streams
from afferent visual, somatosensory, and vestibular systems
within a unified “postural schema” (Bronstein 1986; Holmes
and Spence 2004; Iodice et al. 2015; Massion 1992; Pezzulo
et al. 2013). Developing such an expert skill requires the
progressive adjustment of the patterns of motor commands
regulating movement generation and an improved temporal
and spatial synchronization of muscular contractions. This,
in turn, requires coordinated learning processes across the
central nervous system and the musculoskeletal system.
The central nervous system (CNS) uses two main strate-
gies to maintain and restore balance: feedforward control,
which consists in executing anticipatory postural adjust-
ments (APA) prior an expected body disturbance (Mas-
sion 1992) and feedback control, which consists in execut-
ing compensatory postural adjustments (CPA) initiated by
sensory feedback signals after the disturbance (Alexandrov
et al. 2005). Several studies have assessed the importance
of these two control systems for skilled performance, but it
is still incompletely known how they interact and how their
Abstract Athletes such as skaters or surfers maintain
their balance on very unstable platforms. Remarkably, the
most skilled athletes seem to execute these feats almost
effortlessly. However, the dynamics that lead to the acquisi-
tion of a defined and efficient postural strategy are incom-
pletely known. To understand the posture reorganization
process due to learning and expertise, we trained twelve
participants in a demanding balance/posture maintenance
task for 4 months and measured their muscular activity
before and after a (predictable) disturbance cued by an
auditory signal. The balance training determined signifi-
cant delays in the latency of participants’ muscular activity:
from largely anticipatory muscular activity (prior to train-
ing) to a mixed anticipatory–compensatory control strategy
(after training). After training, the onset of activation was
delayed for all muscles, and the sequence of activation sys-
tematically reflected the muscle position in the body from
top to bottom: neck/upper body muscles were recruited first
and in an anticipatory fashion, whereas leg muscles were
recruited after the disturbance onset, producing compensa-
tory adjustments. The resulting control strategy includes a
mixture of anticipatory and compensatory postural adjust-
ments, with a systematic sequence of muscular activation
reflecting the different demands of neck and leg muscles.
Our results suggest that subjects learned the precise tim-
ing of the disturbance onset and used this information to
* Giovanni Pezzulo
giovanni.pezzulo@istc.cnr.it
1
Institute of Cognitive Sciences and Technologies,
National Research Council, Via S. Martino della Battaglia,
44 - 00185 Rome, Italy
2
Department of Neuroscience, Imaging and Clinical Sciences,
Institute for Advanced Biomedical Technologies,
G. D’Annunzio University, Chieti, Italy