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Learning Intermittent Strategy

substantial differences in neural control mechanisms between            mathematically modeled with a state predictor for compensating a
discrete and persistent (including rhythmic) movements [22].            feedback delay [38]. In this case, the anticipatory active feedback
                                                                        control that operates intermittently plays a key role for stabiliza-
   Here we critically reexamined the established theory of              tion, where the intermittency ensures the computational time for
impedance control as a stabilization strategy in a simple postural      the anticipation [39,40]. The third version considers open-loop
balancing task using a novel EMG-based human-computer                   periods (off-periods) representing a sensory dead-zone
interface. In this psychophysical experiment, we asked subjects         [41,42,43,44], in which a feedback control during the closed-loop
to balance a virtual inverted pendulum with physical parameter          periods (on-periods) with appropriate feedback gains is responsible
values of a typical human body. The pendulum was actuated by a          for stabilizing the pendulum. The fourth version is similar to the
pair of antagonist joint torques that were determined by                third one, and has been referred to as the ‘‘act-and-wait
activations of the corresponding pair of antagonist ankle muscles       control,’’by which a delay-induced unstable system can be
of subjects standing upright. Positional information of the             stabilized by an appropriate placement of finite number of poles,
pendulum was visually and continuously fed back to subjects             if the off-period is larger than the delay time [45,46,47]. The fifth
through a computer screen. The interface developed here                 version may be termed as the ‘‘noise-induced stabilization’’with a
provided a motor-task environment similar to stick balancing on         state-dependent multiplicative motor noise [23,25], which arises
a fingertip [23,24] or on a computer screen [25] as well as             when the delay-affected system is tuned at, or near, the edge of
balancing a virtual mass in an unstable force-field environment         stability and a critical control parameter is stochastically forced
using a manual planar robot [12,26]. These tasks typically lead to      back and forth across the boundary. The second to fourth (maybe
a common motor behavior in which subjects tend to simply keep           also the fifth) versions of the intermittent control consider that
track of the motion of the inverted pendulum, the stick or the          dynamics during the off-periods do not contribute much to the
mass. A novel experimental setup used in this study allowed us to       stability, but to producing intermittent behaviors. Therefore,
address the issue of whether subjects adopt impedance control for       although there might be connections among those versions of the
stabilizing the pendulum using antagonist muscles.                      intermittent control, the first version is a singularity in terms of the
                                                                        stabilization mechanism.
   The motor-task employed in this study raises an interesting
frustrated environment at adopting a motor strategy: On the one            A primary question in this study was whether or not at least
hand, a large feedback time delay in the sensorimotor loop, as a        some subjects adopted an intermittent control strategy. Moreover,
source of instability, might favor adopting the non-reactive,           if there were subjects adopted an intermittent control, which
preprogrammed impedance control, leading to a natural outcome           version of the intermittent control, among five versions listed
such that subjects adopted impedance control, because it does not       above, could better characterize the active control performed by
require subjects to react to a sequence of falling motions of the       those subjects and the corresponding dynamics of the controlled
pendulum, as traditionally hypothesized in the theory of human          pendulum?
postural control [27,28]. However, on the other hand, the known
difficulty of achieving tonic co-activation of antagonist ankle            As we show in this paper, it was remarkable that the majority of
muscles [29,30], might hinder subjects from adopting the                subjects controlling the virtual inverted pendulum adopted an
impedance control. Thus, we could also anticipate that an               intermittent stabilization strategy, and only small population of
alternative strategy aside from impedance control might emerge          subjects adopted an impedance-like control. Moreover, character-
under our experimental conditions. This study aimed at discov-          izations of temporal patterns of muscle inactivations and postural
ering how experimental subjects resolved this frustrated motor-task     sway of the pendulum showed that the intermittent strategy
environment through motor learning.                                     adopted by the subjects was consistent specifically with the one (the
                                                                        first version) that utilizes a stable manifold of saddle-type unstable
   Possible candidates for emerging strategies alternative to the       upright equilibrium in the absence of active feedback control
impedance control might be with either time-continuous or               (during the off-periods). Note that multiple strategies could be
discontinuous, intermittent controller. Note that the conventional      adopted by different experimental subjects for a single goal of
impedance control is the representative of the continuous control.      motor task, as pointed by Saha and Morasso [12].
A controller may or may not be established by acquiring a forward
model for state prediction to compensate the destabilizing effect of       Stochastic fluctuation is unavoidable during postural fixation.
feedback delay [8,9,11], which is often characterized experimen-        Intermittency during arm movement of manual tracking
tally by a decrease in reaction time through motor learning of          [12,26,48,49] and gaze fixation [50,51] has been reported. Those
anticipation. If subjects adopt a discontinuous, intermittent control   fluctuations, including during human standing and stick balancing,
strategy in particular, we might observe ‘‘on-periods’’ and ‘‘off-      often exhibit double power-law behaviors and/or non-Gaussian
periods’’ of time in activations of the antagonist muscles. In recent   Le´vy-like distribution associated with intermittency
years, a variety of (seemingly) different versions of the intermittent  [23,24,50,51,52]. There has been a growing interest in those
motor control have been proposed, mostly during balancing an            fluctuations whether they are associated with functional roles
inverted pendulum. The first version exploits the fact that the state   [50,51]. Since a goal of visuomotor tracking is to minimize the
point of the pendulum transiently approaches the upright position       tracking error, there might be another trade-off between stability
along a stable manifold of an unstable saddle-type equilibrium that     for minimizing the error and flexibility for reacting to motor
appears in off-periods during which the active feedback control         demands other than the goal of fixation as well as for reducing
(i.e. activation of the antagonist muscles) is turned off [31,32,33].   energetic cost. In this study, we also characterized stochastic sway
This version of intermittent control is effective if a mechanical       of the virtual inverted pendulum controlled by subjects in
plant in the absence of active control exhibits saddle-type             frequency domain, and showed that the postural sway of the
instability, as during pendulum balancing. It is characterized by       pendulum controlled by the intermittent strategy exhibited the
the fact that the unstable, but transiently converging saddle-type      power law behavior as reported by Collins and De Luca [52] and
dynamics during the off-periods are primarily responsible for           as predicted by a mathematical model of the intermittent control
stabilizing the pendulum, supplemented by the active feedback           [43,53]. Moreover, we showed that the intermittent control
control during the on-periods. The second version assumes               adopted by the majority of subjects was energetically more
anticipatory ballistic bais control [34,35,36,37], which has been

PLOS ONE | www.plosone.org                                              2 May 2013 | Volume 8 | Issue 5 | e62956
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