http://journal.frontiersin.org/Journal/10.3389/fnhum.2014.00518/full?
Penelope A. McNulty- 1Neuroscience Research Australia, Sydney, NSW, Australia
- 2School of Medical Sciences, UNSW Australia, Sydney, NSW, Australia
Introduction
Stroke is the leading cause of adult-acquired motor disability in developed countries (WHO, 2003).
The most common outcome after stroke, and the most common cause of
motor disability, is hemiparesis or weakness on the side of the body
contralateral to the stroke lesion (e.g., Chang et al., 2013).
Although the acute lesion is restricted to the brain, secondary
adaptive and maladaptive changes may contribute to hemiparesis. There
are four principal sites where such degeneration has the capacity to
contribute to muscle weakness: (i) cerebral diaschisis (Feeney and Baron, 1986); (ii) reduced corticospinal tract integrity (Fries et al., 1993; Pineiro et al., 2000; Sterr et al., 2010; Stinear et al., 2012); (iii) changes to peripheral motor axon properties (Jankelowitz et al., 2007; Huynh et al., 2013);
and (iv) anatomical and physiological changes within the muscle and its
constituent single motor units. This study will consider single motor
unit discharge behavior.
There are both anatomical and physiological changes
within the muscles of the more-affected side after stroke. The
anatomical changes may include disuse atrophy (Jørgensen and Jacobsen, 2001; Ryan et al., 2002; Hara et al., 2004; Arasaki et al., 2006; Li et al., 2011); altered muscle phenotype (Jakobsson et al., 1991; De Deyne et al., 2004; Lukács et al., 2008; McKenzie et al., 2009); and reinnervation (Dattola et al., 1993; Hara et al., 2004; Lukács, 2005).
Physiological changes include altered motoneuron pool activation so
that there is a reduction in the mean motor unit discharge rate and the
variability of this discharge (Rosenfalck and Andreassen, 1980; Dietz et al., 1986; Gemperline et al., 1995; Chou et al., 2013);
disrupted recruitment threshold (including lower recruitment
thresholds, reversed recruitment thresholds so that fast motor units are
recruited before slower motor units, and a reduced range over which
recruitment occurs), reduced modulation of firing rates, and compression
of the dynamic range of motor unit discharge rates (Rosenfalck and Andreassen, 1980; Gemperline et al., 1995; Hu et al., 2012; Chou et al., 2013).
Such changes contribute not only to hemiparesis, but also to reduced
control of muscles on the more-affected side after stroke.
Single motor units are the smallest functional division
of muscles. They represent the most distal component of the motor
pathway and their discharge behavior reflects the intrinsic properties
of both the motoneuron and the muscle fibers in addition to the net
synaptic drive through this pathway. Recent data from our group recorded
during post-stroke therapy demonstrated that the activity of isolated
single motor units in severely paretic muscles precedes the development
of compound muscle activity (i.e., multiple motor units recruited
through voluntary commands), and that this progression is a hallmark of
improved movement ability, even many years post-stroke (see McNulty et al., 2013; Thompson-Butel et al., 2013).
To understand the process of recovery from isolated single motor unit
activity to compound activity during dynamic movements it is simpler to
begin with more controlled static tasks so that changes in the
properties of single motor units, and the mechanisms controlling this
behavior, can be investigated more systematically. The aim of this study
was to examine the pattern of motor unit behavior during sustained
static contractions.
The changes in motor unit discharge properties noted
above have been measured over brief periods, usually from 5–20 s with a
range of different tasks and levels of voluntary contraction. Each of
these differences may be sufficient to alter the net synaptic drive to
the motoneuron pool. For this reason, we extracted the action potentials
of single motor units that were either spontaneously active or
task-driven during a sustained isometric voluntary contraction at a
functionally relevant duration and force intensity during ankle
dorsiflexion, wrist flexion and elbow flexion. Motor units were recorded
from both the more- and less-affected side after stroke and on both the
dominant and non-dominant side in healthy subjects. Motor unit activity
during contractions acting on three joints was studied because there
are anatomical and functional differences in the control of muscles in
the upper and lower limbs, and between proximal and distal muscles of
the upper-limb. These differences include different innervation ratios (Buchthal and Schmalbruch, 1980), more numerous monosynaptic corticospinal (Palmer and Ashby, 1992) or bilateral (Colebatch et al., 1990) projections, and differences in mean firing rates (Petajan and Philip, 1969; de Luca, 1985).
These differences are superimposed on functional recovery after stroke
that is typically greater for the lower-limb than for the upper-limb
although the reason for this is not clear. To ensure the results of this
study do not simply reflect the differences listed here, data were
collected during contractions at three joints. We compared differences
in firing rates and the variability of the firing rate between sides and
between the upper and lower limb. Data were recorded during elbow
flexion from stroke subjects only to examine the effect of hand
dominance on the control of motor unit behavior after stroke. Our
results suggest that although motor units on the more-affected side have
a reduced firing rate compared to the less-affected side as reported
previously, the important difference is that the firing rate of motor
units on the less-affected side after stroke is higher than both the
more-affected side and motor units of healthy subjects.
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