Motor Control, 2015, 19, 135-141

http://dx.doi.org/10.1123/mc.2014-0055
2015 Human Kinetics, Inc.

COMMENTARIES

Neural Control of Hand Movements

Monica A. Perez
University of Pittsburgh
Most of our daily actions involve movements of the hand. The neuronal pathway
contributing to the control of hand movements are complex and not yet completely
understood. Recent studies highlight how task-dependent changes in cortical and
subcortical pathways driven by contralateral and ipsilateral influences may open
avenues to further understand the complexity of hand actions in healthy and
disease. In the following section studies using transcranial magnetic and electrical
stimulation in healthy subjects and in individuals with chronic incomplete spinal
cord injury will be highlighted to further understand neuronal pathways involved
in the control of voluntary activity by hand muscles.
Keywords: voluntary contraction, corticospinal drive, spinal motoneurons, primary
motor cortex, precision grip, spinal cord injury

The neural control of precision hand movements has been associated with
the contribution of the primary motor cortex (M1) and the corticospinal system
(for review see Lemon, 2008). Electrophysiological studies in primates showed
that monosynaptic corticomotoneuronal cells are significantly active during tasks
requiring fractionated digit movements (Buys et al., 1986; Bennett & Lemon,
1996). Lesions of the M1 or the corticospinal tract at the brainstem level impaired
dexterous finger movements (Lawrence & Kuypers, 1968; Galea & Darian-Smith,
1997; Zaaimi et al., 2012; Hoogewoud et al., 2013). Studies also have shown
differences in the organization of rostral and caudal regions of the M1 based on
the distribution of corticomotoneuronal cells, which might have broad implications
for the generation and control of hand movements (Rathelot & Strick, 2006, 2009).
Most corticospinal tract neurons located in the rostral region of the M1 made
monosynaptic connections with interneurons in the intermediate region of the spinal
cord, whereas corticospinal tract neurons in the caudal region made monosynaptic
connections with motoneurons. It has been argued that the direct connection to
motoneurons might enable a more flexible and complex pattern of muscle activity
than less indirect inputs.
In humans, the contribution of the M1 and the corticospinal system to the
control of hand movements has been demonstrated in patients with damage to these
CNS structures which results in a reduced ability to perform individuated finger
movements (Lang and Schieber, 2003, 2004). Transcranial magnetic stimulation
The author is with the Dept. of Physical Medicine and Rehabilitation, University of Pittsburgh, Pittsburgh, PA. Address author correspondence to Monica A. Perez at perezmo@pitt.edu.
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(TMS) has been employed for noninvasive and painless stimulation of the hand
representation of the M1 of intact and injured subjects through the scalp. TMS
has been used most extensively in the corticospinal system since the output of the
motor cortex can be easily assessed in the form of a motor evoked potential (MEP)
by using surface electromyographic (EMG) recording electrodes. Experimental
studies using TMS have suggested that both the M1 contralateral and ipsilateral
to a moving hand contribute to the generation of EMG responses in hand muscles
in a task-specific manner. For example, during unilateral voluntary contraction of
intrinsic finger muscles an increase in the amplitude of MEPs in finger muscles and
a decrease in the magnitude of short (SICI) and long (LICI) interval intracortical
inhibition compared with rest can be found (Wassermann et al., 1996; Ortu et al.,
2008; Kouchtir-Devanne et al., 2012). The changes in SICI and LICI suggest that
GABAergic activity is significantly weaker during voluntary activity compared
with rest, which may contribute to modulation of excitability of corticospinal
neurons involved in the intended movement. Interestingly, patients with chronic
incomplete cervical spinal cord injury (SCI) showed a descrease in SICI (probably
involving GABAA receptors) but not LICI (probably involving GABAB receptors)
during small levels of isometric voluntary contraction with intrinsic finger muscles
(Barry et al., 2013; Figure 1). The results from this study demonstrated that longterm use of baclofen selectively maintained activity of largely subcortical but not
cortical GABAergic neuronal pathways during voluntary activity involving finger
muscles after human SCI. Therefore, cortical GABAA circuits may be less sensitive
to baclofen than spinal GABAB circuits, which might to some extent contribute to
the limited effects of baclofen on voluntary motor output, including hand function,
in subjects with motor disorders affected by spasticity.
More recent studies proposed that subcortical neuronal networks also make
a significant contribution to the control of precision hand movements. Single
unit recordings in primates demonstrated that spinal interneurons exert postspike
effects in hand muscles during a precision grip in a task-dependent manner (Takei
& Seki, 2010, 2013). Lesions of the corticospinal tract at the cervical spinal cord
level showed in most cases complete recovery of the ability to grasp with the
index finger and thumb (Sasaki et al., 2004; Alstermark et al., 2011) which most
likely reflects central compensatory mechanisms underlying the recovery of finger
dexterity (for review see Isa et al., 2013). In agreement, a recent study demonstrated
that the control of precision grip in humans involves premotoneuronal subcortical
mechanisms, which are deficient in patients with SCI and restored by long-term use
of baclofen (Bunday et al., 2014). Thus, spinal GABAergic interneuronal circuits
might be part of the subcortical premotoneuronal network shaping corticospinal
output during human skilled hand actions. Spinal neuronal circuits, which can
rapidly translate and shape inputs and outputs according to behavioral contexts
(Cheney and Fetz, 1980; Prut and Perlmutter, 2003), might represent a critical
source for the control of skilled hand movements.
Evidence has shown that the M1 ipsilateral to a moving hand also contributes to
the control of hand movements. During unilateral isometric voluntary contraction of
intrinsic finger muscles, the excitability in the M1 that controls the resting hand changes
in a task-dependent manner (Stedman, Davey, & Ellaway, 1998; Muellbacher et al.,
2000; Perez & Cohen, 2008, 2009). A possible functional role of these interactions
is to suppress unwanted EMG activity in the resting limb through interhemispheric
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Figure 1 The effect of voluntary contraction of intracortical inhibition in healthy controls and patients with SCI. Short-interval intracortical inhibition
(SICI, A) and long-interval intracortical inhibition (LICI, B) were recorded at rest and during 25% of maximal voluntary contraction (MVC) of the first
dorsal interosseous muscle. Traces show MEPs elicited at rest (top) and during 25% of MVC (bottom). Black and gray traces represent test MEP and conditioned MEP, respectively. Conditioning stimulation (black arrows) preceded test stimulation (gray arrows) by 2 ms for SICI and 100 ms for LICI. Note
that SICI was decreased during voluntary contraction compared with at rest in both healthy controls and in SCI patients. However, LICI was decreased
during voluntary contraction compared with at rest in healthy controls but not in SCI patients. (Modified with permission from Barry et al., 2013).

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Figure 2 Ipsilateral silent period (iSP) during movement execution. A, B. Raw traces
showing rectified EMG in representative subjects during iSP testing in self-paced and ballistic index finger (left traces) and elbow flexion (right traces) movements. Traces show the
average 40 trials tested with (gray traces) and without (black traces) TMS. Traces below
iSPs show the rectified EMG and angular displacement during each movement condition.
Vertical solid lines show the time of TMS during testing and vertical dashed lines show
onset and offset of the iSP. C, D. Group data (index finger task, n = 14, C; elbow task, n
= 11, D). The abscissa shows all conditions tested (self-paced and ballistic). The ordinate
shows the normalized iSP area. Note the increased in the iSP during ballistic index finger
and elbow movements compared with self-paced movements. Error bars indicate SEs. *p
< .05. (Modified with permission from Tazoe and Perez, 2013).
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Neural Control of Hand Movements 139

inhibitory pathways (Cincotta & Ziemann, 2008; Hbers et al., 2008; Beaul et al.,
2012). More recent results showed that during unilateral isotonic hand movements
the resting M1 contributes to modulate activity in the contralateral voluntarily
active hand also in a task-specific manner (Tazoe and Perez, 2013; Figure 2).
It has been shown that the contribution of transcallosal inhibition to ipsilateral
movements at different speeds is widespread and has a functional role during rapid
movements. Thus, at faster speeds transcallosal inhibition toward the moving hand
decreases in the preparatory phase, which might contribute to starting movements
rapidly. However, transcallosal inhibition toward the moving hand increases in the
execution phase, which may contribute to stopping the movement. It is argued that
transcallosal pathways enable signaling of the time of discrete behavioral events
during ipsilateral movements, which is amplified by the speed of the movement.
Importantly, the contribution of the ipsilateral M1 to modulate corticospinal
excitability in the resting hand is impaired in humans with chronic incomplete
SCI (Bunday & Perez, 2012; Bunday et al., 2013). In patients, strong voluntary
contraction of a hand muscle was able to increase the corticospinal output in the
contralateral resting hand, as in healthy controls, when the motoneurons for the hand
muscle tested were located above the injury. However this modulation was absent
in muscles at or within 5 segments below the injury and present in muscles beyond
5 segments below the injury. Importantly, crossed corticospinal facilitation was
aberrantly high in muscles distant (>15 segments) from the injury and accompanied
by increased motoneuronal excitability.
In summary, the neuronal pathways contributing to the generation and control
of hand movements are complex and involve cortical and subcortical structures from
the contralateral and ipsilateral sides. Studies points to the view that transmission
in pathways contributing to modulation of EMG activity in hand muscles changes
in a task-dependent manner, which emphasizes the need for a careful interpretation
when extrapolating results between different hand motor actions. Thus, a better
understanding of the modulation of pathways contributing to the control of motor
skills involving hand muscles may highlight new targets for recovery of the hand
function after CNS injury.

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