http://journal.frontiersin.org/article/10.3389/fnhum.2015.00293/full?utm_source=newsletter&utm_medium=email&utm_campaign=Neurology-w35-2015
Trudy A. Pelton
Dagmar Fraser- 1School of Psychology, College of Life and Environmental Sciences, University of Birmingham, Edgbaston, UK
- 2School of Health Sciences, Faculty of Health and Medicine, The University of Newcastle, Callaghan, NSW, Australia
- 3Hunter Medical Research Institute, The University of Newcastle, Callaghan, NSW, Australia
Background: The differential contributions of
the cerebellum and parietal lobe to coordination between hand transport
and hand shaping to an object have not been clearly identified.
Objective: To contrast impairments in
reach-to-grasp coordination, in response to object location
perturbation, in patients with right parietal and cerebellar lesions, in
order to further elucidate the role of each area in reach-to-grasp
coordination.
Method: A two-factor design with one between
subject factor (right parietal stroke; cerebellar stroke; controls) and
one within subject factor (presence or absence of object location
perturbation) examined correction processes used to maintain
coordination between transport-to-grasp in the presence of perturbation.
Sixteen chronic stroke participants (eight with right parietal lesions
and eight with cerebellar lesions) were matched in age (mean = 61 years;
standard deviation = 12) and hand dominance with 16 healthy controls.
Hand and arm movements were recorded during unperturbed baseline trials
(10) and unpredictable trials (60) in which the target was displaced to
the left (10) or right (10) or remained fixed (40).
Results: Cerebellar patients had a slowed
response to perturbation with anticipatory hand opening, an increased
number of aperture peaks and disruption to temporal coordination, and
greater variability. Parietal participants also exhibited slowed
movements, with increased number of aperture peaks, but in addition,
increased the number of velocity peaks and had a longer wrist path
trajectory due to difficulties planning the new transport goal and thus
relying more on feedback control.
Conclusion: Patients with parietal or
cerebellar lesions showed some similar and some contrasting deficits.
The cerebellum was more dominant in controlling temporal coupling
between transport and grasp components, and the parietal area was more
concerned with using sensation to relate arm and hand state to target
position.
Introduction
Successful control of reach-to-grasp requires
coordination, “an ability to maintain a context-dependent and
phase-dependent cyclical relationship between different body segments or
joints in both spatial and temporal domains” (Krasovsky and Levin, 2010)
of various body segments including the arm with the trunk, the shoulder
with the elbow, and the hand with the arm. Studies in healthy adults
have suggested hand and arm function are controlled as a single
coordinated unit (Jeannerod, 1984; Wallace et al., 1990)
demonstrated by significant correlations between reach and grasp
components, including between the start time of the opening of the hand
and the start time of hand movement toward the object (Jeannerod and Biguer, 1982; Jeannerod, 1984), between the time of maximum hand aperture and the time of peak deceleration (PD) of the hand (Jeannerod, 1984; Castiello et al., 1993), and between time of maximum aperture (TMA) and the time of peak velocity (TPV) of the hand (Wallace et al., 1990). Apart from a few situations (Gentilucci et al., 1991; Kudoh et al., 1997),
for example, where correlations between the time of PD and the time of
MA are not reliable when transport and grasp were manipulated by the
distance and type of grasp (Gentilucci et al., 1991), temporal coupling of these events is a fairly consistent finding across reach-to-grasp tasks.
Stroke can adversely affect reach-to-grasp coordination (Pelton et al., 2012; vanVliet et al., 2013).
Spatiotemporal relationships between transport and grasp in a
heterogenous group of stroke patients with mild to moderate impairments,
were investigated in a study where movements were performed at both
fast and preferred speeds and to small and larger objects (vanVliet and Sheridan, 2007). There were significant correlations (p
< 0.05) between times of start of hand movement and hand opening and
between times of MA and PD in all conditions for both groups, although
some of the correlations were numerically small (Pearson product-moment
correlation coefficient r for the two groups ranged from 0.3 to
0.71). However, transport and grasp in patients were not as tightly
coupled. In the condition which most challenged accuracy (i.e., the fast
paced condition with small objects), the two events were less
correlated in participants with stroke.
One informative paradigm used to investigate
underlying control mechanisms for coordination of reach-to-grasp is to
perturb the object location at movement onset in order to examine the
resulting temporal adjustments made to the grasp component (Paulignan et al., 1990, 1991a,b), requiring modification of a pre-defined program (Goodale et al., 1986).
Typically, the unexpected perturbation in the object produced
adjustments to both the transport and grasp components, where the
initial wrist acceleration was aborted and a new one started, and the
initial grasp aperture was also aborted and reincreased in synchrony (Paulignan et al., 1990, 1991a,b) demonstrating that the two components are coordinated spatiotemporally.
The premise of a tight-coupling between the two
components prompted the development of a model for the temporal
coordination of transport and grasp (Hoff and Arbib, 1993).
The model proposed that neural processes controlling transport and
grasp are monitored on-line and adjusted for temporally so that the
expected duration of each trajectory to reach the target is matched to
the other component according to a consistent enclose time of the hand.
The coordinated control of transport-to-grasp with object location
perturbation also involves the integration of sensory signals from
multiple modalities (principally visual information concerning the
object and its relative position; and proprioceptive information about
the position of the arm and the hand). It requires the feed-forward
selection of perhaps one or two coupled motor commands for transport and
grasp together with a forward representation of the desired movement.
Smooth movement is dependent upon on-line updating of the initial
pattern of muscle activation and detection of error between the actual
positions of object relative to the hand. Large errors which are
instigated by the introduction of a perturbation require either rapid
modification of an ongoing internal forward model or rapid onset of a
new internal forward model and cessation of the old forward model.
Two key brain areas responsible for processing of
information pertaining to reach-to-grasp coordination are the parietal
lobe and the cerebellum. Current theories attribute similar
contributions by parietal and cerebellar regions. For example, both
areas have been identified as potential areas that integrate the
independent motor processes for reach and grasp into one common motor
program (Desmurget et al., 1999; Zackowski et al., 2002).
Given the specialization of cortical areas, it is unlikely that these
areas perform identical roles. Thus, further research is needed to
elucidate their exact role in control of reach-to-grasp. It has been
pointed out that the two regions may work as a functional loop in
estimating the current status of the motor system, since the parietal
cortex receives input from the cerebellar dentate nucleus, and there are
connections from parietal cortex to cerebellum via the pontine nuclei (Blakemore and Sirigu, 2003; Ramnani, 2012). Below, we review the current knowledge about roles of parietal cortex and cerebellum in control of reach-to-grasp.
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