1Motoriklab, Department of Woman and Child Health and MR Research Center, 171 76 Stockholm; 2Division of Human Brain Research, Department of Neuroscience, Karolinska Institute, Stockholm; and 3Department of Physiology, Umeå University, Umeå, Sweden
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ABSTRACT |
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Ehrsson, H. Henrik, Anders Fagergren, Tomas Jonsson, Göran Westling, Roland S. Johansson, and Hans Forssberg. Cortical Activity in Precision- Versus Power-Grip Tasks: An fMRI Study. J. Neurophysiol. 83: 528-536, 2000. Most manual grips can be divided in precision and power grips on the basis of phylogenetic and functional considerations. We used functional magnetic resonance imaging to compare human brain activity during force production by the right hand when subjects used a precision grip and a power grip. During the precision-grip task, subjects applied fine grip forces between the tips of the index finger and the thumb. During the power-grip task, subjects squeezed a cylindrical object using all digits in a palmar opposition grasp. The activity recorded in the primary sensory and motor cortex contralateral to the operating hand was higher when the power grip was applied than when subjects applied force with a precision grip. In contrast, the activity in the ipsilateral ventral premotor area, the rostral cingulate motor area, and at several locations in the posterior parietal and prefrontal cortices was stronger while making the precision grip than during the power grip. The power grip was associated predominately with contralateral left-sided activity, whereas the precision-grip task involved extensive activations in both hemispheres. Thus our findings indicate that in addition to the primary motor cortex, premotor and parietal areas are important for control of fingertip forces during precision grip. Moreover, the ipsilateral hemisphere appears to be strongly engaged in the control of precision-grip tasks performed with the right hand.
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INTRODUCTION |
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Napier (1956) divided handgrips
into precision and power grips from a functional and a phylogenetic
perspective. The power grip is a palmar opposition grasp in which all
digits are flexed around the object to provide high stability. The
precision grip has developed in primates for the manipulation of small
objects with the tips of the thumb and fingers. It requires for
stability independent finger movements that involve fine control of the directions and magnitudes of fingertip forces (Flanagan et al. 1999
; Johansson 1996
).
In nonhuman primates, the primary motor cortex (M1) plays a fundamental
role in the execution of skilled manipulatory tasks, especially those
that involve a precision grip (Kuypers 1981; Porter and Lemon 1993
). Lesions of the pyramidal tract
abolish independent finger movements while the capacity to flex all
fingers together remains (Lawrence and Kuypers 1968
).
Interestingly, subpopulations of neurons in M1 that project to
motoneurons that innervate hand muscles are active while conducting a
precision grip but not during power grip although their target muscles
may be activated in either grasp (Muir and Lemon 1983
).
As such, this indicates that the control of fingertip actions with a
precision grip engages neural circuits that are different to those
engaged during the phylogenetically older power grip. However, results
from neuroimaging studies in humans have shown that M1 is active during
many types of voluntary hand movement (Roland and Zilles
1996
). Furthermore the M1, the supplementary motor area (SMA)
and the premotor area (PM) are all active while making individual
finger movements and when opening and closing the whole hand
(Colbatch et al. 1991
). However, in none of these
brain-imaging studies has the task of the subjects been to grasp real
objects using different grip configurations. Here we explore the
possibility that healthy human subjects engage different cortical areas
when they apply forces under practically isometric conditions using a
precision grip between index finger and thumb and during a power grip
that engages all digits. We use functional magnetic resonance imaging
(fMRI) to measure brain activity. By contrasting the activity recorded
during the two tasks, we attempted to localize those regions of the
brain that were involved selectively in one grasp configuration or the
other. Preliminary results from this study have been reported
(Ehrsson et al. 1998
).
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METHODS |
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Subjects
Five healthy male subjects (21-27 yr) participated in the
study. All subjects were right-handed (Oldfield 1971)
and had given their informed consent. The Ethical Committee of the
Karolinska Hospital had approved the study.
Tasks
The subjects performed two different grip tasks with the right hand and two matching rest tasks. The grip tasks involved the production of force under almost isometric conditions. During the tasks, the subjects rested comfortably in a supine position in the MR scanner. The extended right arm was oriented parallel to the trunk in a relaxed position. We used appropriate supports to minimize movements of the arm and hand during the force production. The room was dark and the subjects kept their eyes closed. The subjects wore headphones to reduce the noise from the scanner and to present auditory cues.
To perform the precision-grip task, the subjects used the tips of the thumb and the index finger to grasp a nonmagnetic instrumented handle with vertical flat parallel contact surfaces spaced 30 mm apart (Fig. 1A). The handle was connected by a beam to a force motor (not shown). We used a nonmagnetic optic transducer system to record the grip force (the force applied perpendicular to the contact surfaces). The data were stored and analyzed using the SC/ZOOM data-acquisition system (Department of Physiology, University of Umeå). The subjects changed the grip force cyclically, being paced by a metronome that generated click sounds at 0.67 Hz through the headphones. When they squeezed the handle, at a target force of 2 N, they received a weak tactile cue through the handle. This was a brief force pulse delivered tangential to the contact surfaces (10-ms duration and <0.5 N peak force). The subjects then held the force until the click sound, which indicated that they should relax the grip and then squeeze the handle again. Figure 1C illustrates the resultant grip force profile together with the occurrence of the auditory and tactile cues; note the plateaus in the force during each grip cycle. For the matching rest condition, the subjects held the thumb and index finger in weak contact with the grip surface while they received tactile pulses as they had during the precision-grip task (Fig. 1D). The pulses were delivered at 0.67 Hz, and again the subjects heard the metronome sound (0.67 Hz) through the headphones. In this task, the subjects applied virtually no force to the handle.
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During the power-grip task, the subjects clenched a cylindrical plastic-tube in a palmar opposition grasp that engaged all digits (Fig. 1B). Paced by the metronome, they generated a time-varying grip force like that applied for the precision-grip task, but the overall force output was much higher. The diameter of the vertically oriented tube was 40 mm, and it had a 10-mm longitudinal gap. When the overall grip force reached some 20 N, the edges of this gap closed. This provided a mechanical cue for the target force. This mechanical event resembled the tactile cue received by the subjects when performing the precision-grip task. During the matching rest condition, the subject held the cylinder in the palm without applying a noticeable force and heard the metronome sound through the headphones.
Before the scanning commenced, the subjects practiced the grip tasks until they produced the requested time-varying grip forces. During the precision-grip task, we recorded the grip force during the scanning by the nonmagnetic transducer system. Technical limitations meant that the force could not be recorded during the power-grip task in the MR environment. Instead, the experimenter followed the performance of the subjects by visual inspection.
After the scanning, we measured the grip force during maximal voluntary contraction (MVC) as subjects grasped a standard dynamometer (cylindrical handle, 30 mm diam) with a precision or a power grip. We also recorded surface electromyograms (EMGs; Myo115-electods with in-built 2,000 × preamplifiers, Liberty Technology, Hopkinton, MA) in four subjects while they performed the precision- and power-grip tasks outside the MR scanner. We recorded from the right first dorsal interosseous (1DI), abductor pollicis brevis (AbPB), flexor digitorum superficialis, biceps-brachii, and deltoid muscles. We also recorded from the left 1DI and AbPB to check for possible nonvoluntary synergistic movements of the nonoperating hand. The electromyographic signals were sampled, stored and analyzed (root-mean-squared value) off-line on a portable PC using the Visual Designer and ZOOM software packages.
Brain imaging
fMRI was conducted on a clinical 1.5 T scanner (Signa Horizon
Echospeed, General Electric Medical Systems) equipped with a head coil.
We collected gradient-echo, echo-planar (EPI) T2*-weighted image
volumes with blood oxygenation level-dependent (BOLD) contrast (Kwong et al. 1992; Ogawa et al. 1992
).
[The parameters were: echo time (TE) = 50 ms; field of view
(FOV) = 22 cm; matrix size = 64 × 64; pixel size = 3.4 mm by 3.4 mm; flip angle = 90°]. Twenty contiguous axial
slices of 3.4-mm thickness were collected in each volume. We selected
slices from the dorsal surface of the brain to cover the frontal and
parietal lobes. The cerebellum and part of the basal ganglia were
outside the field of view. A plastic bite bar restricted head
movements. A high-resolution, three-dimensional gradient echo
T1-weighted anatomic image volume of the whole brain was collected
[3D-SPGR, echo time (TE) = 13 ms; field of view (FOV) = 24 cm; matrix size 128 × 256; 124 2-mm coronal slices; flip
angle = 10°; 2 NEX].
Functional-image volumes were collected in separate runs, each of which either included the precision-grip task and the matching rest condition or the power-grip task and the matching rest condition. These runs were conducted in alternate order to reduce possible time effects. During each run, functional-image volumes were acquired continuously every 5,000 ms (TR = 5s) while the subjects performed the different tasks; for each run, a total of 104 volumes was collected (a time series). The tasks were performed in epochs that lasted 25 s (5 volumes being collected in this time), and the epochs of movement (precision-grip task or power-grip task) were alternated with the epochs of the matching rest condition. To allow for T1 equilibration effects, we started each run by recording four "dummy" volumes that we subsequently discarded. A total number of 954 volumes were collected for each participant; 780 were used in the analysis (some data were not used for technical reasons). Each task consisted of an equal number of image-volumes.
Data analysis and image processing
We used SPM-96 to analyze the functional images (Friston
et al. http://www.fil.ion.ucl.ac.uk/spm). The volumes were realigned, coregistered to each individual's anatomic T1-weighted image
(3D-SPGR), and normalized to the stereotactic space of Talaraich and
Tournoux (Friston et al. 1995a; Talaraich and
Tournoux 1988
). The time series were smoothed spatially with an
isotropic Gaussian filter of 8 mm full width at half-maximum, and
temporally smoothed with a Gaussian kernel of width 2.83 s. We
estimated the task-specific effects using the general linear model
(GLM) with a delayed boxcar wave form (Friston et al.
1995b
; Worsey and Friston 1995
). Each of the
time series was modeled with regressors for the tasks and the mean
value using the standard model implemented in SPM-96. The significance
of the effects was assessed using Z statistics for every
voxel from the brain, and these sets of Z values were used
to create statistical parametric maps (SPMs). A high-pass filter was
used to remove low-frequency drifts and fluctuations of the signal
(Holms et al. 1997
), and proportional scaling was applied to remove global changes in the signal. To disclose activity that was robust across subjects and to increase the sensitivity of the
analysis, we analyzed time series from the five subjects as a group.
Linear contrasts between the different tasks were used to create SPMs,
and these were arbitrarily thresholded at a Z value of 3.09. From these SPMs we report peaks (local maxima) of activity which, when
corrected for multiple comparisons for the whole brain volume,
corresponded to P < 0.05 on the basis on a test of
peak height (Friston et al. 1995b
). We also confirmed the consistency of the activity by examining statistical contrasts for
individual subjects. The precision- and power-grip tasks were compared
with the matching rest tasks with the contrasts
(precision-grip
matching rest) and (power-grip
matching rest).
Because the precision- and power-grip tasks were acquired in different
runs (and the contrasts should have weights which sum to 0 over
the task effects within each run), we compared the grip tasks with the
two contrasts: [(precision-grip task
matching rest)
(power-grip task
matching rest)] and [(power-grip task
matching
rest)
(precision-grip task
matching rest)], respectively.
In the present analysis, we compared data acquired in different runs, this might be inappropriate if the data had been collected under nonstationary conditions. However, there was no reason to believe that this was a problem because there was no obvious variability among corresponding runs in the manner in which subjects performed the task, because the different runs were conducted alternately to reduce any eventual time effects, because we modeled each time series as a regressor in the GLM remove variability between series, because we found similar activity for a given task when examining the equivalent series separately, and finally because we found no relevant task-by-series interactions when we contrasted the same tasks using subsets of time series.
Anatomic localizations of the activated regions were determined from an
average image made from normalized (and intensity standardized)
T2*-weighted images form each of the five subjects. In this average
image, most of the major gyrus and sulci were clearly identifiable. We
use the terminology of Roland and Zilles (1996) for the
cortical motor areas with the exception of the cortex in the depth of
the central sulcus, which we termed SMC (primary sensori-motor cortex).
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RESULTS |
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General task performance
The performance during the precision-grip task was consistent across the force cycles, and subjects generated the requested grip force profiles in >99% of the cycles. The mean grip force during the plateau phases was 3.61 ± 1.06 N (mean ± SD for data pooled across subjects). During the power-grip task, we observed no errors that indicated that the performance deviated from the requested pattern of force generation.
The mean grip-force across subjects during MVC was 80 N (range: 62-96 N) for the precision grip and 416 N (range: 355-456 N) for the power grip. Thus the mean grip force in the precision-grip task corresponded to 4.5% of that of the MVC, and the target force in the power-grip task (20 N) corresponded to 4.8% of that of the MVC.
The surface EMG of the right 1DI, AbPB, and flexor digitorum superficialis showed stronger activity during the power-grip task than during the precision-grip task (P < 0.05, paired t-tests). Neither the proximal muscles of the right arm (biceps and deltoid) nor the 1DI and AbPB muscles of the left hand showed reliable EMG activity in any of the tasks.
Regions active during both grip tasks
Table 1 shows brain regions with significantly stronger BOLD contrast signal while performing the grip tasks than during the matching rest conditions (P < 0.05, corrected for multiple comparisons) (see also Fig. 2). Because the cerebellum was outside and the basal ganglia was only partially within the field of view, we do not report activity in these structures.
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Both the precision- and power-grip tasks activated the SMC contralateral to the grasping hand. The activations extended into the dorsal premotor cortex (PMD) and the postcentral sulcus. Furthermore the ventral premotor cortex (PMV) showed bilateral activation with peaks of activity in the inferior part of the precentral gyrus. The SMA was active with an anterior and a posterior peak with activity extending into the cingulate sulcus (rostral cingulate motor area). We also observed activity in the contralateral parietal operculum (PO) and in the left thalamus. The activation extended into the right thalamus in the precision-grip task.
Regions differentially activated by the two grip tasks
Table 2 and Fig. 2 indicate regions
that showed a significant difference in the BOLD contrast signal when
the precision- and power-grip tasks were compared (P < 0.05, after correction for multiple comparisons). The left primary
sensory cortex (SI) showed stronger activity during the power-grip task
with a peak of activation located in the postcentral gyrus. Similarly
we observed a stronger response in the anterior bank of the left
central sulcus during the power-grip task. It is likely that this
corresponds to the border between M1 (area 4a) and PMD (area 6)
(Geyer et al. 1996). The cluster extended deeply into
the central sulcus and, anteriorly, to the precentral gyrus and the
superior precentral sulcus (PMD). During the power-grip task, we also
observed stronger activity in the left PO.
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Several regions showed significantly stronger activity during the
precision-grip task than during the power-grip task (Table 2 and Fig.
2; P < 0.05 corrected for multiple comparisons). Many of these were located in the right hemisphere, i.e., in cortical areas
ipsilateral to the operating hand. We observed higher activity in the
upper part of the right intraparietal sulcus (IPS) at two locations,
and bilaterally in the supramarginal gyrus. In the prefrontal cortex,
there were peaks of activity bilaterally in the inferior frontal sulcus
with the activations extending to the middle frontal gyrus (more
extensive in the right hemisphere). We also found stronger BOLD
contrast signal in the inferior part of the right precentral sulcus,
i.e., in the PMV. The cluster extended into the opercular cortex.
Activation of the left inferior precentral sulcus (Z =4.08,
P = 0.28 corrected for multiple comparisons) did not
reach the significance criterion. However, we descriptively report this
finding to illustrate the tendency for a bilateral response in the PMV
region. Furthermore an activation was found 8 mm rostral from the
anterior commissural line (vertical line passing through the anterior
commissure) in the cingulate sulcus, i.e., in the rostral cingulate
motor area (CMAr) (Roland and Zilles 1996). This
location corresponds to the "posterior portion of the rostral
cingulate zone" in the classification of mesial areas by
Picard and Strick (1996)
. The activity appeared to
extend into the cingulate sulcus bilaterally, but the resolution of the
statistical images did not allow reliable separation into two peaks.
We confirmed the consistency of the main findings in the group analysis by descriptively examining contrasts in individual subjects. At Z >1.66, all subjects showed extensive (>600 mm3) activations of the right PMV, right IPS, right supramarginal cortex, right inferior frontal sulcus and the CMAr when the precision-grip task was compared with the power-grip task. Furthermore four of five subjects showed activity in the left supramarginal cortex and three in the left inferior frontal sulcus. When power grip was compared with precision grip, we observed stronger activity in the contralateral SMC in all subjects and in the contralateral PO in four of our five subjects. We concluded that the results acquired from the group analysis was representative of the observations made for individual subjects.
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DISCUSSION |
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The generation of grip forces by a precision grip between the index finger and thumb was associated with a different pattern of brain activity than that observed when making a power grip that engaged all digits. Our power-grip task was associated with stronger activity in the contralateral SI, M1 and PO, whereas the precision-grip task was associated with stronger activity in the right PMV, CMAr and the prefrontal and posterior parietal cortex bilaterally. Many of the regions that were more active in the precision-grip task were right-sided, i.e., they were located in the hemisphere ipsilateral to the operating hand.
During both grip tasks, the subjects rhythmically changed the grip force under virtually isometric conditions. A metronome paced the force production and a tactile signal provided feedback from the target force. Thus auditory and somatosensory information was used to guide the motor acts. In this respect, the two grip tasks were thought to be well balanced.
In addition to the grip configuration, the precision- and power-grip
tasks differed in terms of the overall force exerted. The higher force
output applied while conducting the power-grip task might explain the
higher activity observed in the SMC because the hemodynamic response in
this and other posterior motor regions [i.e., SMA and the caudal motor
field of the cingulate sulcus (CMAc)] increases with increased manual
force (Dettmers et al. 1995; Thickbroom
et al. 1998
). Likewise the involvement of more digits in the
power-grip task may have contributed to the stronger responses in these
areas. Furthermore the higher activity in the PO may have been caused
by a more spatially distributed tactile sensory input because this
region also is activated by tactile stimuli (Burton et al.
1997
; Coghill et al. 1994
; Ledberg et al. 1995
). A possible confounding factor may be differences in the general level of effort during the two grip tasks. However, relative to
the corresponding MVC forces the forces applied during the two tasks
were similar, which suggest that this factor is of little importance.
It is also noteworthy that two of the prime movers (1DI and AbPB) in
the precision-grip task were more active when performing the power
grip. These results indicate that the hemodynamic responses exclusively
associated with the precision-grip task were specific for this task and
not related to additional activity of the intrinsic hand muscles.
A difference in the tactile input in the two reference conditions
(matching rest) is another factor that may have influenced the results
of the comparisons of the precision- and power-grip tasks: the
reference condition for the precision-grip task involved the subjects
receiving weak tactile pulses at 0.67 Hz, whereas the reference
condition for the power-grip task did not include this tactile stimuli.
Although the tactile pulses were brief and weak and did not evoke any
grip force responses, we cannot exclude that their absence in the
reference condition could have augmented the hemodynamic response
estimated during the power-grip task. This primarily would have
concerned regions that tactile stimulation would activate in passive
subjects, i.e., SMC and PO. Another concern is whether the neural
signals evoked by the auditory and tactile signals when present in the
rest conditions were processed differently than when they guided the
motor acts. Indeed, data obtained using evoked potential methods in man
and single-cell recordings in monkey at the level of the primary
somatosensory cortex have shown that voluntary movements attenuate the
overall transmission of cutaneous signals from the distal forelimb
(Chapman et al. 1996; Knecht et al.
1993
). However, if present such "gating effect" could
probably not explain the increases in the hemodynamic response during the grip tasks because previous positron emission tomography (PET) and fMRI studies have failed to record
increased activity specifically related to tactile or auditory
triggering of movements (Jasanshahi et al. 1995
;
Naito et al. 1999
) or to self-produced tactile stimuli
generated by movements of the hand (Blakemore et al.
1998
).
Regions selectively activated during the precision-grip task
Studies in nonhuman primates indicate that M1 and other posterior
motor areas that send direct projections to the spinal cord (i.e., SMA,
CMAc) are of utmost importance for the control of force output during
precision-grip tasks (Cadoret and Smith 1995, 1997
;
Hepp-Reymond 1988
; Maier et al.
1993
; Picard and Smith 1992
; Porter and
Lemon 1993
; Wannier et al. 1991
). The results in
the present study indicate that the rostral part of the right PMV, CMAr, and bilateral parietal and prefrontal regions also are engaged in
skilled force production by an isometric precision grip but not by a
power grip. Presumably this difference between grips reflects the need
for additional sensory-motor control mechanisms to control force during
pulp-to-pulp opposition engaging pairs of individual digits. Because
two-fingered precision grips are inherently less stable than multidigit
grips, the control of direction and magnitude of the applied finger
forces needs to be more constrained at the level of individual digits
(Flanagan et al. 1999
). Thus the precision grip
therefore may be more demanding in terms of neural control. Indeed a
refined use of cutaneous afferent information is required to control
fingertip force vectors during precision-grip tasks (Johansson
1996
).
Frontal regions
We observed higher activity in the two nonprimary motor areas PMV
and CMAr during the precision-grip task. By virtue of their projections
to the cervical spinal enlargement (Dum and Strick 1991;
Galea and Darian-Smith 1994
; He et al.
1993
, 1995
) and to the primary motor cortex (Mukkasa and
Strick 1979
; Tokuno and Tanji 1993
),
both areas are likely to contribute to the control of the hand. The
activation of PMV agrees with recent studies on object grasping in the
macaque (Jeannerod et al. 1995
; Rizzolatti et al.
1988
, 1998
). Interestingly, in our precision-grip task we
specifically observed activity in the inferior part of the precentral
sulcus. This activity was located some 10 mm rostral to that reported
in previous PET studies during more general movements of individual
digits (Fink et al. 1997
; Kawashima et al.
1998
; Matsumura et al. 1996
; Sadato et
al. 1996
). Likewise it was located 16 mm rostral to the
activity that we found in the right inferior precentral gyrus when we
contrasted the power-grip tasks to the matching rest condition. The
rostral border of the human PMV is not known (Roland and Zilles
1996
), but it has been proposed that the human inferior
precentral sulcus corresponds to the PMV in the macaque
(Petrides and Pandya 1994
; Rizzolatti et al.
1998
). Indeed there are neurons in the rostral PMV (area F5) in
the macaque that show activity that is specific for precision-grip
configurations used to pick up small objects. Such neurons are more
common than neurons related to whole-hand grips (Rizzolatti et
al. 1988
).
The CMAr was more active in the precision-grip task than in the
power-grip task. Importantly, this region is separate from the CMAc
(Dum and Strick 1991; Matelli et al.
1991
; Roland and Zilles 1996
; Shima et
al. 1991
) that was active when the power-grip task was
contrasted to the matching rest condition (see Table 1). The location
of the CMAr activity in the present study (8 mm rostral from the
anterior commisural line) corresponded to a site predominately
activated by movements of individual digits in previous human brain
imaging studies (Fink et al. 1997
; Grafton et al.
1993
; Jahanshahi et al. 1995
; Kawashima
et al. 1996
; Larsson et al. 1996
; Picard
and Strick 1996
). Furthermore movements of individual digits
activate neuronal populations in macaque CMAr (Shima et al.
1991
). Hence our findings in humans, combined with previous
observations in monkeys, strongly indicate that PMV and CMAr play an
important role in the control of precision grips.
Overall, the activity we observed in the frontal lobes during the
precision-grip task was located more anteriorly than that during the
power-grip task. As such, this novel finding supports the notion of
Fuster (1995) that phylogentically old motor skills are
represented in posterior parts of the frontal lobes, whereas more
skilled movements also involve more anterior regions. Previously, prefrontal activity has been observed in several PET studies during execution of simple movements when a rest condition was used as the
control. (e.g., Jasanshahi et al. 1995
; Larsson
et al. 1996
; Sadato et al. 1997
). Activation of
the prefrontal cortex also has been associated with several other
behavioral factors relevant for motor control such as spatial attention
(Jonides et al. 1993
; Pardo et al. 1991
),
short-term retention of tactile information (Klingberg et al.
1996
), selection of motor responses (Frith et al.
1991
), and attentive self-monitoring of ongoing motor
performance (Fink et al. 1999
; Jueptner et al.
1997
). The novel finding in the present study was that the
activity in the lateral prefrontal cortex differed depending on the
particular grasp-configuration used in a simple force production task.
Specifically the inferior frontal sulcus was engaged only when force
was applied using the precision grip. In the macaque monkey, the
ventrolateral prefrontal cortex (ventral area 46) has strong reciprocal
connections with the PMV and the parietal operculum (Preuss et
al. 1989
), and similarly, the dorsolateral prefrontal cortex
(area 46) has connections with the PMV, CMAr, and the posterior
parietal cortex (Cavada and Goldman-Rakic 1989
;
Lu et al. 1994
). Thus given the existence of these
pathways in the monkey and the activity recorded in the present study, it is interesting to speculate that the prefrontal cortex could be
involved in skilled force production with a precision grip.
Parietal regions
Another interesting result from the present study was the
selective involvement of the right intraparietal and bilateral
supramarginal cortex during the precision-grip task. The posterior
parietal cortex is a heterogeneous region with little information
available concerning the possible anatomic correspondence between the
human and monkey brain (Eidelberg and Galaburda 1984;
Milner 1997
). In the nonhuman primate, numerous
studies have shown that populations of neurons in the intraparietal
sulcus are likely to be involved in visuomotor transformations during
reach and grasp (Jeannerod et al. 1995
; Sakata et
al. 1997
). Of special interest is a region within the macaque
anterior intraparietal sulcus that contains neurons that show activity
specific to the grasping of small objects (Sakata et al. 1995
,
1997
; Taira et al. 1990
). In addition, neurons in area 7 increase the discharge rates during voluntary hand movements and in response to visual and tactile stimuli (Hyvärinen
et al. 1981
). The anatomic connections between these parietal
regions and the premotor fields, including the ventral premotor area, are considered of particular importance for the sensory control of the
hand (Rizzolatti et al. 1998
). In humans, lesions in the posterior parietal cortex, involving intraparietal cortex cause disorders of grip formation (Jeannerod 1986
;
Pause et al. 1989
). Indeed previous PET and fMRI studies
have reported right- and left-sided activity in the intraparietal and
supramarginal regions during visually guided reach, grasp, and
graphomotor movements performed with the right hand (Binkofski
et al. 1998
; Grafton et al. 1998
; Inue et
al. 1998
; Matsumura et al. 1996
; Seitz et al. 1997
). Similar regions also are activated in sensorimotor manipulatory tasks performed without vision, i.e., when subjects rotate
two small cylindrical objects held in the right hand (Kawashima et al. 1998
) and somatosensory discrimination of objects shape with exploratory finger movements (O'Sullivan et al.
1994
; Roland et al. 1998
; Seitz et al.
1991
). However, our precision-grip task differed from all these
previous studies in that neither vision nor overt arm or finger
movements were involved. Instead somatosensory input was used to
control isometric grip force. Hence our findings suggests that the
control of fingertip forces in the precision-grip task might require
processing of somatosensory signals in the posterior parietal cortex in
addition to the processing required for the control of force during the
power-grip task.
Activity in the ipsilateral hemisphere during the precision-grip task
The two grip configurations exhibited differences in the
hemispheric lateralization of the activation patterns. The power grip
was associated predominately with contralateral left-sided activations,
whereas the precision-grip task involved extensive activity in both
hemispheres. As such, the ipsilateral activity in the precision-grip
task agrees with previous findings that many motor regions are
activated bilaterally during unimanual motor tasks (Kawashima et
al. 1998; Rao et al. 1993
; Roland and Zilles 1996
). Furthermore brain-damaged patients often have
contralateral but not ipsilateral deficits in simple movements tasks,
whereas more complex sensory-motor tasks requires the integrity of both hemispheres (Haaland and Harrington 1996
). Lesions of
the right hemisphere have been associated with ipsilateral impairment
of skilled finger movements and of motor tasks that depend on
movement-to-movement sensory feedback (Arrigoni and DeRenzi
1964
; Haaland and Harrington 1996
;
Warrington et al. 1966
; Winstein and Pohl
1995
). Thus the right-sided activity in the
precision-grip task may reflect additional demands in terms of
somatosensory control and sensory-motor processing compared with the
power-grip task. During the precision-grip task, we observed a
preponderance of activity in the right PMV and the right intraparietal
cortex. However, we also measured an increased hemodynamic response in
the contralateral left inferior precentral sulcus (PMV), which was
close to being statistically significant.
In conclusion, in addition to previously well-recognized sensorimotor areas, our results reveal novel premotor and association areas that are activated in the control of precision grip but less so in power grip. Our findings also indicate that the right hemisphere is engaged in important control mechanisms during precision-grip tasks executed by the right hand.
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ACKNOWLEDGMENTS |
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The authors thank Prof. Per E. Roland for comments on the manuscript and A. Ledberg for software development (both are at the Dept. of Neuroscience, Karolinska Institute). We also thank S. Skare and Dr. Anders B. A. Wennerberg (both of whom are at the MR Center, Karolinska Institute) for technical developments of the fMRI system.
This work was supported by the Axel and Margaret Axson Johnssons Foundation and the Swedish Medical Research Council (Projects 5925 and 8667).
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FOOTNOTES |
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Address for reprint requests: H. Ehrsson, Motoriklab, Dept. of Woman and Child Health, Astrid Lindgren Hospital/Karolinska Hospital, 171 76 Stockholm, Sweden.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 29 March 1999; accepted in final form 21 September 1999.
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REFERENCES |
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