Download Involvement of the Ventral Premotor Cortex in Controlling Image

Cerebral Cortex July 2005;15:929--937
doi:10.1093/cercor/bhh193
Advance Access publication October 13, 2004
Involvement of the Ventral Premotor Cortex
in Controlling Image Motion of the Hand
During Performance of a Target-capturing
Task
The ventral premotor cortex (PMv) has been implicated in the visual
guidance of movement. To examine whether neuronal activity in the
PMv is involved in controlling the direction of motion of a visual image
of the hand or the actual movement of the hand, we trained a monkey
to capture a target that was presented on a video display using the
same side of its hand as was displayed on the video display. We found
that PMv neurons predominantly exhibited premovement activity that
reflected the image motion to be controlled, rather than the physical
motion of the hand. We also found that the activity of half of such
direction-selective PMv neurons depended on which side (left versus
right) of the video image of the hand was used to capture the target.
Furthermore, this selectivity for a portion of the hand was not affected
by changing the starting position of the hand movement. These
findings suggest that PMv neurons play a crucial role in determining
which part of the body moves in which direction, at least under
conditions in which a visual image of a limb is used to guide limb
movements.
Keywords: arm movement, frame of reference, image motion, premotor
cortex
Introduction
Several lines of evidence suggest that the ventral premotor
cortex (PMv) of primates is involved in the visual guidance of
limb movements. Anatomical studies have revealed inputs from
regions of the posterior parietal cortex that provide visuospatial
information (Matelli et al., 1986; Dum and Strick, 1991; Kurata,
1991; Murata et al., 1997, 2000; Lacquaniti and Caminiti, 1998;
Luppino et al., 1999). Lesion studies (Moll and Kuypers, 1977;
Kurata and Hoshi, 1999; Fogassi et al., 2001) and studies in
which cellular activity during the performance of visually guided
forelimb movements was examined (Wise, 1985; Rizzolatti
et al., 1988; Kurata, 1993; Hoshi and Tanji, 2002) have suggested
that the PMv is involved in the visual guidance of limb movements when reaching for or manipulating objects. However, it is
not known precisely which behavioral factor is represented in
the activity of individual cells in the PMv during the visual
guidance of motor behavior.
A recent report demonstrated that most PMv neurons that are
tuned to the direction of movement encode movement information in an extrinsic frame of reference (Kakei et al., 2001).
This finding revealed that the PMv is involved in encoding the
direction of movement in space, rather than the direction of
joint movement or the activity in the forelimb muscles that is
required to achieve the limb movement. Although Kakei et al.’s
report opened up a new avenue for studying the nature of neural
representation in the PMv, it is still necessary to examine
whether the reported PMv activity represents the direction of
the moving hand itself, the direction of movement of the object
Cerebral Cortex V 15 N 7 Ó Oxford University Press 2004; all rights reserved
Tetsuji Ochiai1,2, Hajime Mushiake1,3 and Jun Tanji1,3
1
Department of Physiology, Tohoku University school of
Medicine, Japan, 2Miyagi Organization for Industry Promotion,
Sendai, Japan and 3The Core Research for Evolutional Science
and Technology Program, Japan
that is acted upon, or the end point (target) of the movement.
Therefore, in the present study we investigated whether the
activity of PMv neurons encoded the direction of hand movement or whether the PMv neurons were concerned with
controlling an image of the moving hand, under experimental
conditions in which these two factors were dissociated. We
show that the majority of PMv neuronal activity reflects the
motion of the hand image being controlled rather than the
movement of the physical hand or the target.
Materials and Methods
We trained a monkey (Macaca fuscata) to move its right hand while
viewing an image of the same hand that was projected onto a video
display unit after being captured with a video camera. The animal was
cared for in accordance with National Institutes of Health guidelines and
the Guiding Principles in the Care and the Guidelines for Animal Care
and Use published by our institute. The motor task and devices that
were employed in this study have been described in detail by us
previously (Ochiai et al., 2002). The motor task was the capture of
a target spot that was displayed on the video display unit with a specific
part of the projected image of the hand; this was specified by the
presentation of an instructional spot signal (Fig. 1A). The target and
instructional spots were overlaid onto the video image of the hand. The
task began when the animal placed its hand in the hold position that was
displayed on the video display. If the hold was maintained for 1.0 s, a red
spot was projected onto either the right or left side of the video image of
the hand; this instructed the animal as to which side of the hand was to
be used to capture the target (Hand-Cue; turned off after 1 s).
Subsequently, after a delay period of 1.0 s, a green spot appeared at
one of four target positions (Target-Cue). The animal was required to
wait for 1.5 s after the appearance of the target spot until the initial hold
position and the target cue had disappeared from the video display; this
served as a ‘go’ signal to start the target-capturing movement within
500 ms. If the onset of movement occurred within 200 ms of the ‘go’
signal, the trial was aborted. The target cue was turned on when the
animal reached the target with the instructed position of the hand
image. The physical hand movement was either straight ahead or 30° to
the right or left in the horizontal plane. The hand movement appeared
either upward or to the right or left on the video display.
The monkey was also trained to perform the same motor task with the
video image of the hand inverted horizontally. In this case, the motion of
the video image of the hand was dissociated from the true motion of the
hand. Under this inverted viewing condition, the video image of the
hand was a mirror image of the visual image under the normal viewing
condition; the hand image moved upward and to the left on the video
display when the monkey moved its hand forward and to the right. After
extensive training, the animal was able to adapt to this dissociation, and
was able to capture the target without difficulty. After a transition
period (10 trials under the inverted viewing condition), the animal’s
movement trajectories and muscle activities were indistinguishable
from those that were observed under the normal viewing condition.
Therefore, we analyzed the neuronal activity that was recorded after the
initial 10 trials under the inverted viewing condition. In addition, the
initial hold position of the hand was occasionally shifted to the right or
left to examine the possible relation between neuronal activity and the
location of the target (Fig. 1B).
We monitored eye positions at a sampling frequency of 250 Hz using
an infrared corneal reflection monitor system (RMS Hirosaki). We
monitored the trajectory of hand movement with an infrared position
sensor (C5949 Hamamatsu Photonics). We also measured the activity of
the arm and wrist muscles using electromyography. We used conventional electrophysiological techniques to obtain single-cell recordings
from the monkey (Mushiake et al., 1991). An acrylic recording chamber
was attached to the monkey’s skull under aseptic conditions. During
surgery, the monkey was anesthetized with ketamine hydrochloride
(10 mg/kg i.m.) and pentobarbital sodium (30 mg/kg i.m.). We applied
intracortical microstimulation with 10--20 pulses of 0.2 ms duration at
333 Hz. After the electrophysiological recording had been completed,
histological examination of the recording sites was carried out in Nisslstained coronal sections of brain. Electrode tracks were reconstructed
with reference to microlesions that were made by passing direct current
through Elgiloy alloy electrodes.
In the present study, we focused on premovement activity in the PMv
and did not examine activity that was associated with visual responses to
visual instructions or moving stimuli. We analyzed neuronal activity
during the premovement period (200 ms following the GO signal) with
reference to the activity during a control period (500 ms preceding the
presentation of the initial hold position). If neuronal activity during the
premovement period differed from that during the control period
(Mann--Whitney U-test, P < 0.01), neuronal activity was defined as
movement-related. Using this criterion, 154 PMv neurons were classified
as movement-related neurons. Initially, we also analyzed neuronal
activity during a waiting period (1 s preceding the GO signal), but
because only 31 neurons were significantly active during this period
(Mann--Whitney U-test, P < 0.01), we proceeded to examine only
movement-related activity during the premovement period in the
present study. We used a two-way analysis of variance (ANOVA) to
determine whether movement-related neuronal activity reflected the
direction of motion of the hand image or the part of the hand image that
the animal was instructed to use to capture the target (right or left side
of the hand). To evaluate the effects of changing the initial hold position
of the hand, we used a three-way ANOVA, in which the direction of
motion, side of the hand and initial hold position were used as factors.
Thereafter, we compared premovement activity under the normal and
inverted viewing condition to examine the effect of image inversion on
neuronal activity.
Results
Figure 1. (A) Temporal sequence of behavioral events. A monkey was required to
capture a target (one of four spots) with the side of the hand that was cued by means
of a spot that appeared on the video image of the animal’s hand. (B) Alterations of
starting position of the hand movement. The initial hold position of the hand was
shifted to the right or left of the normal starting position by a distance that was equal
to the distance between the targets that were to be reached. Such a shift in the
starting position did not alter movement directions. (C) Cortical map of the recording
sites. In the enlarged surface view (left), small dots indicate the points at which
microelectrodes entered the brain, and large dots indicate penetration sites at which
direction-selective neurons were recorded. The anteroposterior (AP) and mediolateral
(ML) axes of the Horsley--Clarke stereotaxic coordinates are shown. Arc, arcuate
sulcus; CS, central sulcus.
Behavioral Data
Prior to analyzing neuronal activity, we examined the trajectories of hand movements to determine whether these were
influenced by the following behavioral factors: viewing condition (normal versus inverted), side of the hand used to capture
the target (left or right), and the initial hold position. As shown
in Figure 2, the trajectories of movement in three different
directions were not affected by the aforementioned factors. We
also analyzed the response time (between the onset of the ‘go’
signal and the onset of movement), peak velocity of movement,
Figure 2. Traces showing the trajectories of hand movements under three behavioral conditions: normal starting position under the normal viewing condition (left); normal starting
position under the inverted viewing condition (middle); and right- or left-shifted starting position under the normal viewing condition (right).
930 Controlling Image Motion in PMv
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Ochiai et al.
and activity of the forehand muscles. None of these variables
was affected by the three behavioral factors (ANOVA, P > 0.05).
We also analyzed the position and movement of the eyes, and
failed to detect any influence on oculomotor behavior of image
inversion or the side of the hand that was used to capture the
target.
Directional Selectivity
We recorded 154 neurons exhibiting premovement activity
within the PMv, posterior to the arcuate sulcus and lateral to the
arcuate spur (Fig. 1C). Some recorded neurons were located
within the upper portion of the posterior bank of the arcuate
sulcus. We first investigated whether neuronal activity reflected
movement direction. Among the 154 PMv neurons, 47 (31%; see
Table 1) were found to be selective for the direction of the
target-capturing movement (ANOVA, P < 0.001). In an example
of a direction-selective PMv neuron (left column in Fig. 3),
activity was most prominent when the monkey moved its hand
leftward to capture a target. To investigate whether the
directional selectivity of PMv neurons reflected the forthcoming direction of motion of the video image or the physical hand,
we inverted the video image horizontally. For example, under
this condition, rightward motion of the hand would appear to
be leftward on the video display unit. In the example of the PMv
neuron that is presented in Figure 3, when the video image was
inverted horizontally, the neuron was highly active when the
forthcoming motion of the image was in a left--forward direction (right column in Figure 3), despite the fact that the
monkey was actually moving its hand in a right--forward
direction. By comparing the activity in the two columns in
Figure 3, it is obvious that the activity of this neuron reflected
the forthcoming motion of the hand on the video display unit,
rather than the motion of the physical hand. We tested the
effect of image inversion on 35 direction-selective PMv neurons,
and found that the activity of 23 (65%; see Table 2) directionselective neurons was selective for image motion rather than
the motion of the physical hand. Only two (6%) of the directionselective PMv neurons were selective for the motion of the
physical hand. For the remaining 10 (29%) neurons, we found
that direction selectivity was lost under the inverted viewing
condition.
Table 2
Distribution of motion selectivity revealed by image-inversion
Table 1
Classification of activity of PMv neurons during premovement period
Numbers
examined
Image motion
Selective
Hand-movement
Selective
Non-selective
Total
Direction selective
Hand-side selective
Both
Neither
Direction-selective cells
35 (100%)
23 (65%)
2 (6%)
10 (29%)
154 (100%)
47 (31%)
67 (43%)
37 (24%)
77 (50%)
Hand-side-selective cells
39 (100%)
30 (77%)
0 (0%)
9 (23%)
Figure 3. Discharges of a PMv neuron exhibiting selectivity for the direction of motion of the hand image to be controlled but not for the actual movement of the hand. The activity
of this neuron was greatest when a hand movement was initiated for which the video image of the hand moved in a left--forward direction, regardless of whether the movement of
the physical hand was left--forward (top left) or right--forward (top right). Histograms of the summed neuronal discharges in raster displays are aligned to the onset of movement. In
this display, the animal was instructed to use the right side of the hand to capture a target. The bin width in the histograms is 100 ms.
Cerebral Cortex July 2005, V 15 N 7 931
Hand-side Selectivity
We subsequently investigated whether neuronal activity reflected which side of the video image of the hand was used to
capture the target. We found that the activity of 67 (24%; see
Table 1) of 154 movement-related PMv neurons differed
according to which side of the hand the animal was instructed
to use to capture the target. Of these neurons, 37 (37%; see
Table 1) were found also to be direction-selective. Figures 3 and
4 illustrate a typical example of hand-side selectivity: the activity
of a PMv neuron that was recorded during the capturing of
a target using the right side of the video image of the hand (Fig.
3) is compared to the activity of the same neuron when the left
side of the hand image was used to capture the target (Fig. 4). It
is apparent that the PMv neuron displayed in Figures 3 and 4 was
active selectively when the animal used the right side of its hand
to capture the target. To further investigate whether such handside selectivity reflected selectivity for the anatomical features
of the video image of the hand (such as selectivity for the radial
or ulnar side of the hand) or the relative position (right or left
side) of the hand image, we analyzed 39 hand-side-selective PMv
neurons and compared the activity of these neurons under the
normal and inverted viewing conditions. In this paradigm, the
right side of the image of the hand corresponded to the ulnar
side of the hand under the normal viewing condition, but
corresponded to the radial side under the inverted viewing
condition. In the example shown in Figures 3 and 4, neuronal
activity was much greater when the animal was instructed to
capture the target with the right side of the hand image,
regardless of whether the image was inverted. Therefore,
neuronal activity did not reflect selectivity for the anatomical
position of the hand. We found that 30 (77%; see Table 2)
neurons exhibited selectivity for the side of the hand image
irrespective of whether the image was inverted; in the remaining nine neurons (23%; see Table 2), hand-side selectivity was
lost when the image was inverted. Thus, selectivity for the side
of the hand that the animal was instructed to use to capture the
target was selective for the relative position of the hand in the
video image, rather than for a particular anatomical feature or
posture.
Effect of the Initial Hold Position
Our finding (see above) that the majority of PMv neurons that
were selective for the forthcoming motion of the video image of
the hand were also selective for the side of the hand in the video
image that the animal was instructed to use to capture the
target could be interpreted as indicating that the activity of
these neurons reflected the spatial location of the target or the
relative location of the movement trajectory with respect to the
video screen. To rule out this possibility, we carried out an
additional analysis under a behavioral condition in which the
initial hold position of the hand was shifted to the right or left.
An example of this analysis is presented in Figure 5. The neuron
that was examined (the same neuron as in Figure 3) was highly
active when the monkey captured a target with the right side of
the hand, regardless of whether the initial hold position was
shifted to the right or left (Fig. 5B,C ). It is noteworthy that the
activity of this neuron did not depend on the spatial position of
the target. In Figure 6, the activity of the same neuron during
the premovement period is replotted against either the direction of motion of the image (left panel) or target position
(right panel) on the abscissa. For this neuron, activity clearly
depended on the direction of motion of the image, irrespective
Figure 4. Discharges of the same neuron shown in Figure 3 while the animal was capturing a target using the left side of the hand. The activity of this neuron was greatly
diminished, irrespective of whether the animal was instructed to use the left side of the hand to capture the target under the normal (left column) or inverted viewing condition
(right column).
932 Controlling Image Motion in PMv
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Figure 5. Selectivity for the side of the hand that the animal was instructed to use to capture the target was not affected by a change in the starting position of the movement. An
example of a PMv neuron (the same neuron shown in Fig. 3) that was selective for a left--forward direction of movement. (A) Activity of the neuron when the movement was started
from the normal starting position. Activity was much greater when the right side of the hand image was used to capture the target. (B) Neuronal activity when the starting position
of the hand was shifted to the right. Activity was relatively low when the left side of the hand was used to capture the same target (second left) that was captured with the right
side of the hand from a normal starting position (top right panel). (C) Neuronal activity when the starting position was shifted to the left. Activity was intense even when the leftmost
target was captured with the right side of the hand.
of the target location. We performed the same analysis for 13 PMv
neurons that exhibited selectivity for both the direction of
movement of the video image and the side of the hand that the
animal was instructed to use to capture the target. For nine such
neurons (69%), neither type of selectivity was affected by
changing the initial hold position of the hand image (P > 0.05).
For the remaining four neurons (31%), the magnitude of
selectivity either increased or decreased significantly when the
initial hold position of the hand was shifted, but for all of these
neurons, neither type of selectivity was altered. These results
demonstrate that the selectivity of PMv neuronal activity did not
reflect the location of the target and that neuronal activity did
not depend on the relative position of the image of the hand on
the video screen.
motion, under normal and inverted-view conditions. For this
purpose, we plotted peri-movement population activity based
on averaging of peri-movement histograms constructed for
individual neurons with 50 ms bin width. As shown in Figure
7a, the image direction was clearly distinguishable under
normal, as well as under inverted view. The direction of actual
hand-movement was distinguishable in only two neurons (Fig.
7b). Subsequently, we compared population activity, by plotting
activity of neurons that were selective only for the hand side
(Fig. 8a). Furthermore, we compared the direction selectivity of
neurons that were selective only for the image-motion direction
(Fig. 8b). In addition, we also compared population activity of
neurons that were selective both for the image direction and
hand side, under four behavioral conditions (Fig. 8c).
Examination of Population Activity
It seems of interest to know the extent to which the direction
of image motion or the side of the moving hand was distinguishable with a population of PMv cells selective for either of the
two behavioral factors. We first compared population activity
observed in preferred and non-preferred directions of image
Comparison of Activity Properties among Neurons
in PMv and PMd
As mentioned in a previous section, PMv neurons were active
more often in the premovement period than during the delay
period. In contrast, we reported previously (Ochiai et al., 2002)
that PMd neurons were predominantly active during the delay
Cerebral Cortex July 2005, V 15 N 7 933
period. Despite the difference of behavioral phases in which
activity was observed, we examined similarities and differences
in activity properties among PMv and PMd neurons. The
population of neurons exhibiting selectivity for the image
motion rather than actual hand-movement (tested by image
inversion) was similar in PMv and PMd. On the other hand, in
PMv the proportion of neurons that were selective solely for
hand side (39%) was significantly more than that of neurons that
Figure 6. Plotting discharges of a PMv neuron to show their dependence on the
direction of image motion but on the position of targets. (A) The magnitude of
the activity in the premovement period (ordinate, mean discharges/s) is plotted against
the image-motion direction (abscissa). (B) Neuronal activity is plotted against the
target position. Data for the three different start positions are indicated with three
lines: red, black dot, and green for right-deviated start, normal start, and left-deviated
start, respectively. L, leftward; U, upward, and R, rightward image motion.
were selective only for image motion (13%), whereas the
proportions were indistinguishable in the PMd (Table 3).
Discussion
In this study, we found that neuronal activity in the PMv during
the premovement period of a target-capturing task in which an
animal was guided by a visual image of its hand predominantly
reflected the motion of the image of the hand to be controlled,
rather than the motion of the physical hand. We also found that
the activity during the premovement period of half of the
direction-selective PMv neurons differed according to which
part of the image of the hand the animal was instructed to use to
capture the target. Such selectivity for a particular side of the
hand was not affected by altering the initial position of the hand
in the video screen. These findings suggest that the PMv is
involved in controlling the motion of the visual image of the
moving hand with reference to a starting point that was defined
within the hand.
Neurons that were selective for forthcoming image motion
were located within the rostral part of the PMv in the present
study. Previous studies have reported that neuronal activity in
the same area is related to motor acts that are performed with
the forelimb (Weinrich et al., 1984; Wise, 1985). In other
studies, neuronal activity in the PMv has been reported to
reflect spatial target location (Godschalk et al., 1985; Gentilucci
et al., 1988; Mushiake et al., 1997; Hoshi and Tanji, 2002), the
three-dimensional shape of motor targets (Murata et al., 1997)
and visual objects in the peripersonal space (Graziano et al.,
1994; Fogassi et al., 1996). Our findings accord with the view
proposed in these reports that PMv neurons predominantly
reflect visual factors in spatial guidance of forelimb movements.
The most salient property of PMv neurons we found was that
the selectivity of the premovement activity corresponded to the
visual coordinates created by the video system. This observation
is in line with a report by Iriki et al. (2001) that the visual
Figure 7. Peri-event plots of population activity of PMv neurons showing direction selectivity under normal- and inverted-view conditions. (A) population activity of image-motionselective cells. (B) Population activity of hand-movement-selective cells. Each data plot in the peri-event plot is calculated by averaging peri-event histograms of individual neurons
aligned on the onset of movement. The data in histogram, with 50 ms bin, were normalized by taking a peak value as 1. In A, red arrows labeled a and b denote preferred and nonpreferred image-motion directions. Under inverted-view conditions, the direction of actual hand movement to the direction labeled a9 with a black arrow will appear, in the image, to
the direction indicated with a green solid arrow (labeled with a9). In B, red arrows labeled a and b mean preferred and non-preferred direction of actual hand movement.
934 Controlling Image Motion in PMv
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Ochiai et al.
Figure 8. Peri-event plots of population activity of PMv neurons belonging to three categories. (A) Neurons selective for hand side only. Comparison of activity for motions of
preferred and non-preferred hand side. (B) Neurons selective for image direction only. Comparison of activity of preferred and non-preferred directions. (C) Neurons selective for
both hand side and image direction. Display formats are basically the same as for Figure 7.
Table 3
Distribution of direction-selective and hand-side-selective cells in PMv and PMd
PMv
Exclusively direction selective
Exclusively hand-side selective
Selective to both
Subtotal
10(13%)a
30(39%)a
37(48%)
77
PMd
36(35%)b
31(30%)b
36(35%)
103
a
P \0.001.
Not significant.
b
receptive fields of the polysensory neurons of the parietal
cortex were transferred to the video screen, after training the
monkey to grasp the food morsel guided by the video image.
Kurata and Hoshi (2002) also described the representation of
screen-based visual coordinates by PMv neurons, and reported
further that the PMv is concerned with the transformation of
visual coordinates created by prism adaptation of reaching. A
previous report from our laboratory (Ochiai et al., 2002) also
demonstrated that PMd neurons reflected the direction of
image motion in the video system, in a similar fashion as PMv
neurons, despite the fact that neuronal activity was observed
predominantly during a delay period.
Our study has direct relevance to a recent study by Kakei
et al. (2001) in which the activity of PMv neurons was examined
in a monkey that performed wrist movements in four directions
while maintaining three different postures. Kakei et al. reported
for the first time that the activity of PMv neurons reflected the
direction of wrist movement independent of forearm posture.
This observation implied that direction selectivity was independent of the changes in the angles of joints or the combination of
muscle activity that was required for each of the four directional
movements. It is remarkable that the findings of Kakei et al.
revealed that the activity of PMv neurons encoded the direction
of movement in space. Nevertheless, as the authors pointed out
in their paper, these findings may be interpreted in at least three
different ways: PMv neurons may represent the direction of limb
movement in space, the direction of movement of the object
that is acted upon, and/or the goal or target of the movement.
The findings of the present study appear to support the second
of the three explanations, although we studied neuronal activity
during the performance of a motor task that was dependent on
the visual display of the moving hand, which differs from the
conditions of the task that was used by Kakei et al. In our study,
the hand image served as a visual object to be acted upon,
equivalent to a cursor to be operated in the video screen.
Alternatively, the animal might have recognized the hand image
as a part of its own body. Either way, under this requirement, the
PMv activity appeared not to be concerned with controlling
movement in an intrinsic limb-based coordinate frame. Instead,
it seems to be involved in controlling movement in a coordinate
frame that adapted to the visual reference frame provided by the
hand image projection system. Our finding is consistent with
recent observations by Schwartz et al. (2004) demonstrating
cortical activity as representing image motion to be controlled.
The properties of our PMv activity, however, favor the interpretation of action rather than perception as a primary
representation of the PMv.
In the dorsal part of the premotor cortex (PMd), Shen and
Alexander (1997) reported neuronal activity reflecting the
spatial target being reached for. At first sight, our present findings
appear to contradict this report because PMv activity did not
reflect the spatial location of the target on the screen (see Fig. 6).
However, it is possible that neuronal activity in the PMv may
reflect the spatial location of the target in a hand-centered frame
of reference, rather than a body-centered frame of reference.
Also, the target representation of Shen and Alexander might
have been centered on a cursor that moved with the hand.
Such coordinate representation was reported by Buneo et al.
(2002), who found that neurons in the posterior parietal cortex
(the parietal area projecting to the PMd) are coding target
locations with respect to the hand, as well as the eye.
On the other hand, our findings demonstrating hand-side
selectivity emphasize one additional aspect of representation in
Cerebral Cortex July 2005, V 15 N 7 935
the PMv, namely the spatial coding of the PMv centered on
a specific point in the object to be moved. PMv neurons have
been reported to encode the spatial position of a body part
(Graziano et al., 1994) or space based on objects that are acted
upon (Murata et al., 1997; cf. Galati et al., 2000). This is different
to the representation of the relative position of a target within
objects that are to be captured (Olson and Gettner, 1995). In
our study, the image of the hand was a visual object that was to
be moved towards a target in space. Furthermore, hand-side
selectivity was unaffected by shifting the initial position of the
hand in the video image, which suggests that the neuronal
activity in the PMv depended on the spatial relationship of the
point of interest referenced both to the moving hand and the
target. Therefore, our findings suggest that the PMv determines
which part of the body moves in which direction. Namely, the
PMv seems to be involved in controlling movement in a coordinate frame that adapts to the reference frame of the object
to be moved. PMv neurons appeared to be relatively more
involved in specifying a specific point of interest in the moving
object than PMd neurons (Table 3), though direct comparison
of both areas was not possible. Although our results were
obtained under artificial conditions in which hand movements
depended crucially on the visual image of the motion of the
hand, such behavioral conditions are often applicable to
behavioral conditions in everyday life, such as operating
a computer mouse or other tools that are used to point to
a target that is presented on a video display unit. One weakness
of this study is that our findings are based on one animal.
Although the sample size of neurons was large enough to
identify properties of PMv cells reported, our findings need
ideally to be confirmed in a different animal. Thus, interpretation of the present data should proceed with caution.
Based on the present findings, we wish to propose a view that
PMv is representing the action of a controlled object in visual
coordinates, as a part of a general concept of higher-order
representation in cortical motor areas. Such a concept of
representation at an abstract level has been proposed in studies
reporting cognitive control of spatiotemporal motor variables
(Georgopoulos, 2002), in multilevel visuomotor transformations
(Caminiti et al., 1998; Buneo et al., 2002; Battaglia-Mayer et al.,
2003), and in effector-independent representations of action
(Cisek et al. 2003; Fujii et al. 2002).
Notes
We thank M. Kurama and Y. Takahashi for technical assistance. This
work was supported by CREST, JST, RR2002 and the Ministry of
Education, Culture, Sports, Science and Technology, Japan. This work
was supported by the Cooperation Research Program of Primate
Research Institute, Kyoto University.
Address correspondence to Jun Tanji, Department of Physiology,
Tohoku University School of Medicine, 2-1 Seiryo-Cho, Aoba-Ku, Sendai
980, Japan. Email: [email protected]
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