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The Journal of Neuroscience, April 15, 2001, 21(8):2784-2792
Consistent Features in the Forelimb Representation of Primary
Motor Cortex in Rhesus Macaques
Michael C.
Park1,
Abderraouf
Belhaj-Saïf1,
Michael
Gordon2, and
Paul
D.
Cheney1
1 Department of Molecular and Integrative Physiology
and Mental Retardation Research Center, and 2 Departments
of Pharmacology and Surgery, University of Kansas Medical Center,
Kansas City, Kansas 66160
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ABSTRACT |
The purpose of this study was to systematically map the
forelimb area of primary motor cortex (M1) in rhesus macaques in an effort to investigate further the organization of motor output to
distal and proximal muscles. We used stimulus-triggered averaging (StTAing) of electromyographic activity to map the cortical
representation of 24 simultaneously recorded forelimb muscles. StTAs
were obtained by applying 15 µA stimuli to M1 sites while the monkey
performed a reach and prehension task. Motor output to body regions
other than the forelimb (e.g., face, trunk, and hindlimb) was
identified using repetitive intracortical microstimulation to evoke
movements. Detailed, muscle-based maps of M1 revealed a central core of
distal (wrist, digit, and intrinsic hand) muscle representation
surrounded by a "horseshoe"-shaped zone of proximal (shoulder and
elbow) muscle representation. The core distal and proximal zones were separated by a relatively large region representing combinations of
both distal and proximal muscles. On the basis of its size and
characteristics, we argue that this zone is not simply the result of
stimulus-current spread, but rather a distinct zone within the forelimb
representation containing cells that specify functional synergies of
distal and proximal muscles. Electrode tracks extending medially from
the medial arm of the proximal muscle representation evoked trunk and
hindlimb responses. No distal or proximal muscle poststimulus effects
were found in this region. These results argue against the existence of
a second, major noncontiguous distal or proximal forelimb
representation located medially within the macaque M1 representation.
Key words:
forelimb; muscles; stimulus-triggered averaging; poststimulus facilitation; EMG; macaque; primary motor cortex
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INTRODUCTION |
Using intracortical microstimulation
(ICMS) (Asanuma and Sakata, 1967 ) to evoke movements or
electromyographic (EMG) responses in monkeys, several studies have
described a central core of distal forelimb muscle representation
surrounded by a proximal forelimb muscle representation in the primary
motor cortex (M1) (Kwan et al., 1978a,b; Strick and Preston, 1978,
1982a; Gould et al., 1986; Hepp-Raymond, 1988; Nudo et al., 1992, 1996;
Stepniewska et al., 1993; Karrer et al., 1995; Nudo and Milliken,
1996). In macaque monkeys, Kwan et al. (1978a,b) concluded that the M1
representation of forelimb muscles is organized as concentric rings in
which the intrinsic hand muscles are represented as a central core
surrounded by rings of increasing diameter representing the wrist,
elbow, and shoulder muscles.
After injecting the fluorescent tracers fast blue and diamidino
yellow into different segmental levels of spinal cord in pig-tailed macaques to label forelimb corticospinal neurons supplying proximal (C2-C4 injections) and distal (C7-T1 injections) motoneuron pools, He
et al. (1993) found evidence consistent with the existence of a central
core of distal (wrist, digit, and intrinsic hand) muscle
representation, largely contained within the wall of the precentral
gyrus, surrounded by a "horseshoe"-shaped proximal (shoulder and
elbow) muscle representation that was open at the area 3a/4 boundary.
In addition, they suggested the existence of noncontiguous second
representations of distal and proximal forelimb muscles in M1 (He et
al., 1993, their Fig. 18). These second representations appeared
to be located medial to the medial arm of the core proximal forelimb
representation. However, there currently is no electrophysiological
evidence of major noncontiguous distal and proximal forelimb
representations within M1 of macaque monkeys. Multiple representations
have been demonstrated electrophysiologically within the core primary
distal forelimb representation in squirrel monkeys as alternating bands
of wrist and digit muscles with differing sensory input. The caudal
bands of wrist and digit representation receive input predominantly
from cutaneous receptors, whereas the rostral bands receive input from
deep receptors (Strick and Preston, 1978, 1982a,b).
Therefore, the purpose of this study was to systematically map
the forelimb area of M1 in an effort to further investigate motor
output organization and the issue of multiple noncontiguous representations of distal and proximal muscles. To maximize the potential for detecting multiple representations, we recorded EMG
activity from 24 different forelimb muscles simultaneously while the
monkey performed a movement task (Park et al., 2000). Stimulus-triggered averaging (StTAing) of EMG activity was used to
detect the latency and strength of output effects on individual muscles
(Cheney and Fetz, 1985; Cheney, 1996). The resulting motor output maps
of M1 show a central core of distal muscle representation surrounded by
a horseshoe-shaped proximal muscle representation, confirming the
findings from corticospinal labeling studies (He et al., 1993).
However, there was no evidence of a second, major distal or proximal
forelimb representation within M1 of rhesus macaques. In addition, a
large zone producing effects in both proximal and distal muscles
separated the pure distal muscle core from the surrounding pure
proximal muscle zone.
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MATERIALS AND METHODS |
Behavioral task. Data were collected from two male
rhesus monkeys (Macaca mulatta; ~9 kg, 6 years old). The
monkeys were trained to perform a reach and prehension task requiring
coactivation of multiple proximal and distal forelimb muscles in
natural, functional synergies. Training procedures and the behavioral
task have been described in detail previously (Belhaj-Saïf et
al., 1998; McKiernan et al., 1998). Briefly, during each data
collection session, the monkey was seated in a custom primate chair and
placed in a sound-attenuating chamber. The left forelimb of the monkey
was restrained during task performance, whereas the right forelimb had
freedom of movement. The monkey was guided in performance of the task
by audio and video cues provided by an IBM-compatible computer. The
monkey initiated the task by placing its right hand on a pressure plate located at waist height directly in front of him. Having the hand on
the plate for a preprogrammed length of time triggered the release of a
food reward and a "go" signal. The monkey then reached out
to a small food well located at shoulder level, a little less than one
arm length away and oriented ~20° from vertical. The monkey used a
precision grip to extract a food pellet from the well and bring the
pellet to its mouth. The task was completed by returning the hand to
the pressure plate.
Surgical procedures. On completion of training, each monkey
was implanted with a cortical recording chamber and EMG electrodes. For
all implant surgeries, the monkeys were tranquilized initially with
ketamine, administered atropine, and subsequently anesthetized with
isoflurane gas. Both monkeys received prophylactic antibiotic before
and after surgery and analgesic medication postoperatively (Park
et al., 2000). All surgeries were performed in a facility accredited by
the Association for Assessment and Accreditation of Laboratory Animal
Care using full sterile procedures. All procedures conformed to
the Guide for the Care and Use of Laboratory Animals, published by the United States Department of Health and Human Services
and the National Institutes of Health.
A magnetic resonance imaging (MRI)-compatible plastic chamber allowing
exploration of a 30-mm-diameter area (see Fig.
3A,B) was stereotaxically implanted
over the forelimb area on the left hemisphere of each monkey as
described previously (Kasser and Cheney, 1985; Mewes and Cheney, 1991;
McKiernan et al., 1998). The chambers were centered at anterior 21.6 mm, lateral 11.4 mm (monkey M), and anterior 16.0 mm, lateral 7.4 mm
(monkey D), at a 30° angle to the midsagittal plane. For MRI
compatibility, titanium screws (Bioplate, Los Angeles, CA) and titanium
restraining nuts (McMaster-Carr, Chicago, IL) were used. In addition, a
titanium screw (Synthes, Monument, CO) in contact with the dura served as a reference ground for electrophysiology.
EMG activity from 24 muscles of the forelimb was recorded using pairs
of multistranded stainless steel wires (Cooner Wire, Chatsworth, CA)
implanted during a sterile surgical operation. One monkey was implanted
using a modular subcutaneous implant technique, and the other was
implanted using a cranial subcutaneous implant technique. These
procedures were described in detail previously by Park et al.
(2000). Briefly, for both techniques, pairs of wires for each
muscle were tunneled subcutaneously to their target muscles. The
modular subcutaneous implant technique used four connector (ITT Canon,
New Britain, CT) modules, two placed above and two below the elbow. The
cranial subcutaneous implant technique used one circular connector
(Wire Pro Inc., Salem, NJ) module placed near the cortical recording
chamber. The wire insertion points for specific muscles were identified
on the basis of external landmarks and palpation of the muscle belly.
The wires of each pair were bared of insulation for ~2 mm at the tip
and inserted into the muscle with a separation of ~5 mm. We tested
proper placement by stimulating electrically through the wires with
short trains or single pulses while observing the evoked movements. The
wires were removed and reinserted if necessary.
EMGs were recorded from five shoulder muscles: pectoralis major
(PEC), anterior deltoid (ADE), posterior deltoid (PDE), teres major
(TMAJ), and latissimus dorsi (LAT); seven elbow muscles: biceps short
head (BIS), biceps long head (BIL), brachialis (BRA), brachioradialis
(BR), triceps long head (TLON), triceps lateral head (TLAT), and
dorso-epitrochlearis (DE); five wrist muscles: extensor carpi radialis
(ECR), extensor carpi ulnaris (ECU), flexor carpi radialis (FCR),
flexor carpi ulnaris (FCU), and palmaris longus (PL); five digit
muscles: extensor digitorum communis (EDC), extensor digitorum 2 and 3 (ED23), extensor digitorum 4 and 5 (ED45), flexor digitorum
superficialis (FDS), and flexor digitorum profundus (FDP); and two
intrinsic hand muscles: abductor pollicis brevis (APB) and first dorsal
interosseus (FDI). At regular intervals, the monkeys were tranquilized
with ketamine, and the implants were tested to confirm electrode location.
Data recording. For cortical recording and stimulation, we
used glass- and mylar-insulated platinum-iridium electrodes with typical impedances between 0.7 and 1.5 M (Frederick Haer & Co., Bowdoinham, ME). Electrode penetrations were made systematically in
precentral and postcentral cortex in a 1 mm grid interval. In some
areas, electrode tracks were placed in the center of the 1 mm square
formed by four adjacent tracks to achieve greater spatial resolution.
The electrode was advanced with a manual hydraulic microdrive, and
stimulation was performed at 0.5 mm intervals, starting from the first
cortical electrical activity encountered. In some tracks, stimulation
was performed at 0.25 mm intervals. Cortical electrical activity and
EMG activity were simultaneously monitored along with task-related signals.
While the monkey performed the reach and prehension task, stimuli (15 µA at 15 Hz) were applied through the electrode and served as
triggers for computing StTAs. Individual stimuli were symmetrical
biphasic pulses: a 0.2 msec negative pulse followed by a 0.2 msec
positive pulse. EMGs were digitized at a rate of 4 kHz, and averages
were generally compiled over a 60 msec epoch, including 20 msec before
the trigger to 40 msec after the trigger. Stimuli were applied
throughout all phases of the reach and prehension task, and the
assessment of effects was based on StTAs of at least 500 trigger
events. Segments of EMG activity associated with each stimulus were
evaluated and accepted for averaging only when the average of all EMG
data points over the entire 60 msec epoch was  5% of full-scale
input. This prevented averaging segments in which EMG activity was
minimal or absent (McKiernan et al., 1998).
At some stimulation sites, averages were computed at 30 µA if no
poststimulus effects (PStEs) were obtained at 15 µA. When no PStEs
were detected with 30 µA, repetitive ICMS (R-ICMS) was performed to
determine the motor output representation, if any, from that site.
R-ICMS consisted of a train of 10 symmetrical biphasic stimulus pulses
(negative-positive with total duration of 0.4 msec) at a frequency of
330 Hz (Asanuma and Rosén, 1972) and intensity of 15 and/or 30 µA. Evoked movements and muscle contractions detected with palpation
were noted.
Data analysis. At each stimulation site, averages were
obtained from all 24 muscles. Poststimulus facilitation (PStF) and suppression (PStS) effects were computer-measured as described in
detail by Mewes and Cheney (1991). The focus of this study was on maps
of PStF effects; hence, PStS effects were excluded. Nonstationary,
ramping baseline activity (Lemon et al., 1986) was routinely subtracted
from StTAs using custom analysis software. Mean baseline activity and
SD were determined for the average of EMG activity in the
pretrigger period consisting of the first 12.5 msec of each average.
StTAs were considered to have a significant PStF effect if the envelope
of the StTA crossed a level equivalent to 2 SD of the mean of the
baseline EMG for a period 0.75 msec. Onset and offset latencies of
PStF were defined as the points at which the envelope of the StTA
crossed a level equivalent to 2 SD of the mean of the baseline EMG. The
peak of each effect was defined as the highest point in PStF between
the onset and offset latencies.
The strengths of PStF effects were categorized as follows. Peaks <2 SD
of baseline and peaks that remained >2 SD for <0.75 msec period were
considered insignificant, and the average was categorized as having no
effect (Fig. 1A). Weak
PStF effects had peaks >2 SD of mean baseline activity but  5 SD of
mean baseline activity (Fig. 1B). Moderate and strong
effects had peaks >5 SD and, for the purposes of this study, were
lumped together (Fig. 1C). Our maps were based on either
moderate and strong effects alone or moderate and strong effects
combined with weak effects.
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Figure 1.
Examples of stimulus-triggered averages of
rectified EMG activity (15 µA at 15 Hz) illustrating the criteria
used for categorizing the strength of poststimulus facilitation
(PStF) effects. Time 0 corresponds to the
stimulus event used as a trigger for averaging. A pretrigger period of
12.5 msec (baseline) was used to determine mean baseline
activity (mean) and SD for each average.
A, Peaks <2 SD of baseline and peaks that remained >2
SD for <0.75 msec period were considered insignificant, and the
average was categorized as having no effect. B, Weak
effects had peaks >2 SD of mean baseline activity but 5 SD of mean
baseline activity. C, Moderate and strong effects had
peaks >5 SD of mean baseline activity. LAT, Latissimus
dorsi; FDI, first dorsal interosseus;
APB, abductor pollicis brevis. The number
of trigger events is given in parentheses.
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Magnetic resonance imaging and analysis. MRI was used for
confirmation of electrode track locations rather than actual histology, because the monkeys are part of another ongoing study. MRI studies were
performed ~5 months after the cortical recording chamber implant but
before the EMG implant. The monkeys were tranquilized with ketamine and
atropine and subsequently anesthetized with isoflurane gas. To give the
magnetic resonance (MR) images a reference framework, a custom-designed
chamber cap filled with MR opaque marker (liquid vitamin E) was used to
identify the x and y axes [anterior-posterior
(A-P) and medial-lateral (M-L) axes, respectively] of the cortical
recording chamber (see Fig. 3A,B)
as a cross.
MRI studies were performed using a 1.5 Tesla Siemens 63SPA system
(Siemens, Iselin, NJ) with a circularly polarized knee coil. Three-dimensional Magnetization Prepared Rapid Gradient Echo
(3D-MPRAGE) sequence was acquired with the following parameters:
repetition time = 10 msec, echo time = 4 msec, inversion
time = 750 msec, flip angle 10, matrix 192 × 256, slice
thickness 1.5 mm, and field of view 250 mm. MR images were transferred
by local area network to an HP9000 C360 computer system
(Hewlett-Packard, Palo Alto, CA) with an FX-4 graphics subsystem. MR
image analysis was performed using Omniview 2D and 3D visualization
software (3D Biomedical Imaging, Inc., Shawnee Mission, KS). The
3D-MPRAGE protocol was used to obtain axial images with a slice
thickness of 1.0 mm. This protocol typically yielded 100-130 MR axial
images and offered excellent spatial resolution because of thin slice
thickness, minimizing volume-averaging effects. The thin slice
thickness made it possible to maintain adequate resolution after
multiplanar image reformations.
MR image analysis software allowed visualization of an acquired image
set in any plane of interest. Thus, computer-assisted multiplanar image
reformations were performed with respect to the reference framework
previously highlighted with vitamin E marker. The resulting oblique
parasagittal images were orthogonal to the M-L axis and in register
with the chamber coordinate system. The images were parallel to a
series of electrode tracks having the same M-L coordinate. For example,
an oblique parasagittal image at lateral 4 would represent a slice
through the cortex showing all electrode tracks for which the M-L
chamber coordinate was lateral 4. The reformed images were then traced
to highlight gray matter, white matter, and the central sulcus (Fig.
2C).
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Figure 2.
Method for flattening and unfolding cortical layer
V in the anterior bank of the central sulcus for two-dimensional
representation. A, Parasagittal diagram representing the
stimulated cortex, constructed from electrode tracks with the same M-L
coordinate (4L) organized in an anterior-to-posterior
order. Identification of white matter-gray matter border (thin
line), central sulcus (CS), and sensory cortex
were based on electrophysiological observations. Then, reference lines
(dashed lines), similar to those used by Sato and Tanji
(1989), were placed onto the diagram to represent cortical layer V. A
horizontal reference line
(h) was placed at 1.5 mm depth, and a
vertical reference line (v) was
placed at 1.5 mm from the estimated central sulcus to approximate the
position of layer V. The intersection of the reference lines
(asterisk) was defined to be the convexity of the
precentral gyrus. Projecting the selected stimulation sites ( ) onto
the reference lines, when necessary, flattened the curvature of layer
V. In the case of track 2P, stimulation at a depth of 1.0 mm () is
projected onto the reference line h ( ). In this
track, the 1.5 mm site was not used because the effects at 1.0 mm were
much stronger. B, Flattened and unfolded two-dimensional
map of cortical layer V. Layer V was unfolded by rotating the reference
line v with respect to the convexity of the
precentral gyrus (asterisk). This straightened
the two reference lines into one line (dashed line).
Completing this manipulation for all tracks yielded a two-dimensional
map of M1. C, Tracing of an MR image through the same
parasagittal plane as 4L with overlaid electrode tracks and stimulation
sites corresponding to layer V (). A, Anterior;
P, posterior; L, lateral;
M, medial.
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Unfolding the cortex. A two-dimensional rendering of
cortical layer V in the anterior bank of the central sulcus required flattening and unfolding its curvature. First, all electrode tracks were grouped according to their M-L coordinate. Within each group, the
tracks were then ordered according to their A-P coordinate. On the
basis of electrophysiological data and observations, a parasagittal
diagram was constructed to represent the cortex that was explored and
stimulated (Fig. 2A). White matter was identified by
a sharp decrease or loss of background cell activity. Sensory cortex
was identified by the presence of distinctive spike activity and
characteristic receptive fields (Widener and Cheney, 1997). For each
electrode track, sites corresponding to cortical layer V were
identified using a combination of electrode depth, strength of PStF
effects, and reconstruction of precentral geometry in relation to MRI
sections. Electrode penetrations on the convexity of the gyrus
traversed cortical layers perpendicularly, and in these cases, it was
relatively easy to identify the stimulation site closest to layer V. For electrode penetrations traversing the depth of the precentral gyrus
and extending roughly parallel to the cortical layers, it was more
difficult to identify layer V sites. In these cases, output effects
from sites at the same depth from different electrode tracks along the
A-P axis were compared. Selection of sites closest to layer V was based
on the strength of PStF and reconstruction of the position of the sites in relation to MRI parasagittal sections oriented along the same A-P
axis as the electrode tracks. This analysis yielded a series of
reconstructed parasagittal cortical sections oriented along the A-P
axis of the chamber in the plane of the electrode tracks (Fig.
2A,C).
Reference lines, similar to those used by Sato and Tanji (1989), were
then placed on the diagram to represent cortical layer V. A horizontal
reference line (h) was placed at a depth of 1.5 mm,
and a vertical reference line (v) was placed typically at 1.5 mm anterior to the estimated location of central sulcus (Fig. 2A). The intersection of the reference lines, marked
with an asterisk in Figure 2A, defined the
convexity of the precentral gyrus. Stimulation data (PStEs) from sites
corresponding to cortical layer V were projected onto the reference
lines (Fig. 2A). Then, layer V was unfolded by
rotating the reference line v with respect to the convexity of the
precentral gyrus. This straightened the two reference lines into one
line. The resulting unfolded reference line then gave rise to the
coordinates for each stimulation site on the two-dimensional map (Fig.
2B).
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RESULTS |
Data were collected from the left M1 in two rhesus monkeys. There
were a total of 248 electrode tracks, 115 tracks in monkey D (Fig.
3A) and 133 tracks in monkey M
(Fig. 3B). StTAing (15 µA) of rectified EMG activity from
24 forelimb muscles was performed at 2477 sites, 1072 (43.3% of total)
sites in monkey D and 1405 (56.7% of total) sites in monkey M,
resulting in a total of 59,448 StTA records. In addition, R-ICMS was
performed at 359 sites, 210 in monkey D and 149 in monkey M. R-ICMS was
performed at sites where no PStEs were observed with StTAing at
intensities up to 30 µA. On the basis of the criteria described
earlier, stimulation sites corresponding to cortical layer V were
selected, and only their PStEs and evoked movements were used for
mapping. This yielded a total of 361 sites and 8664 StTA records (209 sites in monkey D and 152 sites in monkey M). Forty-eight percent of
PStF effects were in extensor muscles, and 52% were in flexor muscles
(excludes intrinsic hand muscles). Forty-nine percent of sites
facilitated a combination of at least one flexor muscle and one
extensor muscle at the same joint (cofacilitation site). Overall,
effects in distal muscles were two times greater than effects in
proximal muscles. StTAs were obtained from all 24 muscles at each
stimulation site. An example of PStEs obtained at one layer V site is
shown in Figure 4. In this case, clear
PStF effects were observed in both proximal and distal forelimb
muscles. Accordingly, this site was categorized as one producing
effects in both proximal and distal muscles.
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Figure 3.
A, B, Cortical
recording chambers implanted over M1 cortex in monkeys D and M,
respectively. The coordinate system (5 mm grid) is
overlaid in yellow, and locations of electrode tracks
are indicated with black-outlined red dots. The
large black rectangle overlying each chamber identifies
the cortical area represented in maps C-F. In monkey D, a 15 mm
incision was made in the dura for visual identification of the central
sulcus. C-F, Maps of motor cortex for
two monkeys represented in two-dimensional coordinates after unfolding
the precentral gyrus. C, D, Maps for
monkeys D and M, respectively, based on strong and moderate PStF
effects together with R-ICMS-evoked movements. E,
F, Maps for monkeys D and M, respectively, based on
weak, moderate, and strong effects together with R-ICMS-evoked
movements.
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Figure 4.
Distribution of PStF effects in forelimb muscles
from a PDC site. Time 0 corresponds to the stimulus event used for the
average. Stimulation was 15 µA at 15 Hz. Moderate and strong PStF
effects were observed in both proximal (BIS,
BIL, BRA, BR,
TLON, PEC) and distal
(APB, FDI, FDP,
ED23) forelimb muscles. The range of number of trigger
events for different channels is given in parentheses.
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Ninety (25.1%) of the total R-ICMS sites (45 sites in monkey D and 45 sites in monkey M) were judged as corresponding to layer V. R-ICMS was
used mainly to identify sites that did not produce any poststimulus
effects, i.e., representations of trunk, hindlimb, and face. However,
in one monkey, evoked movements from R-ICMS were also used to
define some forelimb sites. Specifically, 14 of 71 sites (20%) mapped
as proximal sites were defined solely by R-ICMS. However, these sites
were located between sites already defined by PStE (for example in the
center of the 1 × 1 mm grid defined by StTA). Because the site
category based on R-ICMS matched the category of adjacent sites based
on PStE, many of these sites did not affect the map boundaries. Only 8 of 71 sites (11%) helped to define the anterior (6 sites) and
medial (2 sites) borders of the proximal muscle representation. Also,
only 1 of 47 sites (2%) was categorized as producing effects in both
proximal and distal muscles solely on the basis of R-ICMS data.
Motor output maps (Fig. 3C-F) constructed from
effects at all layer V sites revealed a central core of distal forelimb
muscle representation contained largely within the wall of the
precentral gyrus. This core distal representation extended
mediolaterally along the caudal border of M1 and was surrounded on all
sides, except at the area 4/3a border, by a horseshoe-shaped zone of proximal forelimb muscle representation. The medial and lateral arms of
the horseshoe extend posteriorly down the wall of the precentral gyrus
and terminate at the area 4/3a border. Also, there was a substantial
region separating the core distal and proximal representations at which
StTAing produced effects in both proximal and distal forelimb muscles.
On the basis of arguments presented in Discussion, we believe this area
is not simply the result of current spread to the core distal and
proximal representations. Accordingly, we will refer to it as the
proximal-distal cofacilitation (PDC) zone. In a few places, the
proximal muscle representation is fragmented into small islands by the
PDC zone. Similarly, in both monkeys, the PDC zone is fragmented into
noncontiguous medial and lateral components by the distal
representation. The inclusion of weak PStF effects in the motor output
maps (Fig. 3E,F) did not
significantly alter the general features of the maps (Fig. 3C,D). However, when weak effects were included,
the PDC zone did appear as one contiguous representation, although
small islands of proximal muscle representation remained.
The boundary of the core forelimb representation was determined
carefully. Stimulation sites immediately anterior to the primary forelimb representation yielded no PStE with StTA at 15 and 30 µA,
and no movements were evoked with R-ICMS at 15 and 30 µA. Stimulation
sites posterior to the primary forelimb representation or deep in the
sulcus were characterized as being either sensory cortex or white
matter. Stimulation sites extending laterally from the horseshoe also
produced no PStE with StTA at 15 and 30 µA. However, at these sites,
R-ICMS at both 15 and 30 µA evoked movements of the upper and lower
lips, thus revealing a face representation. Similarly and most notably,
stimulation sites extending medially from the medial arm of proximal
muscle representation produced no PStE with StTA at 15 and 30 µA.
However, at these sites, R-ICMS at both 15 and 30 µA revealed
components of a trunk and hindlimb representation. No evidence of a
second noncontiguous distal or proximal forelimb representation was
found (Fig. 3C-F).
Figures 5 and
6 illustrate the StTAs obtained from
sites in M1 for a proximal muscle, BIS, and for a distal muscle, EDC.
Each record in these figures is color-coded for strength of the PStF (see color key at the top of the Figures). The distribution of PStF
effects for BIS and EDC revealed multiple foci of strong effects
(SD > 5.0) for individual muscles represented over the forelimb
area of M1. In the case of BIS, these multiple foci are separated by
sites that yielded no effects, whereas in the case of EDC, the multiple
foci represent peaks in output separated by valleys in which weaker but
clear effects were present. Most importantly, the sites with EDC PStF
effects are contained completely within the distal muscle zones. This
includes both the distal-only zone (dark blue) and the PDC
zone (purple). Similarly, the sites with BIS PStF
effects are contained completely within the proximal muscles zones.
This includes both the proximal-only zone (pink) and
sites yielding effects on both distal and proximal muscles (purple).
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Figure 5.
Stimulus-triggered averages of rectified EMG
activity (15 µA at 15 Hz) of a proximal muscle, biceps shorthead
(BIS), for monkey D plotted on a two-dimensional map of
M1. Each record is color coded for strength of PStF according to the
number of SDs above pre-trigger baseline activity (color
bar at top of Figure). The color-shaded motor
representation map is taken from Figure 3E.
Yellow line, Convexity of the precentral gyrus;
black dashed line, fundus.
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Figure 6.
Stimulus-triggered averages of rectified EMG
activity (15 µA at 15 Hz) of a distal muscle, extensor digitorum
communis (EDC), for monkey D plotted on a
two-dimensional map of M1. Each record is color coded for strength of
PStF according to the number of SDs above pre-trigger baseline activity
(color bar at top of Figure). The
color-shaded motor representation map is taken from Figure
3E. Yellow line, Convexity of the
precentral gyrus; black dashed line, fundus.
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DISCUSSION |
Figure 7 summarizes the consistent
features of M1 intra-areal forelimb muscle representation in the rhesus
macaque based on our StTAing data. A central core of distal forelimb
muscle representation, oriented mediolaterally along the caudal border
of M1, is surrounded by a horseshoe-shaped zone of proximal forelimb
muscle representation. The proximal muscle representation is
discontinuous at the area 4/3a border. This pattern of representation
is consistent with the work of others using R-ICMS in stumptail
macaques (Kwan et al., 1978a,b) and squirrel monkeys (Strick and
Preston, 1978, 1982a; Nudo et al., 1992, 1996; Nudo and Milliken,
1996). Separating the core distal representation from the surrounding
core proximal representation is a zone yielding effects in both distal
and proximal muscles (PDC zone). A small zone of overlap between the
distal and proximal core representations would be expected because of the spread of stimulus current at the boundary separating the two
representations. However, the width of the PDC zone suggests that it is
a genuine, separate field with neurons that represent combinations of
distal and proximal muscles as functional synergies. At different
points, the width of the PDC zone ranges from <1 to ~2.8 mm in one
monkey and from <1 to ~3.5 mm in the second monkey. This is based on
measurements of a line oriented perpendicular to the distal zone
boundary and reaching to the inner boundary of the proximal zone. We
estimate that the effective physical spread of current from a 15 µA
stimulus would have a radius of 105 µm. This is based on an
intermediate k of 1350 µA/mm2
in the expression:
|
|
where ro is the radius of the
cortical volume containing the directly activated cells, i
is the stimulus current, and k is the proportionality
constant (Stoney et al., 1968; Ranck, 1975; Cheney and Fetz, 1985).
Even using the most minimal value of k (250 µA/mm2) yields 245 µm as the effective
radius of physical stimulus spread. With 105 µm as the effective
radius of physical spread, the width of the boundary zone exhibiting
combined distal and proximal effects attributable simply to current
spread would be 210 µm, far less than the observed width of the PDC
zone. An effective current spread of 245 µm would yield a boundary
zone width of 490 µm, which again is far less than the observed
width. Also worth noting is the fact that if the PDC zone were solely
the result of physical spread of stimulus current, it would be expected
to have a relatively uniform width at different points along its
length, yet the width is highly variable. Finally, if physical spread
were a factor, we would have expected R-ICMS to yield a sizable zone
producing effects in both proximal forelimb muscles and either
trunk-hindlimb muscles medially or facial muscles laterally, but that
was not observed.
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|
Figure 7.
Summary of proximal and distal forelimb muscle
representation in M1 of rhesus macaques based on the motor output
effects in stimulus-triggered averages. Three separable zones are
consistent across monkeys, a central zone oriented mediolaterally along
the caudal border of M1 representing distal muscle synergies,
surrounded by a zone representing synergies involving both distal and
proximal muscles, which, in turn, is surrounded by a zone representing
only proximal muscle synergies. The latter two zones are not complete
circles; rather, they are horseshoe-shaped and open at the 3a/4 border.
The proximal muscle forelimb representation in M1 is bordered laterally
by a face representation and medially by a trunk and hindlimb
representation. We found no evidence supporting the existence of major
distal or proximal muscle representations, separate from the core
representations. A, Anterior; L, lateral;
CS, central sulcus; Fundus, fundus of the
central sulcus; P, proximal; D, distal;
PDC, proximal-distal cofacilitation.
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|
One additional factor possibly contributing to the PDC zone merits
discussion. Although it seems clear that physical spread of stimulus
current cannot adequately account for the PDC zone, physiological
spread of excitation well beyond the site of stimulation is possible
through horizontally oriented connections within the cortex as well as
branching afferent inputs to cortex. However, on the basis of the
measurements of Huntley and Jones (1991), horizontally oriented axons
generally travel for distances of 0.5 mm within the cortex. Moreover,
cortical cell cross-correlation studies suggest that the radius over
which cells show cross-correlation peaks because of underlying synaptic
coupling is largely limited to the area recorded by a single electrode
(Allum et al., 1982) or 0.5 mm (Fetz et al., 1990). On the other hand,
Baker et al. (1998) showed that single ICMS (20 µA) delivered to the
digit representation of forelimb cortex is capable of facilitating the discharge of cortical cells in other parts of the digit representation located 1.5-2.0 mm away from the site of stimulation. However, although these more distant effects exist in response to ICMS, it is
difficult to explain how they might account for the PDC zone observed
in this study. Finally, the existence of a genuine PDC zone is also
supported by our spike-triggered averaging (SpTAing) data showing that
45.5% of individual cortical cells for which activity was modulated
during a reach and prehension task facilitated at least one distal and
one proximal muscle (McKiernan et al., 1998). We suggest that the PDC
zone contains corticospinal cells representing different combinations
of distal and proximal muscles and that these cells are substrates for
coordinated, multijoint movements underlying the reach and prehension task.
Systematic mapping based on stimulus-triggered averaging of EMG
activity from 24 muscles simultaneously in the presence of movement is
a highly sensitive and focal method for which spatial resolution is
exceeded only by SpTAing of EMG activity (Cheney, 1996). StTAing
reveals the motor output effects of neuronal aggregates activated by
the stimulus in the vicinity of the electrode tip (Fetz and Cheney,
1980; Cheney and Fetz, 1985). Previous work has shown that although the
individual effects are stronger, the pattern of the PStF across muscles
obtained with StTAing in the intensity range from 5 to 15 µA closely
matches the pattern of postspike facilitation obtained with SpTAing
from cells at the same site (Cheney and Fetz, 1985). This result
suggests the presence of cell aggregates or modules in which each cell
of the module possesses a similar target muscle field. Such minimal
cortical output modules can be viewed as representing different
combinations of muscles that constitute functional synergies for the
execution of single and multijoint limb movements.
Our data also directly address the issue of multiple distal and
proximal muscle representations within M1. On the basis of retrograde
labeling studies in rhesus macaques, He et al. (1993) suggested the
existence of a second distal representation and possibly even a second
proximal representation located medial to the core proximal
representation, although in their summary diagram (He et al., 1993,
their Fig. 18), the existence of these second representations is
qualified by question marks. We were unable to find clear evidence for
the existence of a major noncontiguous second representation of either
distal or proximal muscles within primary motor cortex, despite running
additional electrode tracks to increase the spatial resolution in
regions in which we anticipated the presence of second representations
based on the maps of He et al. (1993). Stimulation sites located medial
to the medial arm of the proximal muscle representation yielded no
effects in StTAs, but using R-ICMS to evoke movements revealed a
representation of trunk and hindlimb muscles. Similarly, tracks located
laterally to the lateral component of the proximal forelimb
representation yielded no effects in StTAs of forelimb muscle activity,
but R-ICMS revealed a representation of facial muscles. Although
it is true that islands of proximal muscle representation are present
along the lateral and caudal borders of the forelimb representation, these islands are relatively small, and their position is
inconsistent with the second representations described by He et al.
(1993). Moreover, the distal representation in our maps appeared as one continuous representation lacking even small noncontiguous islands. Given the sensitivity of the StTA method, we consider it unlikely that
major second representations of distal or proximal muscles exist within M1.
The accuracy of motor output maps depends on the spatial resolution of
the assessment technique. Most of the data for our maps was based on an
electrode track spacing of 1 mm. Although a 0.5 mm surface grid
interval would have provided finer spatial resolution, it would have
required four times the number of electrode penetrations. We could not
justify this disproportional increase in the number of additional
electrode penetrations. However, to increase spatial resolution in
critical regions, additional electrode penetrations were placed in the
center of the squares formed by the 1 mm grid. Stimulation was
performed at 0.5 mm intervals over the depth of our electrode
penetrations, providing higher resolution for sites located in the bank
of the precentral gyrus. Given that a 15 µA stimulus current should
have a 105-245 µm radius of physical spread, coupled with our
spacing of stimulation sites, it seems improbable that we missed
possible second representations within M1.
| |
FOOTNOTES |
Received July 31, 2000; revised Jan. 16, 2001; accepted Jan. 24, 2001.
This work was supported by National Institute of Neurological Disorders
and Stroke Grant NS39023 and National Institute of Child Health and
Human Development Grant HD02528.
Correspondence should be addressed to Dr. Paul D. Cheney, Mental
Retardation Research Center, University of Kansas Medical Center,
Kansas City, KS 66160-7336. E-mail: pcheney{at}kumc.edu.
| |
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TOP
ABSTRACT
INTRODUCTION
