Download Functional Specialization Within the Cat Red Nucleus

J Neurophysiol
87: 469 – 477, 2002; 10.1152/jn.00949.2000.
Functional Specialization Within the Cat Red Nucleus
K. M. HORN, M. PONG, S. R. BATNI, S. M. LEVY, AND A. R. GIBSON
Division of Neurobiology, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona 85013
Received 29 December 2000; accepted in final form 14 August 2001
The accompanying report (Pong et al. 2002) demonstrates
that projections of the parvicellular red nucleus (RNp) are
stronger at upper cervical levels than at lower cervical levels.
In contrast, projections of magnocellular red nucleus (RNm)
are stronger at lower cervical levels than at upper levels. RNm
receives a major input from the cerebellar interpositus nucleus,
and RNp receives a major input from the cerebellar dentate
nucleus. It is likely that RNm and RNp serve different functions in movement control.
Cells in the red nucleus (RN) discharge strongly during
reaching to grasp an object (Gibson et al. 1985, 1994; van Kan
and McCurdy 2001). The differential spinal projections indicate that RNp may be more important for control of muscles in
the proximal limb, whereas RNm may be more important for
control of muscles of the distal limb. However, most termina-
tions of rubrospinal (RST) fibers are to spinal interneurons
rather than to motor neurons, and terminations at one spinal
level might influence motor neurons at other levels via propriospinal connections (Alstermark et al. 1990; Robinson et al.
1987). The object of the present study was to test the hypothesis that activation of RNp neurons will produce activity in
muscles of the proximal limb and activation of RNm neurons
will produce activity in muscles of the distal limb.
Fetz and Cheney (1980) developed the technique of spiketriggered averaging of electromyography (EMG) to detect
functional relations between cellular activity and muscle activation. By synchronizing the EMG records to the activity of a
single neuron it is possible, with sufficient averaging, to detect
the contribution that the neuron makes to activation of the
target muscle. A variation of spike-triggered averaging is stimulus-triggered averaging, which elicits neural activity with
electrical stimulation. Stimulus-triggered averaging has some
practical advantages over spike-triggered averaging. One advantage is that the experimental demands are less because
single units do not need to be isolated for a prolonged averaging period. A second advantage is that stimulation has a relatively strong effect on muscle activation because more than one
neuron is activated by the stimulus pulse. These advantages
allow more data to be collected from each subject; this is an
important consideration when dealing with behaving animals
with EMG electrodes implanted into several muscles. Direct
comparisons between spike- and stimulus-triggered averaging
in motor cortex (Cheney and Fetz 1985) and red nucleus
(Cheney et al. 1991) indicate that patterns of EMG facilitation
and suppression are in good agreement between the two methods.
However, stimulus-triggered averaging has a drawback in
that activation of fibers passing near the stimulation site may
confound the results. This is a major concern with stimulation
within the RN because cerebellar efferents course through the
nucleus to terminate in more rostral regions of RN as well as
thalamus. Additionally, efferents from lateral regions of RN
pass through medial regions of the nucleus as they decussate to
form the rubrospinal tract (RST). Data from the cases reported
in the preceding paper (Pong et al. 2002) show that, for a short
distance after decussation, the fibers from RNp and RNm are
segregated in the RST. The RNm fibers travel dorsally to fibers
from RNp until they reach caudal pontine levels where they
intermingle. In this paper, we compare stimulus-triggered averages (StTAs) of forelimb muscles with stimulation sites in
Address for reprint requests: K. M. Horn, Div. of Neurobiology, Barrow
Neurological Institute, St. Joseph’s Hospital and Medical Center, 350 W.
Thomas Rd., Phoenix, AZ 85013 (E-mail: [email protected]).
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.
INTRODUCTION
www.jn.org
0022-3077/02 $5.00 Copyright © 2002 The American Physiological Society
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Horn, K. M., M. Pong, S. R. Batni, S. M. Levy, and A. R.
Gibson. Functional specialization within the cat red nucleus. J Neurophysiol 87: 469 – 477, 2002; 10.1152/jn.00949.2000. Magnocellular
(RNm) and parvicellular (RNp) divisions of the cat red nucleus (RN)
project to the cervical spinal cord. RNp projects more heavily to upper
cervical levels and RNm projects more heavily to lower levels. The
cells in RN are active during reaching and grasping, and the differences in termination suggest that the divisions influence different
musculature during this behavior. However, the spinal termination
may not reflect function because most rubrospinal terminations are to
interneuronal regions, which can influence motor neurons at other
spinal levels. To test for functional differences between RNm and
RNp, we selectively stimulated RNm and RNp as well as the efferent
fibers from each region. Electromyographic activity was recorded
from seven muscles of the cat forelimb during reaching. The activity
from each muscle was averaged over several thousand stimuli to
detect influences of stimulation on muscle activity. Stimulation within
the RN produced a characteristic pattern of poststimulus effects. The
digit dorsiflexor, extensor digitorum communis (edc), was most likely
to show facilitation, and several other muscles showed suppression.
The pattern of activation did not differ between RNm and RNp. In
contrast, stimulation of RNp fibers favored facilitation of shoulder
muscles (spinodeltoideus and supraspinatus), and stimulation of RNm
fibers favored facilitation of digit and wrist muscles (edc, palmaris
longus, and extensor carpi ulnaris). Fiber stimulation produced few
instances of poststimulus suppression. The results from fiber stimulation indicate that the physiological actions of RNm and RNp match
their levels of spinal termination. The complex pattern of facilitation
and suppression seen with RN stimulation may reflect synaptic actions
within the nucleus.
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HORN, PONG, BATNI, LEVY, AND GIBSON
METHODS
Behavioral paradigm
Five cats were trained to reach, grasp, and retrieve a handle on
presentation of a tone. The cats received a small quantity of pureed
chicken and cod liver oil extruded from the end of the handle. Cats
typically performed 200 –500 trials during daily training sessions of
1–2 h. The cats were provided supplemental food in their home cages
to maintain their body weights between 80 and 100% of free-feeding
weight.
Implant surgery
Surgery was performed in an American Association of Laboratory
Animal Care-approved surgical suite using aseptic techniques. All
procedures were approved by the St. Joseph’s Hospital Institutional
Animal Care and Use Committee and were in accordance with National Institutes of Health guidelines. Each cat was initially anesthetized with an intramuscular injection of ketamine hydrochloride
(10 –15 mg/kg), and anesthesia was maintained with intravenous
administration of pentobarbital sodium. A recording chamber and a
head restraint device were fastened to the skull with stainless steel
screws and dental acrylic. For three cats, the chamber was positioned
to provide access to the RN (A4.0, Berman 1968). In one cat, the
chamber was positioned (P2.0) to provide access to the RST at
mesencephalic levels, and, in another, the chamber was positioned to
provide access to the RST at medullary levels (P10.0).
For each cat, seven pairs of insulated multi-stranded stainless steel
wire were implanted into forelimb muscles. Each electrode had a tip
exposure of 4 – 6 mm, and the tips of each pair were separated by 5–10
mm. Placement was confirmed by electrical stimulation through the
electrodes. Table 1 lists the implanted muscles and their physiological
actions.
RST tracing
TABLE
1. Implanted forelimb muscles
Muscle
Joint Action
Physiological Role
Extensor digitorum
communis (edc)
Palmaris longus (pl)
Extensor carpi ulnaris (ecu)
Triceps (long head) (tri)
Brachialis (br)
Spinodeltoidius (sd)
Supraspinatus (ss)
Digit extensor
Digit flexor
Wrist extensor
Elbow extensor
Elbow flexor
Shoulder flexor
Shoulder adductor
Flexor
Extensor
Flexor
Extensor
Flexor
Flexor
Flexor
The actions that the muscles with implanted electromyographic electrodes
exert about the forelimb joints and their physiologic anti-gravity roles.
Neural and EMG recordings
Neural activity within the RNm or RST was recorded with tungsten
microelectrodes. Cells in RNm and RNp discharged during movements of the contralateral limbs. Spike amplitudes from cells in RNp
tended to be smaller than amplitudes of cells in RNm, and fiber
recordings in RST were characterized by waveforms with initial
positive deflections (van Kan et al. 1993).
EMG activity was recorded with a band-pass of 10 –10,000 Hz,
full-wave rectified, integrated with a 1-ms time constant and sampled
at 4 kHz. Prior to each recording session, the amplifier gain for each
muscle was set to provide peak amplitudes of 5 V during the behavioral task. This procedure was meant to help compensate for changes
in electrodes over time as well as for variations between muscles and
cats. Examples of the rectified and integrated EMG signals from four
muscles during a reach trial are illustrated in Fig. 1A.
StTA and data analysis
StTA of rectified EMG activity were calculated for the different RN
and RST sites. The techniques used in the present study are similar to
those of Cheney et al. (1991). Stimuli were applied at 500- or
1,000-␮m increments along each electrode track. During stimulation,
monophasic negative pulses (0.2-ms duration, 10 Hz, 5–30 ␮A) were
delivered through the tungsten recording electrode while the cat
performed the reaching task. The patterns of muscular activation near
threshold (5–10 ␮A) resulted in similar StTA patterns as generated
with the suprathreshold current of 20 ␮A. Data presented in this report
were collected using stimuli of 20 ␮A with EMG averaged for 2,000
pulses.
StTAs were calculated by computing an average baseline activity
and standard deviation (SD) from 10-ms periods preceding the stimulus pulses. Data were standardized relative to the SD of the baseline
activity. Figure 1B illustrates examples of significant StTAs for the
four muscles shown in A. Several criteria were required for a StTA to
be considered significant. First, the amplitude of the waveform needed
to exceed ⫾3 SDs of baseline activity. Second, the duration of the
significant elevation needed to exceed 2 ms. Third, only StTAs with
waveforms beginning between 3 and 15 ms following the stimulus
pulse were considered as occurring within a physiologically relevant
time frame.
Verification of stimulation sites
The RST tracing presented in this paper is based on case BRN1 of
the previous paper (Pong et al. 2002), and the anatomical methods are
fully described in that paper. For case BRN1, injections of wheat germ
agglutinin-horseradish peroxidase (WGA-HRP) were placed in RNm
on the right side and in RNp on the left side (Fig. 3, see also Fig. 2 of
Pong et al. 2002). By plotting the location of anterogradely labeled
fibers, the trajectories of the descending fibers from these two regions
could be compared across sides of the same frontal sections.
J Neurophysiol • VOL
Marking lesions (⫺10 ␮A for 10 s) were placed at the end of the
experiment. Prior to perfusion, cats received an intramuscular injection of ketamine (20 mg/kg) followed by a lethal dose of sodium
pentobarbital (approximately 25 mg/kg) delivered in a single rapid iv
bolus. Cats were perfused with 10% formalin. The brains were frozen
and sectioned at 50 ␮m. Every section through areas of interest was
collected and stained with either cresyl violet or neutral red/luxol blue.
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RN, RST at caudal mesencephalic levels (segregated fibers),
and RST at medullary levels (mixed fibers).
Stimulation within RN produced both facilitation and suppression of limb muscle activity and showed a strong bias in
favor of facilitating a digit muscle, extensor digitorum communis (edc). However, the overall pattern of muscle activation
was similar for stimulation sites in RNm and RNp. At the
mesencephalic stimulation site, stimulation of dorsal regions of
the RST (RNm fibers) produced strong facilitation of edc but
weak facilitation of the shoulder muscles spinodeltoideus (SD)
and supraspinatus (ss). Stimulation in the ventral regions of the
RST (RNp fibers) produced strong facilitation of the shoulder
muscles but weak facilitation of edc. Stimulation of the RST at
medullary levels produced facilitation in all limb muscles with
few instances of suppression. The results indicate that anatomical differences in spinal terminations between RNp and RNm
are reflected by physiological action and suggest that the complex effects seen with RN stimulation may be due to activation
of local neural elements.
FUNCTIONAL SPECIALIZATION WITHIN THE RED NUCLEUS
471
FIG. 1. Records generated during a reaching trial. A: leg position
was monitored with a lever attached at the wrist. Examples of the
rectified and integrated (1 ms) electromyogram (EMG) for 4 fourlimb muscles [extensor digitorum communis (edc), palmaris longus
(pl), brachialis (br), and supraspinatus (ss)] are illustrated below the
position trace. B: the stimulus-triggered averages (StTAs) from the
muscles after averaging of 2,000 stimulus pulses. Red nucleus (RN)
stimulation produced significant StTAs for all of the illustrated
muscles, although pl responded with poststimulus suppression rather
than facilitation. The long horizontal dashed lines represent ⫾3 SDs
of pretrigger EMG activity.
RESULTS
Stimulation in RN
We first attempted to determine functional relations of RNm
and RNp by stimulating at 51 sites within the RN of three cats.
Sites located in the caudal 2 mm of the RN (n ⫽ 35) are
referred to as RNm, and sites in the rostral 2 mm of the nucleus
(n ⫽ 16) are referred to as RNp. Figure 2 illustrates averages
from a proximal (ss) and a distal (edc) forelimb muscle for one
stimulating track that passed through RNm.
For the track illustrated by Fig. 2, two sites (black circles)
within RNm produced significant facilitation. Cells at the dorsal site were active during movements of the contralateral
forelimb, and cells at the ventral site were active during movement of the contralateral hind limb. Presumably, the current
spread of the 20-␮A pulses either included forelimb regions of
RN or activated passing fibers related to forelimb musculature.
The StTAs from the illustrated track (Fig. 2) mirror the
results obtained from all of the RN stimulation tracks. No
significant StTAs were produced by stimulation outside of the
borders of the RN (27 sites dorsal to RN and 28 ventral), and
the pattern of poststimulus facilitation and suppression was
consistent between cats. Figure 6A plots the percentage of
significant StTAs for three cats with stimulation sites in RNm.
For each cat, the most frequently facilitated muscle was edc
(91% of sites), while several other muscles, such as palmaris
longus (pl), displayed a high incidence of poststimulus suppression. For both RNm and RNp, the distribution of poststimulus effects between muscles differed significantly from
chance (RNm, ␹2 ⫽ 48.2, 6 df, P ⬍ 0.01; RNp, ␹2 ⫽ 22.8, 6
df, P ⬍ 0.01).
Our hypothesis predicted that proximal limb muscles would
more likely be activated by RNp stimulation and distal muscles
J Neurophysiol • VOL
by RNm stimulation. Although the shoulder muscles, sd and ss,
were more likely to be facilitated by RNp stimulation (49 vs.
21%), the overall pattern of muscle activation between RNm
and RNp was not significantly different (␹2 ⫽ 2.9, 6 df, P ⬎
0.50). Therefore stimulation within RN did not support a
functional difference between RNm and RNp.
Anatomical separation of RNm and RNp fibers in the RST
Stimulation within RN is likely to be confounded by
activation of passing fibers. The double injection case
(BRN1) of the previous paper (Pong et al. 2002) indicated
that stimulation of the RST at the appropriate level might
avoid this problem. Figure 3, A and B, illustrates injections
(0.008 ␮l) of WGA-HRP (1%) made in RNm (A) and RNp
(B) on opposite sides of the brain. Figure 3, C and D,
illustrates the locations of RST fibers as they descend to the
spinal cord. Position of the labeled fibers was plotted onto
images of the sections with the use of a computer-aided
plotting system (Image Tracer™). Because the fibers exiting
from the RN cross immediately to the opposite side, labeled
fibers from the RNp injection (vertical striping) are on the
right and those from RNm (horizontal striping) are on the
left. The section shown in Fig. 3C is at the level of the
caudal mesencephalon and rostral pontine nuclei (A1.6). At
this level, fibers from RNm (left) travel immediately below
fibers of the superior cerebellar peduncle (BC). Fibers from
RNp (right) lie ventral to those from RNm and are bounded
on their ventral border by the medial lemniscus (ML).
Therefore a stimulating track through the RST at this level
would pass first through RNm efferent fibers and then
through RNp efferent fibers. Figure 3D illustrates the location of labeled RST fibers at the level of the rostral inferior
olive (P12.7). At this level, fibers from RNm and RNp are
intermingled and occupy corresponding locations on either
side of the brain.
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Locations of unmarked sites were reconstructed relative to lesion
locations.
472
HORN, PONG, BATNI, LEVY, AND GIBSON
FIG. 2. Reconstruction of a stimulating track through
the caudal RN. Stimulation sites producing significant
StTAs are indicated by black circles, and sites without
significant StTAs are indicated by white circles. Right:
StTAs from a proximal (ss) and distal (edc) forelimb
muscle. Only sites within the RN produced significant
StTA’s (heavier traces), and both muscles were activated
at each site.
A fourth cat received RST stimulation
in the caudal mesencephalon. The RST was localized by re
cording fiber discharge during movement of the ipsilateral
limb, and its ventral border was identified by the sensory
responses of the underlying ML.
Figure 4 illustrates StTAs produced on one track through the
mesencephalic RST. An outline of the corresponding frontal
MESENCEPHALIC LEVEL.
section from BRN1 is included to demonstrate the relative
location of fibers from RNm and RNp (labeled fibers from the
RNm injection have been transposed to the right side). The
plane of section was not identical between the cases so sections
were matched by comparing ventral structures.
StTAs were collected at 0.5-mm steps in depth along the
track. Stimulation sites above the BC or below the ML did not
elicit significant StTAs (Fig. 4, white circles). During stimu-
FIG. 3. Trajectory of rubrospinal tract (RST)
fibers from magno- and parvicellular divisions of
the RN (RNm and RNp). A: wheat germ agglutinin-horseradish peroxidase (WGA-HRP) injection site in the caudal pole of the right RNm. B:
injection site rostral and lateral in left RNp. C:
labeled fibers in the caudal mesencephalon. Due
to decussation of the RST fibers, fibers labeled
by the RNm injection (horizontal hatching) are
on the left side and fibers labeled by the RNp
injection (vertical hatching) are on the right. At
this level, RNm fibers occupy a location dorsal
to the location of RNp fibers. D: location of
labeled fibers at the medulla. At medullary levels, fibers from RNm and RNp occupy equivalent locations on either side of the brain stem.
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Stimulation of RST
FUNCTIONAL SPECIALIZATION WITHIN THE RED NUCLEUS
473
lation, significant StTAs ceased abruptly as the electrode entered the ML. However, the anatomical reconstruction of this
track placed the two most ventral stimulation points within ML
fibers. It is likely that the anatomical reconstruction has some
inaccuracy because marking lesions were made during electrode withdrawal.
Stimulation sites within the RST produced significant poststimulus facilitation (black circles, Fig. 4). Dorsal stimulation
sites facilitated edc but not ss, whereas ventral stimulation sites
facilitated ss but not edc. Similar muscle activation patterns
were seen on the other stimulation tracks. The histograms in
Fig. 6, C and D, illustrate the probability of significant StTAs
for the various muscles at stimulation sites within either the
dorsal (C) or ventral (D) halves of the RST. The probability of
obtaining significant StTAs for edc, pl, and extensor carpi
ulnaris (ecu) is higher at dorsal sites, whereas the probability
for obtaining significant StTAs for triceps (long head; tr), sd,
and ss is higher at ventral sites. Brachialis (br) was activated
with approximately equal frequency from dorsal and ventral
J Neurophysiol • VOL
sites. Poststimulus facilitation was much more commonly produced by mesencephalic stimulation than was poststimulus
suppression (88% of the stimulation sites produced facilitation).
The largest differences in activation were seen for edc, sd,
and ss. At dorsal stimulation sites edc was activated 77% of the
time but only 15% of the time at ventral sites. In contrast, sd
and ss were activated 7 and 3% at dorsal sites but 35 and 65%
at ventral sites. The patterns of activation between dorsal and
ventral stimulation sites were significantly different (␹2 ⫽
41.2, 6 df, P ⬍ 0.01).
At the level of the caudal pons, the fibers
of the RST form a relatively compact bundle that travels along
the ventrolateral edge of the brain stem. At this level, fibers
from RNm and RNp intermingle and disperse evenly throughout the RST. Therefore stimulation should provide an overall
picture of relations between RN output and forelimb muscles
regardless of the site within the RST.
Figure 5 illustrates results from one track passing through
MEDULLARY LEVEL.
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FIG. 4. Reconstruction of a stimulating track in caudal mesencephalon. Sites at the depth of and immediately
ventral to the superior cerebellar peduncle (BC)-activated edc but not ss, whereas more ventral sites activated
ss but not edc. Sites below the medial lemniscus (ML)
did not produce significant StTAs. Significant StTAs are
shown as heavy traces. The lower schematic illustrates
the relative positions of fibers from RNm (RST-m) and
RNp (RST-p). The sections were chosen to match AP
level at the depth of the effective stimulation sites. Differences in plane of section and histological processing
produced a mismatch at other depths.
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HORN, PONG, BATNI, LEVY, AND GIBSON
the RST at medullary levels. Stimulation dorsal and ventral to
the RST (white circles) failed to produce significant StTAs, but
stimulation within the RST (black circles) did. StTAs for ss
and edc are illustrated in Fig. 5, right. Significant StTAs
commence at the same depth for both muscles and the largest
StTAs are elicited at the same stimulation site.
To test for a potential topography within the RST at medullary levels, we grouped the stimulation sites into dorsal and
ventral halves based on recording depth (as was done for the
RST at mesencephalic levels). Figure 6, E and F, illustrate the
results. The patterns of activation for the dorsal and ventral
sites were not significantly different (␹2 ⫽ 0.93, 6 df, P ⬎
0.50). As with stimulation of the mesencephalic RST, few
instances of poststimulus suppression were observed (95% of
the sites produced facilitation).
DISCUSSION
The primary objective of this study was to determine if
spinal terminations of RNm activate different forelimb muscuJ Neurophysiol • VOL
lature than those of RNp. Stimulation of fibers from RNm
activated muscles of the distal limb (edc, pl, and ecu) more
strongly than muscles of the proximal limb and shoulder (tr and
ss). Stimulation of fibers from RNp activated muscles of the
proximal limb and shoulder more strongly than those of the
distal limb. Therefore the physiological actions of RNm and
RNp are consistent with the anatomical observation that RNm
fibers terminate more heavily at lower cervical segments and
RNp fibers at upper segments (Pong et al. 2002).
Patterns of activation
Stimulation within the RN produces a highly characteristic
pattern of StTAs. Digit (edc) and wrist (ecu) extensor muscles
are strongly facilitated, whereas other limb muscles often show
instances of suppression as well as facilitation. There are no
other reports of StTAs resulting from stimulation of the cat
RN, but stimulation in the monkey produces similar effects
(Belhaj-Saif et al. 1998; Mewes and Cheney 1991). Digit and
wrist extensor muscles are strongly facilitated, and several limb
muscles show a high incidence of suppression (especially pl).
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FIG. 5. Reconstruction of a stimulating track in
the medulla. Stimulation above and below the RST
failed to produce significant StTAs, whereas stimulation within the RST produced significant StTAs
(heavier traces). The lower schematic illustrates
the relative positions of fibers from RNm (RST-m)
and RNp (RST-p) at the same brain stem level as
that of the stimulating track.
FUNCTIONAL SPECIALIZATION WITHIN THE RED NUCLEUS
475
Surprisingly, neither a favoring of edc nor a significant
number of poststimulus suppressions occurred with stimulation
of the RST. At medullary levels, RST stimulation produced a
high probability of facilitation for all seven muscles (range
55–90% facilitation), and poststimulus suppression was limited
to one muscle at one site.
The lack of preferential facilitation of edc from the RST
stimulation is especially surprising, since motor pools at C8
receive a selective input from the RN for the cat and monkey
(Fujito et al. 1991; Holstege and Tan 1988; McCurdy et al.
1987; Ralston et al. 1988). However, most RN projections to
the cord terminate in interneuronal regions rather than in motoneuronal pools, and it may be that the motoneuronal projections account for a relatively small portion of the poststimulus
J Neurophysiol • VOL
effects. If this is the case, why does stimulation within RN
favor edc?
One possibility is that input to edc (and other digit muscles)
might arise from RN neurons with larger dendritic fields. Input
to C7–C8 motoneuronal pools arises from the caudal RNm
(Pong et al. 2002), which contains the largest cells in the
nucleus. The dendritic fields of the large cells extend over a
substantial portion of the nucleus in both cat and monkey
(Burman et al. 2000; Condé and Condé 1973; Wilson et al.
1987), and stimulation in the nucleus could favor these cells.
Afferents to the nucleus might also favor neurons projecting to
edc, and stimulation anywhere within the nucleus could activate these afferents. The large dendritic fields of RNm neurons
and fiber activation might contribute also to the failure to find
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FIG. 6. Summary of muscle activation at
different stimulation sites. Poststimulus facilitation is indicated as a positive percentage, whereas poststimulus suppression is indicated as a negative percentage. A:
histogram indicating percentage of the significant StTA sites in the RNm of 3 cats.
RNm stimulation most frequently facilitated
edc and often produced suppression in other
forelimb muscles. B: results of stimulation
in RNp for 2 cats. The patterns of muscle
activation were similar to RNm stimulation,
although 2 shoulder muscles (sd and ss)
were facilitated more frequently. C: stimulation in the dorsal half of the RST at mesencephalic levels frequently activated edc
but not ss or sd. D: stimulation in the ventral
half of the RST at mesencephalic levels
frequently activated ss and sd but not edc.
Stimulation in the dorsal (E) and ventral (F)
halves of the RST at medullary levels activated all muscles with a relatively high
probability.
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HORN, PONG, BATNI, LEVY, AND GIBSON
a significant difference in the pattern of muscle activation when
stimulating within RNm and RNp.
Poststimulus suppression
Functional considerations
Although the RN can influence all forelimb muscles, the
emphasis on activation of distal muscles is supported by many
lines of evidence. RN cells fire especially well during digit
extension (Gibson et al. 1985, 1994; Jarratt and Hyland 1999;
van Kan and McCurdy 2001). Cells in interpositus, the major
input to RNm, discharge only if hand movements are included
in the behavioral task (van Kan et al. 1994). Lesions of the RST
most strongly affect digit use (Lawrence and Kuypers 1968;
Schrimsher and Reier 1993; Sybirska and Gorska 1980;
Whishaw and Gorny 1996), and temporary inactivation of
RNm (Gibson et al. 1994) or interpositus (Mason et al. 1998;
Milak et al. 1997) impairs the ability to properly position the
digits for a variety of tasks such as grasping, walking, and
standing.
If the RN is specialized for control of distal musculature,
why does stimulation of the RST produce postspike effects in
proximal as well as distal muscles? Lesions or inactivation of
the RN or lateral cerebellum impair the ability to position and
maintain stability of the limb to support hand movements
(Goldberger and Growdon 1973; Mason et al. 1998; Sybirska
and Gorska 1980; Whishaw and Gorny 1996). It is likely that
the RN helps coordinate proximal muscle activity with distal
muscle activity to achieve a successful movement, such as
grasping an object at the end of a reach or placing the foot
properly for walking or standing.
This work was supported by National Institute of Neurological Disorders
and Stroke Grant NS-36820 (A. R. Gibson) and National Research Service
Award NS-10726 (M. Pong).
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Activation of synaptic mechanisms could account for the
high incidence of poststimulus suppression seen with RN stimulation. Poststimulus suppression requires that some inhibitory
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at C6–C8 respond with inhibitory postsynaptic potentials
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to account for the 21% incidence of poststimulus suppression
observed with RN stimulation. [Behaj-Saif et al. (1998) reported a 25% incidence of poststimulus suppression from RN
stimulation in the monkey.]
It is possible that poststimulus suppression results from
activation of inhibitory synapses within the RN, which would
not be activated by RST stimulation. There is evidence that the
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