Department of Physiology, Emory University, Atlanta, Georgia 30322
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ABSTRACT |
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Sokoloff, Alan J., Sondra G. Siegel, and Timothy C. Cope. Recruitment order among motoneurons from different motor nuclei. The principles by which motoneurons (MNs) innervating different multiple muscles are organized into activity are not known. Here we test the hypothesis that coactivated MNs belonging to different muscles in the decerebrate cat are recruited in accordance with the size principle, i.e., that MNs with slow conduction velocity (CV) are recruited before MNs with higher CV. We studied MN recruitment in two muscle pairs, the lateral gastrocnemius (LG) and medial gastrocnemius (MG) muscles, and the MG and posterior biceps femoris (PBF) muscles because these pairs are coactivated reliably in stretch and cutaneous reflexes, respectively. For 29/34 MG-LG pairs of MNs, the MN with lower CV was recruited first either in all trials (548/548 trials for 22 pairs) or in most trials (225/246 trials for 7 pairs), whether the MG or the LG MN in a pair was recruited first. Intertrial variability in the force thresholds of MG and LG MNs recruited by stretch was relatively low (coefficient of variation = 18% on average). Finally, punctate stimulation of the skin over the heel recruited 4/4 pairs of MG-LG MNs in order by CV. By all of these measures, recruitment order is as consistent among MNs from these two ankle muscles as it is for MNs supplying the MG muscle alone. For MG-PBF pairings, the MN with lower CV was recruited first in the majority of trials for 13/24 pairs and in reverse order for 9/24 pairs. The recruitment sequence of coactive MNs supplying the MG and PBF muscles was, therefore, random with respect to axonal conduction velocity and not organized as predicted by the size principle. Taken together, these findings demonstrate for the first time, that the size principle can extend beyond the boundaries of a single muscle but does not coordinate all coactive muscles in a limb.
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INTRODUCTION |
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The explanation of how the CNS controls posture
and movement requires an understanding of how the activation of
motoneurons (MNs) is organized during these tasks. Within muscles, MNs
are activated in an orderly sequence: the last MNs recruited into activity are preceded by MNs that have slower conduction velocities and
that connect with muscle fibers that contract with lower force, slower
contraction time, and lower susceptibility to fatigue (for review, see
Calancie and Bawa 1990; Henneman and Mendell
1981
; see also Cope and Clark 1991
). This
orderly recruitment sequence of MNs and their muscle fibers, i.e.,
motor units, commonly is referred to as the size principle
(Calancie and Bawa 1990
; Cope and Pinter
1995
; Henneman and Mendell 1981
).
Recruitment by the size principle has been documented extensively
within skeletal muscles (see reviews by Calancie and Bawa 1990; Henneman and Mendell 1981
). In contrast,
order among MNs supplying different muscles has not been examined
directly to our knowledge. Indirect support for operation of the size
principle across muscles comes from the seminal experiments of Elwood
Henneman. In 1965, Henneman and coworkers observed a strong tendency
for motor axons in a single ventral root filament in the decerebrate cat to be recruited in order according to spike amplitude
(Henneman et al. 1965a
,b
). Because the recruitment
stimuli used in these studies typically activate multiple muscles, it
is possible that the sample of motor axons exhibiting order supplied
different muscles. Definitive conclusion about order across muscles
cannot be reached, however, because the identities of motor axons were not established in these studies.
Wyman, Waldron, and Wachtel (1974) recognized that the
experimental findings just described were consistent with orderly
recruitment among different possible groups of MNs. They used the term
"motor pool" to define a functionally coordinated group of MNs
recruited in accordance with the size principle, and suggested that the motor pool might consist of "all the motoneurons innervating a single muscle, all the motoneurons in a given ventral root (probably subdivided into flexor and extensor groups), or all the motoneurons activated by a given stimulus." Either of the latter two schemes might result in orderly recruitment across motor nuclei. Wyman et al. (1974)
, however, did not test these possibilities, and in the ensuing 25 yr, this issue has not been investigated further.
Expansion of the size principle across muscles could have some important benefits that can be appreciated by recognizing that tens to hundreds of MNs are selected into activity from multiple muscles in virtually all movements and postures. Because muscles and their motor units have diverse mechanical actions, the smooth and predictable trajectory of limb movement would seem to require coordination of the sequence in which MNs are recruited. Recruitment by the size principle could meet this requirement. Additionally, this scheme would simplify the task of coordinating large numbers of MNs by relying on differences in the intrinsic excitability of MNs to rank order MN firing sequence. In this way, the group of MNs selected into activity would self-organize.
Here we directly test the hypothesis that MNs selected into activity
from different muscles can be recruited in accordance with the size
principle. Also tested is the hypothesis that all MNs brought into
activity from different motor nuclei in a discrete movement or reflex
necessarily are recruited in order by the size principle (cf.
Bawa and Calancie 1989; Riek and Bawa
1992
). These tests require that the MNs under study supply
muscles that can be coactivated. This condition was met for pairs of
muscles activated reflexively in decerebrate cats. The medial and
lateral gastrocnemius muscles (MG and LG, respectively) are coactivated
by muscle stretch applied through the Achilles tendon (e.g.,
Nichols 1989
), and in a putative nociceptive reflex (see
Sokoloff and Cope 1996
). The posterior biceps femoris
muscle (PBF) is activated together with MG in the cutaneous reflex
elicited by stimulation of the caudal cutaneous sural nerve (see
Siegel et al. 1999
). Studies reported here of MNs
recruited from these muscles demonstrate that recruitment order by the
size principle can cross muscle boundaries but that this order does not
necessarily encompass the entire set of MNs recruited in a discrete
motor reflex.
Preliminary results of this work were reported in abstract form
(Sokoloff and Cope 1995).
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METHODS |
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Experimental preparation
Thirteen cats of either sex ranging in weight from 2.5-3.5 kg
were studied in acute experiments similar to those detailed in earlier
reports from this laboratory (Cope and Clark 1991; Cope et al. 1997
). Anesthesia was induced and maintained
with a gaseous mixture of 1.5-3% halothane in O2 and
NO2 (1:1). Surgery proceeded when withdrawal and eye-blink
reflexes were suppressed completely. A cannula was inserted into the
trachea and connected to a respirator for delivery of gases throughout
the surgery described in the following text. The rate and volume of
artificial respiration were adjusted to maintain end-tidal
CO2 between 3.5 and 4%. Cannulae were secured in the right
common carotid artery to measure blood pressure and in the right
external jugular vein for infusion of dextran (10%) in Ringer solution
and, on occasion, a sympathomimetic amine (Aramine) as needed to
support mean blood pressure >60 mmHg. The left common carotid was
ligated in preparation for decerebration (see below). Body temperature
was monitored continuously and held at 36-38°C by radiant heat. At
the end of the experiment, cats were killed by barbiturate overdose
[pentobarbital sodium (Nembutal): 150 mg/kg].
Spinal roots L5-S1 were exposed by laminectomy and by opening the overlying dura mater. An incision was made in the left posterior hindlimb. In one set of experiments (n = 7), the MG and LG muscles were freed from surrounding tissues but the continuity between these muscles was not disturbed. The common MG/LG tendon was severed at the insertion on the calcaneus and tied with Dacron cord for later attachment to a force transducer. The nerves supplying the MG, LG, and soleus were dissected for later placement, in continuity, on bipolar electrodes. In a second set of experiments (n = 6), the nerves to the MG and the PBF were dissected for later placement, in continuity, on bipolar electrodes. The cat was secured in a rigid recording frame with the left hindlimb clamped at the distal ends of the femur and the tibia. Exposed tissues were bathed in warm-oil pools (36-38°C). Cats were decerebrated by removal of brain structures rostral to intercollicular transection of the brain stem after which anesthetic was discontinued.
Data acquisition
The axons of two individual MNs, either one LG and one MG MN,
one MG and one PBF MN, or two PBF MNs, were penetrated simultaneously in S1 or L7 ventral rootlets each axon by a
glass micropipette (2 M K-acetate; 10-25 M). MNs were identified by
antidromic action potentials produced when stimulating their respective
peripheral nerves. Because the nerve to the LG contains axons
projecting to the soleus, in the LG/MG experiments the soleus muscle
nerve also was stimulated to allow conclusive discrimination of LG and soleus MNs. The delay and distance traveled by the antidromic action
potentials from stimulus to recording sites were used to calculate
axonal conduction velocity (CV) for each MN (see Cope and Clark
1991
). Because of the variability in repeated measures of
conduction delay (
25 µs), we adopted the criterion that the difference in CV must exceed 2 m/s for MNs in a pair to be reliably ranked by CV. Motoneuron pairs not meeting this criterion are excluded
from this report. We relied on axonal conduction velocity to test
recruitment order because under the conditions of this study, i.e., MN
recruitment in stretch and cutaneous reflexes in decerebrate cats, CV
is as good as other parameters for testing the size principle
(Cope and Clark 1991
; see also Bawa et al. 1984
). MN action potentials were digitized and collected on
videotape and computer for later analysis.
LG-MG MN pairs
To study LG and MG behavior, MNs were recruited primarily during
the reflex evoked by the combined stretch of the LG and MG muscles. The
combined tendon of insertion of these muscles (the Achilles tendon with
the soleus tendon removed) was attached to a strain-gauge transducer (a
semiconductor strain gauge attached to a U-shaped aluminum beam)
connected in-series with a feedback-controlled servomotor. This
arrangement allowed us to apply constant ramp-hold-release stretches
(100 ms each for the ramp and release phases and 300 ms for the hold
phase) of the LG and MG muscles while simultaneously recording muscle
force (bandwidth DC-5 kHz; ADC sampling at 2.5 kHz). We are confident
that this sampling rate did not introduce aliasing because the upper
frequency band in the force power spectra (250 Hz) was well below the
Nyquist limit of 1.25 kHz (Lynn 1989). The initial
muscle length and the ramp-stretch amplitude (4, 6, or 8 mm) were set
at levels that consistently recruited action potentials in the
penetrated motor axons during the ramp phase of muscle stretch. The
speeds and amplitudes of triceps surae stretch were adopted from those
used by Nichols (1989)
to mimic length changes
experienced by the triceps surae during locomotion in the cat.
Motoneuron recruitment was scored when at least one action potential in
each MN was elicited during the ramp phase of muscle stretch. The
reproducibility of recruitment order was checked for each MN pair in
replicate trials of muscle stretch repeated once every 4 s. Some
MNs also were recruited in reflex contractions elicited in the LG and
MG muscles by penetrating the skin over the heel pad with the fine
points of jeweler's forceps (see Sokoloff and Cope
1996
).
Recruitment order among pairs of LG-MG motor axons was studied in two
ways. The primary method was to determine which MN in a pair was the
first to fire an action potential during the ramp phase of muscle
stretch (differences in firing onset were reliably distinguishable
within 250 µs). Recruitment by the size principle was supported when
the MN with the lower CV fired before the MN with the higher CV. Order
was measured only when both motoneurons in the pair were recruited
because order can be determined unequivocally only when this criterion
is met (see Cope and Pinter 1995). The advantage of this
pair-wise analysis is that recruitment sequence is determined
unequivocally and with no underlying assumptions. A disadvantage is
that each MN's recruitment sequence is specified in relation to only
one other MN. For this reason, we also measured MN force threshold,
i.e., the muscle force recorded at the time when the MN is recruited
into activity. Force threshold has been used to specify one MN's
recruitment in relation to the population of all previously recruited
MNs (e.g., see Henneman et al. 1965a
). Recognizing that
muscle force represents the population of recruited MNs only indirectly
and probably inaccurately to some extent (see Cope et al.
1997
), we used force threshold merely to obtain a rough
estimate of the stability in recruitment order of one MN (LG or MG) in
relation to all other active LG and MG MNs. For each of nine LG and
nine MG MNs, we measured the coefficient of variation in force
threshold expressed as a percentage [(SD/mean force threshold) × 100] over repeated recruitment trials (>20). To minimize
contributions to force threshold variation from sources other than the
recruitment process itself, trials were selected for low variation
(<20% coefficient of variation in base and peak forces) in the muscle
responses to stretch (see Cope et al. 1997
).
MG-PBF and PBF-PBF MN pairs
These pairs were recruited during reflex contraction elicited by stimulating the ipsilateral caudal cutaneous sural nerve (100 pulses/second for 2 s). Stimulus strength was adjusted to levels that consistently recruited both motor axons. The stimulus strength was not the same for different axon pairs but was similar for all recruitment trials for a given pair. Intermittent tests using widely different stimulus strengths (up to 10-fold range) revealed no dependency of recruitment order on stimulus strength. Moreover, when tested by pinching the skin overlying the ipsilateral lateral malleolus (dermatome of the caudal cutaneous sural nerve), recruitment order was invariably the same as that produced by electrical stimulation of the nerve. To allow for stable MN recordings during sural stimulation, Pancuronium (0.1 mg/ml iv) was administered as needed to maintain paralysis. Because of the paralysis, muscle force, and thus MN force threshold, were not determined.
Six or more stimulation trials, with intertrial intervals of 1 min
were conducted for each muscle pair. MG and PBF MNs typically fired
repetitively in response to sural stimulation. Recruitment order was
judged in PBF-PBF MN pairs and in MG-PBF MN pairs only when the
activity of the two MNs of a pair overlapped. In two pairs, sural nerve
stimulation produced alternating activity between the MG MN and the PBF
MN. Because recruitment order by the size principle can be determined
only when both MNs are active together, these two cases were not
included in our analysis. Alternating activity was never observed among
PBF-PBF pairs.
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RESULTS |
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Recruitment order among MG-LG motoneurons
Thirty-four MN pairs, each composed of one LG and one MG MN, were
studied in replicate trials of stretch of the combined LG and MG
muscles. Stretch recruited both of the MNs in 4 and
66 stretch
trials. Axonal conduction velocity for MNs included in these 34 pairings (each MN was used in
3 pairings) ranged from 68 to 131 m/s
for LG MNs [n = 32; 101 ± (SD) 18 m/s] and from 71 to 130 m/s for MG MNs (n = 29; 105 ± 15 m/s),
ranges similar to those reported for MG MNs in previous studies (see
Emonet-Denand et al. 1988
; McDonagh et al.
1980
).
In 22 of the 34 pairs, the order of recruitment was unchanged in all
(548/548) stretch trials. Figure 1 shows
that these MNs always were recruited in order by increasing conduction
velocity, whether the MN recruited first was LG (14 pairs, ) or MG
(8 pairs,
). Thus recruitment by muscle stretch was as orderly among
MG and LG motor axons as it is among MG motor axons (Table
1).
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Some intertrial variation in recruitment order was observed for the remaining 12/34 pairs (Fig. 2). In 7 of these 12 pairs, recruitment was ordered predominantly from the MN with the slowest to fastest conduction velocity (225/246 stretch trials). In four pairs, the MN with the fastest conduction velocity was the first recruited in most trials (95/111 stretch trials). In one pair, recruitment order was equivocal (slowest CV recruited first in 19/37 stretch trials). Overall, recruitment order was predominantly from low to high CV for 29/34 pairs of motor axons or 85% of the sample.
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Motoneurons recruited by mechanical stimulation of heel
Mechanical stimulation of the skin over the heel produces reflex
excitation of LG and MG muscles (see Sokoloff and Cope
1996). The strong extensor response to this stimulus often
displaced the microelectrodes from the axon(s) under study, thereby
precluding reliable determination of recruitment order by this
stimulus. However, order was determined for four pairs of MNs recruited in four or more stimulation trials. These pairs are reported to allow
evaluation of recruitment order across the LG and MG during an
additional natural stimulus. In all trials of these pairs (27/27), the
MN with the slowest CV was recruited first. This was true regardless of
which MN was the first recruited of the pair (MG MN first in 3 of the 4 pairs).
Motoneuron force threshold
We measured intertrial variability in force thresholds for nine LG
MNs and nine MG MNs. At least 20 stretch trials were collected for each
MN (see Cope et al. 1997). The samples of LG and MG MNs were similar in measures of CV (for LG, range 71-110 m/s, mean = 92 m/s; MG range 68-111 m/s, mean = 91 m/s) and included 13 units
used in the pair-wise analysis. Values for the coefficient of variation
in force threshold ranged from 1.3 to 37.3%. For all 18 MNs, the mean
and median values were 18 ± 9 and 19%, respectively. In
comparison, the coefficients of variation obtained under similar conditions for 29 MG MNs in relation to the force of contraction produced by the MG muscle alone (Cope et al. 1997
) were
distributed with range = 2.3-82%, mean = 18 ± 18%
(SD), and median = 10%. Thus force threshold variation was
comparable whether measured from one MN in relation to its parent
muscle or in relation to multiple muscles.
Recruitment order among MG-PBF motoneurons
Twenty-four pairs of MG-PBF MNs were each studied in six or more
trials of sural nerve stimulation. Conduction velocity measures for MG
and PBF MNs were similar, ranging from 78 to 117 m/s for MG MNs
(n = 24; 92 ± 10 m/s) and from 78 to 108 m/s for
PBF MNs (n = 24; 92 ± 8 m/s). In 14/24 pairs, the
order of recruitment was unchanged in 108/108 trials. Figure
3 shows that, in contrast to the results
for LG-MG pairs, only half of the 14 MG-PBF pairs were recruited in
accordance with the size principle. For seven pairs (55/55 stretch
trials) MNs always were recruited in order by increasing CV, whether
the MN recruited first was MG (3 pairs, in Fig. 3) or PBF (4 pairs,
). For seven pairs (53/53 stretch trials), the MN with the highest
CV always was recruited first, whether the MN recruited first was MG (3 pairs,
in Fig. 3) or PBF (4 pairs,
). The proportion of pairs
exhibiting recruitment order from low to high CV was not statistically
distinguishable from random (Table 1).
|
For the remaining 10/24 pairs, recruitment order varied across trials in proportions illustrated in Fig. 4. In 6 of these 10 pairs, recruitment was ordered predominantly from the MN with the slowest to fastest CV (slowest CV recruited first in 46/56 trials). In two pairs, the MN with the fastest CV was the first recruited in most trials (fastest CV recruited 1st in 11/16 trials). And in two pairs, recruitment was equivocal (slowest CV recruited 1st in 8/16 trials). For the sample as a whole, recruitment order from low to high CV in all or most stretch trials was observed in only 13/24 pairs of MG/PBF MNs, i.e., 54% of the sample.
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Recruitment order among PBF-PBF motoneuron pairs
Table 1 presents data taken from earlier studies demonstrating that the size principle holds for MG MNs recruited in sural reflexes. The lack of recruitment according to the size principle among MG-PBF pairs might have resulted if recruitment is not ordered among MG or PBF MNs. To test this possibility among PBF MNs, 27 MN pairs were each studied in six or more trials of sural nerve stimulation. Conduction velocity measures of PBF MNs ranged from 72 to 115 m/s (93 ± 11m/s). In 22/27 pairs, the order of recruitment was unchanged across trials (179/179 stretch trials). For 19 of these pairs, the first recruited MN had the lowest CV; in 3 of these pairs the first recruited unit had the highest CV (Table 1 and Fig. 5). For the remaining five pairs, the lowest CV MN was recruited first in 8/9, 8/9, 7/8, 4/12, and 1/7 trials. In sum, recruitment order from low to high CV was observed in all or in a majority of trials for 22/27 (82%) of this sample of PBF MN pairs.
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DISCUSSION |
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In this study, we tested the hypothesis that motoneurons supplying different coactive muscles can be recruited collectively in order by the size principle. To this end, hindlimb muscles studied in pairs were coactivated reflexively in either muscle stretch or cutaneous reflexes in decerebrate cats. Our findings provide the first direct support of the hypothesis. However, we also found that the extent of this order is limited and not expressed in the complete set of all motoneurons concurrently recruited in a discrete motor reflex. Thus recruitment order by the size principle can but need not cross muscle boundaries.
Recruitment order by the size principle across muscles
LG and MG muscles can be coactivated in muscle stretch reflexes
elicited by stretch of their common Achilles tendon (see Nichols 1989). The reflex response of each muscle is driven by stretch activation of muscle spindle afferents from both muscles, i.e., by both
homonymous and heteronymous afferents (Eccles et al.
1962
; Nichols 1989
; Scott and Mendell
1976
). In this combined stretch reflex, we found that MG and LG
MNs sampled in pairs were most often recruited in order from low to
high CV regardless of whether the MG or the LG MN in a pair was
recruited first. Recruitment order by the size principle also was
observed for a small subset of this sample of LG-MG MN pairs recruited
by a putative nociceptive reflex.
This orderly behavior found among MNs recruited from the LG and MG
motor nuclei is similar to that found among MNs recruited from one of
these motor nuclei, the MG. In the cat MG, MN recruitment in order of
CV was observed in 83% of MN pairs during MG muscle stretch
(Cope and Clark 1991) and 76% of MG MNs recruited by
brain stem stimulation (Tansey and Botterman 1996
).
Bawa et al. (1984)
found 97% of MNs recruited in order
by CV during triceps surae stretch after excluding cases of equivocal
order. We are unaware of any demonstration that LG MNs are recruited in
order by the size principle, but this can be inferred from the order
that we find among MG MNs and among MG/LG MNs.
The simplest mechanistic explanation for the recruitment order observed
across motor nuclei is that MG and LG MNs are collectively rank-ordered
by their intrinsic excitability in relation to axonal CV and that they
share similar amounts of stretch-evoked synaptic input. Supporting this
notion is first, the observation that the ranges in rheobase current, a
measure of intrinsic excitability, overlap for MG and LG MNs (cf.
Fleshman et al. 1981 with Vanden Noven et al.
1986
), as do the ranges in CV (see RESULTS).
Second, the strength of synaptic input from Ia afferents of LG and MG combined (Eccles et al. 1957a
) is about the same onto MG
motoneurons (7.3 mV) as it is onto LG motoneurons (6.0 mV). Taken
together, the intermingling of MG and LG MNs in rank order by
excitability and their receipt of common synaptic input, from muscle
stretch, nociceptive, and possibly other inputs, lead us to expect
orderly recruitment across these motor nuclei. This expectation is
strengthened even further by recent computer simulation which shows
that the distribution of Ia synaptic current, at least from homonymous Ia afferents onto MG motoneurons, promotes orderly recruitment beyond
that generated by intrinsic motoneuron properties alone (Heckman
and Binder 1993
). These considerations suggest that shared Ia
synaptic input may be important for orderly recruitment by the size
principle among motoneurons from different motor nuclei. If this is the
case, then demonstrations of shared Ia synaptic input among a variety
of motor nuclei supplying the cat hindlimb (Eccles et al.
1962
; see also Nichols et al. 1999
) lead us to predict additional instances of orderly recruitment across motor nuclei, e.g., between peronei longus and brevis. We also would anticipate our finding that MG and PBF motoneurons are not recruited in
order (see following text) because these motor nuclei do not share Ia
synaptic feedback (Eccles et al. 1962
).
Functional benefits of orderly recruitment across motor nuclei
The direction of joint movement or torque depends on the relative
activity of musculature (whole muscles, portions of muscles, and motor
units) with different mechanical actions. For example, the triceps
surae of cat produces different torque directions at the ankle in
response to the differential activation of these muscles in ipsilateral
versus contralateral cutaneous reflexes (Nichols et al.
1993). The recruitment order of LG and MG MNs in relation to
one another (as well as with MNs supplying other active muscles)
becomes an important factor, therefore, in determining the
moment-to-moment direction of ankle movement (see Cope and Sokoloff 1998
). One way of coordinating these MNs would be
through the orderly recruitment of the set of all active MNs combined, as shown in this report for LG and MG MNs. This recruitment scheme would ensure reproducibility and, therefore, predictability in the
direction of ankle torque. In addition, ordering the recruitment of
motor units from muscles producing disparate torque directions would
have the effect of smoothing limb trajectory. It remains to be
determined whether the set of active triceps surae motor units are
recruited in order by the size principle under all conditions, irrespective of joint torque direction. Sequencing the recruitment of
different sets of active motor units by the size principle would not
constrain joint direction, which still could be changed dependent on
the set of motor units selected into activity from different muscles.
The goal of coordinating the recruitment sequence of MNs supplying
different muscles might be achieved in a variety of ways. In one case,
MNs supplying each muscle could be recruited in order by the size
principle, and some additional neural mechanism could set the time at
which the recruitment sequence begins for each muscle. This additional
mechanism would not be required if, instead, recruitment among MNs from
different muscles was determined predominantly by intrinsic properties
of the MNs themselves. Differences in the intrinsic properties of MNs
act to distribute varying levels of excitability among MNs (see
Pinter 1990), such that uniform synaptic input to these
MNs results, in computer simulation (Heckman and Binder
1993
), in an orderly sequencing of recruitment, with the most
excitable MNs firing first. On this backdrop of distributed MN
excitability, MNs selected into activity from various motor nuclei by a
common source of synaptic excitation would be expected to fire in a
sequence established automatically by MN excitability. This selection
across nuclei might be achieved by any of a variety of sources of
divergent synaptic drive, whether descending (e.g., cortico-spinal and
rubro-spinal projections) (see for example, Araki et al.
1976
; Hongo et al. 1969
) or segmental (e.g.,
muscle and cutaneous afferents) (see for example, Eccles et al.
1957b
; LaBella et al. 1989
).
Recruitment disorder among coactive pairs of motoneurons
To test whether coactivity is a condition sufficient to ensure
orderly recruitment, as hypothesized first by Bawa and coworkers (Bawa and Calancie 1989; Riek and Bawa
1992
) and later by Cope and Sokoloff (1998)
, we
examined a second pair of muscles. MG and PBF were selected for study
following our observation (Siegel et al. 1999
) that
these muscles are strongly coactivated by sural nerve stimulation in
decerebrate cats. In contrast to LG-MG MN pairs, we found that MG-PBF
MN pairs were not recruited in accordance with the size principle: the
prediction of recruitment order by axonal CV was no better than by
random selection (Table 1).
The recruitment disorder observed among MG/PBF MN pairs was not
explainable by differences in the peripheral stimulus because each MN
in a pair was recruited by the same stimulus and within the same
stimulus trials. Neither did disorder across muscles result from
disorder within these muscles (Table 1) because sural stimulation
recruited pairs of MG MNs in order by the size principle (Cope
and Clark 1991; see also Clark et al. 1993
;
Haftel et al. 1997
) just as it recruited pairs of PBF
MNs in order by the size principle (Fig. 5). Other possible
explanations are more likely. One possibility is that the MNs
themselves differ. Recruitment disorder across nuclei could arise if
the threshold differences, i.e., threshold spacing (Bakels and
Kernell 1994
), between MNs is not the same for the MG and PBF
motor nuclei. Disorder also would result for MG and PBF MNs combined if
the relationship between intrinsic excitability and axonal CV is not
the same for MNs in each motor nucleus.
Other explanations for disorderly recruitment could be accountable to
differences in synaptic input to MG and PBF MNs originating either from
sural nerve or other sources. Studies of synaptic potentials indicate
that input to MG and PBF MNs can arrive via different polysynaptic
pathways. For example, low-frequency sural nerve stimulation produces
primarily excitatory postsynaptic potentials (EPSPs) in
PBF-semitendinosus MNs (Schomburg and Steffens 1986) but
EPSPs, inhibitory postsynaptic potentials (IPSPs), or mixed EPSPs/IPSPs
in MG MNs (Burke et al. 1970
; Pinter et al.
1982
; Powers and Binder 1985
). However, other
studies indicate that these differences in synaptic potentials may
depend on either the method of anesthesia (see LaBella et al.
1989
) or the frequency of presynaptic stimulation
(Heckman et al. 1992
). Thus although we can conclude
from these studies that different sural pathways to MG and PBF MNs
exist, we cannot be sure that they were in operation during our
experiments. It remains a formal possibility, however, that different
synaptic pathways from sural primary afferents to these two motor
nuclei were in operation in our experiments and introduced differences
in synaptic delay or recruitment gain (Kernell and Hultborn
1990
) that perturbed recruitment order across these nuclei.
Another factor to consider is the synaptic input to MG and PBF MNs from
sources other than the sural nerve. Gossard et al.
(1994)
suggest that synaptic noise produces random fluctuations in MN excitability, and if differentially distributed to motor nuclei,
this noise could disrupt recruitment order among the combined set of
MNs as we observed here.
Proposed organizational scheme for motor unit recruitment
Together with earlier descriptions of MN recruitment, the findings
of this study lead us to propose the following scheme for the
functional organization of a group of MNs engaged in a discrete motor
activity. We refer to this group as an ensemble, in which members act
together to produce a specific motor effect. The principles involved in
selecting members of the ensemble in the control of movement and
posture are not yet elucidated, although they undoubtedly involve
consideration of biomechanical actions and probably energy use (see
Windhorst 1988). These selection principles, though
still unclear, are separate from the size principle, which in our
proposal acts as a sequencing principle applied to all MNs selected
into the ensemble. Degrees of freedom in motor unit combinations thus are achieved in the selection process and not in the recruitment process. Support for this notion comes from the recent work of Riek and Bawa (1992)
. This study demonstrates
recruitment order by the size principle within each of two
independently activated subpopulations of MNs as well as within the
group formed when these subpopulations are recruited in combination.
Similarly, recruitment in accordance with the size principle occurs
among MG MNs during recruitment of the MG muscle alone (Cope and
Clark 1991
) and among MG and LG MNs during recruitment of the
parent muscles together as shown in the present study. In this light, the lack of orderly recruitment among MG-PBF pairs is seen to represent
the participation of MNs from each muscle in a different ensemble
during sural reflex excitation.
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ACKNOWLEDGMENTS |
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This work was supported by National Institutes of Health Grant NS-20123.
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FOOTNOTES |
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Address for reprint requests: A. J. Sokoloff, Dept. of Physiology, Emory University, 1648 Pierce Dr., Atlanta, GA 30322.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 2 December 1998; accepted in final form 11 January 1999.
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REFERENCES |
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