Download Common Input to Motor Neurons Innervating the Same and Different

J Neurophysiol 91: 57– 62, 2004.
First published September 10, 2003; 10.1152/jn.00650.2003.
Common Input to Motor Neurons Innervating the Same and Different
Compartments of the Human Extensor Digitorum Muscle
Douglas A. Keen and Andrew J. Fuglevand
Department of Physiology, University of Arizona, Tucson, Arizona 85721
Submitted 7 July 2003; accepted in final form 4 September 2003
A fundamental issue that underlies the coordination of activity among a population of neurons relates to how synaptic
input is distributed across the ensemble. In a landmark study,
Mendell and Henneman (1971) used intracellular recordings to
determine the proportion of motor neurons within a spinal
motor nucleus that received synaptic input from single Ia
afferent fibers. The remarkable finding of that investigation
was that individual afferent fibers made synaptic contact with
most, and in many cases all, homonymous motor neurons as
well as with large numbers of motor neurons supplying synergistic muscles. Subsequent anatomical studies confirmed the
existence of extensive ramification of individual Ia afferents
throughout longitudinally oriented motor nuclei in the spinal
cord (Brown and Fyffe 1978).
Much less is known about the distribution of individual
descending and spinal interneuronal inputs to motor neurons.
Some anatomical evidence indicates that terminal arbors of
individual collaterals from corticomotoneuronal cells are dis-
tributed in longitudinal cylinders coterminous with motor nuclei in lamina IX of the spinal cord (Lawrence et al. 1985).
Such findings are consistent with the possibility that these
specialized descending inputs may contact a large proportion
of neurons in a motor nucleus (Porter and Lemon 1993).
Neurophysiological studies, although indirect, have demonstrated relatively extensive divergence of corticospinal inputs
both within (Mantel and Lemon 1987) and across spinal motor
nuclei (Asunuma et al. 1979; Buys et al. 1986; Fetz and
Cheney 1980). Although little is known about the projection
frequency of spinal interneurons, one estimate suggests that
collaterals from individual Ia inhibitory interneurons may terminate in multiple motor nuclei and contact ⱕ20% of the
motor neurons within these nuclei (Jankowska 1992). These
observations suggest that synaptic inputs, with some exceptions, are broadly distributed across a motor neuron population
(Binder et al. 1996). Therefore an important determinate of
recruitment susceptibility and motor-unit activity appears to be
related to the intrinsic properties of the motor neurons (Henneman and Mendell 1981). Furthermore, the concept of a
motor neuron “pool” representing an assembly of neurons that
receive similar inputs and that control a single muscle derives
in part from these experimental observations on synaptic input
organization.
It is unclear, however, how the inputs to a pool of motor
neurons might be organized for a muscle that is subdivided into
different compartments (Loeb 1990). One possibility is that the
entire array of motor neurons that innervate a multi-compartment muscle may receive more or less similar inputs. Control
over different parts of the muscle, therefore, could be affected
by differences in intrinsic properties of motor neurons that
innervate different parts of a muscle, such as occurs for deep
and superficial regions of some hind limb muscles in rodents
(Kernell 1998). Alternatively, motor neurons supplying different parts of a muscle might receive relatively distinct synaptic
inputs (Botterman et al. 1983; Hamm et al. 1986; Vanden
Noven et al. 1986). In this case, activation of different parts of
a muscle (or subsets of motor units) would depend primarily on
the specific input pathways engaged. Consequently, it was of
interest to determine the extent to which these fundamentally
different organizational frameworks might operate to control a
multi-tendon finger muscle like the human extensor digitorum
(ED). Because it is not possible to measure directly synaptic
input distribution in human subjects, we instead estimated the
extent of divergence in last-order inputs to motor neurons by
measuring the degree of short-term synchrony among motor
Address for reprint requests and other correspondence: A. J. Fuglevand,
Dept. of Physiology, College of Medicine, P.O. Box 210093, University of
Arizona, Tucson, AZ 85721-0093 (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
0022-3077/04 $5.00 Copyright © 2004 The American Physiological Society
57
Downloaded from http://jn.physiology.org/ by 10.220.33.6 on June 14, 2017
Keen, Douglas A. and Andrew J. Fuglevand. Common input to
motor neurons innervating the same and different compartments of the
human extensor digitorum muscle. J Neurophysiol 91: 57– 62, 2004. First
published September 10, 2003; 10.1152/jn.00650.2003. Short-term synchronization of active motor units has been attributed in part to last-order
divergent projections that provide common synaptic input across motor
neurons. The extent of synchrony thus allows insight as to how the inputs
to motor neurons are distributed. Our particular interest relates to the
organization of extrinsic finger muscles that give rise distally to multiple
tendons, which insert onto all the fingers. For example, extensor digitorum (ED) is a multi-compartment muscle that extends digits 2–5. Given
the unique architecture of ED, it is unclear if synaptic inputs are broadly
distributed across the entire pool of motor neurons innervating ED or
segregated to supply subsets of motor neurons innervating different
compartments. Therefore the purpose of this study was to evaluate the
degree of motor-unit synchrony both within and across compartments of
ED. One hundred and forty-five different motor-unit pairs were recorded
in the human ED of nine subjects during weak voluntary contractions.
Cross-correlation histograms were generated for all of the motor-unit
pairs and the degree of synchronization between two units was assessed
using the index of common input strength (CIS). The degree of synchrony for motor-unit pairs within the same compartment (CIS ⫽ 0.7 ⫾
0.3; mean ⫾ SD) was significantly greater than for motor-unit pairs in
different compartments (CIS ⫽ 0.4 ⫾ 0.22). Consequently, last-order
synaptic projections are not distributed uniformly across the entire pool of
motor neurons innervating ED but are segregated to supply subsets of
motor neurons innervating different compartments.
58
D. A. KEEN AND A. J. FUGLEVAND
units within and across compartments of ED (Kirkwood and
Sears 1978; Nordstorm et al. 1992; Sears and Stagg 1976).
METHODS
Force and electromyographic recording
Extension force of the digits was measured by four force transducers (Grass Instruments, Warwick, RI, model FT-10, range 0 –5 N,
sensitivity 780 mN/mV) mounted in a custom-built manipulandum.
The manipulandum allowed each transducer to be aligned both horizontally and vertically with the proximal interphalangeal joint of each
finger. The force signals were amplified (⫻1,000; World Precision
Instruments, Sarasota, FL) and displayed on oscilloscopes.
Motor-unit action potentials were recorded with tungsten microelectrodes inserted into ED (Frederick Haer and Co., Bowdoinham,
ME, 1- to 5-␮m tip diameter, 5- to 10-␮m uninsulated length, 250-␮m
shaft diameter, ⬃200 k⍀ impedance at 1,000 Hz after insertion).
Surface electrodes (4 mm diam Ag-AgCl) attached to the skin overlying the radius served as reference electrodes for the intramuscular
electrodes. Two microelectrodes were inserted at different locations in
ED to record the activity of separate motor units on each electrode.
Weak electrical stimulation was used initially to verify microelectrode
placement in target compartments of ED based on the relative magnitudes of the forces evoked on each finger (Keen and Fuglevand
2003). Such intramuscular stimulation in ED causes force to developed predominately on one digit only (Keen and Fuglevand 2003).
Furthermore, we have shown previously, using intraneural stimulation
of single motor axons, that individual ED motor units develop force
almost exclusively on single digits (Keen and Fuglevand 2001).
Therefore motor units recorded at an intramuscular electrode site that
evoked force on a particular digit were likely primarily confined to the
affiliated compartment. In some cases, it is likely that electrodes were
placed into extensor digiti minimi (EDM), a thin muscle that inserts
into digit 5 and lies medial to and is often fused with ED along most
of its length. Digit 5 may receive tendons from both EDM and ED or
exclusively from EDM (von Schroeder et al. 1990). Therefore motor
units recorded from sites that evoked force on digit 5 could have been
ED or EDM units. After electrical stimulation, electrodes were connected to differential amplifiers and the intramuscular electromyographic (EMG) signals were amplified (⫻1,000), band-pass filtered
(0.3–3 kHz; Grass Instruments), and displayed on oscilloscopes.
Protocol
Subjects performed low-force isometric extension of all four fingers
to ensure that ED was activated. The microelectrodes were gently
manipulated during the contraction until action potentials of motor
units could be clearly identified on each electrode. Once different
J Neurophysiol • VOL
Data analysis
Data were analyzed using Spike 2 and custom-designed software.
Motor-unit discrimination was accomplished using a template-matching algorithm based on waveform shape and amplitude. An event
channel representing the timing of discharges of accepted action
potentials for a motor unit was generated. The discharge times of one
unit, termed the event unit, were plotted relative to the discharge times
of a second unit, termed the reference unit, to generate a crosscorrelation histogram. Cross-correlation histograms had 1-ms bin
widths and included periods 100 ms before and 100 ms after the
discharge of the reference unit. A peak in the cross-correlation histogram around time 0 represents the synchronous firing of the two units
greater than expected due to chance. The magnitude of the synchronous peak is thought to reflect the extent of shared last-order inputs to
the two neurons (Sears and Stagg 1976).
The cumulative sum procedure (cusum) was used to identify a
synchronous peak in the cross-correlogram and was calculated by
adding the successive differences between the count of each bin and
the baseline mean (Ellaway 1978). The baseline mean was calculated
as the mean count in the first and last 60 ms of the cross-correlogram.
A rise in the cusum near time 0 was used to delineate the peak in the
cross-correlation histogram. Specifically, peak boundaries were determined as the bins corresponding to 10 and 90% of the difference
between the minimum and maximum cusum values (Schmied et al.
1993). The magnitude of the peaks in the cross-correlograms were
quantified as number of counts within the boundaries of the peak
above the baseline mean divided by the duration of the recording. This
synchronization index, referred to as common input strength (CIS),
indicates the rate of extra synchronous impulses (i.e., extra imp/s)
above that expected due to chance (Nordstrom et al. 1992).
When cross-correlograms did not exhibit clear peaks, the method
described in the preceding text for identifying the region of the
histogram for calculation of CIS was not reliable. Therefore for cases
of nonsignificant peaks in the cross-correlogram, CIS was automatically calculated for an 11-ms region of the cross-correlogram centered
at time 0 (Semmler and Nordstrom 1995). The significance of the
cross-correlogram peak was determined according to the method
described by Schmied et al. (1993). The number of counts in the peak
was required to be ⬎3 SDs above the mean count in the off-peak (z
score ⱖ 1.96) to be considered significant. All CIS values, regardless
of the method used to delineate the region of the histogram for
calculation of CIS, were included in the analyses.
When both electrodes were confined to the same compartment of
ED, the CIS values were referred to as being intra-compartmental. A
one-way ANOVA was used to compare the intra-compartment CIS
values across the four compartments. When the electrodes were lo-
91 • JANUARY 2004 •
www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.6 on June 14, 2017
Twenty-four experiments were performed on the right ED muscle
in nine healthy human volunteers (5 women, 4 men, ages 21– 40 yr).
The experimental procedures were approved by the Human Investigation Committee at the University of Arizona. All subjects gave their
informed consent to participate in the study. Details of the experimental arrangement are presented in Keen and Fuglevand (2003).
Briefly, subjects were seated in a dental chair with their right elbow
and wrist supported on a horizontal platform. The wrist was stabilized
in a position midway between full supination and full pronation by
padded vertical posts placed on either side of the distal forearm and on
the dorsal and palmer aspects of the hand. The metacarpophalangeal
joints were maintained at a joint angle of ⬃90° by metal cuffs around
the proximal interphalangeal joints that were attached to separate
force transducers with relatively in-extensible string. The metal cuffs
were individually fitted for each digit. The length of each piece of
string was adjusted at the beginning of the experiment so that each
digit was preloaded in this flexed position with a force of ⬃2 N.
motor units were identified on the two electrodes, subjects sustained
weak contractions of ED such that both units remained active. During
the contractions, the forces exerted by individual fingers were not
specified; rather, subjects were instructed to maintain the discharge of
the two units at low rates while also keeping some level of tension on
each finger. Intramuscular EMG signals were recorded for 3 min or
until the motor-unit action potentials could no longer be clearly
discriminated. Subjects received visual and auditory feedback on the
discharge of the motor units and 1–2 min of rest between recordings.
After each recording, the position of at least one and often both of the
microelectrodes was adjusted until the action potentials of a presumably different motor unit could be identified. This occasionally involved removal of a microelectrode and reinsertion at a new site.
Electrical stimulation was performed to ascertain the compartment
location of the electrode when the electrode position was changed.
Successive trials were performed for ⱕ2 h. Extension force of each
finger and intramuscular EMG signals were digitally sampled at ⬃2
and 18.5 kHz, respectively, using the Spike2 data-acquisition and
-analysis system (Cambridge Electronics Design, Cambridge, UK).
MOTOR-UNIT SYCHRONY IN HUMAN EXTENSOR DIGITORUM
59
cated in different compartments of ED, CIS values were referred to as
being extra-compartmental. ANOVA was also used to determine
differences in the degree of synchrony for the extra-compartmental
comparisons. Tukey post hoc analysis was used to identify differences
in CIS across intra- and extra-compartmental groups. A two-tailed
Student’s t-test was used to compare the CIS values for all intracompartmental to all extra-compartmental recordings. Values are reported as means ⫾ SD with a probability of 0.05 selected as the level
of statistical significance.
RESULTS
FIG. 1. Example cross-correlation histograms for combinations of extensor
digitorum (ED) motor unit pairs residing in D2–D3, D3–D3, D3–D4, and
D3–D5 compartments in A–D, respectively. The magnitude of the synchronous
peak was calculated as the total number of counts in the peak above that
expected due to chance divided by trial duration. This index, referred to as
common input strength (CIS), indicates the rate of extra synchronous impulses
(i.e., extra imp/s). The traces above each histogram are the cumulative sum
(cusum) used to determine the location of the peak. The degree of synchrony
was greatest for motor-unit pairs within the same compartment (D3–D3)
indicating that last-order inputs project differentially across the motor neurons
supplying different compartments of ED.
J Neurophysiol • VOL
FIG. 2. Matrix of mean (⫾SD) common input strength (CIS) within (■) and
across (䊐) compartments of ED. Each element of the matrix indicates the mean
CIS value for motor-unit pairs within the corresponding compartments indicated on the abscissa and ordinate. For motor units within the same compartment, the CIS values for D2/D2 were significantly less than for D4/D4. For
extra-compartment motor-unit pairs, the CIS values for D2/D3 were significantly less than for either D3/D4 or D4/D5. No statistical comparisons were
made for the three pairs of D3/D5 motor units. The total number of motor-unit
pairs used for each comparison between and within compartments is given.
peaks. The duration of the synchronous peak, assessed from the
cusum, was on average 9.9 ⫾ 2.6 ms for those cross-correlograms that had a significant peak. The average CIS for all pairs
of ED motor units (including those with nonsignificant peaks)
was 0.57 ⫾ 0.31. The mean CIS values for motor-unit pairs
recorded both within and across compartments are shown in
Fig. 2. Eighty motor-unit pairs in total were recorded from
within the same compartment (Fig. 2, ■). These had mean CIS
values of 0.54 ⫾ 0.14 (n ⫽ 24), 0.66 ⫾ 0.28 (n ⫽ 23), 0.9 ⫾
0.39 (n ⫽ 21), and 0.75 ⫾ 0.2 (n ⫽ 12) for D2 through D5
compartments, respectively. A one-way ANOVA revealed a
significant difference between compartments in the CIS values
for intra-compartment motor-unit pairs (P ⬍ 0.001). A Tukey
post hoc analysis revealed that the CIS values for motor-unit
pairs within the D4 compartment were significantly greater
than for motor-unit pairs within the D2 compartment. No other
intra-compartment comparisons were significant.
Sixty-two motor-unit pairs were recorded that resided in
neighboring compartments of ED. The mean CIS values for
extra-compartmental groups were 0.20 ⫾ 0.13 for D2/D3 (n ⫽
12), 0.55 ⫾ 0.26 (n ⫽ 18) for D3/D4, and 0.42 ⫾ 0.15 for
D4/D5 (n ⫽ 32). The CIS values for different extra-compartment motor-unit pairs were significantly different from one
another (P ⬍ 0.001). The CIS values for pairs of motor units
in the D2/D3 finger compartments were significantly smaller
than for motor-unit pairs in the D3/D4 or D4/D5 compartments. Only three pairs of motor units were recorded in nonadjacent compartments with each of these having one unit in
the D3 compartment and the other unit in the D5 compartment
of ED. The mean CIS for these three pairs of motor units was
low at 0.14 ⫾ 0.07.
The mean CIS value for all 80 intra-compartment motor-unit
pairs was 0.7 ⫾ 0.3 (Fig. 3). In comparison, the mean CIS
value for the 65 extra-compartment motor-unit pairs was 0.4 ⫾
91 • JANUARY 2004 •
www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.6 on June 14, 2017
A total of 272 motor units in ED were recorded that were
used to generate 145 cross-correlation histograms. In 17 trials,
more than one unit was discriminated on an electrode which
yielded multiple correlations. The mean firing rate for all recorded
motor units was 10.6 ⫾ 2.0 Hz, and the mean number of events
used to generate the cross-correlograms was 1,864 ⫾ 836.
Four examples of cross-correlograms are shown in Fig. 1.
The labels at the top of the figure indicate the compartments
within which each of the microelectrodes was located. Substantial synchrony was found for the pair of units both located
in the D3 compartment with a CIS value of 0.76 (Fig. 1B). A
significant degree of synchrony was also observed for a D3–D4
pair of units with a CIS value of 0.63 (Fig. 1C). However, little
synchrony was found when the two electrodes were in nonadjacent compartments i.e., D3-D5, (Fig. 1D) or in the neighboring compartments of D2 and D3 (Fig. 1A) with CIS values of
0.22 and 0.28, respectively.
Of the total of 145 cross-correlograms, 84 had significant
60
D. A. KEEN AND A. J. FUGLEVAND
0.22, which was significantly smaller (P ⬍ 0.001) than the CIS
values for intra-compartment motor-unit pairs.
DISCUSSION
The main finding of the present study was that the degree of
synchrony for motor units within compartments of ED was
markedly greater than across compartments. A modest degree
of synchrony also existed for motor-unit pairs in neighboring
compartments. Therefore last-order synaptic projections are
not likely to be distributed uniformly across the entire pool of
motor neurons innervating ED. Rather, last-order projections
appear to supply predominantly subsets of motor neurons innervating specific finger compartments of ED. Consequently,
motor neurons innervating specific compartments may be activated differentially to facilitate movements of individual fingers. Nevertheless, the existence of extra-compartmental synchrony indicates some degree of across-compartment divergence that may contribute to inadvertent movement of
neighboring fingers when attempting to move a single finger
(Häger-Ross and Schieber 2000; Kilbreath and Gandevia 1994;
Robinson and Fuglevand 1999).
One limitation of the present study was that synchrony was
examined during a single task only, namely, during extension
of all four fingers together. This task was selected to promote
specific activity in ED. Tasks involving extension of individual
fingers, particularly of the index or little finger, might be
accomplished by activation of muscles other than ED. Nevertheless, it would be of interest to compare the level of synchrony across compartments of ED during extension of all the
fingers to that during extension of individual digits. Bremner et
al. (1991c) have clearly shown that motor-unit synchrony can
be modulated as a function of the task performed. Therefore it
seems feasible that the extra-compartmental synchrony in ED
might be attenuated during tasks in which subjects attempt to
J Neurophysiol • VOL
91 • JANUARY 2004 •
www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.6 on June 14, 2017
FIG. 3. Mean (⫾SD) CIS for all intra-compartment motor-unit pairs (■)
and extra-compartment pairs (䊐) of ED. The mean CIS value (0.7 ⫾ 0.3) for
the 80 motor-unit pairs within a single compartment was significantly greater
(P ⬍ 0.001) than the mean CIS value (0.4 ⫾ 0.22) for the 65 motor-unit pairs
that resided in different compartments. Therefore last-order projections appear
to predominantly supply subsets of motor neurons innervating specific finger
compartments.
extend a single finger. This possibility awaits future investigation.
Numerous other studies have examined the extent of motorunit synchrony in a variety of human muscles. There is a
modest tendency for greater motor-unit synchrony to be observed in muscles of the distal extremities compared with more
proximal muscles (Datta et al. 1991; Kim et al. 2001). For
example, Datta et al. (1991) showed that the degree of synchrony for pairs of motor units in first dorsal interosseus (an
intrinsic hand muscle) was nearly twice that of motor units in
tibialis anterior and about four times greater than motor units in
medial gastrocnemius. However, exceptions to such a proximal-distal gradient in synchrony have been reported (Adams et
al. 1989; De Luca et al. 1993; Huesler et al. 2000). Huesler et
al. (2000), for example, found significantly greater synchrony
among motor units in extrinsic than in intrinsic hand muscles.
In the present study, the overall mean CIS value for all pairs of
motor units in the extrinsic hand muscle ED was 0.57. This
value is comparable to the mean CIS values of 0.40 reported
for ED motor units by Schmied et al. (1993) and 0.47 for
extensor carpi radialis units (Schmied et al. 1994). These CIS
values for forearm muscles are not less than, and in some cases
slightly greater than, mean CIS values reported for first dorsal
interosseus (0.46, Nordstrom et al. 1992; 0.35, Semmler and
Nordstrom 1995). Consequently, the magnitude of motor-unit
synchrony is not obligatorily greater in intrinsic hand muscles
than in more proximal muscles.
In addition to extensive distribution of synaptic input across
motor neurons supplying an individual muscle, there is also
strong anatomical (Shinoda et al. 1981) and physiological
(Buys et al. 1986; Cheney and Fetz 1985; Fetz and Cheney
1980; McKiernan et al. 1998) evidence that cortico-spinal
axons in non-human primates diverge to supply more than one
motor nucleus. Consistent with these findings, the discharge
times of motor units residing in different hand muscles of
humans also exhibit synchrony, but usually to a lesser extent
than motor units residing in the same muscle (Bremner et al.
1991a,b; Gibbs et al. 1995; Huesler et al. 2000). In general, the
amount of synchrony for motor-unit pairs residing in the same
muscle is usually about twice as great compared with motorunit pairs in different hand muscles (Bremner et al. 1991b;
Huesler et al. 2000). We found a qualitatively similar ratio of
about double the amount of synchrony for motor-unit pairs
within compartments (CIS ⫽ 0.7) versus across compartments
(CIS ⫽ 0.4) in ED. This suggests that the extent of shared
last-order inputs onto motor neurons supplying different compartments of a multi-tendoned hand muscle is roughly similar
to the common input across motor neurons innervating separate
hand muscles.
Consistent with previous observations (Bremner et al.
1991b), the magnitude of synchrony was shown in the present
study to decline with increasing separation between pairs of
units. For example, as shown in the bottom row of the matrix
depicted in Fig. 2, the mean CIS for pairs of units in the same
compartment (D5–D5) was about twice that for pairs of units
in residing in neighboring compartments (D4 –D5), and was
about five times greater than that for pairs of units located in
nonadjacent compartments (D3–D5). Interestingly, Kilbreath
and Gandevia (1994) demonstrated a similar pattern in the
degree of coactivation across compartments of multi-tendoned
finger flexors when human subjects attempted to move indi-
MOTOR-UNIT SYCHRONY IN HUMAN EXTENSOR DIGITORUM
J Neurophysiol • VOL
directed to motor neurons innervating the D4 compartment of
ED. This distributed input may result in an inability to selectively activate neurons innervating specific compartments and
contribute to the extension of other fingers when attempting to
move only one finger.
GRANTS
This work was supported by National Institute of Neurological Disorders
and Stroke Grant NS-39489 to A. J. Fuglevand.
REFERENCES
Adams L, Datta AK, and Guz A. Synchronization of motor unit firing during
different respiratory and postural tasks in human sternocleidomastoid muscle. J Physiol 413: 213–231, 1989.
Asanuma H, Zarzecki P, Jankowska E, Hongo T, and Marcus S. Projection
of individual pyramidal tract neurons to lumbar motor nuclei of the monkey.
Exp Brain Res 34: 73– 89, 1979.
Binder MD, Heckman CJ, and Powers RK. The physiological control of
motoneuron activity. In: Handbook of Physiology. Exercise: Regulation and
Integration of Multiple Systems. Neural Control of Movement. New York:
Am. Physiol. Soc, 1996, sect. 12, vol. I, chapt. 1, p. 3–53.
Botterman BR, Hamm TM, Reinking RM, and Stuart DG. Localization of
monosynaptic Ia excitatory post-synaptic potentials in the motor nucleus of
the cat biceps femoris muscle. J Physiol 338: 355–377, 1983.
Bremner FD, Baker JR, and Stephens JA. Correlation between the discharges of motor units recorded from the same and from different finger
muscles in man. J Physiol 432: 355–380, 1991a.
Bremner FD, Baker JR, and Stephens JA. Variation in the degree of
synchronization exhibited by motor units lying in different finger muscles in
man. J Physiol 432: 381–399, 1991b.
Bremner FD, Baker JR, and Stephens JA. Effect of task on the degree of
synchronization of intrinsic hand muscle motor units in man. J Neurophysiol
66: 2072–2083, 1991c.
Brown AG and Fyffe REW. The morphology of group Ia afferent fiber
collaterals in the spinal cord of the cat. J Physiol 274: 111–127, 1978.
Buys EJ, Lemon RN, Mantel GWH, and Muir RB. Selective facilitation of
different hand muscles by single corticospinal neurones in the conscious
monkey. J Physiol 381: 529 –549, 1986.
Cheney PD and Fetz EE. Comparable patterns of muscle facilitation evoked
by individual corticomotoneuronal (CM) cells and by single intracortical
microstimuli in primates: evidence for functional groups of CM cells.
J Neurophysiol 53: 786 – 804, 1985.
Datta AK, Farmer SF, and Stephens JA. Central nervous pathways underlying synchronization of human motor units studied during voluntary contractions. J Physiol 432: 401– 425, 1991.
De Luca CJ, Roy AW, and Erim Z. Synchronization of motor-unit firings in
several human muscles. J Neurophysiol 70: 2010 –2023, 1993.
Fetz EE and Cheney PD. Postspike facilitation of forelimb muscle activity by
primate corticomotoneuronal cells. J Neurophysiol 44: 751–772, 1980.
Ellaway PH. Cumulative sum technique and its application to the analysis of
peristimulus time histograms. Electroencephalogr Clin Neurophysiol 45:
302–304, 1978.
Gibbs J, Harrison LM, and Stephens JA. Organization of inputs to motoneuron pools in man. J Physiol 485: 245–256, 1995.
Häger-Ross CK and Schieber MH. Quantifying the independence of human
finger movements: comparisons of digits, hands, and movement frequencies.
J Neurosci 20: 8542– 8550, 2000.
Hamm TH, Koehler W, Stuart DG, and Vanden Noven S. Partitioning of
monosynaptic Ia excitatory postsynaptic potentials in the motor nucleus of
the cat semimembranosus muscle. J Physiol 369: 379 –398, 1986.
Henneman E, and Mendell LM. Functional organization of motoneuron pool
and its inputs. In: Handbook of Physiology. The Nervous System. Motor
Control. Bethesda, MD: Am. Physiol. Soc., 1981, sect. 1, vol. I, chapt. 11,
p. 423–507.
Huesler EJ, Maier MA, and Hepp-Reymond MC. EMG activation patterns
during force production in precision grip. III. Synchronization of single
motor units. Exp Brain Res 134: 441– 455, 2000.
Jankowska E. Interneuronal relay in spinal pathways from spinal proprioceptors. Prog Neurobiol 38: 335–378, 1992.
Keen DA and Fuglevand AJ. Intraneural microstimulation indicates that
motor units in human extensor digitorum exert force on individual fingers.
Soc Neurosci Abstr 27: 168.10, 2001.
91 • JANUARY 2004 •
www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.6 on June 14, 2017
vidual digits. The correspondence between the pattern of inadvertent activity in muscle compartments inserting into digits
not intended for movement (Kilbreath and Gandevia 1994) and
the distribution of synchrony across motor units residing in
different compartments of multi-tendoned muscles (Bremner et
al. 1991b; present study) is consistent with the idea that divergence of the descending commands may limit the ability to
move the fingers independently.
Bremner and colleagues (1991b) also observed a tendency
for greater synchrony among motor units in more medial
(ulnar) than lateral (radial) muscles or muscle compartments.
Motor units residing in muscles inserting into the little finger,
however, were not evaluated in that study. We have extended
those findings (Bremner et al. 1991b) to show that the magnitude of synchrony within and across compartments of ED does
not necessarily continue to increase for more medially situated
compartments but rather reaches its apogee with the D4 compartment. The largest value of intra-compartment synchrony
was for D4 motor units and the least synchrony was for D2
units (Fig. 2). Moreover, the degree of extra-compartment
synchrony for D3/D4 motor-unit pairs was not less than (and
indeed was slightly greater than) synchrony for D4/D5 pairs.
Also, extra-compartment synchrony between D4 units and
units in either of the neighboring compartments (D3 or D5)
was significantly greater than extra-compartment synchrony
for D2/D3 motor-unit pairs.
These findings suggests that the last-order inputs onto motor
neurons that predominantly supply the D4 compartment of ED
may branch and terminate to a greater extent on motor neurons
innervating neighboring compartments compared with inputs
that primarily target motor neurons supplying other compartments. Consequently, when attempting to activate motor neurons innervating a compartment of ED, particularly the D4
compartment, branches from last-order inputs may activate
motor neurons innervating muscle fibers in neighboring ED
compartments. If unopposed by antagonistic muscle activity,
this may result in some extension of other digits when attempting to extend just one digit. Indeed, studies that have measured
the relative independence of finger movements in humans
(Häger-Ross and Schieber 2000; Robinson and Fuglevand
1999) have found that fingers do not move independently of
one another. Lack of independence in finger movements does
not appear to be caused primarily by biomechanical factors
(Keen and Fuglevand 2003; Kilbreath and Gandevia 1994).
Furthermore, the least-independent finger movement is extension of D4, whereas extension of D2 is the most-independent
movement compared with extension of the other fingers
(Häger-Ross and Schieber 2000; Robinson and Fuglevand
1999). These behavioral findings roughly coincide with the
general pattern of motor-unit synchrony observed across compartments of ED in the present study.
In summary, the degree of synchrony for motor-unit pairs
within a compartment of ED was significantly greater than for
motor-unit pairs in neighboring compartments, indicating that
the population of motor neurons innervating ED is coarsely
segregated into four separate pools of motor neurons. Furthermore, based on our observations of the degree of synchrony
across compartments, it appears that the last-order projections
supplying motor neurons innervating one compartment of ED
diverge to supply motor neurons innervating other compartments of ED. This was particularly true for inputs primarily
61
62
D. A. KEEN AND A. J. FUGLEVAND
J Neurophysiol • VOL
Nordstrom MA, Fuglevand AJ, and Enoka RM. Estimating the strength of
common input to human motoneurons from the cross-correlogram. J Physiol
453: 547–574, 1992.
Porter R and Lemon R. Corticospinal influences on the spinal cord machinery for movement. In: Corticospinal Function and Voluntary Movement.
Oxford: Oxford Univ. Press, 1993, p. 171–172.
Robinson TL and Fuglevand AJ. Independence of finger movements in
normal subjects and concert-level pianists. Soc Neurosci Abstr 25: 466.5,
1999.
Schmied A, Ivarsson C, and Fetz EE. Short-term synchronization of motor
units in human extensor digitorum communis muscle: relation to contractile
properties and voluntary control. Exp Brain Res 97: 159 –172, 1993.
Schmied A, Vedel J-P, and Pagni S. Human spinal lateralization assessed
from motoneurone synchronization: dependence on handedness and motor
unit type. J Physiol 480: 369 –387, 1994.
Sears TA and Stagg D. Short-term synchronization of intercostal motorneuron activity. J Physiol 48: 875– 890, 1976.
Semmler JG and Nordstrom MA. Influence of handedness on motor unit
discharge properties and force tremor. Exp Brain Res 104: 115–125, 1995.
Shinoda Y, Yokota JI, and Futami T. Divergent projection of individual
corticospinal axons to motoneurons of multiple muscles in the monkey.
Neurosci Lett 23: 7–12, 1981.
Vanden Noven S, Hamm TH, and Stuart DG. Partitioning of monosynaptic
Ia excitatory postsynaptic potentials in the motor nucleus of the cat lateral
gastrocnemius muscle. J Neurophysiol 55: 569 –586, 1986.
von Schroeder HP, Botte MJ, and Gellman H. Anatomy of the juncturae
tendinum of the hand. J Hand Surg 15: 595– 602, 1990.
91 • JANUARY 2004 •
www.jn.org
Downloaded from http://jn.physiology.org/ by 10.220.33.6 on June 14, 2017
Keen DA and Fuglevand AJ. Role of intertendinous connections in distribution of force in human extensor digitorum. Muscle Nerve 28: 614 – 622,
2003.
Kernell D. Muscle regionalization. Can J Appl Physiol 23: 1–22, 1998.
Kilbreath SL and Gandevia SC. Limited independent flexion of the thumb
and fingers in human subjects. J Physiol 479: 487– 497, 1994.
Kim MS, Masakado Y, Tomita Y, Chino N, Pae YS, and Lee KE. Synchronization of single motor units during voluntary contractions in the upper
and lower extremities. Clin Neurophysiol 112: 1243–1249, 2001.
Kirkwood PA and Sears TA. The synaptic connexions to intercostal motoneurons as revealed by the average common excitation potential. J Physiol
275: 103–134, 1978.
Lawrence DG, Porter R, and Redman SJ. Corticomotoneuronal synapses in
the monkey: light microscopic localization upon motoneurons of intrinsic
muscles of the hand. J Comp Neurol 232: 499 –510, 1985.
Loeb GE. The functional organization of muscles, motor units, and tasks. In:
The Segmental Motor System, edited by Binder MD and Mendell LM.
Oxford: Oxford Univ. Press, 1990, p. 23–35.
Mantel GWH and Lemon RN. Cross-correlation reveals facilitation of single
motor units in thenar muscles by single corticospinal neurons in the conscious monkey. Neurosci Lett 77: 113–118, 1987.
McKiernan BJ, Marcario JK, Hill Karrer J, and Cheney PD. Corticomotoneuronal postspike effects in shoulder, elbow, wrist, digit, and intrinsic
hand muscles during a reach and prehension task. J Neurophysiol 80:
1961–1980, 1998.
Mendell LM and Henneman E. Terminals of single Ia fibers: location,
density and distribution within a pool of 300 homonymous motoneurons.
J Neurophysiol 34: 171–187, 1971.