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DOI 10.1007/s00221-008-1479-5
R ES EA R C H A R TI CLE
Received: 1 April 2008 / Accepted: 16 June 2008 / Published online: 3 July 2008
© Springer-Verlag 2008
Abstract Electrical stimulation of the brachioradialis changes in forearm position, and represents a spinal basis
branch of the radial nerve has been shown to inhibit the dis- for a muscle synergy in humans.
charge of voluntarily activated motor units in biceps brachii
during weak contractions with the elbow Xexor muscles. Keywords Motor unit · Inhibition · Biceps brachii ·
The purpose of the present study was to characterise the Brachioradialis · Synergy
inhibitory reXex by comparing its strength in the short and
long heads of the biceps brachii and examining the inXu-
ence of forearm position on the strength of the reXex. Introduction
Spike-triggered stimulation was used to assess the inXuence
of radial nerve stimulation on the discharge of single motor An elbow Xexion torque is produced by the activation of a
units in the biceps brachii of 15 subjects. Stimulation of the number of muscles that cross the elbow joint and insert
radial nerve prolonged the interspike interval (P < 0.001) of onto the radius or ulna. Due to these attachment locations,
motor units in the long (n = 31, 4.8 § 5.6 ms) and short most of the muscles that contribute to an elbow Xexor
heads (n = 26, 8.1 § 12.3 ms) of biceps brachii with no torque also produce actions about other axes of rotation. As
diVerence between the two heads (P = 0.11). The strength a consequence of this anatomical organisation, some mus-
of inhibition varied with forearm position for motor units in cles are synergists for an elbow Xexor torque but are antag-
both heads (n = 18, P < 0.05). The amount of inhibition onists for other actions. One example of this arrangement is
was greatest in pronation (7.9 § 8.9 ms), intermediate in between the biceps brachii and brachioradialis muscles.
neutral (5.8 § 7.1 ms), and least in supination Both contribute to an elbow Xexor torque but biceps brachii
(2.8 § 3.4 ms). These Wndings indicate that the inhibition can also generate a supination torque whereas brachioradi-
evoked by aVerent feedback from brachioradialis to low- alis can produce both supination and pronation torques
threshold motor units (mean force 3–5% MVC) in biceps depending on the orientation of the forearm (Gielen and
brachii varied with forearm posture yet was similar for the van Zuylen 1986; Buchanan et al. 1989; Jamison and Cald-
two heads of biceps brachii. This reXex pathway provides a well 1993; Murray et al. 1995; Zhang et al. 1998). The
mechanism to adjust the activation of biceps brachii with opposing pronation–supination capabilities of these two
muscles modiWes the amount of activity that each generates
during an elbow Xexor task according to the concurrent
demands about the long axis of the forearm (Buchanan
B. K. Barry · Z. A. Riley · M. A. Pascoe · R. M. Enoka et al. 1989; Jamison and Caldwell 1993). For example, the
Department of Integrative Physiology,
University of Colorado, Boulder, CO 80309, USA
EMG activity of biceps brachii is greater when the task
involves concurrent Xexion and supination torques com-
B. K. Barry (&) pared with Xexion and pronation torques (Barry and Carson
School of Medical Sciences, 2004; Shemmell et al. 2005).
The University of New South Wales,
Sydney, NSW 2052, Australia The relative activation of the long and short heads of
e-mail: ben.barry@unsw.edu.au biceps brachii has also been shown to vary with the pronation
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348 Exp Brain Res (2008) 190:347–359
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Exp Brain Res (2008) 190:347–359 349
scapula. EMG signals were ampliWed (100–10,000 times; a mechanical vibrator (LDS V203 vibrator and PA25E
S-series, Coulbourn Instruments) and band-pass Wltered at power ampliWer, Ling Dynamic Systems, Herts, UK). An 8-
13 Hz to 1 kHz. Interference EMGs were sampled at 2 or mm-diameter aluminium probe was mounted on the vibra-
4 kHz and stored as described for the intramuscular signals. tor to interface with the skin. The reaction force against the
skin was measured with an MLP-10 force transducer
Nerve stimulation (Transducer Techniques, Temecula, CA) and maintained at
a background level of 1–2 N. The location and force of the
A Grass S88 stimulator (Grass Technologies, West War- mechanical taps to elicit brachioradialis T-reXexes was
wick, RI, USA) was used in series with an SIU5 isolation determined by averaging the EMG response to 24 mechani-
unit and a CCU1 constant-current unit to deliver a 0.5-ms cal pulses (»0.5 Hz) as the subject maintained a small
rectangular pulse to the brachioradialis branch of the radial background contraction. The intensity during spike-trig-
nerve at 0.9 £ motor threshold (MT). The cathodal stimula- gered stimulation was set at approximately 0.5–0.8£ the
tion was delivered at the lateral side of the upper arm, over threshold for a motor response and the stimulus was deliv-
the humerus and 3–4 cm superior to the lateral epicondyle. ered at a 25 ms delay after each trigger motor unit dis-
After locating an appropriate stimulation site by using a charge. Careful positioning of the vibrator was required to
bipolar metal probe electrode, adhesive electrodes (NDM avoid eliciting monosynaptic 1a excitation of the biceps
Peripheral Nerve Stimulation electrodes, 10 mm Ag–AgCl brachii by activation of muscle spindles in extensor carpi
disc with a 2.4 £ 1.9 cm gel contact area, Conmed, Utica, radialis (Cavallari and Katz 1989). It was necessary to
NY, USA) were positioned to evoke a clear brachioradialis locate the vibrator over the brachioradialis belly rather than
M-wave at a low stimulus intensity, without any activation the distal tendon for some subjects.
of extensor carpi radialis at a stimulus intensity of at least
2 £ MT for brachioradialis (Naito et al. 1996). Although Maximal voluntary contractions
smaller stimulating electrodes would have allowed more
focal stimulation, larger electrodes ensured more consistent Maximal voluntary contractions (MVCs) were performed
activation of the aVerent Wbres when diVerent forearm posi- with the elbow Xexor muscles with the forearm in a neutral
tions were examined and there was movement of the sur- position. Participants were instructed to increase the torque
face electrode relative to the underlying nerve. during the isometric contraction to maximum in »3 s and
Because the brachialis muscle can receive some innerva- then to exert as much torque as possible for an additional
tion from the radial nerve in addition to its primary innerva- 3 s. After several practice attempts, MVCs were performed
tion from the musculocutaneous nerve (Mahakkanukrauh 3 times with successive attempts separated by 2–3 min of
and Somsarp 2002; Vicente et al. 2005; Blackburn et al. rest. The maximal torque achieved in the 3 attempts was
2007), a separate experiment was conducted to evaluate the taken as the MVC torque.
origin of the aVerents responsible for the inhibition from
stimulating the radial nerve. The radial nerve branch to Protocol
brachialis is relatively close to that innervating brachioradi-
alis and near the electrodes that were used to evoke the The strength of the reXex was assessed by recording the
response. To assess the possible involvement of aVerents discharge of single motor units from biceps brachii with a
arising from brachialis, the stimulation was optimised to Wne wire electrode that was inserted into either the long or
elicit an M-wave in either brachialis or brachioradialis while short head of biceps brachii. The subject produced low Xex-
ensuring that there was no activation of extensor carpi radia- ion forces until a single motor unit was isolated that could
lis at intensities up to 2.0 £ MT. The responses to »100 be clearly discriminated using a threshold window discrim-
stimuli were recorded for the same motor unit in biceps inator (S-series, Coulbourn Instruments). Spike-triggered
brachii to the stimulation Wrst optimised for one of the two stimulation (Stephens et al. 1976; Fournier et al. 1986) was
muscles and then optimised for the other muscle. The motor then delivered every 2–3 s as subjects maintained a steady
threshold for both brachialis and brachioradialis was identi- discharge rate of »11 pulses per second (pps). Each of the
Wed for each stimulation location to determine the eVective 100 stimuli was given at a set delay after a selected dis-
stimulation intensity for the non-target nerve branch when charge.
the target nerve branch was activated at 0.9 £ MT. In addition to threshold discrimination, online template
matching of the motor unit action potential was performed
Tendon stimulation with Spike2 software (CED) to verify that the same single
motor unit was monitored throughout the experiment.
Brief mechanical pulses (3 pulses at 200 Hz, 15 ms) were Audio feedback of the motor unit discharge and visual
applied to the distal tendon or belly of brachioradialis using feedback of elbow Xexion force and motor unit discharge
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350 Exp Brain Res (2008) 190:347–359
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Exp Brain Res (2008) 190:347–359 351
approximately 100 stimuli were recorded for each posture, Statistical analysis
but trials were only conducted when the amplitude, width,
and shape of a motor unit action potential were suYciently Discharge rate characteristics, force, and EMG for each
consistent across positions to indicate that the recording muscle were compared with repeated-measures ANOVAs
was from the same motor unit. The arm was moved mini- for each stimulation trial. Peak-to-peak amplitudes of the M
mally between the diVerent positions to avoid disrupting waves were compared between forearm positions with
the single motor unit recording. As an index of stimulus repeated-measures ANOVA. Chi-square statistics were
consistency, brachioradialis M-waves were measured either used to examine the inXuence of stimulation on the PSTHs
prior to or after each sequence in the diVerent forearm for the stimulation and control triggers. PSTHs were com-
positions. pared for 25–95 ms after the stimulation. The observed and
expected counts for calculation of the Chi-square statistic
Data analysis were drawn from groups of 10 bins of the PSTHs to ensure
a mean bin count of ¸5 to satisfy the assumptions of the
Mean force, mean discharge rate, and the coeYcient of var- Chi-square test. Repeated-measures ANOVAs were used to
iation (CV) for interspike interval (ISI) were calculated contrast the mean interspike intervals recorded prior to
around the times when the stimuli were delivered. Template (ISI-pre) and during (ISI-0) the motor unit discharges
matching with Spike2 software was repeated oZine to dis- selected to generate the triggers (stimulation and control)
criminate individual motor unit action potentials. The accu- and to assess the diVerence between the two heads of biceps
racy of this discrimination was veriWed by visual inspection brachii and the diVerent forearm positions. All motor units
of each discriminated action potential and by reviewing the were included in the analysis of the mean interspike inter-
distribution of interspike intervals. The oZine analysis also vals. An alpha level of P < 0.05 was used to identify signiW-
veriWed that no motor unit discharges occurred in the time cant diVerences. All statistical analyses were performed in
period between a stimulation or control event and the pre- SPSS (Chicago, IL). Data are presented in the text and
ceding trigger discharge of the motor unit. Post-stimulus tables as mean § standard deviation (SD).
time histograms (PSTH) were constructed with 0.5-ms bins
for the 100-ms period after the delivery of a stimulus and
for control conditions when no stimulus was provided. Results
Cumulative sums were calculated from the stimulation and
control histograms (Ellaway 1978). Prolongation of the interspike intervals was similar
The degree of inhibition across the motor unit sample (P = 0.59; Fig. 1b) for all three stimulus delays (30, 40, and
was quantiWed by measuring the prolongation of the 50 ms) in 16 motor units; 8 each from the short and long
interspike interval induced by the radial nerve stimulation heads of biceps brachii (3 subjects). SigniWcant inhibition
(Datta and Stephens 1981; Nafati et al. 2005). The three was evident in 14 of 16 PSTHs for the 30-ms delay and in
ISIs prior to stimulation were averaged (ISI-pre) and the 13 of 16 PSTHs for the 40- and 50-ms delays. The peak
ISI that included the stimulation (ISI-0) was measured. negative values for the cumulative sums were
The diVerence between the two values (ms) was used to ¡28.3 § 19.3 impulses/stimulus for the 30-ms delay,
indicate the strength of the reXex inhibition. A positive ¡29.8 § 17.6 impulses/stimulus for the 40-ms delay, and
value for either index corresponded to inhibition, whereas ¡22.0 § 8.5 impulses/stimulus for the 50-ms delay
a negative value indicated facilitation. These intervals (P = 0.13). The latency of the inhibition relative to the trig-
were extracted for every stimulation and control trigger ger motor unit discharge was 64.2 § 8.8 ms for the 30-ms
and the average values for each motor unit were calcu- delay (34.2 ms following stimulation), 69.0 § 6.1 ms for
lated. the 40-ms delay (29.0 ms following stimulation) and
The selectivity of radial nerve stimulation was measured 72.1 § 8.1 ms for the 50-ms delay (22.1 ms following stim-
by averaging the EMG from the brachioradialis and exten- ulation) (P < 0.05). The duration of the trough in the cumu-
sor carpi radialis muscles following stimulation at or above lative sum did not diVer (P = 0.96) for the 3 stimulation
motor threshold for both muscles. The peak-to-peak ampli- delays (30 ms: 19.3 § 13.0 ms; 40 ms: 18.0 § 11.7 ms;
tude of the brachioradialis M-wave in response to stimula- 50 ms: 18.3 § 20.9 ms).
tion at 1–2 £ MT was recorded before and at the end of The time course of reXex input was examined further in
each experimental session or during each change in forearm 66 motor units from 13 subjects by assessing the inXuence
position to ensure that stimulation conditions did not of radial nerve stimulation (30-ms delay) on several inters-
change. The waveform was also averaged during the motor pike intervals after the selected motor unit trigger (Fig. 2).
unit trials to ensure there was no motor response to the There was a signiWcant eVect of the stimulation (P < 0.001)
stimulation during the low-force contractions. that varied across the interspike intervals (P < 0.01).
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352 Exp Brain Res (2008) 190:347–359
94
1 0.95 0.65
92 2 0.54 0.88
3 0.90 0.72
90
4 0.78 0.74
5 0.57 0.82
88
6 0.86 0.56
86 7 0.86 0.64
ISI-pre ISI-0 ISI+1 ISI+2 ISI+3 ISI+4
8 0.72 0.46
Interspike interval
9 0.87 0.73
Fig. 2 The inXuence of stimulating the brachioradialis branch of the Mean (SD) 0.78 (0.15) 0.69 (0.13)
radial nerve on successive interspike intervals. The stimulation was
delivered during ISI-0. Data are shown for 66 motor units recorded
with the forearm in a neutral position. The error bars indicate the 95%
conWdence intervals (P < 0.05). The interspike interval was prolonged by
3.68 § 3.31 ms with radial nerve stimulation compared
with 0.52 § 2.01 ms for cutaneous stimulation (Fig. 3). The
Independent t tests indicated signiWcant diVerences at each strength of the reXex inhibition in the same motor unit
ISI following stimulation (P < 0.05), with the most consis- (n = 4) increased signiWcantly (P < 0.05) with an increase
tent eVect occurring during ISI-0 and ISI + 1. After the ini- in stimulation intensity from 0.5 to 1.1 £ MT (Fig. 4). The
tial prolongation of the interspike interval (ISI-0), the interspike interval was signiWcantly prolonged by the
duration of the next interspike interval (ISI + 1) was mechanical activation of brachioradialis aVerents
shorter, but then increased again for the second interspike (P < 0.05) and by electrical stimulation of the brachioradi-
interval after stimulation (ISI + 2). By the fourth interspike alis branch of the radial nerve (P < 0.05) for six single
interval after stimulation (ISI + 4), the duration of the motor units from six subjects (Fig. 5).
interspike interval was similar to control levels. The strength of the inhibition in motor units from the
Responses were obtained for nine motor units (six sub- long and short heads of biceps brachii was compared to
jects) with the stimulation optimised for the brachioradialis spike-triggered stimulation for 57 motor units (31 long
branch of the radial nerve in one sequence, and for the head, 26 short head) from 11 subjects. On average, the
brachialis branch in another sequence (Table 1). The two responses to 99 § 22 stimuli were recorded over a period of
nerve branches could only be stimulated with limited selec- 271 § 64 s. Subjects exerted a mean force of 3.6 § 2.2%
tivity. Stimulation of the brachioradialis branch at
0.9 £ MT corresponded to an intensity of 0.78 § 0.15 £
MT for the brachialis branch of the radial nerve. Similarly, A) Cutaneous B) Radial nerve
stimulation of the brachialis branch at 0.9 £ MT was asso- 15 15
ciated with an intensity of 0.69 § 0.13 £ MT for the bra-
chioradialis branch. Stimulation at each location elicited
ISI difference (ms)
10 10
signiWcant inhibition of motor unit discharge (P < 0.001),
and although the percentage change in ISI was greater for
5 5
stimulation of the brachioradialis nerve branch (6.1%) than
for the brachialis branch (2.2%), the diVerence was not sig-
0 0
niWcant for the two locations (P = 0.197).
Additional measurements veriWed the speciWcity of the
stimulation used to evoke reXex inhibition of biceps brachii -5 -5
Control Stimulation Control Stimulation
motor unit discharge. The inXuence of stimulating the bra-
chioradialis branch of the radial nerve was compared to Fig. 3 Data for 14 single motor units showing the ISI diVerence
evoked by stimulation of the brachioradialis branch of the radial nerve
electrical stimulation of the skin for 14 motor units (seven
(b) and the combined eVect of two diVerent sites of cutaneous stimula-
subjects). SigniWcant inhibition was only observed after tion (a). These data were obtained with the forearm in a neutral
stimulation of the brachioradialis branch of the radial nerve position
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Exp Brain Res (2008) 190:347–359 353
30 Stimulation Table 2 Summary data for 57 motor unit recordings from the short
and long heads of the biceps brachii during spike-triggered stimulation
25 Control
of the brachioradialis branch of the radial nerve
Long head Short head
ISI Difference (ms)
20
(n = 31) (n = 26)
15
Trial duration (s) 271 § 53 270 § 77
10 Number of stimuli 98 § 20 100 § 24
Mean force (% MVC) 3.0 § 2.0 4.3 § 2.2
5
Mean interspike interval (ms) 89.1 § 5.7 90.9 § 6.4
0 CoeYcient of variation for ISI (%) 18.3 § 5.0 17.7 § 7.6
-5 No signiWcant diVerences between the heads (P > 0.3), except for mean
0.5 0.6 0.7 0.75 0.8 0.9 1.0 1.1
force (P < 0.05)
Stimulation intensity (proportion MT)
2
0 0
4 4 1
Number of counts
Control
0 0 0
Difference
4
5 -1
0 Control Stimulation
0
-4
-5
Radial nerve electrical stimulation
Cumulative Sum Brachioradialis tendon tap
40 0
0
-20
0 70 0 70
Time (ms) Time (ms)
Fig. 5 Mechanical tendon taps (200 Hz, 15 ms) were applied either to duced by mechanical taps applied to the brachioradialis. b Mean data
the distal tendon or belly of extensor carpi radialis and brachioradialis for 6 single motor units in response to randomly intermingled electrical
in two sequences while recording from the same single motor unit. a stimulation to the brachioradialis branch of the radial nerve and
Sample PSTHs and cumulative sums from a single subject reveal the mechanical taps to the tendon or belly of the brachioradialis muscle.
previously described excitatory eVect of stimulating muscle spindles in These data were obtained with the forearm in a neutral position
the extensor carpi radialis, which contrasts with an inhibitory eVect in-
123
354 Exp Brain Res (2008) 190:347–359
heads (n = 13) of biceps brachii in the same experiment ses- Table 3 Force and discharge characteristics for 18 motor units
sion, which permitted comparison with a common stimula- recorded in each of the three forearm positions
tion site. These data also displayed a signiWcant eVect of Pronated Neutral Supinated
stimulation (P < 0.05), with no signiWcant diVerence
between the long and short heads of biceps brachii (ISI Trial duration (s) 234 § 58 275 § 87 233 § 62
diVerence: 4.9 § 5.2 and 9.8 § 15.9 ms, respectively; Number of stimuli 90 § 24 94 § 23 88 § 26
P = 0.22). There was considerable variability in the inXu- Mean force (% MVC) 4.1 § 1.5 3.7 § 1.9 4.3 § 1.9
ence of the stimulation on single motor unit discharge, both Mean interspike 88.3 § 5.2 89.1 § 5.8 86.7 § 6.1
interval (ms)
between and within subjects, especially for the short head
of biceps brachii (Fig. 6). CoeYcient of 15.5 § 5.2 17.1 § 6.3 14.9 § 4.4
variation for ISI (%)
For the second part of the purpose, the response to stim-
ulating the brachioradialis branch of the radial nerve was No signiWcant diVerences for force (P > 0.45) or interspike interval
(ISI) data (P > 0.14). Data are combined for the nine motor units from
recorded for 18 single motor units (9 long head, 9 short each head of biceps brachii because there was no signiWcant diVerence
head) in 3 diVerent forearm positions from 8 subjects. Sub- (P ¸ 0.20) between these samples for the force or discharge rate char-
jects exerted low forces (4.0 § 1.8% MVC forces) with the acteristics
elbow Xexor muscles and maintained an average discharge
rate of 11.4 § 0.8 pps for the active motor unit (Table 3). 8.2 ms), intermediate in neutral (5.8 § 7.1 ms), and least in
There were no signiWcant diVerences in trial duration, num- supination (2.8 § 3.4 ms; P < 0.05; Fig. 8a). There was
ber of stimuli, elbow Xexion force, or discharge characteris- considerable variability between individual motor units,
tics (P > 0.14) across the three forearm positions. and this variability was less in the supination position than
Chi-squared statistics of the PSTH revealed signiWcant in the neutral and pronated positions (Fig. 8b). There was
inhibition in 12/18 histograms when the forearm was pro- no diVerence in the response to stimulation across the three
nated, 11/18 when it was in a neutral position, and 11/18 positions between motor units from the short (n = 9) and
when it was supinated; the peak negative values for the long (n = 9) heads of biceps brachii (P = 0.75).
cumulative sums were ¡21.9 § 18.6 impulses/stimulus in As an index of stimulus consistency, the brachioradialis
pronation, ¡23.1 § 20.0 impulses/stimulus in neutral, and M-wave amplitude did not change (Fig. 8c) across the three
¡17.4 § 13.7 impulses/stimulus in supination. Example positions (expressed as a proportion of the control M-wave:
PSTHs, cumulative sums, and associated motor unit action pronation 0.94 § 0.15; neutral 0.95 § 0.14; supination
potentials are shown in Fig. 7 for the three forearm posi- 1.05 § 0.19; P = 0.9). Furthermore, background levels of
tions. Prolongation of the interspike intervals after radial muscle activity were quantiWed for each of the three arm
nerve stimulation was apparent in all three arm positions, positions by averaging the root mean square of the EMG
with the greatest inhibitory eVect in pronation (7.9 § amplitude over multiple 0.5-s intervals starting 1 s prior to
50 50
40
ISI difference (ms)
40
30 30
20 20
10 10
0 0
-10 -10
Control Stimulation Control Stimulation
Fig. 6 The ISI diVerence for the stimulus and control conditions for tion and stimuli were delivered to the brachioradialis branch of the ra-
each of 31 motor units from the long head (a) and 26 motor units from dial nerve. The 2 motor units from the short head of biceps brachii (b)
the short head (b) of biceps brachii. The diVerence between the base- that displayed the greatest inhibition were both recorded from the same
line ISIs and the ISI that included the stimulation was signiWcant for subject and motor units recorded from this subject’s long head also dis-
both heads (P < 0.001) with no diVerence between the heads played some of the largest inhibition in the sample
(P = 0.11). The data were obtained with the forearm in a neutral posi-
123
Exp Brain Res (2008) 190:347–359 355
4 Stimulation 6 5
Number of counts (% of triggers)
0 0 0
6 Control 5 4
0 0 0
Difference
3 4 4
0 0 0
-6 -4 -4
Cumulative Sum
0 0 0
Fig. 7 Post-stimulus time histograms and overlaid motor unit action tween the stimulation and control histograms; the negative deXection
potentials for the same single motor unit recorded with the forearm in denotes an inhibitory eVect of the stimulation that prolonged the time
pronated, neutral, and supinated positions. The post-stimulus time his- to the next discharge of an action potential by the motor neurone. The
tograms were constructed for the stimulation and control conditions, stimulation was delivered at time 0 ms, which corresponded to a delay
and the cumulative sum procedure was applied to the diVerence be- of 30 ms after the preceding motor unit discharge
each stimulation or control event. There was a signiWcant ergist muscle for elbow Xexion, can slow the ongoing dis-
task £ muscle interaction (P < 0.05) for the normalised charge of a voluntarily activated motor unit in biceps
EMG data. Similar levels of normalised EMG were brachii. The results on the inXuence of forearm position are
recorded for brachioradialis (1.41 § 0.94, 1.42 § 0.86, consistent with the hypothesis, but the similarity of the
1.40 § 0.90% for pronation, neutral, and supination, strength of the reXex in the two heads of biceps brachii con-
respectively), brachialis (8.44 § 11.20, 7.93 § 10.38, trasts with the expected results.
7.97 § 10.41%), and triceps brachii (3.49 § 2.89,
3.41 § 2.86, 3.45 § 3.00%) across the three arm positions Identifying the source of inhibition
although brachialis activity was higher than all of the other
muscles in the three tasks. EMG amplitude was lower when Inhibition was quantiWed by examining the inXuence of
the forearm was in the pronated position for the long head stimulation on the mean duration of the interspike interval
(3.08 § 2.10, 5.29 § 5.85, 5.05 § 3.79% MVC for the (Datta and Stephens 1981; Nafati et al. 2005). Post-stimu-
three positions, respectively) and short head (2.01 § 1.53, lus time histograms were also calculated to permit compari-
2.55 § 1.90%, 2.54 § 2.07% MVC) of biceps brachii. son with previous data (Naito et al. (1996). The mean
interspike interval analysis indicated a progressive increase
in inhibition as forearm position was adjusted from supina-
Discussion tion to pronation. The reliability of the mean interspike
interval analysis was veriWed with the control interspike
The main Wndings of this study were the presence of reXex interval analysis by also assessing the mean interspike
inhibition in both heads of biceps brachii, with no diVer- intervals before and after control triggers interspersed with
ence in the level of inhibition of motor unit discharge stimulation triggers throughout the spike trains.
between the two heads, and modulation of the strength of The latency of the inhibition in the current study was
reXex inhibition with changes in forearm position. These similar to that reported by Naito et al. (1996). When the
results conWrm the original Wndings of Naito et al. (1996) brachioradialis branch of the radial nerve was stimulated at
that a spinal reXex pathway from the brachioradialis, a syn- a delay of 50 ms after the trigger motor unit discharge, the
123
356 Exp Brain Res (2008) 190:347–359
123
Exp Brain Res (2008) 190:347–359 357
sor carpi radialis muscle (Cavallari and Katz 1989) and its origin at the supraglenoid tubercle, appears to be posi-
supports a role for 1a-aVerents from brachioradialis in the tioned for a stronger contribution to a supination torque
inhibition evoked by electrical stimulation of the radial (Athwal et al. 2007; Eames et al. 2007).
nerve. The low electrical threshold of the inhibition It has been proposed that spinal reXex pathways are
(»0.5 £ MT) was consistent with the involvement of group responsible for the diVerence in activation of the motor unit
1 aVerents. The current results also dismiss a role for cuta- populations in the two heads of biceps brachii (Jongen et al.
neous aVerents in the inhibition; the discharge of motor 1989). Results obtained in the present study, however, sug-
units in biceps brachii was not inXuenced by stimulation of gest that reXex inhibition from brachioradialis to biceps
the skin at two diVerent sites on the upper arm. brachii is not one of the pathways that contribute to the
It was not possible to stimulate with suYcient selectivity selective activation of motor units from the two heads of
the branches of the radial nerve to brachialis and brachio- biceps brachii, at least not for low-threshold motor units.
radialis with surface electrodes. The strength of inhibition Ter Haar Romeny et al. (1984) found that the variation in
with brachialis stimulation (2.2%) tended to be less than activation was observed in motor units with recruitment
with brachioradialis stimulation (6.1%), but optimising the thresholds up to 45% MVC force in the long head of biceps
stimulation to the brachialis branch was still »0.7 £ MT brachii, and it could be that the results in the current study
for the brachioradialis branch. Because an intensity of are limited by only having recorded low-threshold motor
0.7 £ MT was suYcient to delay the discharge of a biceps units. Furthermore, the current experiment focused on
brachii motor unit (Fig. 4), this might explain the observed motor unit activity when the task was to exert an elbow
inhibition with brachialis nerve branch stimulation. How- Xexion torque and actions about the pronation–supination
ever, it was not possible to exclude the involvement of axis were not measured.
aVerents from the brachialis muscle. Alternatively, inhibitory reXex pathways from other
upper arm muscles could be responsible for controlling the
Inhibition in the two heads of biceps brachii diVerential recruitment proWles of motor units in the two
heads of biceps brachii (Cavallari and Katz 1989; Jongen
Motor unit recruitment and discharge characteristics in the et al. 1989; Naito 2004). Reciprocal inhibition has been
two heads of biceps brachii can diVer (ter Haar Romeny demonstrated between the biceps brachii and triceps brachii
et al. 1984; van Zuylen et al. 1988; Herrmann and Flanders (Katz et al. 1991), and coactivation of these muscles during
1998). For example, some motor units in the medial portion elbow Xexion tasks results in diVerent patterns of muscle
of the long head of biceps brachii had lower recruitment activation within and between the two heads of biceps
thresholds when supination torques were performed con- brachii (Jongen et al. 1989).
currently with an elbow Xexor torque, whereas motor units
in the lateral portion could only be recruited when a Xexor Forearm position
torque was exerted by itself (ter Haar Romeny et al. 1984).
In contrast, motor units in the short head of biceps brachii Biceps brachii and brachioradialis act as synergists when
could only be recruited when the task involved a combina- producing an elbow Xexion torque, but can be synergists or
tion of Xexion and supination torques (van Zuylen et al. antagonists when exerting a torque about the pronation–
1988). Few motor units were recorded in these studies, supination axis of the forearm (Gielen and van Zuylen
however, and more recent evidence indicates that motor 1986; Buchanan et al. 1989; Jamison and Caldwell 1993;
units with diVerent recruitment patterns are distributed con- Murray et al. 1995; Zhang et al. 1998). Biceps brachii
tinuously across biceps brachii rather than being clustered always has a supination moment regardless of forearm
into discrete muscle regions (Herrmann and Flanders position, whereas brachioradialis has a pronation moment
1998). Nonetheless, the activation patterns of motor units when the forearm is supinated and a supination moment
from the long and short heads of biceps brachii does appear when the forearm is pronated (Zhang et al. 1998). Biceps
to diVer (Herrmann and Flanders 1998). brachii EMG activity is greater when the task involves con-
Consistent with a possible functional distinction between current Xexion and supination torques compared to Xexion
motor units in the short and long heads of biceps brachii, a and pronation torques, but brachioradialis EMG remains
cadaveric study found that the distal tendon attachment had relatively constant with variation in forearm position
two distinct parts in 10 of 17 specimens and was interdigi- (Buchanan et al. 1989). Motor units located medially in the
tated in the other 7 specimens (Eames et al. 2007). The ten- long head of biceps brachii that contribute to Xexion and
don for the short head inserted distally on the radial supination torques have also been shown to become silent
tuberosity, which places it in a more advantageous position when even minimal pronation is produced (ter Haar Rom-
to produce Xexion torques. The tendon for the long head eny et al. 1984). It was suggested that the discharge of these
inserted proximally on the radial tuberosity, and based on motor units was “gated” by pronation, which could explain
123
358 Exp Brain Res (2008) 190:347–359
the reduced muscle activity observed in biceps brachii Acknowledgments Brian J. Paulson, Elizabeth Terry, and Kristin E.
when producing pronation torques or when the forearm is Taylor assisted with data collection and analysis. This research was
supported by NIH/NINDS NS43275 to RME.
in a pronated position (Buchanan et al. 1986; van Zuylen
et al. 1988; Buchanan et al. 1989; Jongen et al. 1989; Jami-
son and Caldwell 1993).
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