Brain (1998), 121, 373–380
Electrical stimulation over muscle tendons in
humans
Evidence favouring presynaptic inhibition of Ia fibres due to
the activation of group III tendon afferents
Alberto Priori,1,2 Alfredo Berardelli,1,3 Maurizio Inghilleri,1 Francesca Pedace,1 Morena Giovannelli1
and Mario Manfredi1,3
1Department of Neurological Science, Università
‘La Sapienza’, Roma, 2Division of Neurology, Ospedale
Civile ‘Ettore Spalenza’, Rovato and 3Mediterranean
Institute of Neuroscience ‘Neuromed’, Pozzilli, Italy
Summary
Electrical stimulation over muscle tendons produces a
transient suppression of voluntary EMG activity; its onset
latency is ~55 ms in the forearm extensor muscles. This
phenomenon has been attributed to the activation of a
polysynaptic inhibitory pathway originating from Ib afferent
fibres. To clarify its origin we conducted several experiments
in 10 normal healthy subjects. The EMG silence after
tendon stimulation appeared at relatively high stimulus
intensities (.50 mA); conditioning cutaneous stimulation
left it unchanged, and the inhibition had a short recovery
cycle (50 ms). Tendon stimulation still evoked EMG
suppression during an ischaemic block of fast-conducting
Keywords: muscle tendon; Ia afferents; group III afferents; presynaptic inhibition; silent period
Abbreviation: MEP 5 motor evoked potential
Introduction
Although muscle tendons are generally considered as simple
passive torque transmitters between striated muscles and the
environment they have a dense innervation (Mense and
Meyer, 1985). The functional significance of this innervation
remains largely unknown, particularly in relation to motor
control. Among the many tendon receptors, the best
characterized are the Golgi tendon organs (Jami, 1992).
Various methods have been described for investigating the
Ib pathway originating from Golgi organs in humans (Pierrot-
Deseilligny et al., 1981; Cavallari et al., 1985). More recently,
using a simple attractive method presumed to test Ib
inhibition, Burne and Lippold (1996a) showed that electrical
stimulation over muscle tendons produces a reflex inhibition
© Oxford University Press 1998
Correspondence to: Alfredo Berardelli, MD, Dipartimento
di Scienze Neurologiche, Viale dell’Università 30, 00185
Roma, Italy
afferents. The motor potentials evoked by transcranial
magnetic stimulation of the motor cortex during the EMG
silence remained almost unchanged, whereas the H reflex
was strongly inhibited. Hence we conclude that tendon
stimulation activates slow-conducting tendon afferents,
possibly group III fibres, connected not through a
polysynaptic pathway originating from Ib afferents but
through an oligo- or disynaptic inhibitory circuit. The EMG
suppression after tendon stimulation probably represents a
dysfacilitation of the α-motor neurons due to presynaptic
inhibition of Ia fibres produced by tendon afferent input
to the spinal cord.
of the ongoing voluntary muscle activity, appearing in forearm
extensor muscles at an onset latency of ~55 ms. Their
hypothesis proposed that this inhibition arises from Golgi
tendon afferents via a polysynaptic Ib pathway. Yet this
conclusion—especially the long latency of the EMG
suppression (Burne and Lippold, 1996a)—seems difficult to
reconcile with evidence that Ib afferents have a fast
conduction velocity ranging from 60 to 110 m/s (see Jami,
1992) and connect to the homonymous motor neurons through
a di- or trisynaptic inhibitory circuit (Eccles et al., 1957;
Jankowska, 1992). A further argument against the possible
activation of Golgi tendon organ afferents is that because
Burne and Lippold (1996a) stimulated tendons they might
374 A. Priori et al.
not have activated the afferents of Golgi tendon organs which
are located at the musculo-tendinous junction and not within
the tendons themselves (Jami, 1992). In this series of
experiments we therefore sought to clarify the origin and
mechanism of the EMG suppression after stimulation over
muscle tendons.
Material and methods
Experiments were conducted in 10 normal healthy volunteers
aged 24–45 years. Some subjects were tested more than once
in different experiments. The number of subjects for each
experiment is specified in the Results section. Subjects
provided their informed consent to the study. The
experimental design was approved by the local ethical
committee and complied with the Declaration of Helsinki.
During testing subjects were comfortably seated on an
armchair.
Stimulation techniques
Electrical stimuli were delivered to the muscle tendon (Burne
and Lippold, 1996a) and, in some experiments to the
peripheral nerves (the radial superficial nerve 5 cm proximal
to the wrist and the median nerve either at the wrist or at
the elbow) and to the skin of the fingers 2 and 3. The tendon
of the extensor digitorum communis was stimulated with the
anode 1 cm proximal to the styloid process of the ulna and
the cathode ~3–4 cm proximal to the anode over the tendon.
Tendons were localized according to anatomical reference
data (Tobin and Jacobs, 1981) and by palpation. A pair of
ring electrodes (separation 4 cm, cathode proximal) was used
for finger stimulation.
Electrical stimuli were generated either with a Grass
S88 stimulator (Grass Medical Instruments, Quincy, USA)
connected to an isolation unit (Grass SIU5) or with a Digitimer
DS7 constant current stimulator (Digitimer, Welwyn Garden
City, Hertfordshire, UK). Stimuli were square-wave electrical
pulses (duration 0.05 ms for tendons, 1 ms for nerves),
delivered by standard Ag/AgCl surface electrodes (diameter
9 mm) placed over the tendon or the nerve. In some
experiments stimuli for cutaneous stimulation consisted of
trains of 10 pulses at 250 Hz. Stimulus intensities are specified
in the Results section. The nerve action potential at the Erb
point was obtained by stimulating the median nerve at the
wrist at an intensity below motor threshold for evoking a
twitch in the thenar muscles and producing paraesthesias in
the first three fingers. The recovery curve of the EMG
suppression produced by stimulation over muscle tendons
was studied by delivering paired stimuli over the tendon at
various conditioning–test intervals (10–120 ms). The H reflex
in the flexor carpi radialis was evoked by stimulating the
median nerve at the elbow, at the stimulus intensities needed
to produce a maximum sized H reflex for the experiments
with ischaemic block, and at 50% of the maximum when the
H reflex was used as a test reflex (Crone et al., 1990)
In one set of five experiments we stimulated the forearm
area of the left motor cortex using a figure-of-eight coil with
lateromedial current flow connected to a magnetic stimulator
(Novametrix Magstim 200; The Magstim Company, UK).
The intensity of stimulation was 10% above the threshold
for evoking a motor potential in forearm muscles during a
slight voluntary contraction (20–30% of maximum). In a
further series of experiments, the motor cortex was also
stimulated with electrical stimuli (Digitimer D180) via a pair
of scalp surface electrodes; the anode was placed over the
forearm area of the left motor cortex and the cathode over
the vertex. In the two subjects who underwent electrical
stimulation, to minimize the production of indirect waves
(Rothwell et al., 1991; Edgley et al., 1997) and to reduce
discomfort for the subjects the stimulus strength was kept
just above the threshold intensity for obtaining a stable motor
evoked potential (MEP) in the target muscle. During electrical
and magnetic transcranial stimulation, the subjects were asked
to contract the target muscle voluntarily (30% maximum
voluntary contraction).
Signal recording and processing
EMG signals were captured by Ag/AgCl (9-mm diameter)
surface electrodes placed over the muscle belly of the forearm
extensor muscles (extensor digitorum communis) and the
flexor carpi radialis muscle. Signals were pre-amplified,
amplified (Digitimer D160 high gain, AC-coupled amplifiers;
noise level 4.5 µV r.m.s. at full bandwidth), filtered (time
constant 3–10 ms, high frequency cut at 3 kHz), digitized
with an A-to-D converter (Cambridge 1401 plus, Cambridge
Electronic Design, Cambridge, UK) and sampled (sampling
rate 2500 Hz), analysed and stored on a PC with a dedicated
software package (SIGAVG 6.20, Cambridge Electronic
Design). The software and the A-to-D converter were also
used to trigger the stimulators and to perform on-line
conditional averaging. For the recording of EMG suppression,
40–60 sweeps (depending upon the experiment) were
averaged. In the experiments with brain stimulation 6–10
sweeps per condition were averaged, and for the H-reflex
experiments 10 sweeps were averaged. For the experiments
with ischaemic block, we also derived the nerve action
potential at the Erb point in one subject and the H reflex in
the flexor carpi radialis muscle in another. Except for the
experiments during ischaemia, in which the nerve action
potential and the H reflex were recorded at rest, subjects
were asked to exert a tonic contraction ~30% of the maximum.
The onset latency of the EMG suppression was measured
from the point when EMG activity fell below the average
pre-stimulus level and the end as the point when the average
EMG activity reached this level again; the duration of the
EMG suppression was the time difference between these two
points. The amount of EMG activity during the period of
suppression was expressed as a percentage of the pre-stimulus
average level of the EMG during an epoch having the same
duration as the suppression evoked by tendon stimulation.

Fig. 1 The EMG suppression evoked by electrical stimulation
over the tendon of the extensor digitorum communis muscle in a
representative subject. Note that the period of EMG suppression
was followed by a short increase in the rectified EMG signal. The
stimulus strength was 98 mA. The trace is the average of 50
sweeps. Horizontal calibration 5 50 ms, vertical calibration 5
500 µV.
The size of the MEPs elicited by magnetic brain stimulation
and of the H reflex was measured peak-to-peak and was
expressed as a percentage of the unconditioned value.
Ischaemia was produced by inflating (up to 200 mmHg) a
sphygmomanometer cuff around the arm.
Data are presented either as single values or as means 6
SDs in the text.
Results
General characteristics of the EMG suppression
after tendon stimulation
In all subjects tested, electrical stimuli delivered to the
respective tendons elicited a transient suppression of the
EMG activity in the forearm extensor muscles (Fig. 1).
Stimuli at 70.8 6 21.6 mA (n 5 8 subjects) resulted in
consistent suppression of forearm extensor EMG activity.
Stimuli delivered at the intensity for cutaneous perception
did not produce EMG suppression. In forearm extensors,
moving the cathode a few centimetres away from the tendon
significantly reduced or abolished the EMG suppression if
the stimulus was kept at the original threshold intensity. The
lowest stimulus intensity that evoked EMG suppression was
just below the pain threshold. In most experiments, the
subjects defined the sensation evoked by tendon stimulation
as a mild discomfort but not pain. In forearm extensors,
inhibition had an onset latency of 64.4 6 6.6 ms (n 5 10)
and a duration of 51.0 6 12.0 ms (n 5 10). During
suppression, the EMG activity recorded in the forearm
extensor muscles diminished to 54.1 6 11.7% of the pre-
stimulus level (n 5 10). This suppressive phase led
immediately to a phase of increased EMG activity peaking
at 128.3 6 20.3 ms (n 5 10).
In two subjects, stimulation of the radial superficial nerve
at the wrist at an intensity similar to that used for effective
tendon stimulation evoked no inhibition, even though subjects
reported that stimuli delivered to the two sites provoked a
comparable sensation.
Tendon stimulation 375
Fig. 2 The effect of cutaneous input on the EMG suppression
after electrical stimulation over the muscle tendon (extensor
digitorum communis) in a representative subject. (A)
Unconditioned response. (B) Response conditioned by a stimulus
over the radial superficial nerve at three times the perception
threshold given at the same time as the stimulus over the tendon.
A conditioning cutaneous stimulus left the EMG suppression after
tendon stimulation unchanged. Each trace is the average of 40
sweeps. Horizontal calibration 5 50 ms, vertical calibration 5
250 µV.
Effects of cutaneous input on the EMG
suppression after tendon stimulation
Because low threshold skin afferents consistently facilitate
the homonymous Ib pathway, we tested whether tendon and
cutaneous inputs converged. In three experiments, tendon
stimulation, delivered at intensities above the threshold for
EMG suppression, and conditioned by radial stimulation at
intensities able to induce well perceived paresthesiae in the
skin innervated by the radial nerve (about three times the
perception threshold), revealed similar EMG suppression in
unconditioned and conditioned trials (65% versus 73%; 45%
versus 48%; 53% versus 49%) (Fig. 2). Cutaneous input
failed to produce changes even when fingers 2 and 3 (two
experiments) and the radial superficial nerve at the wrist
(three experiments) were stimulated with trains of 10 stimuli
at 250 Hz given at the same time, 10 ms, 20 ms, and 50 ms
after tendon stimulation.
Recovery of the EMG suppression after tendon
stimulation
To find out whether the long latency of the EMG suppression
might depend upon a polysynaptic inhibitory pathway, we
studied the recovery function, which is known to correlate
with the number of synapses involved in a given reflex. For
this purpose, in four subjects, we stimulated the extensor
digitorum communis tendon with paired stimuli at intervals
ranging from 10 to 120 ms. In all subjects, already at the 50
ms interval the EMG suppression had almost fully recovered
(unconditioned versus conditioned: 42% versus 47%; 58.3%
376 A. Priori et al.
Fig. 3 The recovery of the EMG suppression evoked by tendon
stimulation after paired stimuli in a representative subject. (A)
Single stimulus at 83 V; (B) paired stimuli, 10 ms apart; (C)
paired stimuli, 50 ms apart; and (D) paired stimuli, 100 ms apart.
The EMG suppression after tendon stimulation has fully
recovered with the interstimulus interval of 50 ms. Each trace is
the average of 30 sweeps. Horizontal calibration 5 50 ms,
vertical calibration 5 250 µV.
versus 42.5%; 38% versus 43% and 53% versus 35%; 47.8
6 9% and 4% versus 41.8 6 5%) (Fig. 3).
Afferents responsible for the EMG suppression
after tendon stimulation
To see whether the long latency of the EMG suppression
arose from afferents other than fast-conducting fibres, we
tested the effect of tendon stimulation before and after
applying ischaemia to block the conduction along low-
threshold fast-conducting nerve-fibre afferents in the forearm.
In one experiment, we maintained the ischaemic block for
15 min until the nerve action potential recorded at the
Erb point (after median nerve stimulation at the wrist)
disappeared. In the other, we maintained ischaemia for 13
min until the H reflex, recorded in the flexor carpi radialis
(after median nerve stimulation at the elbow) disappeared
(Fig. 4). Under both experimental conditions, tendon
stimulation still evoked almost unchanged EMG suppression,
even when the nerve action potential and H reflex were absent.
The excitability of α-motor neurons during the
EMG suppression after tendon stimulation,
tested with MEPs
To determine motor neuron excitability during EMG
suppression, we studied MEPs evoked by magnetic brain
stimulation in three subjects. MEPs evoked during the silent
period after tendon stimulation were not suppressed. In two
of the three subjects they were even slightly facilitated
(136.2%, 122.8% and 104.6%). In two other experiments,
designed for an even more appropriate comparison with the
H-reflex experiments (see below), magnetic MEPs evoked in
the contracting flexor carpi radialis muscle after stimulation
of the tendon of the extensor digitorum communis remained
substantially unchanged (93.4% and 94.7%). To confirm
further the results of magnetic stimulation, we did two
additional experiments using electrical transcranial
stimulation. In these subjects, the MEPs evoked in the forearm
extensor muscles by electrical transcranial stimulation, and
conditioned by tendon stimulation, remained almost equal to
the unconditioned control responses (93.0% and 94.0%).
These experiments failed to show a consistent inhibition of
the α-motor neurons during the EMG silence (Fig. 5).
Ia afferent input during the EMG suppression
after tendon stimulation, tested with the H
reflex
To test the possibility that EMG suppression after tendon
stimulation could have been due to a gating of Ia inflow to
spinal cord, we studied the H reflex during the suppression
evoked by tendon stimulation in the forearm flexor muscles.
It was not studied in forearm extensors, because the H reflex
can rarely be evoked in these muscles. Stimulation of the
tendon of the extensor digitorum communis muscle produces
a relatively silent period in the flexor carpi radialis muscle,
analogous to that in the extensor digitorum communis muscle.
In five experiments with three subjects, stimulation of the
median nerve at the elbow 60 ms after tendon stimulation,
to evoke an H reflex in the middle of the silent period,
elicited a conditioned H reflex that was far smaller than the
unconditioned control H reflex (42.5%, 19.0%, 26.3%, 58.8%
and 34.4%) (Fig. 6). The last two values were obtained
during the supplementary experiments showing no substantial
change in the MEPs recorded in the flexor carpi radialis.
Coupled with the MEP results, the H-reflex experiment
provides evidence that the EMG suppression after stimulation
over muscle tendons arises from presynaptic inhibition of Ia
afferents.
Discussion
Our experiments confirm previous findings and provide
further insight into the origin and mechanism of the EMG
suppression after stimulation over muscle tendons.
None of the general characteristics of EMG suppression
in the extensor digitorum communis muscles after electrical
stimulation over its tendon (the latency, duration and
percentage change) differed substantially from reported
values (Burne and Lippold, 1996a). Whether the threshold
intensity differed is unclear because we calculated it in terms
of current intensity whereas others have used voltage (Burne
and Lippold, 1996a). Our experiments also showed that
 Tendon stimulation 377

Fig. 4 The effect of ischaemic block in a representative subject. The upper traces (1) show H reflexes recorded from forearm flexor
muscles (flexor carpi radialis); the lower traces (2) show EMG suppression evoked by tendon stimulation in extensor digitorum
communis at 85-mA stimulation strength; traces on the left (A) and right (B) are before and after 13 min of ischaemic block,
respectively. Note that after the disappearance of the H reflex, tendon stimulation still produced an EMG suppression. The upper traces
(1) are each the average of 10 sweeps, and the lower traces (2) averages of 30 sweeps. Horizontal calibration 5 10 ms and 50 ms, and
vertical calibration 5 0.5 mV and 200 µV, in the upper and lower traces, respectively.

stimulation of cutaneous fibres fails to evoke EMG
suppression.
Our findings suggest that the physiological mechanisms
underlying the EMG suppression after tendon stimulation
have origins other than those proposed by Burne and Lippold
(1996a). Overall they imply that tendon stimulation activates
slow-conducting tendon afferents, possibly group III fibres,
connected not through a polysynaptic pathway originating
from Ib afferents but through an oligo- or disynaptic inhibitory
circuit. The EMG suppression after tendon stimulation might
originate from a dysfacilitation of the α-motor neurons due
to presynaptic inhibition of Ia afferents. This conclusion
derives from several points.
To evoke reflex inhibition we had to deliver tendon stimuli
at intensities close to the threshold for local pain (.50 mA).
High stimulation intensities argue against the involvement of
group I muscle afferents because these fibres already respond
to stimulus intensities well below the threshold for activating
motor axons (Pierrot-Deseilligny et al., 1981), as do Ia
afferents, to which Ib fibres are ‘first cousins’ (Burke, 1990).
Even though low-threshold cutaneous afferents facilitate
the Ib inhibitory pathways to the homonymous motor neurons
(Jami, 1992), our experiments combining tendon and pure
cutaneous stimulation showed that these inputs did not
converge. This finding makes the activation of Ib interneurons
unlikely. In humans, weak cutaneous stimulation, giving rise
to a ‘slight tactile sensation’ on the hand, facilitates the Ib
pathway in the upper limb (Cavallari et al., 1985).
The short recovery cycle of the EMG suppression after
tendon stimulation argues against a polysynaptic circuit.
The recovery function of an inhibitory reflex reflects the
complexity of the interneuronal network involved, i.e. more
interneurons and more synapses imply a longer recovery
cycle. This is true for a number of human reflexes whose
interneurons have been characterized. One example is the
recovery cycle of the two silent periods evoked in the
masticatory muscles by mental nerve stimulation. The first
silent period, which originates from the activation of a
disynaptic system, has a rapid recovery (usually recovering
fully in ,100 ms) whereas the second has a much longer
recovery cycle (~500–800 ms) and arises from a complex
polysynaptic system located in the brainstem (Cruccu et al.,
1991). By analogy with the first silent period, the short
recovery cycle of the EMG suppression after tendon
stimulation implies a disynaptic, rather than a polysynaptic
inhibitory circuit.
Because the long latency of the suppression seemed
incompatible with the complexity of the interneuronal system
involved, we tested the remaining possibility—a long afferent
time due to slow conduction fibres. Our experiments using
an ischaemic block practically exclude the involvement
of fast-conduction low threshold sensory fibres. Ischaemia
depresses impulse conduction along group A nerve fibres,
but leaves conduction along C fibres unchanged (for
discussion see Manfredi, 1970). By maintaining the ischaemic
block until the H reflex and the nerve action potential at the
Erb point disappeared, we blocked conduction along A-α
(group I afferents) and A-β (group II) fibres. Because a cuff
placed around the arm and inflated to a pressure of 200
mmHg exerts strong mechanical compression on the
underlying nerve, this kind of ischaemic block presumably
resembles the conduction block after a tight nerve ligature.
Thus it blocks nerve fibres within the A group according to
their size, i.e. α fibres before β and β fibres before δ. In
addition, the sensitivity of Ib and Ia afferents to ischaemia
almost certainly overlaps, because both kinds of afferents
belong to group A-α fibres, both have high conduction
velocities (in Ib afferents, 60–110 m/s) and their thresholds
378 A. Priori et al.
Fig. 5 Magnetically evoked MEPs during the EMG silence
following tendon stimulation in a representative subject. (A)
Superimposition of three traces following tendon stimulation; (B)
control unconditioned MEPs during voluntary contraction; (C)
MEPs during the EMG silence evoked by tendon stimulation.
MEPs were not inhibited during the EMG suppression after
tendon stimulation. Each trace is the average of 10 sweeps.
Horizontal calibration 5 50 ms, vertical calibration 5 500 µV.
to electrical stimulation differ only slightly (Jami, 1992). In
other words, if ischaemia abolishes the H reflex by depressing
the sensory conduction along group I muscle afferents, it
will also depress conduction along Ib afferents. The persisting
EMG suppression must therefore arise from the activation
of other afferents, smaller and slower than group I. Our
experiments using ischaemia and nerve action potential
recording showed that the afferents mediating this reflex are
not A-β fibres (group II) (Moruzzi, 1981). In addition, as far
as we know, group II afferents have never been described in
muscle tendons. Exactly which afferent fibres they might be
remains conjectural. Several types of slow-conducting group
III and IV afferents from muscle tendons have conduction
velocities of ,30 m/s (Mense and Meyer, 1985). Some of
these fibres are believed to signal the level of muscle
contraction, possibly in parallel with Golgi tendon organs,
organs their pattern of response resembles. Conduction
Fig. 6 The H reflex evoked by median nerve stimulation at the
elbow in the flexor carpi radialis muscle during the EMG
suppression evoked by stimulation over the tendon of the extensor
digitorum communis. (A) The EMG silence produced by tendon
stimulation; (B) the control unconditioned H reflex; and (C) the H
reflex conditioned by tendon stimulation. Note that the H reflex
was inhibited during the EMG suppression after tendon
stimulation (compare with Fig. 5). Each trace is the average of 10
sweeps. Horizontal calibration 5 50 ms, vertical calibration 5
100 µV in A, and 500 µV in B and C.
velocities of 20–30 m/s (i.e. in the range of group III
afferents) could well account for the long latency of EMG
suppression evoked by electrical stimulation over the tendon.
A further noteworthy point is that electric and magnetic
brain stimulation during the silent period after tendon
stimulation did not evoke substantially reduced amplitude
MEPs, a finding that implies the absence of an inhibitory
post-synaptic effect on the α-motor neurons. This raises two
important considerations. First, it shows that no active post-
synaptic inhibition impinges on motor neuron membranes
during EMG suppression. Hence, it also makes a direct action
of inhibitory interneurons on the motor neuron unlikely,
because the activation of Golgi tendon organ afferents
certainly evokes inhibitory post-synaptic potentials in
extensor motor neurons (Eccles et al., 1957). Secondly, it

strongly suggests that the EMG suppression after tendon
stimulation originates from a motor neuron dysfacilitation
and that inhibition does not take place at the motor neuron
level. Surprisingly, conditioned magnetic MEPs in these
experiments tended to be larger than their control values in
two subjects, in line with the facilitation of MEPs observed
during the silent period after mixed nerve stimulation (Young
et al., 1995). A final intriguing point, in discussing the results
obtained with brain stimulation, is the lack of substantial
changes in the size of the MEPs during the silent period
evoked by tendon stimulation. The EMG silence evoked by
tendon stimulation is not absolute and its reduction is ~50%.
Hence the background EMG during this relative silence is
probably sufficient to facilitate MEPs, and variation in this
range of background EMG may not influence the MEP size.
A final observation of note is that, during the EMG
suppression after stimulation over the muscle tendons, while
the MEPs remained unchanged the H reflex underwent strong
suppression, though corticospinal and group I afferent inputs
activate the same motor neurons (Priori et al., 1993) in the
same size order (Henneman et al., 1965). An immediate
explanation might be that background EMG activity differed
in the unconditioned and the conditioned conditions. But had
this been so, MEPs would have suffered inhibition as well;
yet they did not. Hence we surmise that the H-reflex
suppression arose from a gating of the Ia input to α-motor
neurons at pre-motor neuronal level, and conclude that the
EMG suppression is caused by presynaptic inhibition of Ia
afferents. The interruption of spindle afferent input to α-
motor neurons would fail to assist α-motor neuron activation
during a voluntary muscle contraction. Vallbo (1970) has
reported that voluntary contraction of a muscle leads to
increased firing in spindle afferents. Despite not being
responsible for muscle activation this event may nonetheless
facilitate it (Rothwell, 1994); available data indicate that,
during voluntary contraction, muscle afferents can contribute
up to 30% of the drive to motor neurons (Macefield et al.,
1993). The brisk interruption of this facilitation from muscle
spindles arising from presynaptic inhibition of Ia afferents
would finally result in an α-motor neuron disfacilitation,
thereby suppressing the ongoing EMG activity. Though A-δ
fibre activation elicits a dorsal root potential (Shimizu et al.,
1995), it is not known which interneurons mediate presynaptic
inhibition of group I afferents after activation of group III
and IV muscle afferents. Presumably they belong to a separate
interneuronal pool (Jankowska, 1992). Despite the current
lack of specific data on presynaptic inhibition arising from
group III afferents, this pathway involves a disynaptic system
(Jankowska, 1992), in keeping with the results of our recovery
cycle experiment.
The functional importance of the slow tendon afferents
activated by electrical stimulation is open to speculation.
They could signal the tension in the tendons and, via
presynaptic inhibition, they could damp the excitatory spindle
input on α-motor neurons. They would thereby smooth the
development of force, thus protecting the tendons themselves
Tendon stimulation 379
from excessive mechanical stress. Whatever the function, the
technique of tendon stimulation promises to be an innovative
method of studying presynaptic inhibition of group I afferents
from group III fibres.
These considerations underscore the need to re-evaluate
the meaning of the loss of inhibition after stimulation over
muscle tendons in Parkinson’s disease (Burne and Lippold,
1996b). One explanation might be a non-specific reduction
of presynaptic inhibition, possibly determined by an abnormal
descending basal-ganglia control over the whole spinal
interneuronal network in this disorder. Yet the interneurons
responsible for presynaptic inhibition in the upper limb have
reduced function in Parkinson’s disease (Lelli et al., 1990).
The abnormal inhibition after tendon stimulation in
Parkinson’s disease also raises the interesting possibility that
these patients’ motor control abnormalities could, at least in
part, depend on the abnormal central processing of slow
tendon afferent input. Abnormalities in the central integration
of slow afferent input to the spinal cord seem in keeping
with the known flexor reflex abnormalities in patients with
Parkinson’s disease (Rothwell, 1994).
Whatever the mechanism, the currently available data show
that stimulation over muscle tendons produces a powerful
suppression of voluntary ongoing EMG activity. This may
prompt a reappraisal of studies that attribute the silent period
after electrical finger stimulation to the effect of cutaneous
input (Leis et al., 1995; Inghilleri et al., 1997). Yet the
fingers contain a number of structures (joints, tendons)
densely innervated by group III afferents and very close to
the skin surface. Their activation by electrical stimulation
could be responsible, at least partly, for the silent period
evoked by electrical stimulation of the fingers.
Acknowledgements
A.P. was supported by a post-doctoral grant, and F.P. by a
doctoral grant, both from the University of Rome ‘La
Sapienza’.
References
Burke RE. Spinal cord: ventral horn. In: Shepherd GM editor. The
synaptic organization of the brain. 3rd ed. New York: Oxford
University Press; 1990. p. 88–131
Burne JA, Lippold OC. Reflex inhibition following electrical
stimulation over muscle tendons in man. Brain 1996a; 119: 1107–14.
Burne JA, Lippold OC. Loss of tendon organ inhibition in
Parkinson’s disease. Brain 1996b; 119: 1115–21.
Cavallari P, Fournier E, Katz R, Malmgren K, Pierrot-Deseilligny
E, Shindo M. Cutaneous facilitation of transmission in Ib reflex
pathways in the human upper limb. Exp Brain Res 1985; 60: 197–9.
Crone C, Hultborn H, Mazieres L, Morin C, Nielsen J, Pierrot-
Deseilligny E. Sensitivity of monosynaptic test reflexes to facilitation
and inhibition as a function of the test reflex size: a study in man
and the cat. Exp Brain Res 1990; 81: 435–45.
380 A. Priori et al.
Cruccu G, Pauletti G, Agostino R, Berardelli A, Manfredi M.
Masseter inhibitory reflex in movement disorders. Huntington’s
chorea, Parkinson’s disease, dystonia, and unilateral masticatory
spasm. Electroencephalogr Clin Neurophysiol 1991; 81: 24–30.
Eccles JC, Eccles RM, Lundberg A. Synaptic actions on
motoneurones caused by impulses in Golgi tendon organ afferents.
J Physiol (Lond) 1957; 138: 227–52.
Edgley SA, Eyre JA, Lemon RN, Miller S. Comparison of activation
of corticospinal neurons and spinal motor neurons by magnetic and
electrical transcranial stimulation in the lumbosacral cord of the
anaesthetized monkey. Brain 1997; 120: 839–53.
Henneman E, Somjen G, Carpenter DO. Functional significance of
cell size in spinal motoneurons. J Neurophysiol 1965; 28: 560–80.
Inghilleri M, Cruccu G, Argenta M, Polidori L, Manfredi M. Silent
period in upper limb muscles after noxious cutaneous stimulation
in man. Electroencephalogr Clin Neurophysiol 1997; 105: 109–15.
Jami L. Golgi tendon organs in mammalian skeletal muscle:
functional properties and central actions. [Review]. Physiol Rev
1992; 72: 623–66.
Jankowska E. Interneuronal relay in spinal pathways from
proprioceptors. [Review]. Progr Neurobiol 1992; 38: 335–78.
Leis AA, Stetkarova I, Beric A, Stokic DS. Spinal motor neuron
excitability during the cutaneous silent period [see comments].
Muscle Nerve 1995; 18: 1464–70. Comment in: Muscle Nerve
1995; 18: 1471–4.
Lelli S, Panizza M, Hallett M. Spinal cord inhibitory mechanisms
in Parkinson’s disease. Neurology 1991; 41: 553–6.
Macefield VG, Gandevia SC, Bigland-Ritchie B, Gorman RB, Burke
D. The firing rates of human motoneurones voluntarily activated in
the absence of muscle afferent feedback. J Physiol (Lond) 1993;
471: 429–43.
Manfredi M. Differential block of conduction of larger fibers in
peripheral nerve by direct current. Arch Ital Biol 1970; 108: 52–71.
Mense S, Meyer H. Different types of slowly conducting afferent
units in cat skeletal muscle and tendon. J Physiol (Lond) 1985;
363: 403–17.
Moruzzi G. Fisiologia della vita di relazione. Torino: UTET, 1981.
Pierrot-Deseilligny E, Morin C, Bergego C, Tankov N. Pattern of
group I fibre projections from ankle flexor and extensor muscles in
man. Exp Brain Res 1981; 42: 337–50.
Priori A, Bertolasi L, Dressler D, Rothwell JC, Day BL, Thompson
PD, et al. Transcranial electric and magnetic stimulation of the leg
area of the human motor cortex: single motor unit and surface EMG
responses in the tibialis anterior muscle. Electroencephalogr Clin
Neurophysiol 1993; 89: 131–7.
Rothwell JC. Control of human voluntary movement. 2nd ed.
London: Chapman and Hall, 1994.
Rothwell JC, Thompson PD, Day BL, Boyd S, Marsden CD.
Stimulation of the human motor cortex through the scalp [Review].
Exp Physiol 1991; 76: 159–200.
Shimizu T, Yoshimura M, Baba H, Shimoji K, Higashi H. Role of
A-delta afferent fibers in modulation of primary afferent input to
the adult rat spinal cord. Brain Res 1995; 691: 92–8.
Tobin CE, Jacobs JJ. Shearer’s manual of human dissection. 6th ed.
New York: McGraw-Hill Book Co., 1981.
Vallbo AB. Discharge patterns in human muscle spindle afferents
during isometric voluntary contractions. Acta Physiol Scand 1970;
80: 552–66.
Young MS, Triggs WJ, Gerstle G. Facilitation of magnetic motor
evoked potentials during the mixed nerve silent period. Muscle
Nerve 1995; 18: 1285–91.
Received September 2, 1997. Accepted September 17, 1997