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In human peripheral nerves, there are a number of
biophysical differences between cutaneous afferents and
a motor axons (Bostock et al. 1998). Cutaneous afferents
probably have greater expression of the hyperpolarization-
activated cation conductance (I
H
) than human motor
axons (Bostock et al. 1994; Lin et al. 2002). They also
undergo smaller threshold changes during the relatively
refractory, supernormal and late subnormal periods
following a conditioning discharge (Kiernan et al. 1996).
They have a longer strength–duration time constant
(Panizza et al. 1994; Mogyoros et al. 1996), a longer time
constant in experiments using ‘latent addition’ (Panizza et
al. 1994, 1998) and lower rheobase (Mogyoros et al. 1996),
all probably due to greater expression of a very slowly
inactivating (‘persistent’) Na
+
conductance (I
Na,P
) (Bostock
& Rothwell, 1997).
It is not known whether the properties of human group Ia
muscle afferents are similar to those of large cutaneous
afferents, though there are some data to suggest that time
constants estimated using latent addition are similar
(Panizza et al. 1994). On the other hand, Honmou et al.
(1994) presented evidence for a difference in a slow Na
+
conductance in the rat, there being greater expression on
cutaneous afferents (and their neurones in the dorsal root
ganglion; DRG) than on either a motor axons or muscle
afferents (and their DRG neurones). This raises the
possibility of differences in the expression of Na
+
channels
on human group I and cutaneous afferents. If any such
difference involved I
Na,P
, there might be differences in
strength–duration properties, with a lower threshold for
group I afferents. In this respect, muscle afferent effects
following stimulation of a mixed nerve can often be
recorded with very weak stimuli, 0.6 times the threshold
for the most excitable motor axons, without the radiating
paraesthesiae that would be expected if the stimulus also
activated cutaneous afferents (see e.g. Pierrot-Deseilligny,
1996). This supports the view that group I afferents are
more excitable than large-diameter cutaneous afferents.
Most human nerves innervating muscle are mixed nerves
that also innervate skin, and it is difficult to study the
Excitability of human muscle afferents studied using
threshold tracking of the H reflex
Cindy S.-Y. Lin, Jane H. L. Chan, Emmanuel Pierrot-Deseilligny * and David Burke
Prince of Wales Medical Research Institute, University of New South Wales, and College of Health Sciences, University of Sydney, Sydney, Australia
and *Neurophysiologie Clinique, Rééducation, Hôpital de la Salpêtrière, 75651 Paris Cedex 13, France
In human peripheral nerves, physiological evidence has been presented for a number of biophysical
differences between cutaneous afferents and amotor axons. The differences in strength–duration
properties for cutaneous afferents and motor axons in the median nerve have been attributed to
greater expression of a persistent Na
+
conductance (I
Na,P
) on cutaneous afferents. However, it is
unclear whether the biophysical properties of human group Ia afferents differ from those of
cutaneous afferents. The present studies were undertaken to determine whether the properties of
human group Ia afferents can be studied indirectly using ‘threshold tracking’ to measure the
excitability changes in the H reflex, and to determine whether the excitability of group Ia afferents
differs from that of cutaneous afferents. The strength–duration properties of the soleus H reflex and
soleus motor axons were measured at rest and during sustained voluntary contractions. Similar
experiments were performed on the median nerve at the wrist to study the strength–duration
properties of cutaneous afferents, amotor axons and H reflex of the thenar muscles. In addition, the
technique of ‘latent addition’ was used to determine whether there was a difference in a low-
threshold conductance on soleus Ia afferent and motor axons. The present findings indicate that the
strength–duration time constant (t
SD
) for the H reflex is longer than that for a motor axons, but
similar to that for cutaneous afferents. There were no differences in t
SD
for the soleus H reflex at rest
and during contractions, suggesting that t
SD
for the H reflex is largely unaffected by changes in
synaptic or motoneurone properties. Finally, the difference in latent addition suggests that the
longer t
SD
of the soleus H reflex may indeed be due to greater activity of a persistent Na
+
conductance on Ia afferents than on soleus amotor axons.
(Received 11 June 2002; accepted after revision 24 September 2002; first published online 25 October 2002)
Corresponding author D. Burke: Prince of Wales Medical Research Institute, Barker Street, Randwick, Sydney 2031, Australia.
Email: d.burke@unsw.edu.au
Journal of Physiology (2002), 545.2, pp. 661–669 DOI: 10.1113/jphysiol.2002.026526
© The Physiological Society 2002 www.jphysiol.org

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properties of a group Ia afferent population in isolation.
However, the excitatory input responsible for the H reflex
is largely, if not exclusively, due to the synaptic effects of
group Ia afferents on the motoneurone pool, and this raises
the possibility of using the motoneurone as a ‘filter’ to allow
the properties of muscle afferents to be studied. Of course,
motoneurone discharge depends on more than just the
properties of the excitatory input, and it would be necessary
to consider whether synaptic processes (particularly those
capable of altering the Ia input, such as homosynaptic
depression and presynaptic inhibition) or changes in
motoneurone properties contributed to the findings.
The latter can be minimized by using the technique of
‘threshold tracking’ (see Bostock et al. 1998) to clamp the
size of the reflex discharge so that it remains the same
percentage of maximum under all experimental conditions.
With threshold tracking the stimulus is adjusted by
computer to keep the response constant and, in studies
on peripheral nerve axons, the findings reflect axonal
excitability at the site of stimulation. As noted above, the
properties of the Ia–motoneurone synapse and of the
motoneurone pool could represent confounding factors
when the measured response is a reflex discharge. Never-
theless, it has recently been demonstrated that the recovery
cycle of the H reflex after a single conditioning volley
subliminal for the H reflex can be explained by the changes
in excitability of the afferent input for the reflex (Chan et
al. 2002). The present studies were undertaken to determine
whether the properties of human group Ia afferents can be
studied indirectly using threshold tracking to measure the
changes in stimulus current necessary to negate changes in
the H reflex. Given this, the studies then addressed whether
the strength–duration properties were different to those of
cutaneous afferents at the same site in the mixed nerve.
METHODS
Subjects
Thirty-four experiments were performed on 11 normal subjects
(aged 23–66 years, 7 male, 4 female), without clinical or
neurophysiological evidence of peripheral nerve disorders. All
subjects gave written informed consent to the experimental
procedures, which had been approved by the Committee on
Experimental Procedures Involving Human Subjects of the
University of New South Wales, in accordance with the Declaration
of Helsinki.
Stimulation and recordings
All experiments were performed using a computerized threshold-
tracking program (QTRAC; Professor Hugh Bostock, Institute of
Neurology, Queen Square, London, UK; see Bostock & Baker,
1988; Bostock et al. 1998). With threshold tracking, the current
required to produce the target potential is referred to as the
threshold. ‘Proportional tracking’ was used, such that the extent
to which the stimulus current increased or decreased was
proportional to the difference between the target and the
measured response (Bostock et al. 1998).
Five sets of studies were performed as outlined below.
H reflex and M wave of soleus
To determine the strength–duration properties of the soleus
H reflex and of soleus motor axons, the thresholds required to
produce an H reflex and an M wave that were each 50 % of their
maxima (H
max
and M
max
, respectively) were measured. The soleus
H reflex was produced by stimulating the tibial nerve at the
popliteal fossa using bipolar electrodes, and the compound
muscle action potential (CMAP) of soleus was recorded using
surface electrodes 4 cm apart, in the midline over the lower third
of the soleus muscle (Hugon, 1973). Stimuli were delivered at 0.5
and 1 Hz for H reflex studies, cycling through a sequence of test
stimuli. The duration of the test stimuli was increased from 0.2 to
1 ms in steps of 0.1 ms. The strength–duration curves were
measured for the H reflex and M wave, as in the left panels of Fig. 1
(Weiss, 1901; Bostock, 1983; Mogyoros et al. 1996). The
strength–duration time constant (t
SD
) was calculated using Weiss’
formula (Weiss, 1901), according to which there is a linear
relationship between stimulus charge and stimulus duration
(illustrated in the right panels of Fig. 1). The t
SD
is given by the
negative intercept of the regression line on the duration axis, and
the rheobase by the slope of the regression line.
Effects of voluntary contraction
In six subjects, the effects of a sustained voluntary contraction on
the soleus H reflex were measured. The intensity of the
contraction was controlled by auditory and visual feedback of the
EMG of soleus, the latter heavily low-pass filtered and expressed as
a percentage of the contraction level produced by maximal tonic
plantar flexion for 10 s. The first set of measurements involved not
changing the size of the target H reflex. In this paradigm, the
stimulus necessary to evoke the target reflex response was reduced
(= ‘contraction, weaker stimulus’ in Fig. 2). The second set of
measurements involved determining the current required at rest
for the 1 ms stimulus, maintaining this current level for the 1 ms
stimulus during the contraction, re-setting the target window to
the larger H reflex, and then resuming tracking using this larger
window. In this paradigm, the reflex response was larger but the
afferent volleys were, presumably, comparable to those at rest
(= ‘contraction, comparable stimulus’ in Fig. 2). To determine the
strength–duration properties, the current required to produce an
H reflex of constant amplitude was measured with test stimuli
of five different durations: 0.2, 0.3, 0.5, 0.7 and 1 ms. For
comparison, the thresholds were normalized to the 1 ms data.
Using Weiss’ formula, the t
SD
for the soleus H reflex was then
calculated at rest and during contractions.
Cutaneous afferent, H reflex and motor axon excitability in
the median nerve
Experiments were performed on the median nerve at the wrist
in six subjects to study the strength–duration properties of
cutaneous afferents, a motor axons and H reflex of the thenar
muscles evoked from the same site in the same experiment.
Surface electrodes were used to stimulate the median nerve at
the wrist. The antidromic compound sensory action potential
(CSAP) was recorded from the index finger using ring electrodes
4 cm apart around the proximal phalanx and the CMAP was
recorded using surface electrodes over the abductor pollicis
brevis. The H reflex of the thenar muscle was measured during
weak voluntary contractions producing an EMG level of 10–30 %
of maximum. To determine the strength–duration properties of
cutaneous and motor axons of the median nerve, the threshold
currents required to produce a CSAP or CMAP of 50 % of
maximum were measured with test stimuli of five different
durations: 0.2, 0.3, 0.5, 0.7 and 1 ms. When studying the H reflex
C. S.-Y. Lin, J. H. L. Chan, E. Pierrot-Deseilligny and D. Burke662
J. Physiol. 545.2