Centre National de la Recherche Scientifique EP 1848, Université René Descartes, Unite de Formation et de Recherche Biomédicale, 75270 Paris 06, France
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ABSTRACT |
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Perrier, Jean-François, Boris Lamotte D'Incamps, Nezha Kouchtir-Devanne, Léna Jami, and Daniel Zytnicki. Effects on Peroneal Motoneurons of Cutaneous Afferents Activated by Mechanical or Electrical Stimulations. J. Neurophysiol. 83: 3209-3216, 2000. The postsynaptic potentials elicited in peroneal motoneurons by either mechanical stimulation of cutaneous areas innervated by the superficial peroneal nerve (SP) or repetitive electrical stimulation of SP were compared in anesthetized cats. After denervation of the foot sparing only the territory of SP terminal branches, reproducible mechanical stimulations were applied by pressure on the plantar surface of the toes via a plastic disk attached to a servo-length device, causing a mild compression of toes. This stimulus evoked small but consistent postsynaptic potentials in every peroneal motoneuron. Weak stimuli elicited only excitatory postsynaptic potentials (EPSPs), whereas increase in stimulation strength allowed distinction of three patterns of response. In about one half of the sample, mechanical stimulation or trains of 20/s electric pulses at strengths up to six times the threshold of the most excitable fibers in the nerve evoked only EPSPs. Responses to electrical stimulation appeared with 3-7 ms central latencies, suggesting oligosynaptic pathways. In another, smaller fraction of the sample, inhibitory postsynaptic potentials (IPSPs) appeared with an increase of stimulation strength, and the last fraction showed a mixed pattern of excitation and inhibition. In 24 of 32 motoneurons where electrical and mechanical effects could be compared, the responses were similar, and in 6 others, they changed from pure excitation on mechanical stimulation to mixed on electrical stimulation. With both kinds of stimulation, stronger stimulations were required to evoke inhibitory postsynaptic potentials (IPSPs), which appeared at longer central latencies than EPSPs, indicating longer interneuronal pathways. The similarity of responses to mechanical and electrical stimulation in a majority of peroneal motoneurons suggests that the effects of commonly used electrical stimulation are good predictors of the responses of peroneal motoneurons to natural skin stimulation. The different types of responses to cutaneous afferents from SP territory reflect a complex connectivity allowing modulations of cutaneous reflex responses in various postures and gaits.
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INTRODUCTION |
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In the peroneal group of cat leg muscles, peroneus
brevis (PB) and peroneus tertius (PT) receive a rich supply of
skeletofusimotor () axons: 30% of their motor units are
innervated (Emonet-Dénand et al. 1992
; Jami
et al. 1982
) [the incidence of
-innervation in peroneus
longus (PL), is not known]. Activation of
motor units elicits
simultaneous contraction and spindle discharges, i.e., group Ia (and
II) afferent inputs to the spinal cord, producing an excitatory
feedback in peroneal motoneurons (Kouchtir et al. 1995
).
Attempts to estimate the possible modulation of this feedback by other
sensory afferents led us to examine the synaptic connections of
peroneal motoneurons: in addition to their mutual links of monosynaptic
Ia excitation, the three populations of peroneal motoneurons share
excitatory influences from low-threshold cutaneous afferents in sural
or superficial peroneal (SP) nerves (Kouchtir et al.
1997
). However, mechanical stimulation of SP-innervated skin
areas did not uniformly evoke excitation of peroneal motoneurons and
has been observed to either enhance or reduce the positive feedback of
PB contraction through convergence at either motoneuronal or
interneuronal level. The various combinations of effects observed when
mechanical skin stimulation was superimposed on PB contraction suggest
that interaction of muscle and cutaneous inputs could occur via four
different pathways (see the companion paper, Perrier et al.
2000
). Many pathways are available for transmission of cutaneous inputs in the lumbosacral spinal cord, and variability of
motoneuron responses to electrical stimulation of cutaneous nerves is a
common observation (see the reviews, Jankowska 1992
; Schomburg 1990
). Furthermore, phasic modulations of
cutaneous effects occur in single motoneurons during fictive locomotion (see e.g., Degtyarenko et al. 1996
; Forssberg et
al. 1977
; Schmidt et al. 1988
).
Data from a few studies using "natural" activation of cutaneous
afferents again emphasized the variability of effects exerted on motor
units and motoneurons (Hongo et al. 1990; Kanda
et al. 1977
; Schomburg and Steffens 1986
).
However, it is not known whether natural activation of cutaneous
mechanoreceptors and electrical stimulation of the SP nerve with
strengths in the A
range elicit volleys in the same afferent
fibers, and the matter is not easy to investigate experimentally. What
could be investigated was whether both kinds of stimulation would
produce similar effects on peroneal motoneurons. This was one of the
questions addressed in the present analysis: the postsynaptic events
evoked in peroneal motoneurons by trains of electric pulses in SP nerve
were systematically compared with the events evoked by mild compression
of SP-innervated skin areas. A second question was whether graded
stimulation strengths would evoke similar evolutions of effects with
both kinds of stimulations. The cutaneous region innervated by the
terminal branches of SP, that is, the skin on lateral and medial
aspects of toes, was chosen for this study because effects of inputs
from these areas were examined in a previous study of a combination of
contraction- and compression-induced effects (see Perrier et al.
2000
). Repetitive electrical stimulation was applied in an
attempt to mimic the discharges of cutaneous receptors occurring on
mechanical stimulation (Burgess et al. 1968
; Hunt
and McIntyre 1960
; see also Edin 1992
for human
data). Electrical stimulation intensities were restricted to a one- to
six-times threshold range, mostly activating A
fibers (and very
few, if any, A
fibers) of SP nerve (see Leahy and Durkovic
1991
), and the strengths of toe compression remained in a range
that did not activate nociceptive receptors.
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METHODS |
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Experiments were carried out on 10 adult cats (2.8-3.5 kg)
anesthetized with pentobarbitone sodium (Sagatal, May and Baker, initial dose of 45 mg/kg ip, supplemented whenever necessary by additional intravenous doses of 4 mg/kg). All the procedures used in
the present study were similar to those described in the companion paper (Perrier et al. 2000), except for the peripheral
preparation, which was as follows. The right hindlimb was extensively
denervated, except for the SP terminal branch kept in continuity with
its innervated skin area and dissected over 2 cm to be mounted on stimulation electrodes in the distal portion of the leg, after the
trunk has given off the nerves to peroneus tertius (PT) and peroneus
brevis (PB) muscles. The nerve to peroneus longus (PL), and those to PB
and PT, were cut and dissected over 2 cm and mounted on stimulation
electrodes. As the nerve to PT is short and difficult to isolate over a
length sufficient to rule out spread of stimulation to PB nerve, it was
associated with the PB nerve in 9 of 10 experiments. Results obtained
from separately identified PB and PT motoneurons did not display
significant differences from those obtained from motoneurons identified
by stimulating both nerves together and were therefore pooled in a
single sample. When present, the PB nerve branch containing afferents
from extensor digitorum brevis and extramuscular foot regions
(Lundberg et al. 1975
) was cut.
Devices for leg fixation and stimulation of SP-innervated cutaneous
areas were as described in Perrier et al. (2000).
Ramp-and-hold movements of a disk attached to a servo-length actuator
(at 50 mm/s, with 2-5 mm amplitudes and 20-120 ms plateau durations), producing a mild compression of the toes between the disk and a
vertical post, were used as mechanical stimulus for receptors in SP
territory. In each sequence, this stimulation was repeated twice at
250-ms intervals (see e.g., Fig. 1), and five successive sequences at
1-s intervals were averaged on-line and recorded as explained in
Perrier et al. (2000)
.
Trains of electric pulses (50 µs width, 20 Hz) were applied to the SP
nerve. The 20-Hz frequency was within the range of the discharge rates
of slow adapting cutaneous receptors (Burgess et al.
1968; Jänig et al. 1968
) (see also
DISCUSSION). Duration of trains was in the 500- to 800-ms
range to match the duration of mechanical stimulation sequences.
Systematical use of trains rather than single pulses allowed display of
the quick decrease in amplitude of potentials in responses to
repetitive stimulation (see Figs. 1B, 3C, and
5B) and of response components that were not readily visible
in the response to the first pulse (see Fig. 6A).
Stimulation strength was graded in multiples of a threshold (T) defined
as the strength eliciting a just detectable afferent volley. The
maximal stimulation strength used in the present experiments was about
6 T.
The responses of peroneal motoneurons were recorded intracellularly
first, and the microelectrode was then withdrawn from the neuron by a
few micrometers allowing extracellular recording of responses to the
same stimulation. Subtractions of extracellular from intracellular
averaged records were performed systematically (see Perrier et
al. 2000). All the records in Figs. 1-3 and 5-6 show the
results of these subtractions.
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RESULTS |
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This report is based on data from 63 peroneal motoneurons of which
32 (26 PB-PT, 4 PL, and 2 motoneurons that could not be ascribed to a
specific pool) were tested for effects of both mechanical and
electrical stimulations, 11 others (7 PB-PT, 3 PL, and 1 unspecified) for effects of the former and 20 (14 PB-PT, 5 PL, and 1 unspecified) for effects of the latter. Total samples of 43 and 52 motoneurons were
thus tested for the effects of skin compression in SP-innervated areas
or electric pulses on SP nerve. Data were collected from motoneurons
with resting membrane potentials (rmp) between 50 and
85 mV (more
than half of this sample had rmp larger than
60 mV). In addition,
four motoneurons with rmp between
40 and
45 mV were included in the
sample because their rmp was stable and their responses showed
consistency. Each motoneuron received excitatory influences from
low-threshold SP afferents whether mechanically or electrically
activated. Stronger stimulations produced one of three patterns of
responses: pure excitation (Fig. 1),
predominant inhibition (Fig. 3), or mixed potentials (Fig. 5). A
majority (24 of 32) of the motoneurons in which the effects of
mechanical and electrical stimulations could be compared gave parallel
responses to both kinds of stimuli (see Table
1).
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Excitatory responses
An excitatory responses to both mechanical and electrical
stimulation is illustrated by Fig. 1. In this PB-PT motoneuron, a brief
toe compression produced by a 3-mm forward movement of the disk-bearing
actuator followed by a 20-ms hold phase, evoked polyphasic excitatory
postsynaptic potentials (EPSPs) of about 1.8 mV amplitude. Extension of
the disk course to 4 and then 5 mm (increasing not only the pressure,
that is, the strength of stimulation, but also the duration of
compression because motion velocity remained constant) elicited longer
lasting EPSPs and, occasionally, higher peak amplitudes. In the example
of Fig. 1A, lengthening of disk course clearly resulted in
extension of the area circumscribed by the EPSP. The polyphasic
appearance of the responses most probably reflected the temporal
dispersion of afferent discharges generated by asynchronously activated
cutaneous receptors in the compressed skin area. It is difficult,
however, to decide whether prolongation of disk course activated more
receptors or simply produced longer lasting discharges from the same
receptors. In the response to 5-mm disk course of Fig. 1A, a
late peak was apparent, whose timing suggested that it could have been
evoked by discharges from receptors activated (or re-activated) (see Hunt and McIntyre 1960) on release of toe compression.
This interpretation was supported by the results of the test
illustrated in Fig. 2 showing that, with
the same disk course and the same velocity, an increase from 20 to 120 ms in the duration of the hold phase of compression produced an
increase in the interval between early and late EPSPs so that the
distinction between the two components of the responses became evident
(Fig. 2, *).
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EPSP amplitudes, rarely exceeding 2.5 mV, were in the same range as
those of the EPSPs evoked by PB muscle contractions in peroneal
motoneurons (Kouchtir et al. 1995). Central latencies, as measured from the onset of the earliest components of afferent volleys to the onset of responses (after subtraction of extracellular from intracellular recordings) (see Pinter et al. 1982
),
were in a range of 7-19 ms (see Fig. 4) with a mean latency of
15.2 ± 3.5 (SD) ms. Excitation was the most frequently
observed effect of mechanical stimulation, in 22 of 43 (51%) peroneal
motoneurons (i.e., 17 of 33 in the PB-PT sample, 3 of 7 in the PL
sample, and 2 of 3 unspecified motoneurons).
Nearly all the motoneurons excited by toe compression were also excited
by trains of electric pulses applied on the SP nerve (Table 1). As
shown in Fig. 1B, trains of 1.4 T pulses elicited small,
quickly declining EPSPs, which disappeared before the end of the train.
Amplitudes equivalent to those of compression-induced EPSPs required
2-4 T pulses, and 4-6 T pulses evoked 4 to 5 mV polyphasic EPSPs with
a much briefer duration than in the responses to skin compression. In
each series of responses and whatever the stimulus strength, the
initial postsynaptic event was larger than the subsequent ones (Fig.
1B), and this was the case not only for excitatory but also
for inhibitory responses (see Fig. 3C). Comparison of EPSP
amplitudes elicited by mechanical and electrical stimulations (Fig. 1,
A and B) suggested that light toe compression
activated but a limited fraction of the cutaneous receptors innervated
by afferent fibers traveling in SP nerve (see also Fig. 1 in
Perrier et al. 2000). Central latencies of excitatory
responses to electrical stimulation of SP nerve, in a range of 3-7 ms
(mean 5.2 ± 1.2 ms) were shorter than the latencies of
compression-induced EPSPs (Fig. 4),
probably because the afferent discharges elicited by electric pulses
were more synchronous than those elicited by toe compression.
Altogether, electrical stimulation elicited excitatory responses in 20 of 52 (38.5%) peroneal motoneurons (i.e., 11 of 40 PB-PT, 7 of 9 PL,
and 2 of the 3 unspecified motoneurons).
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Inhibitory responses
Motoneurons in which toe compression evoked predominant inhibition were found in the same experiments as those showing purely excitatory responses. IPSPs very rarely appeared on weak stimulations. The skin compression produced by 3 mm disk displacements evoked small EPSPs (under 0.5 mV), while inhibitory potentials appeared for disk displacements of 4-5 mm. Hyperpolarizing current passed through the microelectrode was used to reverse compression-induced IPSPs (Fig. 3A), thereby verifying that they did represent inhibitory phenomena. On average, these IPSPs had smaller amplitudes (0.5-2 mV) than the EPSPs observed in excitatory patterns and very long central latencies, with widely dispersed values, mostly beyond 20 ms (mean latency 37.9 ± 18.4 ms, see Fig. 4). These long latencies could be due to long polysynaptic pathways (possibly involving supraspinal loops) or to asynchronous afferent discharges from mechanically activated sensors. Here again, the polyphasic aspect of IPSPs (Fig. 3, A and B1) reflected the temporal dispersion of afferent discharges from cutaneous receptors in the compressed skin area. However, prolongation of the hold phase of compression did not modify the timing of any component of inhibitory responses, and there was no suggestion of any off-effect. Inhibitory responses were observed in 8 of 43 (21%) motoneurons, all from PB-PT. All eight motoneurons belonged to the sample in which effects of mechanical and electrical stimulations could be compared, and, with a single exception (see Table 1), they also displayed inhibition on electrical stimulation of SP nerve (Fig. 3B2).
Of the 52 peroneal motoneurons that were tested for effects of electrical stimulation, 15 (28%) showed inhibitory responses, all from PB-PT. On graded electrical stimulations, weak pulse trains produced small EPSPs following a single IPSP (Fig. 3C1). Repetitive IPSPs appeared for pulses of at least 2 T strength (Fig. 3C, 2 and 3) with amplitudes in the same range as those of EPSPs. Their central latencies (Fig. 4) were consistently longer (range 5.5-8.5 ms, mean 6.8 ± 0.9 ms) than those of EPSPs. In contrast to the dispersed long latencies of compression-induced inhibitory responses, the distribution of the shorter latencies of IPSPs elicited by electric pulses was restricted within a relatively narrow range (Fig. 4) probably because the synchronous afferent volleys generated by electrical stimulation readily activated inhibitory interneurons. The earliest IPSPs had 1.5 ms longer latencies than the earliest EPSPs, indicating that the inhibitory pathway comprised more steps than the excitatory pathway with at least one supplementary interposed interneuron. On repetitive stimulation, the initial IPSP consistently had a larger amplitude than the subsequent ones (Fig. 3C), as already mentioned in the description of excitatory responses (Fig. 1B). For stimulation strengths above 3 T, inhibitory patterns often displayed two components: IPSPs with a fast time course appeared superimposed on a slow wave of hyperpolarization (Fig. 3, B2 and C3). Occasionally a slow component was also detectable in responses to mechanical stimulation (Fig. 3B1). While fast IPSPs could appear without any slow component, the reciprocal situation was never observed.
Mixed responses
Responses to skin compression showing mixed excitatory and inhibitory potentials occurred in 13 of 43 (28%) peroneal motoneurons (8 of 33 PB-PT, 4 of 7 PL, and 1 of 3 unspecified motoneurons). Mixed responses were met in the same experiments as purely excitatory or inhibitory responses. A characteristic feature of mixed patterns was the fact that EPSPs always appeared first, i.e., for weaker stimuli and with shorter latencies than IPSPs, as shown in Fig. 5A. In motoneurons displaying excitatory responses, increases in strength of mechanical stimulation (within the experimental range) failed to evoke inhibitory components of responses, whereas in motoneurons showing mixed responses, these components appeared on strong compression of toe skin, as could be obtained by changing the initial position of the disk (Fig. 5A). Both EPSP and IPSP components had similar amplitudes and the polyphasic appearance already observed in other patterns of responses.
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Mixed responses could appear on electrical stimulation of SP nerve (Fig. 5B) with EPSPs again displaying lower thresholds and shorter latencies than IPSPs. In all respects, the mixed responses showed the combined characteristics of purely excitatory or inhibitory responses. Altogether, this response pattern was evoked in 17 of 52 (32.5%) motoneurons, including 14 of 40 PB-PT, 2 of 9 PL, and 1 of 3 unspecified motoneurons.
Twelve of the 32 peroneal motoneurons that were tested for both modes
of stimulation displayed mixed responses to train stimuli on the SP
nerve. With toe compression, only half of these motoneurons showed a
similar mixed response (Table 1) while in the other half, purely
excitatory responses were observed (Fig.
6). This would be in agreement with the
assumptions that mechanical stimulation activates fewer receptors and
produces less afferent input than electrical stimulation (see Fig.
1B in Perrier et al. 2000) and that
activation of excitatory interneurons requires less input than
operation of inhibitory pathways. In other terms, the relatively weak
and dispersed volleys elicited by toe compression are sufficient to
fire excitatory interneurons but not to pass through the longer chain
of inhibitory interneurons.
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A comparison of the distribution of responses to both kinds of stimulation in the 32 motoneuron sample (Table 1) would further support these assumptions: on light toe compression, the total incidence of purely excitatory responses was higher (17 motoneurons) than the incidence of the two other types of response taken together (15 motoneurons).
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DISCUSSION |
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A striking observation made in the present study is the correspondence between peroneal motoneuron responses to electrical stimulation of SP nerve and mechanical compression of SP-innervated skin areas. As shown by Table 1, all but one of the motoneurons that were excited by electric pulses were also excited by toe compression, and all but one of the motoneurons that were inhibited by electric pulses were also inhibited during toe compression. Mixed responses were more readily elicited by electric pulses than by mechanical stimulation, but altogether, parallel responses to both modes of stimulation were observed in three quarters of the experimental sample. This result indicates that motoneuron responses to electrical stimulation, as used in most experimental studies, are fairly good predictors of their qualitative responses to more physiological stimuli.
To our knowledge, this is the first comparative study of the effects on
hindlimb motoneurons of cutaneous afferents activated by two different
modes of stimulation. In previous studies using mechanical
stimulation of cutaneous sensors, observations mostly concentrated on
mechanical or electromyographical effects (Engberg 1964;
Hongo et al. 1990
; Kanda et al. 1977
;
Loeb 1993
; Schieppatti and Crenna 1984
).
Schomburg and Steffens (1986)
examined, in decerebrate preparations, the responses of 35 triceps surae motoneurons, 37 posterior biceps-semitendinosus motoneurons, and 20 anterior
biceps-semimembranosus motoneurons to light manual strokes of the hairy
skin of the foot. In this large sample, a majority of motoneurons were
weakly excited by the stimulus and a small fraction displayed
inhibitory responses.
Quantitative comparison of electrically and mechanically induced
responses is difficult because, in the first place, it is not known
whether both modes of stimulation generate exactly the same afferent
input. Our assumption, however, is that at least some of the afferent
fibers present in the terminal portion of SP were activated by both
mechanical and electrical stimuli. Electric pulses of 1-6 T strength
will activate the fast-conducting afferent fibers in the SP nerve, and
it is known that these fibers supply hair, touch, and pressure sensors
in cutaneous areas of the cat foot (Hunt and McIntyre
1960). Whatever may be the case, the amplitudes and time
courses of both afferent volleys and postsynaptic potentials depend not
only on the number of afferent fibers recruited by each mode of
stimulation but also on the duration and synchrony of discharges, two
crucial factors for activation of interneurons. The relatively mild
mechanical stimuli used in the present experiments were most likely to
activate rapidly adapting receptors associated with hairs, known for
their low threshold and high dynamic sensitivity, and possibly also
some pacinian corpuscles responding to both on and off phases of toe
compression but not to the hold phase (Brown and Iggo
1967
; Hunt and McIntyre 1960
). Slow adapting
receptors with low thresholds respond to maintained skin displacements
by static discharges following an initial dynamic burst (Burgess et al. 1968
). Our mechanical stimuli possibly activated such
receptors, but their static discharges, even though they persisted
throughout the hold phase of toe compression, were not clearly
reflected in either afferent volleys or motoneuron responses. The major components of afferent inputs evoked by toe compression were thus generated during disk movements (mostly during forward movements, but
also on release of compression, see Fig. 2), that is, over 40- to
100-ms periods corresponding to 2- to 5-mm disk courses at 50 mm/s. A
further cause of dispersion of incoming impulses is the 35- to 85-m/s
range of conduction velocities of afferent fibers supplying
mechanoreceptors in hairy skin (see Birder and Perl
1994
). Given the distance between toes and spinal cord, this might result in a delay of 5 ms between the arrival at the spinal cord
of impulses carried by the fastest and slowest fibers. Investigations on discharges of single fibers in dorsal root filaments would be
necessary to obtain more data on the exact type of mechanoreceptors activated by both the mechanical and electrical stimuli used in the
present study.
Low-threshold effects were uniformly excitatory, whether exerted by
electrically or mechanically activated afferents, while inhibitory
effects required stronger stimulations. Longer chains of interneurons
are interposed in inhibitory than in excitatory pathways, as suggested
by longer latencies for IPSPs than for EPSPs (Fig. 4). At each step of
an interneuronal chain, a given stimulation is likely to elicit
discharges of some interneurons and only subliminal excitation in
others. The threshold difference between EPSPs and IPSPs raises
questions about qualitative differences between motoneurons displaying
different response patterns. It is not certain whether each response
pattern actually corresponds to a distinct pattern of connections with
SP cutaneous afferents. Possibly, the difference is only quantitative,
in the sense that every motoneuron has inhibitory as well as excitatory
connections but the range of stimulation strengths used in the present
experiments did not allow inhibitory potentials to appear in all the
tested motoneurons. This assumption would be in keeping with previous observations suggesting that apparently purely excitatory responses of
peroneal motoneurons to single SP pulses in fact masked inhibitory components that could be facilitated by convergence (see Fig. 5 in
Kouchtir et al. 1997). The distribution of both
excitatory and inhibitory influences from cutaneous afferents to every
motoneuron in the peroneal pool (rather than a selective distribution
of excitation or inhibition to functional subgroups of motoneurons) would allow modulations of cutaneous reflexes over wide ranges as
observed in normal and fictive cat locomotion (see e.g., Duysens and Loeb 1980
; Forssberg et al. 1977
) and in
humans (see e.g., Burke et al. 1991
; Tax et al.
1995
).
However, the existence of at least two different pathways for
motoneuron inhibition by cutaneous inputs is suggested by the observation of two components, fast and slow, in inhibitory potentials. The existence of at least two different pathways for excitation, respectively processing the early and late components of the response (as illustrated in Fig. 2), is suggested by the differences observed in
interaction of each component with contraction-induced inputs (see Fig.
4 in Perrier et al. 2000). Further studies of the four pathways would require observations of motoneuronal responses after
systematical hyper- or depolarizations of the membrane. This was
attempted in the present study, but it has been our experience that
maintaining a stable depolarization of peroneal motoneuron membrane
throughout the kind of mechanical and electrical stimulation we used is
quite difficult because it causes discharges and often leads to the
loss of the neuron. Hyperpolarization, on the other hand, readily
reversed the fast component of IPSPs (Fig. 3A) but not the
slow component. Anatomical evidence for the multiplicity of spinal
pathways mediating the transmission of cutaneous inputs has been
provided by demonstrations that afferent fibers supplying different
types of receptors distribute axon collaterals in different zones of
laminae III and IV in the dorsal horn of lumbosacral cord (Brown
1981
). A recent example where actions from several excitatory
and inhibitory pathways could be traced is the complex organization of
premotoneuronal circuitry delivering cutaneous influences to ankle
flexor motoneurons during fictive locomotion (Degtyarenko et al.
1996
).
A consistent feature of both EPSPs (Figs. 1B and
5B) and IPSPs (Fig. 3C) evoked in peroneal
motoneurons by electrical stimulation of SP nerve was the rapid
decrease in amplitude between the first and second potential in
response to a train of repetitive pulses. Similar decline in amplitude
of EPSPs evoked by 10/s stimulation of saphenous nerve in tibialis
anterior and semi-tendinosus motoneurons was reported by Leahy
and Durkovic (1991; see also Heckman et al.
1992
). The reasons for this decline are not obvious; causes such as synaptic depletion, desensitization of membrane receptors or
changes in membrane conductance or even inhibition of excitatory interneurons, would be difficult to test under the present experimental conditions. Presynaptic inhibition of cutaneous afferent fibers is
known to result from the action of these afferents themselves (Eccles et al. 1963
; Schmidt et al. 1967
;
see the review of Schmidt 1973
). A specific system of
presynaptic inhibition triggered by impulses in fibers innervating
rapidly adapting cutaneous receptors is thought to act precisely on
these afferents (Jänig et al. 1968
) in a phasic
manner that would be compatible with the very short delay of the
decline in postsynaptic events. If this was the case, the present
observations would suggest that the phasic system of presynaptic
inhibition of cutaneous afferents is very efficient because decline of
EPSPs occurred with the lowest intensities of stimulation supposed to
engage but a limited population of afferent fibers.
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ACKNOWLEDGMENTS |
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The authors are indebted to Dr. Lee Moore, who kindly revised the English. Our thanks to J.-J. Guilbard and G. Jandeau for outstanding technical help with development of a computer-based stimulator and electro-mechanical devices. The gift of Plasmagel by France Pharma is gratefully acknowledged.
This work was supported by grants from Delegation aux Recherches et Etudes Techniques-DGA (95 062), from CNES (920250), and from the European Commission (ERBCHRXCT 930190). J.-F. Perrier was a DRET-DGA research fellow.
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FOOTNOTES |
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Address for reprint requests: L. Jami, CNRS EP 1848, Université René Descartes, 45 rue des Saints-Pères, 75270 Paris Cedex 06, France.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 9 August 1999; accepted in final form 23 February 2000.
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REFERENCES |
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