Journal of Electromyography and Kinesiology 12 (2002) 167–176

www.elsevier.com/locate/jelekin

Spinal and supraspinal effects of activity in ligament afferents

Per Sjölander ab,∗, Håkan Johansson b, Mats Djupsjöbacka b
a
Southern Lapland Research Department, S-912 22 Vilhelmina, Sweden
b
Centre for Musculoskeletal Research, National Institute for Working Life, S-907 13 Umeå, Sweden

29 October 2001

Abstract

In this paper available knowledge on effects from joint and ligament afferents on spinal neurones and pathways are briefly
reviewed, and possible functional implications discussed. Ligament afferents may contribute to joint stability, muscle coordination
and proprioception through direct polysynaptic reflex effects onto ascending pathways and skeletomotoneurones, and/or indirectly
via reflex actions on the γ-muscle spindle system. Theoretical and experimental evidence indicate that ligament afferents, together
with afferents from other joint structures, muscles and the skin, provide the CNS with information on movements and posture
through ensemble coding mechanisms, rather than via modality specific private pathways. The existence and functional relevance
of ligamentomuscular protective reflexes, that are triggered when the ligament is threatened by potentially harmful loads, has been
seriously questioned. It seems more likely that peripheral sensory inputs from ligament afferents participate in a continuous control
of the muscle activity through feedforward, or preprogramming, mechanisms. In line with these ideas it has been suggested that
ligament mechanoreceptors have an important role in muscle coordination and in the reflex regulation of the functional joint stability,
by contributing to the preprogramming of the muscle stiffness through reflex modulation of the γ-muscle spindle system.  2002
Elsevier Science Ltd. All rights reserved.

Keywords: Ligament; Afferents; Proprioception; Motor control; Joint stability; Muscle spindle; Fusimotor neurone; Skeletomotor neurone

1. Introduction
Ideas of ligaments as sensory structures that, via affer-
ent input to the CNS, contribute to proprioception, motor
control and joint stability have been discussed for more
than a century. As a consequence of a growing number
of experimental and clinical evidence, both from studies
on animals and on human subjects and patients, such
sensory functions of ligaments have recently become
widely accepted.
Recordings from joint and ligament afferents in ani-
mals have shown that there is a wide variety of response
characteristics represented in the sensory output from
ligaments (for reviews, see [1–5]). There are receptors
within the ligaments that have low thresholds to mechan-
ical stimulation, and others that are activated only when
the tension of the ligament is very high. Among the low
∗
Corresponding author: Tel.: +46-940-144-94; fax: +46-940-153-
53.
E-mail address: persjola@vilhelmina.se (P. Sjölander).
threshold nerve endings there are both slowly and rap-
idly adapting ones, whereas the high threshold endings
appear to be mainly slowly adapting. Although there are
nerve endings in the joint that are active throughout the
normal range of joint rotation, it has been demonstrated
that the majority of the low threshold nerve endings of
the joints are most active when the joint approaches the
limits of its normal working range. Nevertheless, the fact
that the ligaments contain mechanosensitive nerve end-
ings with low thresholds and with static and dynamic
response qualities, clearly suggest that these nerve end-
ings are involved in providing the CNS with information
about joint positions and movement.
Afferents emanating from joint mechanoreceptors
have been shown to project to spinal motoneurones and
interneurones, as well as to a number of supraspinal
structures. Fig. 1 shows a schematic representation of the
principal pathways by which mechanosensitive ligament
receptors can contribute to joint stability, muscle co-
ordination and proprioception. The conscious ability to
recognise positions and movements of our extremities in
relation to each other and the body can be transmitted to

1050-6411/02/$ - see front matter  2002 Elsevier Science Ltd. All rights reserved.
PII: S 1 0 5 0 - 6 4 1 1 ( 0 2 ) 0 0 0 1 7 - 2
168 P. Sjölander et al. / Journal of Electromyography and Kinesiology 12 (2002) 167–176
Fig. 1. Schematic organisation plan of the mechanisms and pathways by which the mechanical and sensory properties of the ligaments may
contribute to joint stability, muscle coordination and proprioception.
cortical areas through direct spinal actions on ascending
pathways, or indirectly through reflex effects on the γ-
muscle spindle system. The latter implies that signals
from ligament afferents, via reflex actions onto γ-
motoneurones, are integrated in the proprioceptive input
provided by the primary and secondary muscle spindle
afferents. The ligament afferents can contribute to motor
control and co-ordination through polysynaptic interneu-
ronal pathways, and, again, via reflex actions on the γ-
muscle spindle system.
In addition to the sensory properties, the ligaments
have a mechanical role by causing restraints to hyper-
rotation of the joint (Fig. 1). However, the functional
stability of the joint (i.e. stability during active
movements) is not only a result of the mechanical
properties of the ligaments, but also of the restraint
caused by the joint capsule, the joint geometry, the fric-
tion between the cartilage surfaces, and the compression
force caused by the body weight and the muscle activity
around the joint. Among these factors, an appropriately
adjusted muscular activation pattern around the joint has
been convincingly demonstrated to be of crucial impor-
tance (for references, see [5–8]). Thus, since afferents
originating in ligaments are involved in the control of
muscle stiffness and co-ordination, it can be conclude
that the ligaments contribute to the functional joint stab-
ility by a combination of their mechanical and sensory
characteristics (Fig. 1).
The objective of the present review is to give a brief
overview of available knowledge on effects from joint
and ligament afferents on spinal and supraspinal struc-
tures, and to discuss some functional implications of
these observations. Special emphasis has been put on
interpreting known effects on supraspinal structures, ske-
letomotoneurones and the γ-muscle spindle system.
2. Ascending pathways, supraspinal projections and
proprioception
Most knowledge on supraspinal projections from joint
afferents originates from electrophysiological studies
made on cats and monkeys. The pioneering work was
made by Mountcaste and Gardner in the mid 20th cen-
tury (e.g. [9–14]). Based on their and others work it has
become evident that information from joint afferents
reaches supraspinal structures via several ascending
pathways. Thus, signals from joint afferents are trans-
mitted, through the dorsal column and the spinothalamic,
the spinoreticular, the spinocervical and the spinocereb-
ellar pathways, to different parts of the brain stem, the
cerebellum, the reticular formation, the thalamus and the
somatosensory cortex. Neurones in several of these sup-
raspinal structures are significantly influenced by activity
in low threshold joint afferents emanating both from
slowly and rapidly adapting receptors.
The ascending transmission of information from joint
afferents appears to be rather powerful. In early animal
studies it was shown that a high proportion of the thal-
amic neurones is extremely sensitive to joint movements
(some as sensitive to alterations in joint angle as the low
threshold joint receptors themselves [13,14]). By using
microstimulation technique, which permits selective
electrical stimulation of individual afferents in human
subjects, it was found that activation of single afferents
from finger and wrist joints can induce distinct sen-
sations, i.e. a sensation of innocuous deep joint pressure
or joint rotation [15]. There is also evidence that sensory
nerve endings in ligaments in humans have ascending
projections that reach consciousness. Electrical stimu-
lation of afferents in the normal anterior cruciate liga-
ment (ACL) during arthroscopic surgery has been pro-
 P. Sjölander et al. / Journal of Electromyography and Kinesiology 12 (2002) 167–176
ven to elicit clear-cut somatosensory evoked potential,
indicating that ACL afferents indeed have cortical pro-
jections in man [16,17]. The finding that joint and liga-
ment afferents have potent supraspinal effects are per-
haps somewhat surprising in view of the relatively small
number of afferents emanating from joint mechano-
receptors, and of the fact that the information mediated
by these afferents are transmission in polysynaptic
ascending pathways with convergent input from a num-
ber of different types of muscle, skin and joint afferents
[e.g. 14, 18–21]. Nevertheless, these findings show that
joint afferents have strong supraspinal projections, and
that activation of just a few joint or ligament mechano-
receptors might be enough to induce conscious feeling
of joint rotation.
Over the last decades, a number of studies have
reported reduced proprioceptive ability following liga-
ment injuries, i.e. a reduced accuracy of the perceived
sensation of position and movement of body segments in
relation to each other (for references, see [4,22]). These
observations indirectly support the idea that ligament
afferents have supraspinal projections with access to
consciousness. However, it should be remembered that
the proprioceptive deficit caused by a ligament injury
rarely is due only to sensory and mechanical dysfunction
of the ligament. A ligament injury is often accompanied
by damages to other joint structures, e.g. the joint cap-
sule and the menisci, implying that the disturbed sensory
feedback from these structures are likely to contribute
to the reported proprioceptive deficits. Even in cases of
an isolated ligament injury, contributing effects from the
surrounding tissue cannot be excluded since the sprained
or ruptured ligament induces alterations of the normal
biomechanics of the joint. Thereby the loads imposed on
different joint structures and muscles will change, caus-
ing altered sensory feedback from mechanoreceptors
within and around the joint (cf. [23]). Thus, disturbances
found after a joint injury regarding e.g. proprioception,
muscle strength and motor co-ordination, are usually
caused by a combination of altered sensory input from
the injured tissue and surrounding structures, implying
that such disturbances rarely can be ascribed exclusively
to deafferentation of the injured joint or ligament.
3. Skeletomotoneurones and muscle responses
From early animals studies it is known that electrical
activation of high threshold joint afferents elicits clear-
cut reflex effects on skeletomotoneurones (α-
motoneurones). The reflex actions induced from these
afferents, which largely emanate from nociceptors, are
characterised by excitatory effects on flexor motoneu-
rones and both excitatory and inhibitory effects on exten-
sor motoneurone [24,25]. Joint afferents originating from
low threshold mechanosensitive receptors, on the other
169
hand, are causing infrequent and week postsynaptic
reflex effects directly onto skeletomotoneurones [24–
27]. However, when effects from low threshold joint
afferents are facilitated by simultaneous activation of
descending or spinal reflex pathway, significant inhibi-
tory and excitatory postsynaptic potentials can be evoked
on extensor as well as flexor motoneurones [26,27].
The findings of week reflex effects on skeletomotone-
urones from low threshold joint afferents are supported
by studies indicating that knee joint ligaments have to
be heavily stretched before measurable EMG responses
are evoked in passive muscles [28–31]. Recently, how-
ever, it was demonstrated that low intensity electrical
stimulation of the intact ACL in humans could induce
clear-cut excitations or inhibitions of the isometrically
contracting quadriceps and semitendinosus muscles [32].
Similar findings were reported from prestretched, ton-
ically active quadriceps and hamstrings muscles during
application of small traction forces to the ACL of the
cat and dog [33]. The latter indicates that low threshold
mechanosensitive ligament receptors may evoke con-
siderable changes of the EMG signals, provided that the
activity level is high in the motoneuronal pool and/or in
the γ-muscle spindle system (i.e. a tonic stretch reflex or
a high gain in the γ-muscle spindle loop). Miyatsu and
collaborators suggested that the EMG-effects were likely
to be mediated via reflex effects on γ-motoneurones,
rather than directly onto the skeletomotoneurones [33].
Yet, to what extent these effects are mediated through
interneuronal pathways directly to the skeletomotoneu-
rones, or indirectly via reflex actions on the γ-muscle
spindle system, is not possible to elucidate using only
EMG-registration technique.
For quite some time it was generally believed that the
principal role of joint afferents was to prevent joint injur-
ies by activating protective muscle reflexes (for review,
see [4]). It was supposed that when the joint approaches
the limits of their normal working range, high threshold
mechanoreceptors in the capsule and ligaments would
prevent damaging hyperrotations by activating fast reflex
pathways to surrounding muscles. Although the exist-
ence of synaptic connections between joint/ligament
afferents and the muscles acting at the joint, is proven,
there is no evidence that these reflexes actually provide
joint protection through ordinary feedback mechanisms.
On the contrary, there are both experimental and theor-
etical arguments against the concept of joint protective
reflexes [3,4]. As described above, the experimental and
clinical results are ambiguous as to what extent joint
mechanoreceptors are able to induce reflex effects that
are powerful enough, and appropriately co-ordinated, in
order excite and inhibit a set of muscles that could pre-
vent the joint from damages. Even if such reflexes do
exist, the functional relevance must be regarded as mar-
ginal since they would be too slow to provide joint pro-
tection other than during very slow movements (cf.
170 P. Sjölander et al. / Journal of Electromyography and Kinesiology 12 (2002) 167–176
[32,34,35]). It should be pointed out, though, that this
does not rule out, of course, the possibility that sensory
endings in the joint may contribute to muscle co-ordi-
nation and joint stability through feedforward or prepro-
gramming mechanisms (see Section 6).
Based on the limited functional relevance of the
hypothesised joint protective reflexes, it seems some-
what surprising that these ideas have attracted a renewed
interest over the last decade. One concept that has been
rather intensely discussed is a potentially protective
ACL-hamstrings reflex loop [30,31,36–39]. The ration-
ale behind this idea is the synergistic action of the ham-
strings and the ACL in preventing posterior tibial trans-
lation. In an attempt to investigate the properties of this
putative neuromuscular linkage, it has been found that
the latency between the application of a posterioanterior
shear force at the knee joint and the appearance of an
EMG-response in the hamstrings muscles, was signifi-
cantly longer in ACL deficient knees as compared to in
uninjured knee joints [38]. It was suggested that the lat-
ency differences observed could provide an indirect
measure of the proprioceptive ability of the joint, as well
as an objective measure of the protective ability of the
hamstrings muscles. In addition to the fact that it is
impossible to selectively stimulate sensory receptors in
a ligament by application of an external shear force at
the intact, or nearly intact, joint (cf. [31,32]), it should
be emphasised that these suggestions lack experimental
support and are based on the misconception that the pro-
prioceptive ability can be measured by analysing simple
motor responses that are evoked by spinal reflexes. Later
studies have unsuccessfully tried to repeat the obser-
vations of Beard and coworkers [38], and it has been
proposed that the prolongation of the EMG response
could have been due to an absence of a normal short-
latency autogenic stretch reflex in the hamstrings muscle
[39,40]. This seems conceivable since the experiments
were carried out only a few weeks after surgery,
implying that nociceptive afferents activity could have
suppressed the excitability of the α- and/or γ-motoneu-
rone pools.
Lately it has been claimed that investigations of motor
effects elicited by activity, or lack of activity, in joint
afferents provide an indirect measure of the propricep-
tive ability of the joint. This is questionable, however,
since it is unlikely that the perception of positions and
movements, on the one hand, and the unconscious motor
responses, on the other hand, are similarly influenced by
activity in given sets of joint mechanoreceptors. Infor-
mation transmitted to the CNS from joint afferents is
spread to a number of ascending and reflex pathways
within the spinal cord. These pathways do not only
mediate joint afferent information, but also afferent
information emanating from sensory endings in the skin
and various muscles. Since there are large differences
between various central pathways with regard to the
qualitative and quantitative properties of the convergent
input influencing the individual pathways (e.g. [20,21]),
a given input from a set of joint afferents will be differ-
ently mixed with input from skin and muscle afferents
in various pathways. In addition, the muscle activity, in
contrast to the conscious impressions of movement, is
also the result of inherent motor control properties. Thus,
spinal motoneurone pools and supraspinal areas are dif-
ferently influenced from a given population of afferents
in various postures and movements. This implies that,
based on motor responses induced from an injured joint,
it is impossible to draw safe conclusions on the ability
of that joint to provide sensory information of relevance
for proprioception.
4. The g-muscle spindle system
It has been firmly established that the muscle spindle
afferents have a crucial role in position and movement
sensations (for reviews, see [4,41,42]). This has become
evident from a number of observations, of which the
most important are that:
1. muscle spindle afferents have strong projections to
several supraspinal structures, including cortical
areas;
2. activation of muscles spindle afferents, by muscle
vibration in a stationary limb, induce illusions of
joint movements;
3. removal of input from the joint and the skin around
the joint, leaving muscle afferents unaffected, reduces
the proprioceptive acuity only marginally; and
4. microstimulation of single muscle spindle afferents
may evoke distinct sensations of movements.
Based on these findings it has become widely accepted
that the muscle spindle afferents are the prime contribu-
tor to proprioceptive sensations, although maximal accu-
racy requires information also from joint and cutaneous
receptor afferents.
With different methods, on animals as well as on
humans, it has been shown that the normal co-ordination
of the muscle activity and muscle stiffness to a large
extent rely on input from muscle spindle afferents (for
reviews, see [4,5]). The importance of input from spindle
afferents is evident, for instance, from the fact that about
50% of the muscle stiffness (i.e. change in force/change
in length), during activity levels comparable to those
occurring during standing and walking, is explained by
effects of the stretch reflex [43]. It is also known that the
muscle stiffness vary during co-contractions, voluntary
dynamic muscle activities and rhythmic movements, and
that input from autogenic and heterogenic muscle
spindle afferents can increase the muscle stiffness by up
to 100% [43–46]. Since the sensitivity of the muscle
 P. Sjölander et al. / Journal of Electromyography and Kinesiology 12 (2002) 167–176
spindle afferents is controlled by γ-motoneurones
(fusimotoneurones), it would be expected that peripheral
afferents which induce reflex effects on the γ-motoneu-
rones should participate in shaping the information
mediated by the muscle spindle afferents. Accordingly,
if ligament afferents have strong reflex projections to the
γ-motoneurones, then they could have a significant
impact on proprioception and motor control through the
γ-muscle spindle system.
In the 1980s and 1990s it was shown that electrical,
as well as physiological, activation of afferents from low
threshold joint mechanoreceptors in the cat could evoke
potent excitatory and inhibitory reflex spinal effects on
static and dynamic γ-motoneurones of muscles around
the joint (for review, see [47]). The static and dynamic
γ-motoneurones are controlling the static and dynamic
sensitivity of the muscle spindles to various muscle
lengths and length changes, and are thereby essential in
generating optimal muscle spindle output in different
postures and movements (cf. [69]). Recordings from
muscle spindle afferents have revealed that the reflex
effects on the γ-motoneurones, evoked from low thres-
hold joint receptors, are powerful enough to significantly
modulate the activity of the spindle afferents. Clear-cut
effects on the γ-muscle spindle system have been found
to mechanical stimulation of ankle and knee joint cap-
sules and of knee joint ligaments [48–51], and to chemi-
cal stimulation (e.g. bradykinin, seratonin and lactic acid
and ions) of the capsules of the knee and cervical facet
joints [52–54]. A remarkably high responsiveness was
demonstrated for the muscle spindle afferents to low lev-
els of knee ligament loading (i.e. loads compatible with
those generated during normal activities like walking
and running). Another major observation was a high
degree of heterogeneity in the response patterns found
on individual spindle afferents to stimulation of different
ligaments. Yet, behind this complexity there was a trend
towards dynamic fusimotor effects to loading of the
ACL, dynamic, static or mixed dynamic and static
effects to loading of the posterior cruciate ligament, and
dynamic or mixed effects to loading of the collateral
ligaments. These findings suggest not only that the syn-
aptic coupling between mechanosensitive ligament affer-
ents and the γ-muscle spindle system is strong, but also
that ligament afferents are significantly involved in the
complex reflex control of the static and the dynamic out-
put from the muscle spindles [49–51].
A comparison of the reflex control of γ- and α-
motoneurones shows that the γ-motoneurones are more
easily influenced from low threshold joint afferents (for
reviews, see [4,55–57]). Another difference is that the
reflex control of the γ-muscle spindle system is consider-
ably more complex than that of the α-motoneurones
[4,56–61]. This is mainly a result of larger and more
individualised receptive fields of the γ-motoneurones,
but also of the network properties of the γ-muscle
171
spindle system. Since the γ-muscle spindle system is
influenced by descending information and reflex inputs
from joint, muscle and skin receptor afferents, it operates
as a premotoneuronal system that integrates descending
and reflex input [57]. The structural basis of the network
is the interconnections between secondary muscle
spindle afferents and γ-motoneurones [62–64]. In con-
trast to the primary muscle spindle afferents, the second-
ary spindle afferents project back to γ-motoneurones
innervating spindles both in the homonymous and other
ipsi- and contralateral muscles [57,65]. This implies that
each muscle spindle is influenced, via the secondary
spindle afferents and γ-motoneurones, by the activity in
other parts of the network [57,65]. Such a network would
be able to encode mechanical stimuli with a very high
fidelity, and it has been suggested that, due to its intrinsic
reflex regulation, the γ-spindle network would be highly
suited to integrate and mediate sensory feedback of parti-
cular importance for muscle coordination and execution
of finely tuned movements [57,65,66]. In contrast, the
rather stereotypic reflex pattern found on α-motoneu-
rones appears to be more efficient for initiation of auto-
matic motor responses and for regulation of coarse
movements [57].
5. Coding of afferent information
The research on neuronal coding of peripheral inputs
has for a long time been dominated by studies aimed at
identifying receptor properties and pathways that trans-
mit specific sensory modalities or qualities. As a result,
sensory endings in peripheral tissues have been divided
into different modality specific categories, like e.g.
touch, pressure, vibration, muscle length, muscle force,
ligament tension, temperature, and chemosensitive
receptors. Attempts have also been made to subdivide
ascending pathways and cortical neurones according to
similar modality principles (for references, see [65,67]).
However, the assumption that sensory information is
coded in a modality specific manner, and that modality
specific information is transmitted separately in different
ascending and reflex pathways (i.e. the labelled line
concept), has been seriously questioned over the last
decades [65,67–70]. The functional relevance of
modality specificity based on adequate stimulus is
ambiguous since most sensory endings are sensitive to
more than a specific stimulus quality, and since the sen-
sitivity of the sensory endings can be significantly modu-
lated by other stimuli (e.g. sensitisation due to changes
of the chemical environment). The hypothesised trans-
mission in modality or receptor specific pathways does
not conform to known convergence and divergence pat-
terns in central pathways and neurones (for references,
see [4,56,71]). Finally, a system that relies on specific
modality transmission in separate pathways would be
172 P. Sjölander et al. / Journal of Electromyography and Kinesiology 12 (2002) 167–176
open to dramatic sensory disturbances as a result of loss
of even a small number of receptors, afferents or neuron-
es.
A more compelling concept on how peripheral stimuli
are coded in afferent signals, is the ensemble, or popu-
lation, coding theory [67]. In this concept it is assumes
that several receptors are responsive to a given stimulus,
or set of stimuli, but that their individual responses are
different (Fig. 2). Ensemble coding implies several
advantages over the labelled line concept [65,67–70].
The assumption that the individual afferent and neurone
participates in the coding of several different stimuli is
in accordance with the polymodal characteristics of most
Fig. 2. The population coding concept illustrated by the response of
three hypothetical neurones. (A) Neural response function of the neu-
rones. Note the overlapping sensitivity along the stimulus dimension.
The different stimuli are represented as P, Q, R and S. (B) Histograms
demonstrating the responsiveness of the three neurones to the four dif-
ferent stimuli. Note that a single neurone cannot adequately encode a
stimulus since an identical response can be evoked by more that one
stimulus. (C) Ensemble coding patterns (i.e. across fibre patterns). The
histograms show the specific patterns of activity in the ensemble of
the three neurones (i.e. ensemble codes) evoked by each stimulus.
Adapted with permission [67] (copyright  1968 American Psycho-
logical Association).
sensory nerve endings, afferents and central neurones.
The polymodality is an advantage since the number of
different messages that can be encoded in a given popu-
lation could greatly exceed the number of units within
the population (cf. Fig. 2). The signal-to-noise ratio is
reduced in population responses, as compared to single
unit responses, which assure reduced response variability
to identical stimuli. The accuracy of sensory coding in
discharge patterns in a population of units would also
be less vulnerable to irreversible damages of some of
the units.
In addition to the theoretical arguments in favour of
ensemble sensory coding, there is experimental support
for the concept. In animal studies, using principal
component analysis of simultaneous recorded individual
afferent responses, it has been demonstrated that the
information content in ensemble responses is consider-
ably larger than in individual afferents [65,69,70,72–74].
By recording from slowly adapting receptor afferents
from the knee joint of the cat, it was found that the popu-
lation response, generated by even a rather small number
of afferents, demonstrated unique response patterns to
different joint angles and movements [72]. Similar find-
ings have been reported from studies of ensemble
response properties of muscle spindle afferents. Thus,
the ability to discriminate between different muscle
length stimuli is considerably larger in ensembles of pri-
mary muscle spindle afferent responses, than in the indi-
vidual afferent responses [69,70,73,74]. Furthermore, the
information content in the ensemble responses is con-
siderably reduced after denervation of the muscle
spindles, i.e. after removal of the fusimotor innervation,
suggesting that the reflex control of the γ-motoneurones
is critical for optimal sensory transmission in the muscle
spindle afferents. This proposal was reinforced by obser-
vations that muscle fatigue, which alters e.g. the activity
of the γ-motoneurones, reduces the ability of populations
of muscle spindle afferents to discriminate between vari-
ous muscle lengths [74]. When the discrimination ability
was compared between populations containing only pri-
mary muscle spindle afferents, and populations contain-
ing both primary and secondary spindle afferents and
Golgi tendon afferents, it was shown that the information
content was significantly larger in the ensemble
responses from mixed populations [73].
In line with the ensemble coding idea, it seems con-
ceivable that the sensory information on movements and
joint positions are transmitted to the CNS in population
codes created by those muscle, joint and cutaneous
receptors that are currently active. An implication of this
is that it would not be very relevant to ascribe specific
proprioceptive or motor control functions to particular
classes of peripheral receptors, e.g. joint mechano-
receptors as end-range sensors, muscle spindles as mus-
cle length sensors, Golgi tendon organs as force recep-
tors, ACL mechanoreceptors as initiators of protective
 P. Sjölander et al. / Journal of Electromyography and Kinesiology 12 (2002) 167–176
hamstring reflexes etc. On the contrary, the ensemble
coding places the emphasis on response patterns in func-
tional subsets of different types of receptor afferents,
rather than on the response properties and the principal
function of the individual receptors.
6. Reflex regulation of muscle stiffness and joint
stability
As discussed above there are several lines of argu-
ments against a significant role of ligament afferents as
initiators of joint protective reflexes through servoregul-
ation mechanisms (see 3. Skeletomotoneurones and mus-
cle responses). The major limitation in these feedback
mechanisms is that they are slow, i.e. they involve a
certain delay between the time at which a stimulus is
applied and activates peripheral sensory endings, and the
initiation of the motor response or movement adjust-
ment. Therefore servoregulation mechanisms are only
efficient in the control of slow movements. For the
execution of fast movements, the motor programs need
information about the conditions of the limb prior or
early in the movement [75–78]. In such control mech-
anisms, feedback delays are avoided as they assume pre-
paratory adjustments based on sensory information gen-
erated prior to the movement. There are evidence that
preprogramming of fast movements to a large extent
relies on velocity information, in contrast to servoregul-
ation of slow movements that largely depends on pos-
ition information (e.g. [77]). It has also been demon-
strated that peripheral input about position and velocity
of joint rotations can trigger additional motor responses
during the execution of a movement [79,80]. Although
explicit evidence remains to be shown, these findings
indicate that both rapidly and slowly adapting joint and
ligament mechanoreceptors could have a significant
function in feedforward mechanisms controlling muscle
coordination in various movements.
It has been suggested that a significant function of
mechanosensitive nerve endings in ligaments, and other
joint structures, is to contribute to the functional joint
stability by preprogramming the muscle stiffness
through a continuous reflex modulation of the γ-muscle
spindle system [3,49,50]. The idea is based on the obser-
vations that low threshold joint receptors exert potent,
but complex, reflex effects on the γ-muscle spindle sys-
tems of extensor and flexor muscles, and that the activity
of the muscle spindle afferents is crucial in the control
of the muscle stiffness (see section 4). The muscle stiff-
ness, i.e. change in force over change in length, is com-
posed of two interacting components, the reflex mediated
and the intrinsic stiffness [81,82]. The reflex mediated
stiffness is determined by the excitability of the α-
motoneurones, whereas the intrinsic stiffness is the result
of the viscoelastic properties and the existing actomyosin
173
bounds in the muscle. It should be pointed out in this
context that increased muscle stiffness does not show up
as an increased electromyographic activity in the passive
muscle, but rather as an increased resistance to length
changes of the muscle. Since the intrinsic stiffness is
always present and thereby provides a continuous, but
not constant, restraint to muscle elongation, it has been
denoted the body’s first line of defence against pertur-
bations [82]. If the joint mechanoreceptors have a sig-
nificant impact on the reflex mediated muscle stiffness,
via the γ-muscle spindle system and perhaps through
direct effects on the α-motoneurones, then they would
also have an impact on the intrinsic stiffness. This is
because the number of actmyosin bridges, which to a
large extent determines the intrinsic stiffness, is related
to the excitability of the α-motoneurone pool. Conse-
quently, the capacity of the muscles to protect the joint
against potentially damaging movements or rapid pertur-
bations would to some extent be determined by the
effects on reflex mediated and intrinsic muscle stiffness
induced by joint and ligament receptors. Yet, the relative
importance of signals from joint afferents in the normal
stiffness regulation in various movements and postures
remains to be clarified.
The relations between the activity in joint and liga-
ment afferents, the reflex control of γ-muscle spindle
system and the regulation of muscle stiffness, have also
been suggested to be a contributing factor to the patho-
physiology behind some chronic musculoskeletal pain
disorders [54,64,83]. The essence of the idea is that
when the ensemble excitatory input on the γ-muscle
spindle system reach a certain threshold, positive feed-
back loops consisting of γ-motoneurones and secondary
muscle spindle afferents are activated [54,63]. The rever-
berating activity in these feedback loops is suggested to
maintain a high static sensitivity of the muscle spindles,
an increased muscle stiffness, and to amplifies input
from other sensory endings and descending pathways on
the γ-muscle spindle system. The positive feedback
loops could be triggered in various conditions, i.e. as a
result of a small but long lasting increase of the afferent
or descending input to the γ-muscle spindle system,
and/or of a sudden massive afferent input to the system.
A whiplash trauma, for instance, is bound to cause a
substantial excitation of afferents from mechano-
receptors and nociceptors of cervical ligaments, joint
capsules, tendon and muscles. This acute and massive
input, together with a delayed inflammatory activation
of chemosensitive nerve endings in injured joints and
muscles, could trigger the positive feedback circuits and
result in increased muscle stiffness. Due to the elevated
muscle stiffness, the blood flow would be reduced in the
muscles and the production and liberation of ions and
metabolites increased (e.g. K+, arachidonic acid, hista-
mine and bradykinin). The increased intra-muscular con-
centrations of these substances would then excite chemo-
174 P. Sjölander et al. / Journal of Electromyography and Kinesiology 12 (2002) 167–176
sensitive muscle afferents that, via their reflex actions on
the γ-motoneurones, add further to the excitatory load
on the γ-muscle spindle system and the α-motoneurone
pools (e.g [64,84–88]). This could induce a chronic state
of increased muscle stiffness and pain, which is pre-
served by the positive feedback loop and a high activity
in chemosensitive muscle and joint afferents and/or
descending pathways. In addition to inducing increased
muscle stiffness, the disturbed activity of the γ-muscle
spindle system would cause deficiencies in both muscle
coordination and proprioception, which are common
symptoms in whiplash patients with chronic pain.
Another implication would be that if an elevated excit-
atory load on the γ-muscle spindle system is preserved
by the positive feedback circuits, then one would not
expect patients suffering from whiplash induced sensory
and motor disorders to be fully recovered after selective
anaesthesia or denervation of the injured joint structures
(cf. [89,90]).
Acknowledgements
The financial support from The Swedish Council for
Work Life Research, Inga-Britt and Arne Lundbergs
Forskningsstiftelse, and The Saami Parliament of
Sweden (mål 1 Sápmi) is gratefully acknowledged.
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Per Sjölander graduated in 1986 from the Uni-
versity of Umeå (Sweden) with a B.Sc. degree
in Biology and Zoology. His postgraduate stud-
ies involved electro-physiological examination
of effects on motor control and proprioception
elicited by activation of nerve endings in differ-
ent joint structures. For these studies he earned
a Ph.D. from the University of Umeå in 1989.
He continued his work as an assistant professor
at the University of Umeå until 1992, when he
moved to Canada to commence a 2-year post-
doc training period at the Department of Clinical
Sciences, University of Calgary. In Calgary he studied sensory properties
of Golgi tendon organs in an animal model. In 1994 he received an associ-
ate professorship at the Swedish National Institute for Occupational Health
in Umeå, where he began studying the pathophysiology behind chronic
musculoskeletal pain conditions. After a year as principal at the senior
high school in Storuman, Sweden (1996–97), he has held the post as direc-
tor at the Southern Lapland Research Department, Vilhelmina, Sweden.
Over the last few years his research interests have been expanded to
include clinical studies of the efficiency of various treatment and rehabili-
tation methods fro chronic musculoskeletal pain conditions, and epidemi-
ological studies of the health and living conditions of the Sami people
(the natives of Scandinavia). He is a member of the International Brain
Research Organization, the European Neuroscience Association, the
Society for Neuroscience, and the Nordic Society for Physiology.
Mats Djupsjöbacka graduated in 1989 from the
University of Umeå (Sweden) with a B.Sc.
degree in biology. His postgraduate studies
involved electrophysiological examination of
the reflex regulation of the muscle spindle sys-
tem from chemosensitive muscle afferents and
joint afferents in animal models. He earned a
Ph.D. from the University of Umeå in 1996. Fol-
lowing that he did a one-year post-doc training
period at the Department of Clinical Sciences,
University of Calgary. In Calgary he studied
fatigue related changes in electrophysiological
and mechanical properties of single motor units. After his post-doc he
returned to Umeå to work as an assistant professor at the Centre for Mus-
culoskeletal Research, National Institute for Working Life. Over the last
few years his research interests have focused on the pathomechanisms
behind work related musculoskeletal disorders, with an emphasis on the
effects of muscle pain and fatigue on proprioception and motor control.