The response of muscle spindles to sinusoidal stretching of

the muscle has been extensively studied in decerebrated

cats, leading to an understanding of the basic properties of

muscle spindles (Matthews & Stein, 1969; Poppele & Brown,

1970). The prominent feature of muscle spindle primary

endings is that the linear response to stretching is limited to

amplitudes lower than a few fractions of a millimetre

(Matthews & Stein, 1969). In the linear range, primary

endings possess a high stretch sensitivity. At larger

amplitudes, the response to stretching is no longer linear

and the stretch sensitivity is markedly reduced.

High stretch sensitivity at low amplitudes and amplitude

non-linearity may be crucial in determining the response of

primary endings to any input during natural movements

(e.g. Matthews, 1981). Thus, to explain the meaning of

spindle signals during natural movements, it is necessary to

explore in intact animals how muscle spindle afferents behave

during stretches for a wide range of amplitudes. Previous

studies of human muscle spindle afferents examined the

response to stretches of large amplitudes (Vallbo, 1973;

Vallbo et al. 1979; Edin & Vallbo, 1990). However, the

response to stretches at low amplitudes has not been

quantitatively described.

The purpose of the present study was to give quantitative

data for the human muscle spindle response to low

frequency sinusoidal stretching and to analyse the effect of

stretch amplitude. It will be shown that the response of

primary afferents is linear to sinusoidal stretching at low

amplitudes and that stretch sensitivity is markedly higher

in the linear range.

METHODS

Subjects

Fifteen experiments were performed on healthy volunteers, 4 males

and 11 females, aged 20—37 years. All subjects gave informed,

written consent according to the Declaration of Helsinki. The

experimental plan was approved by the Human Ethical Committee

of the National Rehabilitation Centre for the Disabled, Japan.

Experimental set-up

Each subject sat comfortably in a reclining chair, with the left

forearm supported on a platform and clamped in mid-position

Journal of Physiology (2000), 527.2, pp.397—404 397

Response of human muscle spindle afferents to sinusoidal

stretching with a wide range of amplitudes

Naoyuki Kakuda

Department of Neurology, National Rehabilitation Centre for the Disabled,

Tokorozawa, Saitama, Japan

(Received 16 February 2000; accepted after revision 23 June 2000)

1. Impulses of human single muscle spindle afferents were recorded from the m. extensor carpi

radialis, while 1 Hz sinusoidal movements for a wide range of amplitudes (0·05—10 deg, half

of the peak-to-peak amplitude) were imposed at the wrist joint.

2. The response was considered as linear when the discharge was approximately sinusoidally

modulated. The linearity was further checked by a linear increase in the response with the

amplitude and a constancy of the phase and mean level.

3. Fifteen of 25 primary afferents were active at rest with a mean rate of 10·6 impulses s¢

(median). The linear response to sinusoidal stretching was limited to amplitudes lower than

about 1·0 deg. The sensitivity was 5·6 impulses s¢ deg¢ (median) in the linear range and

decreased at larger amplitudes. The other 10 primary afferents were silent at rest and lacked

a linear response at low amplitudes.

4. Nine secondary afferents were active at rest with a mean rate of 9·5 impulses s¢. The linear

range extended up to about 4·0 deg with a sensitivity of 1·4 impulses s¢ deg¢.

5. In the linear range, the phase advance of the response to sinusoidal stretching was about

50 deg and was similar between the two types of spindle afferents. In primary afferents, the

phase advance increased to nearly 90 deg outside the linear range.

6. The findings suggest that high sensitivity to small stretches is important in determining

primary afferent firing during natural movements in intact humans.

10726

Keywords:

between supination and pronation. The hand was fixed to a

manipulandum, which was connected to a servo-controlled torque

motor, enabling measurement of joint angle, velocity and torque.

An insulated tungsten electrode was percutaneously inserted into

the radial nerve 5 cm proximal to the elbow joint to record nerve

activity (Vallbo et al. 1979). The location of the muscle belly of the

m. extensor carpi radialis brevis was confirmed by palpation and

surface electrical stimulation. To record muscle activity, a pair of

surface electrodes was attached near the motor point.

Kinematic signals were sampled at 400 Hz. Surface EMG was

filtered at 1·6—800 Hz and sampled at 1600 Hz. Nerve signals were

recorded and sampled at 12 800 Hz using a SCÏZOOM system

(Department of Physiology, Ume�a, Sweden). Each recorded nerve

spike was inspected off-line on an expanded time scale. When it

was judged to be from a single unit based on the regularity of firing

and shape invariance of consecutive spikes, the nerve signal was

converted to a spike train at 400 Hz for later analysis.

Unit identification

Slowly adapting muscle afferents from the m. extensor carpi radialis

brevis were identified by prodding the muscle and tendon. Care was

taken to confirm the origin of each afferent as the m. extensor carpi

radialis brevis. Further identification procedures consisted of a

passive ramp stretch and release of 16 deg and maximal twitch

contraction by surface stimulation of the motor point. Muscle

spindle afferents were tentatively classified as primary and

secondary based on the response during ramp stretch and release.

An initial burst at the start of a stretch, deceleration at the end of a

stretch and the silence during the releasing phase of a stretch were

considered as primary afferent signs (Edin & Vallbo, 1990).

Experimental protocol

The wrist joint was held in position at a 10 deg flexion from the

horizontal. Sinusoidal movements were imposed at the wrist joint

with this position taken as 0 deg. The subject was instructed to

relax completely during imposed movements.

When a single muscle spindle afferent was recorded, 1 Hz sinusoidal

movements of 8·0, 5·0, 2·5, 1·0, 0·50, 0·25 and 0·10 deg (half of the

peak-to-peak amplitude, throughout the text) were tested in this

order. Sinusoidal movements of fixed amplitude were imposed for

10—20 s (Fig. 1A) and the recording started after a few initial

cycles. When recording conditions were stable, the stretch amplitude

was adjusted with finer steps in the range of 0·05—10·0 deg.

Size of movements

The excursion of the tendon during the test movement can be

roughly estimated in the following way. If the radius of the joint is

approximated to 13·0 mm (Brand, 1985) and the muscle length of

the m. extensor carpi radialis brevis is 186 mm (Loren & Lieber,

1995), then a 1·0 deg flexion corresponds to a 0·23 mm stretch. If it

is supposed that any movement in the tendon corresponds to a

muscle fibre stretch of the same amount, a 1·0 deg flexion

corresponds to a 0·12% relative stretch of the resting muscle length.

Data analysis

The records of 8—12 cycles of 1 Hz sinusoidal movements of

constant amplitude were used for analysis. The procedure in this

study was almost the same as the methods used in previous studies

in decerebrated cats (Matthew & Stein, 1969; Hulliger et al. 1977a).

The cycle of sinusoidal movement was divided into 400 bins. The

mean interspike interval of all the spikes occurring in each bin was

then calculated over a number of cycles. The inverse of the mean

interval was the mean discharge rate. The sine curve was fitted to

the mean discharge rate by the least mean square method.

The mean level, depth of modulation and phase were measured in

the fitted sine (Fig. 1B). The depth of modulation was assessed as

half of the peak-to peak-amplitude. The phase was defined as the

difference between the fitted sine and the sinusoidal movement.

The correlation coefficient (rÂ) was calculated to check what

proportion of variance in the mean discharge rate was attributed to

the fitted sine. In the present study, data were used when the

correlation coefficient was higher than 0·6. Moreover, the root-

mean-square (r.m.s.) deviation of the mean discharge rate from the

fitted sine was calculated to check for a goodness of fit. It was

represented by the percentage of the depth of modulation.

When the amplitude of sinusoidal movements was large, primary

afferents ceased firing for part of the whole cycle. In such cases, the

silent period in the mean discharge rate was determined by eye and

was not used for fitting the sine curve, which was allowed to project

below zero (Fig. 2C). The correlation coefficient and the root-mean-

square deviation were calculated in the same period as used in the

fitting procedure.

RESULTS

Twenty-five muscle spindle primary afferents and nine

secondary afferents were recorded from the m. extensor

carpi radialis brevis. The resting discharge was assessed

while the wrist joint was held in position at a 10 deg flexion

from the horizontal. Fifteen primary afferents were active

and the median value of the mean discharge rate was

10·6 impulses s¢ (range, 3·4—18·9). The other 10 primary

afferents were silent. All secondary afferents were active

and the median value of the mean discharge rate was

9·5 impulses s¢ (range, 3·4—14·9).

When the subjects relaxed completely, the spindle discharge

was relatively regular and the discharge rate was low.

Spontaneous fluctuations in the mean level of discharge rate

were not observed. Fusimotor action was therefore probably

low and henceforth will be considered negligible, in

agreement with previous conclusions for human subjects

(e.g. Vallbo et al. 1979).

Measurement of spindle response to sinusoidal

stretching

Figure 1 shows a representative result of primary afferent

behaviour during sinusoidal stretches at low amplitudes.

Figure 1A shows the raw record while 1 Hz sinusoidal

movements of 0·25 deg (half of the peak-to-peak amplitude)

were imposed at the wrist joint. The discharge is clearly

modulated by sinusoidal movements, as seen in the

instantaneous discharge rate.

Figure 1B shows the instantaneous discharge rate averaged

cycle by cycle (thin line) and the fitted sine curve (thick line),

and illustrates the measurement of the response. The

discharge was sinusoidally modulated (r = 0·98) around the

mean level of 6·8 impulses s¢. The depth of modulation was

1·15 impulses s¢ (half of the peak-to-peak amplitude) and

the phase advance to the sinusoidal movement was 75 deg.

The root-mean-square deviation of the mean discharge rate

from the fitted sine was 0·13 impulses s¢, equal to 11·1% of

the depth of modulation.

N. Kakuda J. Physiol. 527.2398

Response of a primary afferent to stretching with a

widely ranging amplitude

Figure 2 shows the mean discharge rates (thin line) and the

fitted sine curves (thick line) of a primary afferent. The

mean level of resting discharge was 13·2 impulses s¢. The

amplitude of sinusoidal movements increased by a factor of

four and was 0·25 (A), 1·0 (B) and 4·0 deg (C).

In Fig. 2A and B, the discharge was approximately

sinusoidally modulated (r = 0·98 in both). The depth of

modulation was 1·7 impulses s¢ at 0·25 deg (A) and

6·7 impulses s¢ at 1·0 deg (B), and the increase was

proportional to the amplitude. The mean level

(13·0 impulses s¢) and phase advance (44 and 41 deg) held

constant between A and B. Accordingly, the response in A

and B may be regarded to fall in the linear range. The root-

mean-square deviation held at about 10%.

When the amplitude increased by a further factor of four,

the afferent ceased firing for about half of a whole cycle (C).

The response was not sinusoidal and apparently outside the

linear range. The silent period was not used for fitting the

sine curve (see Methods). The fitted sine ranged between

−9·7 and 26·0 impulses s¢ and the mean level decreased to

8·1 impulses s¢. The depth of modulation was

17·9 impulses s¢ and the increase was less than proportional

to the amplitude. The phase advance increased to 67 deg,

which was a further sign of non-linearity. The root-mean-

square deviation increased to 14·3%.

Relation between amplitude of stretching and

response of a primary afferent

Figure 3 shows the relation between the amplitude of

stretching and the response of the primary afferent in

Fig. 2. The amplitude ranged between 0·05 and 8·0 deg. The

r value was higher than 0·6 at any amplitude, indicating

that the discharge was significantly modulated. The depth

of modulation (A), the mean level (B), the phase advance (C)

and the root-mean-square deviation (D) are plotted against

the amplitude.

The depth of modulation (A) linearly increased at amplitudes

between 0·05—2·0 deg. On the other hand, the mean level

(B) held constant up to only 1·0 deg and progressively

decreased at larger amplitudes. This reduction was related

with the distortion of the response from the sine curve, and

in particular with the cessation of discharges for part of the

whole cycle. Thus, the increase in the depth of modulation

between 1·0—2·0 deg was, in part, due to the reduction in

the mean level. Similarly to the mean level, the phase

advance (C) held constant up to 1·0 deg and then increased

at larger amplitudes. From A—C, it is confirmed that the

Muscle spindle response to sinusoidal stretchJ. Physiol. 527.2 399

Figure 1. Measurement of the response of a primary afferent to sinusoidal stretching

A, raw record during 1 Hz sinusoidal movements imposed at the wrist joint. The amplitude was 0·25 deg

(half of the peak-to-peak amplitude). From top to bottom, joint angle, primary afferent activity and its

instantaneous discharge rate and surface EMG. B, mean instantaneous discharge rate (thin line) and the

fitted sine curve (thick line). The horizontal axis shows the phase of sinusoidal stretching with a range of

−180 and 180 deg. The vertical axis shows the discharge rate. The horizontal line indicates the mean level,

while the vertical and horizontal arrows indicate the depth of modulation and the phase advance,

respectively. The depth of modulation was defined as half the peak-to-peak amplitude. The phase was

defined as the difference between the fitted sine and the sinusoidal stretching.

linear response was limited to amplitudes up to 1·0 deg. In

Fig. 3A, linear regression was applied to the points below

1·0 deg (r = 0·98). The line passes near the origin and the

slope indicates a sensitivity of 6·3 impulses s¢ deg¢.

The root-mean-square deviation (D) stayed at about 10%

between 0·2 and 1·0 deg and increased at larger amplitudes.

This suggests that the fitting of the sine curve to the mean

discharge rate was good in the linear range. (The value at

both 0·05 and 0·10 deg was about 30%. The depth of

modulation was less than 0·5 impulses s¢ at amplitudes

lower than 0·10 deg, so that the spontaneous variation in

the discharge was not negligible.)

N. Kakuda J. Physiol. 527.2400

Figure 2. Response of a primary afferent to 1 Hz sinusoidal stretching at different amplitudes

Mean instantaneous discharge rates (thin lines) and the fitted sine curves (thick lines). The stretch

amplitude increased by a factor of four and was 0·25 (A), 1·0 (B) and 4·0 deg (C). The horizontal axis shows

the phase of sinusoidal stretching with a range of −180 and 180 deg. The vertical axis shows the discharge

rate. Note that the vertical scale in C is twice than that in A—B. The horizontal lines indicate the mean level

in the fitted sine, while the vertical and horizontal arrows indicate the depth of modulation and the phase

advance, respectively. In C, the mean discharge rate fell silent for about half of the cycle. The silent period

was not used for fitting of the sine curve and the fitted sine projected below zero.

Linear range of primary and secondary afferents

Fifteen of 25 primary afferents were active at rest. The

discharge was significantly modulated (r > 0·6) in 10

afferents at 0·10 deg and in all afferents above 0·25 deg. The

median value of the linear range was 1·0 deg (range, 0·2—1·9).

In the linear range, the median value of the sensitivity was

5·6 impulses s¢ deg¢ (range, 3·0—22·6). The medians and

quartiles (25 and 75%) of the depth of modulation were

plotted against the amplitude of stretching in the upper

graph of Fig. 4A. The linear increase was limited to

amplitudes lower than 1·0 deg in the total sample.

The other 10 primary afferents were silent at rest. They

started firing during sinusoidal movements at 0·90 deg

(median). At any amplitude, they ceased firing for part of

the whole cycle and the response was different from the sine

curve. They lacked a linear response to stretches at low

amplitudes, while the response at amplitudes above about

1·0 deg was similar to that in Fig. 4A.

All nine secondary afferents were active at rest. The

modulation of the discharge was significant in three afferents

at 0·10 deg, in seven afferents at 0·25 deg and in all afferents

above 0·50 deg. The median value of the linear range was

3·6 deg (range, 1·0—8·0). The median value of the sensitivity

was 1·4 impulses s¢ deg¢ (range, 0·88—3·1). The upper graph

of Fig. 4B plots the depth of modulation in the total sample,

which linearly increased with the amplitude up to 8 deg.

Phase advance

The phase advance of the response to sinusoidal stretching

in the total sample was plotted in the lower graphs of Fig. 4.

In primary afferents (A), the phase advance increased from

50 to 70 deg at amplitudes between 0·1 and 1·0 deg. Some

afferents fell outside the linear range at 0·5 or 1·0 deg,

accompanying the increase in the phase advance. In

secondary afferents (B), the phase advance ranged between

40 and 60 deg. Therefore, the phase advance was about

50 deg in the linear range and similar between the two

types of spindle afferents. Both types of afferents respond

Muscle spindle response to sinusoidal stretchJ. Physiol. 527.2 401

Figure 3. Relation between the amplitude of stretching and the response of a primary afferent

The effect of stretch amplitude is shown in the same primary afferent as Fig. 2. The stretch amplitude

ranged between 0·05 and 8·0 deg. The depth of modulation (A), the phase advance (B), the mean level in

the fitted sine (C) and the root-mean-square deviation of the mean discharge rate from the fitted sine (D) are

plotted against the amplitude of sinusoidal stretching. In A, linear regression was applied to the points

below 1·0 deg (r = 0·98). The y-intercept was −0·19 impulses s¢ and the slope was 6·3 impulses s¢ deg¢.

to the compound of the position and the velocity components

of sinusoidal stretching.

In primary afferents, the phase advance increased to about

80 deg at amplitudes above 1·0 deg. This indicates that the

velocity component was dominant in determining the

response of primary afferents outside the linear range.

Response of spindle afferents to large amplitude ramp

stretching

The sensitivity of muscle spindles to large stretches was

measured for comparison to the stretch sensitivity at low

amplitudes. A ramp stretch of 16 deg was applied at the

wrist joint over 0·9 s with a speed of about 18 deg s¢.

The static position response was defined as the difference in

discharge rate between that just before the start of the

stretch and that during the static phase of the stretch. The

latter was assessed as the mean rate during the holding

phase between 0·5—1·5 s after the end of the stretch. The

dynamic response was measured as the dynamic index,

which was defined as the difference in discharge rate

between that just before the end of the stretch and that

during the static phase of the stretch (Edin & Vallbo, 1990;

Kakuda & Nagaoka, 1998).

The response to the ramp stretch was recorded in

ten primary and seven secondary afferents of Fig. 4. The

median value of the static position response was

5·3 impulses s¢ (range, 3·3—10·2) and 6·7 impulses s¢

(range, 5·8—10·4) in the primary and secondary afferents,

respectively. The static sensitivities were calculated as

0·33 impulses s¢ deg¢ and 0·42 impulses s¢ deg¢,

respectively, and similar between the two types of spindles.

The median value of the dynamic index was 10·5 impulses s¢

(range, 6·1—15·0) and 4·6 impulses s¢ (range, 1·8—7·4) in

the primary and afferents, respectively. The dynamic index

of primary afferents was larger than that of secondary

afferents. These results are compatible with previous data

recorded in human forearm muscles (Vallbo, 1973; Edin &

Vallbo, 1990) and in isolated human intercostal muscles

(Newsom Davis, 1975).

N. Kakuda J. Physiol. 527.2402

Figure 4. Summary of the response of 15 primary and 9 secondary muscle spindle afferents to

1 Hz sinusoidal stretching

The effect of stretch amplitude on the response of primary and secondary afferents is summarised in A and B,

respectively. The upper graphs plot the depth of modulation against the amplitude of stretching, while the

lower graphs plot the phase advance. 1, medians, and horizontal bars indicate the quartiles (25% and 75%).

The sensitivity of the primary afferents to sinusoidal

stretching at low amplitudes (5·6 impulses s¢ deg¢) was

more than 10-fold of the static sensitivity (0·33 impulses

s¢ deg¢). It was also much higher than the dynamic index

(10·5 impulses s¢), considering the amplitude (16 deg) and

the speed (18 deg s¢) of the ramp stretch. In secondary

afferents, the sensitivity to sinusoidal stretching

(1·4 impulses s¢ deg¢) was of the same order of magnitude

as the static sensitivity (0·42 impulses s¢ deg¢) and the

dynamic index (4·6 impulses s¢) of the large ramp stretch.

DISCUSSION

The present study gives the first quantitative description of

the response of human muscle spindle afferents to low

frequency sinusoidal stretching over widely ranging

amplitudes.

The main finding was that the response of primary afferents

to 1 Hz sinusoidal stretching at amplitudes below about

1·0 deg was linear. The stretch sensitivity in the linear range

was markedly higher, compared with the sensitivity at larger

amplitudes. In secondary afferents, the linear range extended

to larger amplitudes and the stretch sensitivity was about

one_fourth to one_fifth of that of the primary afferents. In

the linear range, both position and velocity components of

stretching contributed to the response and the two types of

spindle afferents were similar in this respect. The appearance

of non-linearity in the spindle responses provides further

evidence that fusimotor activity is low for relaxed human

muscles (Hulliger et al. 1977a; Cussons et al. 1977).

Comparison to muscle spindles in the decerebrated cats

The linear range of human primary afferents was 1·0 deg at

the wrist joint, estimated to be 0·23 mm and 0·12 percentage

of the resting muscle length (see Methods). The stretch

sensitivity of 5·6 impulses s¢ deg¢ corresponded to

24 impulses s¢ mm¢ and 47 impulses s¢ (percentage of the

resting muscle length)¢. In the primary endings of the

soleus muscle (length 50 mm) in decerebrated cats with

intact ventral roots, the linear range was about 0·1 mm and

0·2 percentage of the resting muscle length. The sensitivity

was about 100 impulses s¢ mm¢ and 50 impulses s¢

(percentage of the resting muscle length)¢ (Matthews &

Stein, 1969; Hulliger et al. 1977a). In absolute modulation

(impulses s¢) and sensitivity (impulses s¢ mm¢), the

present data are smaller than expected from the data for the

cat. However, when the sensitivity is expressed in relation

to resting muscle length, the figures are more uniform.

The morphological evidence suggests that the difference in

absolute modulation (impulses s¢) and sensitivity

(impulses s¢ mm¢) is not attributable to fundamental

differences in structure per se between human and cat

spindles (Hulliger, 1984). It is conceivable that the spindle

sensitivity (impulses s¢ mm¢) is related to the resting

muscle length. In long muscles, spindles need not lie in

parallel with the entire length of extrafusal muscle fibres.

Instead, they often originate from, and insert at, extrafusal

muscle fibres, so that they are arranged in series with

compliant elements (Baker, 1974). Given that human

spindles are not longer than cat spindles, locally effective

length changes during stretch might constitute a smaller

fraction of the change in whole-muscle length than for the

much shorter muscles in cats (Hulliger, 1984).

Although the spindle sensitivity might be related to resting

muscle length, it also seems likely that the lower sensitivity

of human primary afferents is at least partly due to

experimental conditions. The present data were obtained

with the wrist near its mid position, far from the position at

which the m. extensor carpi radialis brevis would be at its

maximal physiological length. On the other hand, the data

for the cat were obtained at the maximal physiological

length of the muscle. If the fusimotor activity is eliminated

after cutting the ventral roots in decerebrated cats, spindle

endings have a high sensitivity when the muscle is at

physiological full extension, but not when the muscle is

shorter (Matthews & Stein, 1969). Therefore, the difference

in sensitivity (impulses s¢ mm¢) between the data for

human subjects and that for the cat might be partly due to

the difference in extension of the muscles and to the low

fusimotor action for relaxed human muscles.

The sensitivity of human secondary afferents was

1·4 impulses s¢ deg¢ (6·2 impulses s¢ mm¢) in the linear

range and it was about one_fourth of that of primary

afferents. Considering the differences in experimental

conditions, it would be worth noting that the difference in

sensitivity to small stretching between the two types of

spindles for relaxed human subjects was of the same order of

magnitude as that for decerebrated cats (Matthews & Stein,

1969; Cussons et al. 1977).

Functional implications

The discharge rate of human spindle afferents is usually

0—30 impulses s¢ and rarely exceeds 50 impulses s¢ during

natural movements (Vallbo et al. 1979). Although the

discharge rate is rather low, the present data show that

small stretches of the muscle appreciably modulate the

discharge rate of the primary afferents. A 1 deg movement

at the wrist joint produces a modulation of 6 impulses s¢ in

a primary afferent, corresponding to 60% of the pre-

existing level (about 10 impulses s¢). It seems reasonable to

conclude that the high stretch sensitivity at low amplitudes

plays an important part in determining the spindle activity,

at least during passive movements.

The stretch sensitivity of muscle spindles may be affected

by the fusimotor activity during voluntary contractions and

it is necessary to address whether the high stretch

sensitivity at low amplitudes is maintained or not during

voluntary contractions. In decerebrated cats, the stretch

sensitivity of the primary endings at low amplitudes is

reduced by stimulation of a fusimotor fibre, irrespective of

dynamic or static fibre. When both dynamic and static fibres

are stimulated, the reduction in sensitivity is dependent on

Muscle spindle response to sinusoidal stretchJ. Physiol. 527.2 403

the balance between the two types of fusimotor actions

(Goodwin et al. 1975; Hulliger et al. 1977a,b). It was

suggested in humans that both dynamic and static fusimotor

neurones are active during voluntary contractions, when the

spindle response was tested by a large amplitude ramp

stretch (Kakuda & Nagaoka, 1998). Thus, the fusimotor

system possibly maintains and controls the stretch sensitivity

of primary endings at low amplitudes during voluntary

contractions. As a result, the primary afferents can signal

small length changes in the muscle occurring during slow

voluntary movements (Wessberg & Vallbo, 1995).

The present data support the view that the muscle spindles

contribute to the detection of small passive movements

(McCloskey, 1978; Proske et al. 2000). This argument is

based on the observation that significant modulation in the

discharge rate was obtained during sinusoidal stretches at

0·10 deg in 10 of 25 primary afferents. The threshold

amplitude of the primary afferents may be compatible with

the psychophysical results. For example, threshold detection

of movements imposed at the elbow joint is about 0·1 deg

(Wise et al. 1998). It was shown in humans that both muscle

spindles and slowly adapting type II cutaneous mechano-

receptors provide reasonable velocity signals of passive

movements at large amplitudes (Grill & Hallett, 1995),

implying the contribution of both types of sensory inputs to

movement perception. To investigate the relative roles of

muscle spindles and cutaneous mechanoreceptors in the

detection of movements, particularly at small amplitudes, it

would be helpful to examine the response of cutaneous

mechanoreceptors to small stretches as used in the present

study.

In conclusion, muscle spindle primary afferents in humans

respond linearly to stretches at low amplitudes with high

responsiveness. This suggests that high sensitivity to small

stretches is important in the determination of primary

afferent firing during natural movement and that muscle

spindles contribute to fine motor control, as well as

kinaesthetic sensibility.

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Acknowledgements

This work was supported by the Ministry of Health and Welfare of

Japan.

Correspondence

N. Kakuda: Department of Neurology, National Rehabilitation

Centre for the Disabled, 4-1 Namiki, Tokorozawa, Saitama

359_8555, Japan.

Email: j90016@simail.ne. jp

N. Kakuda J. Physiol. 527.2404