Journal of Neurology, Neurosurgery, and Psychiatry, 1972, 35, 853-860

Interaction between voluntary contraction and tonicstretch reflex transmission in normal and

spastic patientsPETER D. NEILSON'

From the Division of Neurology, the Prince Henry Hospital, and the Schools ofMedicine and Physics, University ofNew South Wales, Sydney, Australia

SUMMARY Transmission characteristics of tonic stretch reflex (TSR) pathways in both normal andspastic patients have been measured during different levels of sustained voluntary contraction of thebiceps brachii muscle. A cross-correlation technique of analysis was used to separate reflexresponses from the total electromyographic activity. TSR transmission in normal subjects wasobserved to change with the level of voluntary contraction; sensitivity to stretch increased approxi-mately three-fold as the subject stiffened the arm by simultaneously contracting flexor and extensormuscles. In contrast, TSR transmission did not alter during voluntary contraction in spastic patients.It is proposed that in spastic patients supraspinal modulation of reflex transmission is impairedbecause hypersensitive spinal reflexes short-circuit long loop pathways.

Tonic stretch reflexes in man are known chieflyas pathological phenomena, since it is difficult toelicit stretch reflexes in normal man. The limb ofa relaxed subject can be moved passively withoutencountering active resistance. Granit, Kellerth,and Williams (1964) have shown by intracellularrecording experiments in the cat that a certaindegree of background excitation on alpha andgamma motoneurones is essential for the appear-ance of stretch reflexes. It would appear that thisis also true in man, since stretch reflexes can beactivated by the Jendrassik manoeuvre, which isthought to increase bias on gamma and alphamotoneurones (Gassel and Diamantopoulos,1964).Merton (1953) speculated that voluntary

movement might be initiated by gamma moto-neurone activity setting a desired length on theintrafusal muscle fibres. Stretch reflexes wereimagined to act like a length follow-up servo-system to contract extrafusal muscle and reducelength error to zero. Stretch reflex pathwayswhich are normally quiescent in a relaxed sub-ject would have to be biased on during voluntary

1 Centre Industries Research Scholar.853

movement initiated by such a proprioceptiveservosystem.

It is known that voluntary muscle contractionsare supported by alpha and gamma motoneuronecoactivation, the so called c-y linkage (Granit,1966). It has also been shown that when amuscle is lightly contracted the tonic stretchreflex (TSR) of that muscle is activated (Neilson,1972b). Transmission characteristics of thevoluntarily activated TSR in man are morecomplex than those measured in the decerebratecat. It was suggested (Neilson, 1972b) that longloop pathways might contribute to the complexTSR response in normal man. Supraspinalcontrol of reflex transmission might adjust thesensitivity of segmental mechanisms to producean optimum reflex support to voluntary move-ment. Thus the concomitant activation ofstretch reflexes during voluntary contractionmight be expected to be a graded control ofsensitivity rather than an on-off action. It wasdecided to test this suggestion by measuringtransmission characteristics of TSR pathways ofthe biceps brachii muscle in normal subjects sus-taining different levels of voluntary contraction.TSR transmission during voluntary contrac-

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tion has also been measured previously in spasticpatients (Neilson, 1972c). Responses from thesepatients were not as complex as those measuredin normal subjects. TSR transmission approxi-mated to monosynaptic characteristics measuredin the decerebrate cat (Poppele and Terzuolo,1968; Rosenthal, McKean, Roberts, andTerzuolo, 1970). These findings were interpretedas supporting the proposal that short-circuitingof long loop pathways by overactive spinalreflexes is part of the mechanism of spasticity. Ifthis suggestion is valid, supraspinal control ofreflex transmission should be impaired in spasticpatients. This conclusion can be tested bymeasurement ofTSR transmission characteristicsof biceps brachii muscle in spastic patients sus-taining different levels of voluntary contraction.

METHOD

Two groups of 10 subjects were tested. Individualswith no history of any neurological disturbance com-prised the normal group. The second group consistedof 10 cerebral palsied patients who presented aclinical picture of spasticity.The TSR of a muscle is activated by voluntary

contraction of that muscle but the electromyograms(EMGs) of the reflex responses are difficult tomeasure because they are mixed with potentialscaused by the voluntary contraction. A technique toextract the EMG of reflex responses from the totalelectromyographic activity by cross-correlationanalysis between elbow angle and integrated electro-myogram (IEMG) from the biceps muscle has pre-viously been described (Neilson, 1972b). It has beenshown that voluntary EMG activity is not correlated

FlexorEMG

in a tracking test with joint angle changes of theopposite limb caused by external forces at frequen-cies greater than 2 0 Hz. Normal reaction time limitscoherent voluntary responses to less than 2 0 Hz(Neilson, 1972a). Consequently, the component ofthe total EMG activity coherent with joint anglechanges caused by disturbance forces at frequenciesgreater than 2-0 Hz must be due to involuntary orreflex systems.The subject lay supine on a couch with the right

arm strapped into a frame which constrained move-ment of the arm to flexion-extension about theelbow. A goniometer attached to the frame recordedelbow angle on a four channel model 5 Grass poly-graph. The subject flexed his arm so that the elbowangle was in the 900 position. Sinusoidal disturbancetorques were applied about the elbow joint by aspring connected to the arm frame (Fig. 1). The otherend of the spring was connected to an oscillatingcantilever arm on a sinusoidal stretching machine.The frequency of stretching could be varied con-tinuously between 0 and 5 0 Hz. Frequencies weretested in random order at intervals of 025 Hzthrough this range. The oscillating cantilever armstretched the spring and therefore increased thedisturbance force applied to the limb. The change inelbow angle caused by the force was recorded on thepolygraph.Beckman EMG surface electrodes were attached,

5 cm apart, over the bellies of the biceps and tricepsmuscles. The EMG signals were monitored on a17 in. oscilloscope to ensure that they were not con-taminated by movement artefact. The integratedelectromyogram of biceps was recorded (TC=0-16 sec). Amplitude and phase distortion introducedinto the IEMG signal by the integrating filter wascorrected by multiplying gain and phase by the

FIG. 1. Diagram illustratingachine subject's arm strapped in arm

frame which constrained move-ment to flexion-extension about

-P the elbow. Disturbance forceswere applied by stretchingspring.

-Arm frame

To cantilever armon stretching m;

Fd /

Tm

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Interaction between voluntary contraction and tonic stretch reflex transmissionl

inverse frequency response characteristics of thefilter. The IEMG signal from the biceps muscle wascalibrated by adjusting the sensitivity of the IEMGamplifier to produce a 25 mm deflection of the poly-graph pen above the baseline while the subject sup-ported a 10 kg weight attached to a point on the armframe 30 cm from the axis of elbow rotation.During each test instructions were given to stiffen

the arm very slowly by simultaneously contractingelbow flexor and extensor muscles. The level ofvoluntary contraction of the biceps brachii musclewas slowly increased and decreased during each test.The order in which voluntary contraction was in-creased or decreased as well as the order in which thefrequencies were tested was randomized.Each test lasted two to three minutes. A 5 to 10

minute rest period was given between each test toavoid fatigue.

TECHNIQUES OF ANALYSIS

The use of two techniques of analysis allowed theresults from one technique to be verified by theother.

1. Averaging of IEMG and joint angle responses.

2. Cross-correlation and spectral analysis ofIEMG and joint angle signals.

AVERAGING Sinusoidal joint angle and IEMG cycleswere numbered consecutively through each test.Individual cycles were selected for measurement byusing a table of random numbers. Minimum andmaximum values were measured in millimetres asshown in Fig. 2. If the difference between the twominimum values of either the joint angle or theIEMG cycle was greater than 5 mm, all of the datafrom that cycle were rejected on the grounds that thelevel of voluntary contraction was changing toorapidly. The average value of the two minimumIEMG measurements provided an indicator for thelevel of voluntary contraction during that cycle.Using this indicator the data for each cycle weresorted into six levels of voluntary contraction cor-responding to six 5 mm intervals between 0 and30 mm of pen deflection. The average peak to peakamplitude was calculated for each joint angle andIEMG cycle. Approximately 100 randomly selectedcycles were measured for each level of voluntarycontraction at each test frequency. Mean values of

Angle of cantilever1 sec

1 2 3 4 5 6 7 8 9 10extension

f4"\ ,r 1i0o

1 2 3 4 5 6 7 8 9 10

EMAX.

EMINi MIN 2.

IEMG of biceps17 28 15 16 30 19 31 22

EMG of triceps

FIG. 2. Page ofpolygraph recording showing how measurements were made to collect data forthe averaging technique ofanalysis. Individual cycles were numbered consecutively and randomlyselected for measurement. Minimum angle (AMIN], AMIN2) minimum integrated electro-myogram (EMINI, EMIN2), maximum angle (AMAX) and maximum integrated electromyo-gram (EMAX) were measured as shown.

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the peak to peak amplitude of the sinusoidal jointangle movement, peak to peak amplitude of sinu-soidal IEMG changes and gain (defined as the ratioof IEMG amplitude to change in joint angle) werecalculated for each level of voluntary contraction andfrequency. Gain was plotted against the level ofvoluntary contraction for each frequency tested. Thegain curves included correction for distortion by theintegrating filter.A measure of statistical significance of the change

in gain between the lowest and highest levels ofvoluntary contraction was obtained by a Student ttest.

CROSS-CORRELATION AND SPECTRAL ANALYSIS Thistechnique has been described previously (Neilson,1972b). Joint angle and IEMG signals were digital-ized by measuring the deflection above a baseline onthe polygraph at a rate of either 10 or 20/sec (Fig. 3).Average deflection of IEMG above the baselineduring each 1 sec interval was computed and used asa measure of voluntary contraction during thatinterval. Angle and IEMG data collected duringeach 1 sec interval were sorted into six levels ofvoluntary contraction corresponding to six 5 mmincrements of average IEMG deflection between 5and 35 mm. Correlation functions and power spectrawere calculated using the method described byJenkins and Watts (1968). Gain and phase shift werecalculated at each level of voluntary contraction ateach frequency tested. A correction was made forthe distortion in the IEMG signal caused by theintegrating filter.

Angle of cantilever Is

extension

IeionElbow angle K\ f

33272322243133 2 22202231 322623232834312621

T

IEMO biceps \ 10Kg2622232630252a221 25282623172024333320206268

RESULTS

he magnitude of the IEMG responses to sinu-)idal stretching increased with voluntary con--action in all normal subjects tested (Fig. 4).rain of TSR pathways (ratio of the amplitudef sinusoidal variation of IEMG to amplitude ofinusoidal joint angle movement) increased withie level of voluntary contraction for all fre-uencies above 2-0 Hz (Fig. 5). The increase inain between the lowest and highest levels ofoluntary contraction was always found to be;atistically significant beyond 0 10% level.Amplitude of IEMG responses to sinusoidalretching did not vary with voluntary contrac-on in the spastic patients (Fig. 6). Gain of TSRspastic patients was high even at low levels ofDluntary contraction and, if anything, tended) decrease with increasing contraction. Gainas been plotted against level of voluntary con-action and contrasted with the variation inuin observed in normal subjects (Fig. 7).tudent t testing confirmed that the differencesgain between the lowest and highest levels of)luntary contraction in spastic patients was notatistically significant at any frequency.EMG reflex responses were advanced in phasehead of biceps stretch in both spastic andormal subjects. For spastic patients, however,e phase lead did not change significantly with)luntary contraction, whereas in normal sub-

FIG. 3. Page ofpolygraph recordingshowing how measurements were made tocollect data for cross-correlation techniqueof analysis. Deflections of both elbow angletracing and integrated electromyogramabove the baseline were measured inmillimetres at a sampling rate equivalent toeither 10 or 20 samples per second through-out the full length of the test. Approxi-mately 1,000 points were sampled at eachlevel of contraction at each frequency.

EMG triceps

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Interaction between voluntary contraction and tonic stretch reflex transmission8

ELBOWANGLE

IEMG OF BICEPS BRACHII

Baseline

I

161F

FIG. 4. IEMG responses to4

#C extension siniusoidal stretching at in-

fIo- creasing levels of voluntaryflexion contraction in a normal sub-

ject. The average level of theintegrated electromyogramabove the baseline provides ameasure of the level of volun-

\JEJ y U XJ r tary contraction. 25 mm10 Kg deflection corresponds to

10 kg supported at the wrist.Sensitivity of the stretchreflex increases with volun-tary contraction.

14

12

10

a

.0

C._

8

0

-2

5 10 15 20 25 30

Voluntary Contraction in mm

FIG. 5. Gain ofTSR plotted against level ofvoluntarycontraction for a normal subject. A family of curves

has been plottedfor different frequencies of stretchingshowing that the rate of increase in gain with contrac-tion depends upon frequency. Voluntary contraction ismeasured by the average deflection in mm of theintegrated electromyogram above the baseline. IEMGhas beeii calibrated so that 25 mm deflection is equiva-lent to 10 kg weight supported at the wrist. The in-crease in gain between the lowest and highest levels ofcontraction was significant (Student t test) beyond0-1%0 level.

jects it increased by as much as 90° at somefrequencies (2-0 to 3 0 Hz).

Gain vs frequency characteristics of normalsubjects contained resonant peaks at each levelof voluntary contraction confirming the findingreported previously (Neilson, 1972b). The shapeof the frequency response curves changed withthe level of voluntary contraction, whereas thefrequency response curves from spastic patientscontained no peaks of resonance nor did theyvary significantly with voluntary contraction(Fig. 8).

DISCUSSION

The TSR of biceps muscle in normal subjects isactivated during voluntary contraction. Activa-tion, however, is not a simple on-offaction. TSRtransmission characteristics vary with contrac-tion in a complex manner. At any one frequencyof stretch the gain of TSR transmission increaseswith the level of contraction but the rate ofincrease varies from frequency to frequency.This causes the shape of the gain vs frequencycurve to alter as the muscle is voluntarily con-tracted. The size and location of the resonantpeaks vary as the subject stiffens the arm andtherefore the shape of the reflex response to atransient stretch applied to the muscle can alsobe expected to vary.During a voluntary movement the higher

motor centres presumably signal commands notonly to control lengths and tensions of groups ofmuscles but also to set the gains of the reflexpathways. It is proposed that descending activitydetermines the sensitivity, timing, and shape of

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I sec

extension

flexion

IEMG OF BICEPS BRACHII

'p1 /\

10Kg

FIG. 6. IEMG responses tosinusoidal stretching at in-creasing levels of voluntaryconitraction in a spasticpatient. Level of voluntarycontraction increases fromleft to right. An averageIEMG deflection of 25 mmcorresponds to 10 kg sup-ported at the wrist. Reflexsensitivity does not increasewith contraction level.

spastic patient

//X _I -w- ,

\ N 2 5spastic patient \ *- 2 5

XI' x~~- 2-5

the TSR responses as well as the initiation ofmovement. This proposition is not withoutsupport from experiment. Synaptic transmissionof the reflex connections of groups Ib, II, and IIImuscle afferent nerve fibres in the cat hindlimbcan be inhibited by brain-stem stimulation(Holmqvist and Lundberg, 1959) and bothalpha and gamma efferent nerve fibres can beinfluenced by vestibular activity (Andersson andGernandt, 1956). Higgins (1968) demonstratedcontrol of triceps surae muscle stretch reflexcharacteristics by vestibular activity in acutelydecerebrate cats and stimulation of the intact

30

normal subject

C

0

5 10 15 20 25 30Voluntary Contraction

FIG. 7. Gain ofTSR plotted against level ofvoluntarycontraction at two different frequencies of stretching(2-5 and 3-0 Hz). Curvesfor a spastic patient have beencontrasted with those of a normal subject. For thespastic patient reflex gain is high at low levels of con-traction but does not change significantly with in-creasing levels of voluntary contraction.

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6-

4-

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0

- 2

-4-

- 6

- 8

-10

I

(a)

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I:02 3 4

Frequency in Hz

Fig. 8(a)

ELBOW ANGLE

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8

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._

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no

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Frequen

(b)FIG. 8. Gain of TSR of spastic Xsubject plotted against frequencyData collected during a sustainedtion causing a mean IEMG deJequivalent to 4 5 kg supported atcollected during a sustained vol,equivalent to 9 kg supported at thetrate increase in gain and change i

peaks with voluntary contractionwhile no significant change occurs

cerebellum has been shown tcmodification to the myotatic r(Partridge, and Glaser, 1962). Spontine and medullary retiifacilitates and inhibits respecvibration reflex (TVR) of thesoleus muscle in the decerebiBurke, and Lance, 1971). Theby vibration excitation ofspindle endings. TVR in nornsuppressed completely by voluGail, Lance, and Neilson, 19Hagbarth, 1965; Marsden,Hodgson, 1969) but this abilitypatients (Hagbarth and Eklurmond (1956) observed that spistretch reflex responses in man

completely or preset by descending activity. A7E,x study of H-reflex excitability during voluntary

contraction of gastrocnemius-soleus and anteriortibial muscles in man during foot pressure track-ing allowed Gottlieb, Agarwal, and Stark (1970)to demonstrate that the agonist myotatic loopgain is turned up before movement and the antag-onist circuit is turned offto prevent reflex opposi-

ormal tion. They found evidence for the existence of amechanism for the independent regulation of thegain of the monosynaptic reflex arc mediatedcentrally within the cord.The complicated shape of the frequency

response curves measured in normal subjectsemphasizes that the TSR signals are transmittedby neuronal circuits which are sufficiently com-plex to transform the shape of the response. Thetotal JEMG response may well be composed of

J45 the sum of responses from a number of parallelicy in Hz reflexes. At one extreme, corrections for slowly

changing loads on a limb can be mediated bylong pathways to higher centres where muscle

patient and normal contractions can be consciously activated toof stretching. (a) oppose the load. At the other extreme, a rapidvoluntary contrac- change of load can induce fast corrections bylection of 10 mm exciting monosynaptic or short segmental reflexthe wrist. (b) Data circuits. A number of reflex pathways probably'untary contraction exist between these two extremes which correctwrist. Curves illus- for disturbances of intermediate speeds. Inter-nshapeof resonant action between such parallel pathways couldin spastic patisnt. produce the complex frequency response curves

measured. Furthermore, supraspinal control ofthe sensitivity of each pathway could cause thechange in shape of the frequency response

add a dynamic curves observed during changes of voluntaryzsponse (Higgins, contraction.,timulation of the Gain and phase curves did not alter with thecular formation level of voluntary contraction in spastic patients.-tively the tonic The TSR was active even during very low levelse gastrocnemius- of contraction and seemed to be independent ofrate cat (Gillies, the voluntary control exerted by the patient. InTVR is initiated spastic patients a lack of correlation was ob-primary muscle served between voluntary and reflex contractionmal man can be of a muscle. This could lead to a situation inintary effort (De which the reflexes do not support purposive)66; Eklund and movements but rather compete with them.Meadows, and As reported previously and verified in thisis lost in spastic study the transmission characteristics of TSR

nd, 1968). Ham- pathways in spastic patients are not as complexinal polysynaptic as those measured in normal subjects undercan be inhibited similar test conditions. The absence of peaks in

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the gain curves and the smaller phase advance-ment of IEMG responses ahead of stretch areconsistent with the hypothesis that exaggeratedsensitivity of spinal reflexes in spasticity causesthem to dominate or to short-circuit long looppathways. Moreover, the failure of the frequencyresponse curves to change shape as the patientincreased voluntary contraction supports theconcept that the change of gain in normal sub-jects is caused, at least in part, by supraspinalcontrol of long loop pathways. In spasticity, thegain of the reflex loop appears to be set at a near-maximal level so that reinforcement by voluntarycontraction is unable to cause any increment ingain.

I wish to thank Associate Professor J. W. Lance andProfessor E. P. George for their valued advice andencouragement and for their generous provision ofequipment from the Schools of Medicine andPhysics. The figures were drawn by Miss Susan Caseyand prepared by the Department of Medical Illustra-tion, University of New South Wales. The SpasticCentre of N.S.W. provided the Centre IndustriesResearch Scholarship in support of this project.

REFERENCES

Andersson, S., and Gernandt, B. E. (1956). Ventral root dis-charge in response to vestibular and proprioceptivestimulation. Journal of Neurophysiology, 19, 524-543.

De Gail, P., Lance, J. W., and Neilson, P. D. (1966). Differen-tial effects on tonic and phasic reflex mechanisms producedby vibration of muscles in man. Journal of Neurology,Neurosurgery, and Psychiatry, 29, 1-11.

Eklund, G., and Hagbarth, K.-E. (1965). Motor effects ofvibratory muscle stimuli in man. Electroencephalographyand Clinical Neurophysiology, 19, 619.

Gassel, M. M., and Diamantopoulos, E. (1964). The patternof reinforcement of monosynaptic reflexes in normal sub-jects and patients with spasticity or rigidity. Neurology(Minneapolis), 14, 555-560.

Gillies, J. D., Burke, D. J., and Lance, J. W. (1971). Supra-spinal control of tonic vibration reflex. Journal of Neuro-physiology, 34, 302-309.

Gottlieb, G. L., Agarwal, G. C., and Stark, L. (1970). Inter-actions between voluntary and postural mechanisms of the

human motor system. Journal ofNeurophysiology, 33, 365-381.

Granit, R. (1966). Effects of stretch and contraction on themembrane of motoneurones, pp. 37-50. In MuscularAfferents and Motor Control. Proceedings of the FirstNobel Symposium, 1965, Sodergarn. Edited by R. Granit.Almqvist and Wiksell: Stockholm.

Granit, R., Kellerth, J.-O., and Williams, T. D. (1964).'Adjacent' and 'remote' post-synaptic inhibition in moto-neurones stimulated by muscle stretch. Journal of Physi-ology, 174, 453-472.

Hagbarth, K.-E., and Eklund, G. (1968). The effects ofmuscle vibration in spasticity, rigidity, and cerebellar dis-orders. Journal ofNeurology, Neurosurgery, and Psychiatry,31, 207-213.

Hammond, P. H. (1956). The influence of prior instruction tothe subject on an apparently involuntary neuro-muscularresponse. Journal ofPhysiology, 132, P17-18.

Higgins, D. C. (1968). Vestibular component in dynamicmuscle stretch. American Journal of Physiology, 214, 482-487.

Higgins, D. C., Partridge, L. D., and Glaser, G. H. (1962). Atransient cerebellar influence on stretch responses. Journalof Neurophysiology, 25, 684-692.

Holmqvist, B., and Lundberg, A. (1959). On the organizationof the supraspinal inhibitory control of interneurones ofvarious spinal reflex arcs. Archives Italiennesde Biologie,97, 340-356.

Jenkins, G. M., and Watts, D. G. (1968). Spectral Analysisand its Applications. Holden-Day: San Francisco.

Marsden, C. D., Meadows, J. C., and Hodgson, H. J. F.(1969). Observations on the reflex response to musclevibration and its voluntary control. Brain, 92, 829-846.

Merton, P. A. (1953). Speculations on the servo-control ofmovement. In The Spinal Cord: a CIBA FoundationSymposium, pp. 247-260. Edited by J. L. Malcolm andJ. A. B. Gray. Churchill: London.

Neilson, P. D. (1972a). Speed of response or bandwidth ofvoluntary system controlling elbow position in intact man.Medical and Biological Engineering, 10, 450-459.

Neilson, P. D. (1972b). Frequency response characteristics ofthe tonic stretch reflexes of biceps brachii muscle in intactman. Medical and Biological Engineering, 10, 460-472.

Neilson, P. D. (1972c). Voluntary and reflex control of thebiceps brachii muscle in spastic-athetotic patients. Journalof Neurology, Neurosurgery, and Psychiatry. (In press.)

Poppele, R. E., and Terzuolo, C. A. (1968). Myotatic reflex:its input-output relation. Science, 159, 743-745.

Rosenthal, N. P., McKean, T. A., Roberts, W. J., andTerzuolo, C. A. (1970). Frequency analysis of stretch reflexand its main subsystems in triceps surae muscles of the cat.Journal of Neurophysiology, 33, 713-749.

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