A Control Model of Stretch Reflex

W. J. ROBERTS, N. P. ROSENTHAL, AND C. A. TERZUOLO

Laboratory of Neurophysiology, University of Minnesota Medical School,
Minneapolis, Minnesota 55455

IN PREVIOUS PAPERS (14, 15) it was proposed modulation frequencies. Using linear systems
that the two components of the stretch analysis, a “gain” and “phase” were computed
reflex-namely, the “reflex” component from these parameters to describe both the
which results from the activation of the magnitude ratio between output and input and
the phase angle between them (cf. ref 14).
alpha motoneurons by the primary affer-
The same measurements were then repeated
ents, and the “mechanical” component
after interrupting the reflex loop. The sec-
contributed by the viscoelastic properties tioned muscle nerves were stimulated electri-
of the muscle and connective tissues- cally at fusion frequency to obtain the same
summate vectorially. The necessity for this values of mean tension which were present
proposal was prompted by the fact that with the reflex intact (cf. ref 4). From these
the phase angle between muscle length measurements the reflex component could be
and tension is appreciably different before determined by vector subtraction (see RESULTS).
and after interrupting the reflex loop (14). A digital computer (IBM 1800) was used
The dynamic characteristics of the length- to simulate the input-output relations of the
stretch reflex and muscle tissue by combining
tension relationships under these two con-
the linear transfer functions of the individual
ditions were previously studied in decere- subsystems in various configurations. Each sub-
brate cats using both length (14) and force system was assigned a weighting coefficient
(1) inputs. We shall now present data on which was varied until the best fit between
the relative contributions to the stretch the results of the simulation and the experi-
reflex by the reflex and mechanical com- mental data was obtained.
ponents. These data and the linear ap- Subsystem specifications having a transpor-
proximations of the dynamic behavior of tation delay and up to nine first- or second-order
the stretch reflex and its main subsystems, pole and zero terms were entered from punched
presented previously (14), will then be used cards or the keyboard. The frequency response
to formulate a quantitative control model characteristics of any, or all, of the subsystems
for the stretch reflex. From this model, cer- whose specifications had been changed since
the last simulation were then computed at
tain conclusions will be drawn regarding eight different modulation frequencies between
the contribution to the reflex by various 0.1 and 20 Hz. Next, the overall system con-
subsystems.The possible role of the stretch figurations were selected, and changes in the
reflex in the genesisof tremor will also be coefficients linking the subsystems were entered.
discussed. At this point the frequency response charac-
teristics of the selected overall system were
METHODS computed and printed.
Since the experimental methods as well as
the data processing techniques were described RESULTS
in detail previously (14), they will be men- When changes in the muscle length (L)
tioned here only briefly to orient the reader.
are used to induce the stretch reflex, the
Sinusoidal changes in length (cf. ref 14) or
tension (cf. ref 1) were imposed on the gastroc- dynamic muscle stiffness is given by the
nemius muscles of cats acutely decerebrate at vector quantity ‘TO/L (cf. ref 14), where T,
the intercollicular level. The muscle length represents the overall muscle tension and
and tension parameters were recorded over a
range of mean tensions, input amplitudes, and
--
Received for publication December 9, 1970.
@=C)+C) (I)
620

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 CONTROL MODEL OF STRETCH REFLEX 621

The subscripts r and m are used to denote Thus, the reflex and mechanical compo-
the reflex and mechanical components of nents can be compared at each input fre-
the overall tension T,. These components quency and for each mean muscle length
are assumed to act in parallel, L being and tension. The validity of this compari-
common to both. son, however, rests on the contention that
The above expression is valid only the absolute magnitude of the mechanical
within the range of input parameters and component measured after interrupting
mean muscle tensions over which the two the reflex is essentially equal to that pres-
components behave linearly, at least at ent with the reflex intact. To measure this
first approximation (cf. ref 14). Notice that mechanical component the procedure in-
only the quantities T,/L and T,/L can troduced by Brown (2) was used. The sec-
be measured experimentally. The reflex tioned muscle nerve was stimulated elec-
component is obtainable only indirectly by trically at or near the fusion frequency (ZO-
vector subtraction of the mechanical com- 40/set) with a stimulus intensity appro-
ponent from T, since any change in length priate to produce the same muscle tension
used to modulate the reflex component will which was present before interrupting the
simultaneously produce a change in the stretch reflex in the same preparation at
mechanical component. any given mean muscle length. Experimen-
When force changes are used as the in- tal data reported previously (14) indicate
put, the resulting change in muscle length that under these conditions the value of
(L) shall also result from a vector summa- the peak-to-peak changes in muscle tension
tion similar to that given in expression 1. produced by a sinusoidally modulated
However, in this case one must think of length input are not different from those
the length, L, as being the length allowed
obtained when the same mean muscle ten-
by the muscle when subjected to an ap-
sion is attained by stimulating asynchro-
plied tension T,, in the presence of the
reflex. Likewise, the length allowed by the nously four or five ventral root filaments
same input T, in the absence of the reflex at a low rate (lO/sec). The latter condition
is denoted L,, while the length allowed more closely approximates the physiolog-
by the reflex loop (in the hypothetical ab- ical situation which prevails in the pres-
sence of the mechanical muscle stiffness) ence of the stretch reflex since the mean
is denoted L,. These parameters are re- impulse rate is closer to that of the alpha
lated by the following expression: motoneurons during reflex operation (cf.
ref 4, 5, 14). However, under this condition
the impulse rate can vary sinusoidally
C)=(g)+C) (2) (when averaged over several cycles) or it
can be highly discontinuous (burst of im-
from which, by dividing through by T,, pulses), depending on the parameters of
L, can be obtained. Its value is then scaled the imposed length changes. Simulation of
to represent the change in length which these conditions, although feasible, is some-
would result from the force input T, if what laborious. More importantly, different
the mechanical component were to be re- types of motor units (6) may be recruited
moved and only the reflex component was by the electrical stimulus than those acting
responsible for producing the measured during reflex operation (3, 4). Owing to
length changes. Since the mechanical com- these uncertainties the magnitude of the
ponent cannot be removed experimentally mechanical component obtained experi-
(see above), L, can only be determined in- mentally, as described above, can only be
directly. considered as an approximation of that
By the above procedures the absolute present with the reflex intact. With this
quantity of the reflex component of the reservation in mind we can now proceed to
muscle stiffness in response to either a present the data on the comparison be-
length or a force input can be computed tween reflex and mechanical components
for any given experimental conditions. for both length and force input cases.

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 G22 ROBERTS, ROSENTHAL, AND TERZUOLO

Quantitative relationship between phase of T, with respect to the imposed

mechanical and reflex components changes in muscle length is shown in Fig.
of stretch re@ex 1B. In all experiments the phase was near
The amplitude and phase of the reflex zero at 0.5 Hz and showed an increasing
component of the changes in muscle stiff- lag with increasing modulation frequency.
ness in response to length inputs were The data shown in Fig. 2, obtained from
found to varv with the modulation fre- the same preparations used to compile Fig.
quency. Values from representative experi- 1, give the changes in the relative ampli-
ments are shown in Fig. 1 where each sym- tude of the mechanical component of the
bol represents a different preparation. muscle stiffness (ratio between T, and T,
These data were selected to encompass the minimum) under the same conditions of
entire range of values observed. The mag- mean muscle tension and length as in Fig.
nitude of the reflex component is given in 1. It is obvious that the relative contribu-
Fig. 1A as the ratio between the reflex ten- tion to the stretch reflex by the mechanical
sion, T,, computed at each frequency, and component increasesas the modulation fre-
its maximum value within the frequency quency of the input increases. Since the
range shown. It is clear that the relative phase relation between muscle tension and
amtAitude of the reflex tension decreases the imposed changes in muscle length was
with increased modulation frequency if the considered at length in a previous paper
modulation amplitude of the length input (14) it does not need to be mentioned here.
is kept constant. The absolute value of the Figure 3A is a plot of the ratio, R,, of
the reflex stiffness to the mechanical stiff-
nessas a function of modulation frequency.
100 It shows that in the gastrocnemius muscle
1 of in tercollicularly decerebra ted cats the
80
aTR 0 relative magnitude of the reflex component
AT, MAX
IO
of the muscle stiffness may be quite differ-
60
ent from preparation to preparation, the
I \ upper and lower values being the extremes
40-- \ •t
X

1 1 I 11 1L I
.5 1 2 4 8 16
0

-zoo 220
% &L&Lo IO
ATM~l~
4-40 i la0
f

--601 L : .’ ! ! \ 140
.
.5 1 2 4 8 16 xx>I
FREQUENCY (HZ) .5 1 2 4 8 16
FREQUENCY (HZ)
FIG. 1. Changes in the reflex component of the
muscle stiffness as a function of input frequency. FIG. 2. Change in the mechanical muscle stiff-
A shows the percentage change in the magnitude ness as a function of the modulation frequency. The
of the m .uscle tension resulting from reflex activity, plot shows the percent change in the experimen-
relative to its maximum, as a function of the tally measured peak-to-peak muscle tension (or
frequency of the input (sinusoidal modulation of stiffness) during sinusoidal modulation of the mus-
muscle length). B shows the phase relation of this cle length. The mean muscle tension in each case
reflex stiffness with respect to the input. Data were was 800 g-wt and was produced by stimulating the
obtained by vector subtraction of values of the muscle nerves at ‘30 pulses/set. The mean muscle
mechanical component of the stiffness from those lengths were those at which 800 g-wt of tension
of the stretch reflex (see text). Each symbol repre- was produced in the same preparations by reflex
sents a different preparation. The mean tensions activity. The peak-to-peak changes in the muscle
of muscles (gastrocnemius) were either 800 or 1,200 length were either 590 or 780 ~1. Data are from
g-m while the peak-to- *peak changes in muscle the same four preparations (each represented by
length were 780 p in all cases. a different symbol) as in Figs. 1, 3, and 4.

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 CONTROL MODEL OF STRETCH REFLEX 623

in previous figures were either for mean

2.5 muscle tensions of 800 or 1,200 g-wt. Figure
4 shows the changes in the absolute value
of the reflex stiffness (gram-weight of reflex
tensions per micron of displacement) as a
function of the mean muscle tension in the
four representative preparations used in
previous figures. Only the data points ob-
tained at one modulation frequency (2 Hz)
are shown. The increase in stiffness with
increasing mean muscle tension is con-
siderable, the values being representative
0.8
08 of the entire group of experiments.
When force inputs were used, technical
0.6 difficulties prevented the use of frequencies
hT& of modulation above 12 Hz (cf. ref 1).
0.4
Within the frequency range of 0.1-12 Hz
the data obtained with force inputs indi-
cated that the dynamic length-tension
length-ten-&on char-
Q2 acteristics were the same as those obtained
by using length inputs, both with and with-
0.0 .
I I I I out the reflex contribution, as shown in
.5 2 4 8 16
1

MODULATION FFiEQUENCY (Hz) the accompanying paper (1). Because of

this fact these data will be considered only
FIG. 3. Effect of modulation frequency on the briefly in order to show the relative con-
“stiffness ratio” and on the absolute reflex stiff-
ness. A shows the change in the ratio, Rs, of the tribution of the reflex and mechanical
mech nical com-
reflex stiffness relative to the mechanical stiffness ponents in preventing changes
changes in mmuscle
uscle
(ATr/AT,) as a function of the modulation fre- length during changes in applied force.
quency. Data were obtained in each case at a Figure 545A is a plot of the reflex changes
mean tension of 800 g-wt using peak-to-peak length
modulation of either 580 (+) or 780 p,. B gives the in muscle length (L,) in response to a force
relationship between the reflex stiffness and the input computed from the data presented in
modulation frequency for the same experimental the accompanying paper (1) and using ex-
conditions noted above. pression 2. It shows that the reflex is most
effective in preventing changes in muscle
we encountered. These differences are most length for input frequencies up to 2 Hz.
likely due to differences in the influences
of supraspinal origin which contribute to 0.8 --
determine the excitability of neurons par- +/+
ticipating in the segmental activities re- +’
--
0.6 /
sponsible for the reflex. Notice that the 0
contribution by the reflex component to AT,/,/- - +A+
X
the stretch reflex generally becomes rather 0.4 -- .4;
small (E 0.3 times the mechanical com-
l /8/
- r/,.

ponent) at the highest frequency studied. 0.2 --

Finally, in Fig. 3B the absolute value of
the reflex stiffness (TJL) in the same four
preparations is given as a function of the 0.04, :
500
' :
700
' :
900
' :
1100
' :
1300
'

modulation frequency. MEAN MUSCLE TENSION (g-wt)

Since the dynamic stiffness during reflex FIG. 4. Effect of mean muscle tension on the
operation was previously shown to depend, reflex muscle stiffness. Values of the reflex stiff-
among other factors, on the mean muscle ness shown were obtained using the mean muscle
tensions indicated. Sinusoidal modulation of the
tension (14), data on the reflex component
muscle length was imposed at a modulation fre-
of the stretch reflex were obtained at differ- quency of 2 Hz and a peak-to-peak amplitude of
ent mean muscle tensions. Those presented either 590 (+) or 780 p.

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 624 ROBERTS, ROSENTHAL, AND TERZUOLO

226 with the data obtained when using length

O/o - A 0 inputs (Fig. 1B).
180-- Since the dynamic behavior of the me-
AL,
LL rmn - chanical component for a force input was
described previously (I), we can compare
A----

.$5-==
immediately the magnitude of the reflex
I :
and mechanical compliances. The ratio be-
.2 .5 1 2 4 8 tween reflex and mechanical compliances
as a function of modulation frequency is
shown in Fig. 6. These data are in agree-
ment with those obtained by using length
inputs (Fig. 3A). This agreement elim-
inates the necessities of considering sepa-
rately, in the model to be presented, the
1 I
behavior to force and length inputs, at
.2 .5 1 2 4 8 least within the range of input parameters
MODULATION FREQUENCY (Hz)
used in our studies.
FIG. 5.Length change permitted by the reflex
arc during modulation of the muscle tension. A System modeling
shows the relative changes in the modulation of
the muscle length, permitted by the reflex arc The data presented above provide an
alone, that is after correcting for the mechanical estimate of how the reflex component of
compliance, as a function of the modulation fre- the stretch reflex affects the length-tension
quency by using force inputs in four preparations,
each represented by a different symbol. The phase
characteristics during reflex operation inde-
of these length changes relative to the applied pendently from the mechanical properties
force is plotted in B. All data were obtained at of the muscle tissue. Using this information
mean muscle tensions of 800 g-wt using tension together with the linear approximations of
modulation depths between 300 and 500 g-wt. the dynamic characteristics of the main
subsystems responsible for the stretch reflex
For instance, the length changes in re- presented earlier (14), it becomes possible
sponse to a given input at 8 Hz are about to formulate a mathematical model of the
30y0 greater than their minimal value oc- reflex behavior. If this model were to be
curring at 2 Hz.
Figure 5B shows the phase of the reflex
changes in muscle length with respect to 1.5 I--

the modulating input force. The phase

lag of about 20” at the lower frequencies 1.0
indicates that the reflex contraction, which AL/
&n
tends to prevent the muscle length from 0.5
changing, is approximately in phase with
the passive changes in length which result 0
from the viscoelastic nature of the muscle 72 5 i im 4 S 16
MODULATION FREQUENCY (Hz)
tissue (cf. ref 14). This plot also shows that
the phase of L, shifts in a leading direction FIG. 6. Ratio between the reflex and mechan-
with respect to the applied force as the ical compliances as a function of the modulation
input frequency increases. This suggests frequency. The ratio plotted is the length modu-
lation permitted by the reflex arc alone divided
that the phase of the reflex component of
by the length modulation permitted by the teta-
the overall muscle tension must lag more nized muscle in the absence of reflex activity.
and more with increasing modulation fre- Data were obtained from the same four prepara-
quency since, as the phase of the reflex tions of Fig. 5, using force inputs between 300
tension shifts in a lagging direction, the and 500 g-wt at a mean muscle tension of 800
g-wt in each case. At the higher modulation fre-
movement that it acts to prevent will shift quencies the reflex arc becomes more compliant
in a leading direction by a comparable than the tetanized muscle tissue operating at the
amount. These phases are in agreement same mean muscle tension.

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 CONTROL MODEL OF STRETCH REFLEX 625

successful in duplicating the dynamic char- all the data points obtained from six recep-
acteristics of this behavior, one might gain tors, and are discussed in detail in a previ-
some insight into the relative contributions ous paper (14). As stated at that time,
of each of the main subsystems to the over- caution should be used in deriving a trans-
all behavior of the reflex. fer function for the tendon organ since
The stretch reflex was simulated on a the system behavior appears to be depen-
digital computer. The transfer functions dent on the average impulse frequency.
used to simulate the dynamic character- This point has now been confirmed by ex-
istics of the stretch reflex and its mechan- periments currently in progress (J. Ander-
ical components were those presented and son, unpublished observation). However,
discussed in a previous paper (14). For the since the data points within the dashed
primary endings, the transfer function area include a large range of average im-
given in the same paper was intentionally pulse frequencies (between 16 and 70 im-
restricted to include only first-order terms. pulses/set) it seems that the approximation
This restriction led to a discrepancy be- provided by the transfer function given
tween the averaged experimental data and above is adequate to account for the aver-
the transfer function gain of about 7 dB at age behavior of the receptor population in
a frequency of 16 Hz. A more complex response to a length input. Notice that this
transfer function, containing a second- behavior also includes dynamic character-
order zero (cf. ref 14) was therefore derived istics resulting from the mechanical proper-
to be used for the simulation. This expres- ties of the muscle and connective tissues,
sion is: since the appropriate input for the receptor
(s + 0.44)(s + 1.7)(s + 11.3)(s + 200)2(s2 + 37.6s + 3540)
s = 0.009 e-0.002s (3)
(s + 0.82)(s + 2.7)

The solid lines in Fig. 7 are the graphical A

representations of the above expression,

while the shaded area encompasses all the
experimental data points on the behavior
of the primary endings to length changes
which were described in detail in a previ-
ous paper (Fig. 15 of ref 14).
It is pertinent to remember that the pres- 180
zi
ence of fusimotor static background does $135I
not alter these frequency-response charac-
teristics, with the possible exception of the si 90
6
absolute gain, since these characteristics aI 45
t
are the same when large modulation ampli-
0:
tudes are used during repetitive stimula- .2 .4 .6 1 2 4 6 10 20
tion of a fusimotor fiber, or with small MODULATION FREQUENCY (Hz)

stretch amplitudes in the absence of fusi-

FIG. 7. Transfer function characteristics for pri-
motor activity (cf. ref 14). mary muscle spindle afferents. The solid lines in
For the Golgi tendon organs the transfer the two plots represent the frequency response
function used in the model to describe the characteristics of the transfer function used to
input-output relations of these receptors describe the average muscle spindle behavior. The
for a length input is: shaded areas encompass the experimental data
obtained from six receptors and described in detail
(s + 0.44)(s + 1.7)(s + 11.3)(s + 126)2
- e-0.002s previously (14). The upper plot shows the nor-
G(s) =
(s + 0.82)(s + 2.7) malized receptor gain in decibels, that is, 20 log,,
(output amplitude in impulses per second/input
(4
amplitudes in microns). The lower plot describes
The graphical representation of this ex- the phase of the sinusoidally varying output im-
pression is given by the solid lines of Fig. pulse frequency relative to the sinusoidal length
8. The dashed areas in this figure include input function,

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 626 ROBERTS, ROSENTHAL, AND TERZUOLO

TABLE 1. Comparison between average

experimental data and values of derived
transfer function for input-output
relation of tendons organs when muscle
tension is taken as input
Modula- Aw A&
-10 1 II II II I,,
1’. + tion Exptl Exptl GtCsj Gtc,,
180 Gain, Phase,
Fre- Gain, Phase,
G quency dB dB
$935 d% d%
-
# 90 0.2 0.0 15 0 14
0.5 0.7 17 1.2 19
P
CL 45 1 2.1 26 2.2 26
,,r,,, . I I I 11,. 2 3.0 41 3.7 40
.2 .4 .6 I FF&UE~C; t$ 20 4 6.3 58 6.6 59
MODULATION ( 10 14.3 80 11.5 81
20 18.5 90 17.7 95
FIG. 8. Transfer function characteristics of Golgi
tendon organs for stretch inputs. The solid lines
in the two plots show the frequency response
characteristics of the transfer function used to The system configuration shown in Fig.
describe the Golgi tendon organ response. As in 9 was adopted as the most complete repre-
Fig. 7, the shaded areas encompass the experi- sentation for which appropriate data on
mental data from six receptors described pre-
viously (14). The upper plot indicates the receptor subsystems behavior were available. The
gain (see Fig. 7 legend) and the lower plot the lack of adequate data necessitated the omis-
phase of the tendon organ impulse frequency rela- sion of certain subsystems,notably the af-
tive to the length input. ferents from the secondary endings of the
muscle spindles and the Renshaw feedback.
is muscle tension (7, 8). Indeed when this Omission from the model of the secondary
parameter was used to determine the input- endings is partially justified by the fact that
output relations, the same transfer charac- their frequency response characteristics,
teristics were observed whether the tension although difficult to define rigorously since
changes were produced by stretching the they are dependent on the mean impulse
passive muscle (ventral roots sectioned) or frequency of the receptor (1l), are quite
by modulating the impulse frequency of similar to those of the primary endings
the motor fibers (active contraction), ex- (11). Therefore, if the interneuron which is
cept for a difference in the absolute gain interposed between these afferents and the
(cf. ref 14). alpha motoneuron introduces no dynamic
The numerical values for the average changes, the secondary ending afferents
transfer characteristics between receptor would simply change, in the model, the
output (impulse rate) and muscle tension absolute level of the contribution by the
are given in Table 1. The table also gives primary endings. Another reason for omit-
the phase (absolute) and gain (normalized) ting the contribution by these afferents is
values obtained from an empirical expres- the fact that their effects on the alpha
sion which was derived to adequately fit motoneurons (whether excitatory or inhib-
the data. This transfer function relating itory) is presently disputed (cf. ref 5, 10).
the impulse frequency of the tendon organ Renshaw feedback was neglected only be-
to the input tension is: cause of the lack of adequate data. We
(s + 0.63)(s + 3.14)(s + lB.B)(s + 225)
G = e-0.002s
t(s) (9
(s + 0.82)(s + 3.88)

Equations 3, 4, and Z shall be considered hope, however, that data to be obtained

as estimates of the average dynamic char- from experiments now in progress will per-
acteristics of the main inputs responsible mit us to remedy this omission in future
for the reflex corn.ponent of the stretch re- models.
flex. The simplifying assumption is also made

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 CONTROL MODEL OF STRETCH REFLEX 627

sented by a dummy function consisting of

a first-order zero with the corner frequency
at 999 Hz. This is done to prevent any
phase shift between the simulated input
GOLGI (L) PRIMARY MUSCLE and output within the frequency range
encompassed by our study, in agreement
with the results of experiments described
in previous papers (12, 14). Although ade-
quate for the purpose of the present study,
it would be desirable in the future to bet-
ter define the characteristics of this sub-
system also.
Note that in the model the contributions
by the Golgi tendon organs in response to
the length input (L) and to reflex changes
in muscle tension (T,) are separated. This
is desirable since the relative contribution
by these two components is still question-
able (see below) and their transfer charac-
teristics are significantly different, as shown
by the two expressions given above. In
addition, since the transfer characteristics
of both primary endings and Golgi tendon
organs to a change in length also include
the muscle properties, the mechanical com-
FIG. 9. Block diagram of the stretch reflex
model. This schematic diagram represents the most ponent (T,) of the overall muscle stiffness
complex system modeled in this work. The variable (T,) does not need to influence the be-
L represents the muscle length and T the muscle havior of these receptors in the model.
tension, both measured at the muscle tendon. In the model the term C, accompanied
Subscripts for the variable T, namely r, m, and
o, denote the reflex, mechanical, and overall ten-
by a subscript, indicates the weighting fac-
sion components, respectively. The variable MU tor assigned to each subsystem. The box
indicates the motor unit activity in the muscle. denoted nerve-muscle represents the trans-
Boxes denoted Golgi (L) and primary represent the fer characteristics between the motoneuron
transfer functions, given in the text, which de- output (MU) and the contractile tension.
scribe the impulse activity in the tendon organs
and primary muscle spindle afferents in response These transfer characteristics were ana-
to stretch inputs. Golgi (T) symbolizes the tendon lyzed in detail previously (14).
organ behavior in response to active muscle con- The simulation was limited to one mean
traction, while alpha denotes the transfer charac- muscle tension only (800 g-wt) and the co-
teristics across the alpha motoneurons. The muscle
box represents the length-to-tension transforma- efficients adjusted so as to give the experi-
tion of the muscle tissue during steady contraction. mentally measured T, and T, values at
The nerve-muscle box denotes the transfer charac- this mean tension. The value of the coeffi-
teristics from motor unit activity to active muscle cient C, was determined while C, and C,
tension. The subscripted C terms represent con- were set equal zero so as to provide an ab-
stant weighting factors which could be assigned to
the various parts of the system. solute muscle stiffness of -7.8 dB for 800
g-wt of mean tension at 2 Hz. This stiffness,
that the interneuron interposed between which is equivalent to 0.408 g-wt/p was the
the tendon organ afferents and the alpha average value of T,/L obtained experi-
motoneurons does not introduce any dy- mentally in 10 cats when the mean muscle
namics, with the exception of a possible length was that at which 800 g-wt of mean
change in the absolute gain. Data on this tension was produced in the presence of
subject are not likely to become available the reflex. This value of C, (0.115) was
in the near future. Finally, the motoneuron then kept constant throughout the simula-
transfer function (represented by the box tion, except when it was set to zero to de-
denoted alpha in the diagram) is repre- termine the simulated T, component. As

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 628 ROBERTS, ROSENTHAL, AND TERZUOLO

to be expected, both gain and phase plots organ feedback. The subscripts 0.6 and 0.4
for T,/L obtained from the model with indicate the values of C, used to obtain the
the above procedure duplicated quite ac- two curves. With C, = 0.6 the primary
curately the average values for the dynamic ending component was given more weight
characteristics of the muscle and connec- than with C, = 0.4. Thus, the ratio R, was
tive tissues under sustained contraction, higher at each modulation frequency. The
which were presented and discussed in a shaded area encompassesthe range of ex-
previous paper (14). perimental data presented earlier in Fig.
The results obtained with a model con- 3A. The curve obtained with C, = 0.6 fits
figuration in which the input to the alpha the data better, while the Poa4curve pro-
motoneurons is only that provided by the vides a very poor fit of the R, values at fre-
primary endings will first be considered. quencies higher than I Hz. This is also the
Then the tendon organ feedback will be case if one considers the simulated reflex
added and the weighting factors varied to component alone, T,/L, as shown in Fig.
show that only one particular configuration 11. The shaded area of this figure encom-
provides a good fit to all experimental data. passesall the experimental phase and gain
In Fig. 10 the two curves denoted PO 6 values of the T, component with respect
and PO.4 show the simulated stiffness ratio, to the input L, as described in the preked-
R,(AT,/AT,) as a function of input mod- ing section. The curves were obtained from
ulation frequency in the absence of tendon the model after suppressing the T, com-
ponent of the stretch reflex (C, = 0). It
can be seen that the Poe4curve gives a poor
25 fit to the computed values of T, also in this
plot. In particular, the slope of the gain
2.0-- curve is too steep in the midrange of fre-
quencies and the phase appears to deviate
1.5-- considerably from the trend outlined bY
Rs -
IO--

05
. I 1 I
0’ : I

.5 1 2 4 8 ‘16
MODULATION FREQUENCY (Hz)
FIG. 10. Ratio of the reflex muscle stiffness rela-
tive to the mechanical stiffness. Rs is the ratio of
the two stiffness components or ATJAT,, L being
the same under both conditions. The shaded area
shows the range of ratios obtained in four experi-
ments (see Fig. 3A) using sinusoidal length inputs I
over the indicated frequency range. The five curves [L
represent the simulated ratios obtained from five -60
different model configurations. Curves labeled P,., t
I * . . L

and Pas were obtained when the tendon organ

.5 1 2 4 8 16
feedback was suppressed, subscripts indicating the MODULATION FREQUENCY (Hz)
weighting factors assigned to C,, using C, = 0.115.
The curve P + G1 resulted when the stretch was FIG. 1 1. Reflex component to sinusoidal length
also assumed to influence the tendon organ activity inputs The gain (normalized at the lower fre-
in addition to that of the muscle spindles (C, = quency) and absolute phase of the reflex compo-
0.6, C, = 0.3, c, = 0.115). The curve P + Gt was nent are shown in the upper and lower graph,
obtained when the active tension rather than respectively. The shaded areas encompass the en-
muscle length was assumed to determine the ten- tire range of experimental data obtained by vector
don organ activity (C, = 0.6, Ct = 0.8, C, = 0.115). subtraction of the mechanical component from the
The curve labeled P + G1 + G, resulted when all T,/L relationship. The curves describe the be-
components of the model were operational (C, = havior of the model for system configurations and
1.0. c, = 0.3. c, = 1.2, c, = 0.115). parameters identical to those of Fig. 10.

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 CONTROL MODEL OF STRETCH REFLEX 629

the dashed area. The T,/L dynamic char- would be necessary for the mechanical stiff-
acteristics, which describe the overall mus- ness to contribute more to the overall ten-
cle length-tension behavior with the reflex sion than is found experimentally (see Fig.
intact, are also not fit adequately by this 10). Therefore, the addition of the Golgi
model configuration, the gain curve ob- (L) subsystem does not provide a better
tained from the simulation being outside simulation than by using the primary end-
the range of experimental data points (too ing input alone.
high with respect to the latter) and the val- The behavior of the model configuration
ues for the phase being too low and outside in which only the contribution by the
the area encompassing the data points over Golgi tendon organ resulting from reflex
most of the frequency range. A value of contraction of the muscle is added will be
CP = 0.2 produced phase values too high taken up later, after considering the con-
and a gain curve too low, both these curves figuration which allows the best fit to the
being outside the range of experimental average experimental data. This model con-
data points. These discrepancies between figuration includes, in addition to the pri-
the experimental data and the behavior of mary muscle spindle afferents, both the
the model can be largely corrected, how- Golgi (L) and Golgi (T) components. In
ever, if the two components contributed by this case a good fit was obtained when the
the Golgi tendon organs are added to the simulated tendon organ output was influ-
simulation. In so doing the value of C, enced approximately equally by the ap-
necessarily needs to be increased in order plied change in length and by the resulting
to make the reflex component sufficiently T, component of the stretch reflex. The
large with respect to the mechanical com- coefficients of C, and Ct that provide this
ponent. ratio are 0.3 and 0.12, respectively. To fit
When only the Golgi (L) component is the T,/L dynamic characteristics with this
added (cf. Fig. 9), ignoring therefore the contribution by the Golgi tendon organs,
influence of the reflex contraction on the the contribution by the primary endings
tendon organs, the best fit to the dynamic had to be raised to 3.3 times that of the
length-tension characteristics of the stretch stretched tendon organs at 2 Hz (C, = 1).
reflex (T,/L) is found with the combina- With this system configuration the experi-
tion: C, = 0.6 and C, = 0.3. However, as mental T,/L dynamic characteristics were
shown by the curve denoted P + G in Fig. reproduced quite adequately by the simu-
10, the R, values are lower than those ob- lation. More importantly, the R, ratio was
tained from experimental data over the well within the range of the values com-
entire frequency range. This indicates that puted from experimental data (curve P +
in order to produce phase values under Gr + Gt of Fig. 10). Finally, the phase and
closed-loop conditions which are in agree- gain values of the reflex component were
ment with the experimental ones, the re- also adequately reproduced by the model
flex component must be kept unusually (curve P + G1 i- Gt of Fig. 11). Under these
small relative to the mechanical compo- conditions the agreement between the val-
nent. The reason for this is provided by ues of the phase for simulated motoneuron
the curve P i- Gi in Fig. 11. The phase of output (MU in Fig. 9) and the experimen-
the reflex component is lagging the experi- tal data obtained from gastrocnemius sin-
mental data too much at frequencies higher gle motor unit (14) was also very good. The
than 1 Hz, the gain curve being also out- normalized gain curve for this relationship
side the range of experimental data. In also fit the experimental data points quite
conclusion, by adding only the contribu- well.
tion of the Golgi tendon organs due to The reason for the improved fit by using
stretch of the muscle, a slightly better fit to all the subsystems, instead of the primary
the experimental data describing the overall afferents only, resides in the phase changes
length-tension characteristics is observed. introduced by the tension feedback, Golgi
However, the predicted reflex characteris- (T), at the lower frequencies. This allows
tics deviate markedly from the experimen- the reflex component to be increased to the
tal data. To overcome this difficulty it point of being in agreement with the ex-

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 ROBERTS, ROSENTHAL, AND TERZUOLO

perimentally derived R, values, without 2.5 - /

the phase values for the T,/L relationship
h,
falling below those measured experimen- 2.0 -
tally. Moreover, the phase values of the
Golgi (L) component at the higher fre- I.5 -
quency are adequate to compensate for the
Rs -
phase lead imposed at these frequencies by
1.0 -
the Golgi (T) component, thus providing a
good fit with the experimental data also
0.5 -
at the higher frequencies. Notice that if the
activity of the tendon organ population
were to be more dependent on the muscle 0
0
tension produced by contraction than on
the muscle tension produced by passive z
P -4
stretch, then the weight assigned to Golgi .-c c
(T) would have to be increased. While the
R data (curve P + G, of Fig. 10) are fit
’ -8 F
quite well by this system configuration (C,
= 0, c, = 0.6, C, = 0.8), the T,/L data are
fit quite poorly (curve P + Gt of Fig. 11).
The phase lag is less than the computed
one above 4 Hz, and the reflex stiffness
decreases too slowly above 8 Hz.
In the simulations considered above, the
absolute value of the gain of the simulated e
T,/L relationship at 2 Hz was made ap- -60
proximately equal to the average value of F II
I I I I I
the experimental data points. The best fit .5 I 2 4 8 16
was then determined by eye. However, by Modulation Frequency (Hz)
exploring the model behavior over a sig-
FIG. 12. Best fit of the model to the experimen-
nificantly large range of values for C,, C,,
tal data. The continuous lines represent the best
and C, it was found that the above restric- fit to the mean of the experimental data points
tion about the absolute value of the gain (X) by the model parameters given in the text.
could be abandoned since the simulated The dashed areas are the same as in Figs. 10 and
behavior remained within the range of ex- 11 and encompass the entire range of data points.
The discontinuous line (- - -) in graph Rfi
perimental data points. Because of this fact describes the model behavior
l l

by changing C, by
it was of interest to determine the best fit 20%. The dotted lines represent the predicted be-
to the data by the model without imposing havior by increasing and decreasing C, to make
any restriction. These values of C,, C,, and the contribution of the Golgi (T) component 110%
or PO% of that of the Golgi (L) component. The
C, were obtained by minimizing the cumu-
dotted lines in the gain and phase graphs refer
lative quadratic error for the fit of the exclusively to the higher value of C,.
model behavior to the mean values of the
following sets of experimental data: R,, the best fit to our averaged data points for
absolute phase and normalized gain of the the gastrocnemius muscle would be about
T,/L relationship, absolute phase and nor- 26% of that of the- primary endings. As
malized gain of the derived T,/L relation- for the Golgi (T) component, changes in
ship. the value of Ct which make this contribu-
The results are shown in Fig. 12. The tion equal to 80 and 110yO of that of the
continuous lines describe the model be- Golgi (L) component are shown by the
havior while the data points represent the dotted lines of Fig. 12. It will be noted
mean values for all data (dashed areas). that the higher value of Ct produces an
The values for C,, C,, and C, are 0.22, 0.85, appreciable change in the fit to the R, ex-
and 0.75, respectively. Therefore, the con- perimental values (lower dotted line in the
tribution by the Gol,gi (L) component for R, graph of Fig. 12). Moreover, the gain

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 CONTROL MODEL OF STRETCH REFLEX 631

and phase curves are also less well fitted. the simulation suggest that: 1) the contri-
Therefore, the behavior of the model seems bution to the stretch reflex by the tendon
to exclude a nredominant contribution of
organ, which results from stretching the
the Golgi feedback component due to the muscle, is about 26% of that of the pri-
reflex muscle contraction, with respect tomary endings; and 2) the feedback contri-
the Golgi (L) contribution. bution of the tendon organs, which is due
Changes of 20% of the value of C, alone to the reflex muscle contraction, does not
produced marked changes in the simulated seem to differ from that produced by
R, value (discontinuous lines in the R, stretch. This is to be expected if these
graph of Fig. 12). However, too-large devia- organs are functionally in series with the
tions from the best fit could be prevented extrafusal muscle fibers. The large differ-
when the value of C, was increased by in- ence in sensitivity reported for stimulation
creasing simultaneously the values of C, of small ventral root filaments with respect
and Ct. Even so, the quadratic error in-
to that obtained by applying length or
creased markedly because also the fit to the force inputs to the muscle tendon (7, 8) is
phase and gain values of the T,/L relation- obviously the result of a difference in the
ship became less good. focusing of the force onto a single tendon
organ. If instead of a single receptor one
DISCUSSION considers the entire population, it seems
The dynamic characteristics of the main reasonable to assumethat the total output
subsystems responsible for the stretch reflex would be proportional to the net force
were discussed extensively in previous pub- measured at the tendon, whether this is
lications (14, 15). Some of the data were internally generated by active contraction
analyzed in this paper so as to compare the or provided by the input applied to the
reflex and mechanical components of the tendon, assuming that these receptors mon-
muscle stiffness at each input frequency itor the tension in a randomly distributed
and as a function of mean muscle tension. population of extrafusal fibers rather than
The procedure used to compute the reflex in some subgroup of fibers supplying the
stiffness and the limits within which these entire contractile tension. In this respect it
values can be expected to approximate that is worth noting that the behavior of these
present during reflex operation were de- receptors remains approximately linear
fined under RESULTS. It was also shown, in over a very large range of input amplitudes
agreement with previous findings (l), that (14). As for their probable function seeref
force and length inputs led to similar re- 13.
sults, at least within the limits of the input It will be noted that since the simulation
parameters and mean muscle tensions used. was limited to one mean muscle tension
Therefore, only one type of input, namely only, there was no need to incorporate in
changes in muscle length, was used for the the model the nonlineari ties responsible
purpose of simulating the behavior of the for the changes in the absolute magnitude
stretch reflex. As described fully under of the dynamic muscle stiffness as a func-
RESULTS, only one system configuration pro- tion of mean muscle tension. These non-
vided excellent agreement between the sim- linearities were discussed in detail previ-
ulated and experimental dynamic length- ously (14), and are also illustrated in Fig.
tension characteristics for both the reflex 4 of this paper. Since they affect only the
component alone and the behavior of the gain of the T,/L relationship but not the
stretch reflex (including, therefore, the phase, it would be possible to add to the
mechanical component). This agreement model a nonlinear term duplicating this
between experimental data and a unique behavior (cf. ref 14).
model configuration lends support to the Although the successof the model in
contention that an estimate of the relative simulating the inbut-output relations of
contribution by the muscle spindle and the stretch reflex cannot be taken to indi-
tendon organ inputs to the reflex behavior cate that the simplifying assumptions which
is warranted. were used are valid, it would suggest that
If this premise is accepted, the results of the contribvtions by the subsystemswhich

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 632 ROBERTS, ROSENTHAL,
were omitted (mostly the secondary ending
afferents and the Renshaw feedback) do
not introduce significantly different dynam-
ics to the reflex operation in decerebrate
cats. A possible exception, which would be
undetectable in the simulation, would be
the presence of a subsystem with the same
phase relation to the input as that of the
reflex component, or with a zero phase
throughout the frequency range explored.
The addition of such subsystem would
merely require that the now optimum co-
efficients for the muscle spindles and ten-
don organ afferents be adjusted (keeping
their ratio the same) to provide the same
reflex gain that is obtained with the system
configuration used here. Only an indepen-
dent determination of the absolute gain of
the muscle spindle and tendon organ ef-
fects upon the alpha motoneurons would
allow this point to be resolved.
Pending the results of experiments de-
signed to study the contribution to the
dynamic characteristics of the stretch reflex
by antagonistic muscles (12), it would seem
that the stability of the system, as shown
from our studies, is very high. Indeed the
phase lag introduced in the reflex arc by
the transfer characteristics between moto-
neuron output and muscle tension (box
denoted nerve-muscle in Fig. 9) is almost
the same as that of the primary endings of
the muscle spindles and the Golgi tendon
organs (with respect to a length change).
Therefore the net phase shift around the
reflex arc, in the decerebrate cat, is quite
modest, at least up to 8 Hz. A linear anal-
ysis of the motoneuron output above this
frequency is not possible because only burst
activity is present (cf. ref 14). However,
even at frequencies of 16-20 Hz, which can
be safely considered to be the upper limits
for the physiological operational range, os-
cillations do not occur in the simulated
behavior. Indeed to generate such instabil-
ity it would be necessary for the reflex com-
ponent of the muscle stiffness to lag the
input disturbance by 180’. It is easy to see
that the subsystems responsible for the
stretch reflex cannot introduce, per se, the
phase difference necessary to initiate a stability
limit-cycle oscillation, that is, an oscillation
which will not decrease in amplitude with
time, such as a tremor. Indeed the phase of
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AND TERZUOLO
the reflex component never reaches - 180”
with respect to the input (see Fig. 1B). To
do so the motoneuron output would have
to assume, at 20 Hz, a zero phase value with
respect to the length input (and a negative
phase at lower frequencies) since the phase
lag between motoneuron output and mus-
cle tension approximates MO0 at 20 Hz.
Such phase relation does not occur during
operation of the stretch reflex, in decere-
brate cats, as can be seen graphically in
Fig;. 1B. In addition, the magnitude of the
reiex component, that is, the muscle stiff-
ness which results from active muscle con-
traction via the reflex, decreases substan-
tially as a function of the input frequency
(Fig. 1A). However, up to 8 Hz it could be
adequate to support an oscillation (& >
1.0) if the phase lag were sufficient and de-
pending from the mean muscle tension (see
above).
It can be therefore concluded that while
under certain conditions the overall system
(including the mass of the limb and the
viscoelastic properties of the muscle tissues)
might behave as a stable system not crit-
ically damped (presence of oscillations, the
amplitude of which decreases with time),
the presence of a limit-cycle oscillation
such as tremor cannot be attributed to the
dynamic characteristics of the subsystems
responsible for the stretch reflex. A neces-
sary qualification for this statement is that
in the present experiments and in the simu-
lation study the influences of antagonistic
muscles were not included. Without a
knowledge of this factor an extensive dis-
cussion of the tremor mechanisms is unwar-
ranted. It can, however, be stated that fac-
tors such as transport delay, that is, the
time required for the signal to propagate
along the reflex arc, frequently stressed in
the literature (cf. ref 9), are not likely to
play any significant role . in the genesis of
tremor. Indeed if no other phase shifts are
contributed by the action of supraspinal
subsystem, this time delay (even if it were
of the order 7-10 msec) would not pro-
duce sufficient phase shift to create an in-
for frequencies below 50-70 HZ.
At these unphysiological frequencies the
reflex stiffness would be too low to support
any oscillation.
 CONTROL MODEL OF STRETCH REFLEX 633

SUMMARY proximation of the input-output charac-

teristics of the sensory, motor, and muscle
Using procedures previously described dynamic characteristics were used in order
for measuring the dynamic length-tension to simulate, on a digital computer, the dy-
characteristics of the gastrocnemius mus- namic behavior of different system config-
cles, data were obtained on this subject in uration. A few of these simulated behav-
decerebrate preparations with the stretch iors are given. On the basis of the adequacy
reflex intact *and during sustained stimula- of the fit between experimental and simu-
tion of the gastrocnemius nerves following lated behaviors it is proposed that the con-
the interruption of the reflex. The experi- tribution of the tendon organ afferents to
ments having been carried out on the same determine the motoneuron output is about
muscle and under the same conditions of half as much as that of the afferents from
mean muscle length and tension, the mea- the primary endings of the muscle spindles,
surement made during sustained contrac- at least in the decerebrate cat and within
tion in the absence of the reflex was taken the limits of experimental condition used.
as indicative of the absolute values of the In addition it is suggested that the tendon
amplitude and phase (with respect to the organ activity is equally influenced by the
length input) of the component of the mechanical component and by the reflex
stretch reflex resulting from the mechanical tension, due to the reflex modulation of
properties of the muscle tissue. By vector the motoneuron activities.
subtraction of this mechanical component The experimentally determined charac-
from the values obtained in the presence teristics of the reflex component indicate
of the reflex, the dynamic characteristics that the stability of the stretch reflex is too
of the reflex component were determined great, in terms of a control system, to be
indirectly. The length-tension characteris- responsible for originating a limit-cycle
tics of the reflex component, due to the oscillation such as tremor.
modulation of the motoneuron output by
the afferents activities, are given as a func- ACKNOWLEDGMENTS
tion of the frequency of the input and as The authors are grateful to Dr. A. Berthoz for
his contribution in securing the experimental re-
a ratio of amplitude between reflex and sults on force inputs. Thanks are also due to Dr. P.
mechanical component, both for the case Viviani for the computer programming leading to
of length and force inputs. These functions the estimate of the quadratic error.
and the dynamic length-tension character- The data on force inputs presented in this
paper were obtained by analyzing the results of
istics of the stretch reflex and its two com-
experiments performed in connection with the ac-
ponents (defined above) were then used in companying paper by Berthoz et al. (1).
a simulation study in which the behavior This work was supported by Public Health Ser-
of a control model of the stretch reflex was vice Grant NS-2567. The computer facilities were
compared to the experimentally obtained provided by Air Force Grant AF-AFSC-1221-67.
W. Roberts and P. Rosenthal were supported by
data. Training Grants GM-572 and NS-5494, respec-
In this mathematical model a linear ap- tively.

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