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Superposition of motor programs—II. Rapid forearm flexion in man
SUPERPOSITION OF MOTOR PROGRAMS-II. RAPID FOREARM FLEXION IN MAN A.G.
FELDMAN
Institute of Problems of Information Transmission, Academy of Sciences, Ermolova 19, 103051 Moscow, U.S.S.R. Abstract-A
man carried out a rapid change of forearm position while overcoming the resistance of a spring. The spring was suddenly switched off in some experiments either prior to or after the initiation of movement. In these cases another final position of the forearm was achieved providing that the subject had been told not to correct voluntarily the mistake. A similar effect was observed when the subject made the same movements without any external load while the spring was unexpectedly switched on in some experiments. The so-called invariant characteristics of the elbow muscles (static muscle torque versus angle) were determined. It has been found earlier that the nervous system a~omplishes movements by means of the invariant characteristics. If the slope of the invariant characteristics is known, the degree of central coactivation of antagonistic motoneurones can be estimated. Judging by the data obtained, there is considerable, although not maximal, central coactivation of antagonistic motoneurones during this type of movement. The reciprocal activation is also known to be utilized during this movement. Thus, a superposition of two central commands takes place. The functional significance, as we!! as a scheme, of the superposition are discussed. The data obtained give additional support to the hypothesis that the reciprocal and the joint central control of antagonistic motoneurones are universal commands that are used for the construction of any motor program.
EXPERIMENTAL observations have shown that there is a su~rposition of two central commands (reciprocal and joint) to antagonistic motoneurones during rhythmic forearm movements in man (FELDMAN, 1979~). It was suggested that the commands are universal, i.e. the nervous system makes use of them during any movement. In the present study this hypothesis is tested for a non-rhythmic movement, i.e. a rapid change of forearm position in man. The reciprocal activation of antagonistic motoneurones is known to occur during such movement (HUFSCHMIDT& HUFSCHMIDT,1954; TANAKA, 1974; KOTS, 1975). It remains to be shown that the central coactivation of antagonistic motoneurones also occurs during this movement. Usually, the component of the reciprocal activation dominates in the electromyograms (EMGs) of such movements as well as of rhythmical movements (LESTIENNE& BOUISSET, 1972; AIZERMAN, ANDREEVA,KANDEL& TENNENBAUM, 1974; HALLET, SHAHANI& YOUNG,f97.5) and can mask the presence of the coactivat~ng component (FELDMAN,1980). The information about the so-called invariant characteristics (ICs) of the elbow muscles makes it possible to judge the involvement of the coactivating component in the central program of the movement. The IC is a plot of elbow static moment versus angle and is determined by the method of gradual unloading of the muscles when the subject does not correct rising deflections of the arm [(ASA~YAN & FELDMAN, 1965; 19796).] The ICs have been shown to be util-
Ahhreaiations: K(s), invariant characteristic(s) muscles. EMG(s), electromyogram(s).
of 91
ized by the nervous system in order to change the posture (FELD~N, 1966b; 19791. In addition, the present data are relevant to the biomechanical basis of the active regulation of pasture (see also FELDMAN,1966b; 1979; POLIT & BIZZI, 1978). EXPERIMENTAL PROCEDURES Mechanographic analysis of rapid change of forearm position was carried out using an apparatus that permitted flexion and extension of the forearm about the elbow in the horizontal plane. The apparatus has been already described’in detail in the preceding paper (FELDMAN, 19794. It has a goniometer as well as a strain gauge, the readings of which, if the platform of the apparatus was motionless, were proportional to torque of the elbow muscles or of the load. A spring was attached by an electromagnetic lock to the apparatus. The spring was slack in the range of (p > 118”and resisted the elbow flexion beyond this range. The characteristic of the spring (torque vs elbow angle) is indicated by 3 in Fig. l(C). It coincides with the abscissa in the range of r#~> 118”. In this range the subject was free to choose any initial forearm position (&). An initial muscle torque (M,) was obviously equal to zero. The subject was told to relax the elbow muscles in these conditions. Studies were performed on four normal subjects aged from 25 to 30yr. When a short sound signal (SOms, lOOOHz, moderate volume) was switched on, the subject set rapidly without visual control an elbow angle $t (arbitrarily chosen) within the range of 80-100”. The spring resistance was overcome in this case. The experiments were done repeatedly with an interval 15-20s but in one of S-10 trials the spring was unexpectedly switched off at any phase of the movement or prior to its initiation. An electronic device was used to create a delay between the sound
92 Similar experimrms were performed in reverse order. i.c. after a period of retraining the subject carried out the same movement repeatedI!, with the arm unloaded w hue the spring was suddenly switched on in few csperiments. Change of final forearm posltion was also not to ibi: corrected in these cases.
RESULTS
80 -
FIG. 1. Estimation of the slope of the elbow invariant characteristics used during rapid forearm Rexion. (A) Forearm movements to the target angle rpi = 86.3” under spring load (1). The effects of unexpected elimination of the load either prior to the movement (2) or after its end (3) are shown:(B) Unloaded movements to the target angle #r (1. two lower traces). The effect of unexpected application of the load is shown (3). In this case the final position $, was not reached at first. Having broken the instruction ‘not to correct’. the subject corrected the deflection of the arm. For comparison, loaded movements to the target angle Cpi (1, two upper traces) as well as the effect of unexpected elimination of load (2) are shown; (C) In a plot of the muscle and load torque versus angle are shown an initial IC (0) two final KS (1 and 2) and a characteristic of the spring (3). IC 1 or 2 was utilized by the subject to set the angle 4, instead of 4, when the spring was on or off respectively. The angle Cpzwas set in cases of unexpected unloading of the arm. ~quiiibrium points a-d and i are experimental ones determined on the basis of the traces shown in (A) and (B). The IC 0 is drawn through the point i with arbitrary slope while taking into account that it is certainly less than that of the final ICs.
signal and the moment when the spring was off. While being unloaded, the forearm reached the position r& < Cp,. The subject was told not to correct the deflection. The elbow angle was recorded in the experiments. The mean values of &, fp2 and M,, where M, is a static muscle torque when Cp= 4, were determined. The data were employed for estimation of the IC used to accomplish the movement (see Results).
Figure I shows the typical results of the experiments. Two traces marked by I in (A) and two out of four marked also by 1 in (Bf were obtained in those experiments where the subject set an angle 4, = 86.3 + 1.2’ (SD.) while overcoming the spring resistance. The traces marked by 2 in (A) and (B) shows the effect of disconnection of the spring made simultaneously with the signal to the movement, The forearm can be seen to achieve another position, & = 72.0 i 1.5 The deflection is equal to 14.3”. being much greater than occasional variations of 4, in previous experiments. In accordance with the instruction, the subject did not correct the deflection. The same final position of the forearm ~4~) was reached whether the spring was switched off during the movement. prior to its initiation or soon after its end (P < 0.05). In particular, a trace marked by 3 in (A) shows the effect of the unloading when the angle 41 has been achieved. The arm can be seen to pass from +1 to f&. In the reverse series of the experiments, the subject having retrained set the same angle 4, when the arm was unloaded, i.e. the spring was switched off in each trial simultaneously with signal to the movement. Two out of four traces marked by I in Fig. l(B) were obtained in these trials. A trace marked by 3 in (B) shows the effect of unexpected loading of the forearm (the spring was not switched off). It can be seen that the position (p, was not reached at first. In spite of the instruction, the subject corrected the deflection by secondary movement, The data obtained allow one to estimate the ICs used by the nervous system to set the angle 4, when the arm was either loaded or unloaded. Note that 4, = 86.3’ when M, = 6.3 Nm, where M, is static muscle torque determined from the spring characteristic marked by 3 in Fig. I(C). A point a = f#, , Ml) is one of the points of the IC. When the spring was switched off, the angle I& = 72.0’ was reached. Evidently. the finat muscIe torque was equal to zero in this case. So, h = (&. 0) is another point of the same IC. The IC is denoted by 1 in Fig. l(C). Similariy. one can find the IC used in the reverse series of the experiments [a Iine denoted by 2 in Fig. l(C)]. Let us compare these ICs with those obtained under static tension of the elbow flexors and extensors in the same subject and shown in Fig. 3 of the preceding paper (FELDMAN, 1980). It should be borne in mind that the ICs of the family in (A) were recorded when either flexors or extensors of the elbow were active. The flexor ICs are situated above the dashed
Control of rapid change of posture
FIG. 2. Electromyograms of triceps and biceps brachii muscles (tric, bit) and the elbow angle (4) during rapid elbow flexion (the upper traces) and extension (below).
line and the extensors ones are below. The ICs of the family in (B) were recorded against the background of maximal tonic coactivation of the antagonistic muscles. There could well be other families of the ICs corresponding to any intermediate between zero and maximal degree of the coactivation (FELDMAN,1980). The slope of the ICs marked by 1 and 2 in Fig. l(C) is essentially greater than that of the ICs in Fig. 3(A) of the preceding paper. Hence it follows that a strong coactivation of the antagonistic motoneurones was accomplished during a rapid change of posture. However, the coactivation was not yet maximal because the slope of lines 1 and 2 in Fig. l(C) was approximately half as great as that of the ICs in Fig. 3(B) of previous paper. In some cases, indication of the coactivation of antagonistic muscle during a rapid change of the posture could probably be revealed in the EMGs as well. For instance, Fig. 2 shows the surface EMGs of the biceps and triceps brachii muscles and the elbow angle during rapid forearm flexion (upper traces) or extension (lower). The movements were carried out without any load, in a horizontal plane but, for some non-scientific reasons, outside the apparatus. In this case the conditions of the movements were not quite identical to the previous ones, mainly due to the absence of the inertia of the movable platform. One can see that the reciprocal activation of the antagonistic muscles is dominant in a dynamic phase of the movement. It does not mean that a coactivating component is absent in that phase at all but that there is no possibility to detect it reliably. However, when the movement is coming to an end the coactivating component in EMGs dominates. DISCUSSION The present data confirm the hypothesis that the central tonic coactivation of flexor and extensor motoneurones is performed during rapid forearm flexion. The data obtained allow one to judge both the biomechanical basis of active change of the forearm position and the components of the central motor program. The first problem has been already discussed (ASATRYAN& FELDMAN,1965; FELDMAN 1966a,b; 1974; 1980; BIZZI, POLIT8~ MORASS~,1976;POLIT&
93
BIZZI, 1978), in particular, in connection with analogous experimental data (FELDMAN,1966b; BIZZI et al., 1976). So, the first problem will be considered in so far as it is necessary for the discussion of the second one. The static position of the muscle-load system is reached at the so-called equilibrium point (FELDMAN, 1974), i.e. at the point where the IC and load characteristic intersect. In the experiments described above two load characteristics were used, one of which, corresponding to zero load, coincided with the abscissa in Fig. l(C) and another was the spring characteristic [a curve denoted by 3 in Fig. l(C)]. To reach the angle 41, the subject set the IC either 1 or 2 depending on whether the arm was loaded or unloaded in the final position. Every IC has two points of intersection with the load lines, thus, on the whole, there are four equilibrium points [a-d in Fig. l(C)]. Each of the points is a final one, i.e. that which is achieved simultaneously with the end of the movement. However, there is an initial equilibrium point that defines the conditions before the movement. This is the point denoted by i with coordinates 4 = &, and M = 0 [Fig. l(C)]. The initial IC is considered to pass the point. The IC is denoated by 0 in Fig. l(C). The course of the IC 0 was not estimated in this study. But, for the present discussion it is essential only that the slope of the initial IC is certainly less than that of any final IC because the initial IC is a characteristic of the elbow muscles almost (if not completely) relaxed at 4 = #,, (see Experimental Procedures) whereas the final IC is a characteristic of the muscles coactivated to a marked degree (see Results). An active change of elbow angle could be considered as a consequence of the substitution of the initial IC for the respective final IC (FELDMAN,1966b). For instance, to set the position +1 while overcoming the spring resistance, the subject substituted the initial IC for the final characteristic 1 [Fig. l(C)]. As a result, the initial point (i) became non-equilibrium and the forearm was forced to come to a new equilibrium point (a). When in some experiments the spring was switched off, the point a became also non-equilibrium and the forearm was forced to move to a new equilibrium point (b) while setting the angle & # 41. The biomechanics of the movement in those cases when the subject set the angle 4, under zero load can be described in the same way. Certainly, the velocity and other dynamic transfer characteristics of the process have to depend on the dynamics of the establishment of the final IC as well
as on the dynamic properties of the stretch reflex. It should be emphasized, however, that the final forearm position does not prove to be dependent on the dynamic characteristics of the system at all (FELDMAN, 19666; 1979; BIZZI et al., 1976). So the main part of the central program of the movement seems to be reduced to a quick establishment of the final IC, i.e. of certain tension-extension characteristics of the tonic stretch reflex for every elbow muscle.
A. c;.
I
160‘
FIG. 3. Transformation of the initial invariant characteristic (denoted by 0) into the final one (denoted by I) by means of a combination of the reciprocal and joint central influences on the antagonistic motoneurones. Abscissa: elbow angle. Ordinate: active muscle torque. Dashed lines: ICs of the flexors (F) and extensors (E). Continuous lines: total KS. (A) Parallel shift of the total IC (O-+0’) accomplished by an equivalent decrease of the tonic stretch reflex thresholds (/3: - pk. i; = I. 2). (B) Increase of the sope of the total IC (0’4 1) by means of a reciprocal change of the thresholds (/?; -+ Pk. li = I. 2). The ICs denoted by 0 and I are close to the respective ICs in Fig. l(C).
The data described in the preceding report (FELIJhave shown that the position and shape of the final IC are determined by the parameters /&, where k = 1 for the elbow flexors and k = 2 for extensors. The Bk is a threshold angle at which the tonic activation of the respective muscles begins. It should be borne in mind that the elbow flexors are active if 4 > p, while the extensors are active if 4 < /j$. Hence it follows that the unidirectional change of both the parameters /?, and /I2 means the reciprocal change of activity of the antagonistic muscles and vice versa. The nervous system seems to use past experience to choose, presumably in advance of the movement, the necessary final meanings of /?, and f12. How can the nervous system combine the central commands of the reciprocal and joint activation of the antagonistic motoneurones to set the meanings? To answer the question, it should be noted that the initial IC marked by 0 in Fig. l(C) can be shifted along the abscissa so that the new characteristic (0’) will turn out to be
t’iLI)hIA\
~lp~rt~xin~~~leiyin the ~~~)sitl~)l~ ctccupied by the final IC‘ marked h> i in Fig. l(C). The transform;iti~~n can bc accomplished h! an equivalent decrease of both parameters from ,$ to /& I\ ~7 1. 2 [Fig. 3(A)] due to the reciprocal central influences on the antagonistic motoneurones. Besides. the slopr: of the new characttristic (0’) can be increased right up to the firnit. coinciding with the tinal characteristic 1 (F-i&. 3(Bj). h! ;t change of the parameters from /j; to & due to the joint central influences on the antagonistic motoncurones. Thus. the superposition of two central commands can lead to the transformation of the initial IC into the final one. Tho possibility of the superposition of the central commands can be also explained by using their vector symbols. To accomplish this, the area of the normalized meanings (n, and j7?) of the respecticc parameters should be considered (see also FI:LDMAN. 1979n). The area is a square (Fig. 4). The points p and cf symbolize the initial and final combinations of the parameters. A vector prj symbolizes the central program of rapid change of posture. The projections of the vector on the diagonals of the square p,> and pi represent the central programs of pure reciprocal and coactivating influences correspondingly. The data available do not allow one to judge whether two central programs are accomplished simultaneously or in series, However. the fulfilment of the programs strictly in series does not seem to be expedient. For instance, if the program of the coactivation develops at first, the forearm is rigidly fixed in the initial position. i.e. the subseyuent program of the reciprocal activation proceeds against the background
I
MAN, 1979~)
P,
0
B, FIG. 4. Vector representation of the motor programs. The square is an area of the normalized meanings of the parameters PI and pz designating the tonic stretch reflex thresholds of the elbow flexors and extensors, respectively. Initial (p) and final (q) combinations of their meanings are
shown. The vector pq symbolizes the central program of the rapid change of the forearm position. Projections of the vector, ps and pr, symbolize the programs of the pure reciprocal
and
joint
influences motoneurones.
on
the
antagonistic
Control of rapid change of posture of large resistance.
If these programs develop in reverse order the final equilibrium position is achieved after a marked overshoot because the program of the coactivation extinguishing velocity due to
9s
stiffness of the muscles is switched on too late. Therefore, it would be useful if both the programs were carried out with a very short delay if not simultaneously. increasing
REFERENCES AIZERMAN M. A.. ANDREEVA E. A., KANDELE. I. & TEHNENBAUM L. A. (1974)Mechanisms o/the Control of Musclr Actkit? (Morm and Fathobg_y). Publ. House ‘Nauka*, Moscow. (In Russian.) ASATRYAND. G. & FELDMANA. G. (1965) Functional tuning of the nervous system with control of movement or maintenance of a steady posture--I. Mechanographic anatysis of the work of the joint on execution of a postural task. Biophysics
10. 925-935.
B~zzt E.. POL~TA. & M~RAW P. f 1976) Mechanisms underlying achievement of tinal head position. J. /V~,t~rop~~sjo~. 39, 435 444. FELDMANA. G. (1966~) Functional tuning of the nervous system during control of movement or maintenance of a steady posture-II. Controllable parameters of the muscle. Biophysics 1 I, 565-578. FELDMANA. G. (1966h) Functional tuning of the nervous system during control of movement or maintenance of a stead} posture--III. Mechanographic analysis of the execution by man of a simplest motor tasks. Biophysics II. 76G.775. FELDMANA. G. (1974) Control of the length of the muscle. Biophysics 19, 760-771. FELDMANA. G. (1979) Central and Refkx Mechanisms in t/u> Control o/Movements. Pub]. House ‘Nauka‘. Moscow. (In Russian.) FELDMAKA. G. (1980) Superposition of motor programs--f. Rhythmic ,forearm mnrements in morn. R’c~ltrosc.ic~tl1.e 5, 81-90. HALLETM.. SHAHANIE. T. & YOUNGR. R. (1975) EMG analysis of stereotyped voiuntary movements in man. J. Xt~oi. Neurusurg. Psychiut. 38, t 154. f 162. HUFSCHWX H. 3. & HL.F.WHMIDT T. (1954) Antagonist inhibition as the earliest sign of a sensory-motor reaction. Sarure, Land. 174, W-61 9. KOTS Y. M. (1975) Organization 01 Volunr~r~ Mooemenr. Publ. House ‘Nauka’. Moscow. (In Russian.) LEST~ENNE F. & BOUIWT S. (1972) Role played by the antagonist in the control of a voluntary movement. Symposia! pupers of the Fowrh International Biophysics Congress, Moscow. POLITA. & BWZIE. (1978)Processes controlling arm movements in monkeys. Science. h’.Y. 201, 1235 1237. TANAKAR. (1974) Reciprocal Ia inhibition during voluntary movements in man. Espl Bruin Res. 21. 529-540.
(Accepted 21
May
1979)
FELDMAN
Institute of Problems of Information Transmission, Academy of Sciences, Ermolova 19, 103051 Moscow, U.S.S.R. Abstract-A
man carried out a rapid change of forearm position while overcoming the resistance of a spring. The spring was suddenly switched off in some experiments either prior to or after the initiation of movement. In these cases another final position of the forearm was achieved providing that the subject had been told not to correct voluntarily the mistake. A similar effect was observed when the subject made the same movements without any external load while the spring was unexpectedly switched on in some experiments. The so-called invariant characteristics of the elbow muscles (static muscle torque versus angle) were determined. It has been found earlier that the nervous system a~omplishes movements by means of the invariant characteristics. If the slope of the invariant characteristics is known, the degree of central coactivation of antagonistic motoneurones can be estimated. Judging by the data obtained, there is considerable, although not maximal, central coactivation of antagonistic motoneurones during this type of movement. The reciprocal activation is also known to be utilized during this movement. Thus, a superposition of two central commands takes place. The functional significance, as we!! as a scheme, of the superposition are discussed. The data obtained give additional support to the hypothesis that the reciprocal and the joint central control of antagonistic motoneurones are universal commands that are used for the construction of any motor program.
EXPERIMENTAL observations have shown that there is a su~rposition of two central commands (reciprocal and joint) to antagonistic motoneurones during rhythmic forearm movements in man (FELDMAN, 1979~). It was suggested that the commands are universal, i.e. the nervous system makes use of them during any movement. In the present study this hypothesis is tested for a non-rhythmic movement, i.e. a rapid change of forearm position in man. The reciprocal activation of antagonistic motoneurones is known to occur during such movement (HUFSCHMIDT& HUFSCHMIDT,1954; TANAKA, 1974; KOTS, 1975). It remains to be shown that the central coactivation of antagonistic motoneurones also occurs during this movement. Usually, the component of the reciprocal activation dominates in the electromyograms (EMGs) of such movements as well as of rhythmical movements (LESTIENNE& BOUISSET, 1972; AIZERMAN, ANDREEVA,KANDEL& TENNENBAUM, 1974; HALLET, SHAHANI& YOUNG,f97.5) and can mask the presence of the coactivat~ng component (FELDMAN,1980). The information about the so-called invariant characteristics (ICs) of the elbow muscles makes it possible to judge the involvement of the coactivating component in the central program of the movement. The IC is a plot of elbow static moment versus angle and is determined by the method of gradual unloading of the muscles when the subject does not correct rising deflections of the arm [(ASA~YAN & FELDMAN, 1965; 19796).] The ICs have been shown to be util-
Ahhreaiations: K(s), invariant characteristic(s) muscles. EMG(s), electromyogram(s).
of 91
ized by the nervous system in order to change the posture (FELD~N, 1966b; 19791. In addition, the present data are relevant to the biomechanical basis of the active regulation of pasture (see also FELDMAN,1966b; 1979; POLIT & BIZZI, 1978). EXPERIMENTAL PROCEDURES Mechanographic analysis of rapid change of forearm position was carried out using an apparatus that permitted flexion and extension of the forearm about the elbow in the horizontal plane. The apparatus has been already described’in detail in the preceding paper (FELDMAN, 19794. It has a goniometer as well as a strain gauge, the readings of which, if the platform of the apparatus was motionless, were proportional to torque of the elbow muscles or of the load. A spring was attached by an electromagnetic lock to the apparatus. The spring was slack in the range of (p > 118”and resisted the elbow flexion beyond this range. The characteristic of the spring (torque vs elbow angle) is indicated by 3 in Fig. l(C). It coincides with the abscissa in the range of r#~> 118”. In this range the subject was free to choose any initial forearm position (&). An initial muscle torque (M,) was obviously equal to zero. The subject was told to relax the elbow muscles in these conditions. Studies were performed on four normal subjects aged from 25 to 30yr. When a short sound signal (SOms, lOOOHz, moderate volume) was switched on, the subject set rapidly without visual control an elbow angle $t (arbitrarily chosen) within the range of 80-100”. The spring resistance was overcome in this case. The experiments were done repeatedly with an interval 15-20s but in one of S-10 trials the spring was unexpectedly switched off at any phase of the movement or prior to its initiation. An electronic device was used to create a delay between the sound
92 Similar experimrms were performed in reverse order. i.c. after a period of retraining the subject carried out the same movement repeatedI!, with the arm unloaded w hue the spring was suddenly switched on in few csperiments. Change of final forearm posltion was also not to ibi: corrected in these cases.
RESULTS
80 -
FIG. 1. Estimation of the slope of the elbow invariant characteristics used during rapid forearm Rexion. (A) Forearm movements to the target angle rpi = 86.3” under spring load (1). The effects of unexpected elimination of the load either prior to the movement (2) or after its end (3) are shown:(B) Unloaded movements to the target angle #r (1. two lower traces). The effect of unexpected application of the load is shown (3). In this case the final position $, was not reached at first. Having broken the instruction ‘not to correct’. the subject corrected the deflection of the arm. For comparison, loaded movements to the target angle Cpi (1, two upper traces) as well as the effect of unexpected elimination of load (2) are shown; (C) In a plot of the muscle and load torque versus angle are shown an initial IC (0) two final KS (1 and 2) and a characteristic of the spring (3). IC 1 or 2 was utilized by the subject to set the angle 4, instead of 4, when the spring was on or off respectively. The angle Cpzwas set in cases of unexpected unloading of the arm. ~quiiibrium points a-d and i are experimental ones determined on the basis of the traces shown in (A) and (B). The IC 0 is drawn through the point i with arbitrary slope while taking into account that it is certainly less than that of the final ICs.
signal and the moment when the spring was off. While being unloaded, the forearm reached the position r& < Cp,. The subject was told not to correct the deflection. The elbow angle was recorded in the experiments. The mean values of &, fp2 and M,, where M, is a static muscle torque when Cp= 4, were determined. The data were employed for estimation of the IC used to accomplish the movement (see Results).
Figure I shows the typical results of the experiments. Two traces marked by I in (A) and two out of four marked also by 1 in (Bf were obtained in those experiments where the subject set an angle 4, = 86.3 + 1.2’ (SD.) while overcoming the spring resistance. The traces marked by 2 in (A) and (B) shows the effect of disconnection of the spring made simultaneously with the signal to the movement, The forearm can be seen to achieve another position, & = 72.0 i 1.5 The deflection is equal to 14.3”. being much greater than occasional variations of 4, in previous experiments. In accordance with the instruction, the subject did not correct the deflection. The same final position of the forearm ~4~) was reached whether the spring was switched off during the movement. prior to its initiation or soon after its end (P < 0.05). In particular, a trace marked by 3 in (A) shows the effect of the unloading when the angle 41 has been achieved. The arm can be seen to pass from +1 to f&. In the reverse series of the experiments, the subject having retrained set the same angle 4, when the arm was unloaded, i.e. the spring was switched off in each trial simultaneously with signal to the movement. Two out of four traces marked by I in Fig. l(B) were obtained in these trials. A trace marked by 3 in (B) shows the effect of unexpected loading of the forearm (the spring was not switched off). It can be seen that the position (p, was not reached at first. In spite of the instruction, the subject corrected the deflection by secondary movement, The data obtained allow one to estimate the ICs used by the nervous system to set the angle 4, when the arm was either loaded or unloaded. Note that 4, = 86.3’ when M, = 6.3 Nm, where M, is static muscle torque determined from the spring characteristic marked by 3 in Fig. I(C). A point a = f#, , Ml) is one of the points of the IC. When the spring was switched off, the angle I& = 72.0’ was reached. Evidently. the finat muscIe torque was equal to zero in this case. So, h = (&. 0) is another point of the same IC. The IC is denoted by 1 in Fig. l(C). Similariy. one can find the IC used in the reverse series of the experiments [a Iine denoted by 2 in Fig. l(C)]. Let us compare these ICs with those obtained under static tension of the elbow flexors and extensors in the same subject and shown in Fig. 3 of the preceding paper (FELDMAN, 1980). It should be borne in mind that the ICs of the family in (A) were recorded when either flexors or extensors of the elbow were active. The flexor ICs are situated above the dashed
Control of rapid change of posture
FIG. 2. Electromyograms of triceps and biceps brachii muscles (tric, bit) and the elbow angle (4) during rapid elbow flexion (the upper traces) and extension (below).
line and the extensors ones are below. The ICs of the family in (B) were recorded against the background of maximal tonic coactivation of the antagonistic muscles. There could well be other families of the ICs corresponding to any intermediate between zero and maximal degree of the coactivation (FELDMAN,1980). The slope of the ICs marked by 1 and 2 in Fig. l(C) is essentially greater than that of the ICs in Fig. 3(A) of the preceding paper. Hence it follows that a strong coactivation of the antagonistic motoneurones was accomplished during a rapid change of posture. However, the coactivation was not yet maximal because the slope of lines 1 and 2 in Fig. l(C) was approximately half as great as that of the ICs in Fig. 3(B) of previous paper. In some cases, indication of the coactivation of antagonistic muscle during a rapid change of the posture could probably be revealed in the EMGs as well. For instance, Fig. 2 shows the surface EMGs of the biceps and triceps brachii muscles and the elbow angle during rapid forearm flexion (upper traces) or extension (lower). The movements were carried out without any load, in a horizontal plane but, for some non-scientific reasons, outside the apparatus. In this case the conditions of the movements were not quite identical to the previous ones, mainly due to the absence of the inertia of the movable platform. One can see that the reciprocal activation of the antagonistic muscles is dominant in a dynamic phase of the movement. It does not mean that a coactivating component is absent in that phase at all but that there is no possibility to detect it reliably. However, when the movement is coming to an end the coactivating component in EMGs dominates. DISCUSSION The present data confirm the hypothesis that the central tonic coactivation of flexor and extensor motoneurones is performed during rapid forearm flexion. The data obtained allow one to judge both the biomechanical basis of active change of the forearm position and the components of the central motor program. The first problem has been already discussed (ASATRYAN& FELDMAN,1965; FELDMAN 1966a,b; 1974; 1980; BIZZI, POLIT8~ MORASS~,1976;POLIT&
93
BIZZI, 1978), in particular, in connection with analogous experimental data (FELDMAN,1966b; BIZZI et al., 1976). So, the first problem will be considered in so far as it is necessary for the discussion of the second one. The static position of the muscle-load system is reached at the so-called equilibrium point (FELDMAN, 1974), i.e. at the point where the IC and load characteristic intersect. In the experiments described above two load characteristics were used, one of which, corresponding to zero load, coincided with the abscissa in Fig. l(C) and another was the spring characteristic [a curve denoted by 3 in Fig. l(C)]. To reach the angle 41, the subject set the IC either 1 or 2 depending on whether the arm was loaded or unloaded in the final position. Every IC has two points of intersection with the load lines, thus, on the whole, there are four equilibrium points [a-d in Fig. l(C)]. Each of the points is a final one, i.e. that which is achieved simultaneously with the end of the movement. However, there is an initial equilibrium point that defines the conditions before the movement. This is the point denoted by i with coordinates 4 = &, and M = 0 [Fig. l(C)]. The initial IC is considered to pass the point. The IC is denoated by 0 in Fig. l(C). The course of the IC 0 was not estimated in this study. But, for the present discussion it is essential only that the slope of the initial IC is certainly less than that of any final IC because the initial IC is a characteristic of the elbow muscles almost (if not completely) relaxed at 4 = #,, (see Experimental Procedures) whereas the final IC is a characteristic of the muscles coactivated to a marked degree (see Results). An active change of elbow angle could be considered as a consequence of the substitution of the initial IC for the respective final IC (FELDMAN,1966b). For instance, to set the position +1 while overcoming the spring resistance, the subject substituted the initial IC for the final characteristic 1 [Fig. l(C)]. As a result, the initial point (i) became non-equilibrium and the forearm was forced to come to a new equilibrium point (a). When in some experiments the spring was switched off, the point a became also non-equilibrium and the forearm was forced to move to a new equilibrium point (b) while setting the angle & # 41. The biomechanics of the movement in those cases when the subject set the angle 4, under zero load can be described in the same way. Certainly, the velocity and other dynamic transfer characteristics of the process have to depend on the dynamics of the establishment of the final IC as well
as on the dynamic properties of the stretch reflex. It should be emphasized, however, that the final forearm position does not prove to be dependent on the dynamic characteristics of the system at all (FELDMAN, 19666; 1979; BIZZI et al., 1976). So the main part of the central program of the movement seems to be reduced to a quick establishment of the final IC, i.e. of certain tension-extension characteristics of the tonic stretch reflex for every elbow muscle.
A. c;.
I
160‘
FIG. 3. Transformation of the initial invariant characteristic (denoted by 0) into the final one (denoted by I) by means of a combination of the reciprocal and joint central influences on the antagonistic motoneurones. Abscissa: elbow angle. Ordinate: active muscle torque. Dashed lines: ICs of the flexors (F) and extensors (E). Continuous lines: total KS. (A) Parallel shift of the total IC (O-+0’) accomplished by an equivalent decrease of the tonic stretch reflex thresholds (/3: - pk. i; = I. 2). (B) Increase of the sope of the total IC (0’4 1) by means of a reciprocal change of the thresholds (/?; -+ Pk. li = I. 2). The ICs denoted by 0 and I are close to the respective ICs in Fig. l(C).
The data described in the preceding report (FELIJhave shown that the position and shape of the final IC are determined by the parameters /&, where k = 1 for the elbow flexors and k = 2 for extensors. The Bk is a threshold angle at which the tonic activation of the respective muscles begins. It should be borne in mind that the elbow flexors are active if 4 > p, while the extensors are active if 4 < /j$. Hence it follows that the unidirectional change of both the parameters /?, and /I2 means the reciprocal change of activity of the antagonistic muscles and vice versa. The nervous system seems to use past experience to choose, presumably in advance of the movement, the necessary final meanings of /?, and f12. How can the nervous system combine the central commands of the reciprocal and joint activation of the antagonistic motoneurones to set the meanings? To answer the question, it should be noted that the initial IC marked by 0 in Fig. l(C) can be shifted along the abscissa so that the new characteristic (0’) will turn out to be
t’iLI)hIA\
~lp~rt~xin~~~leiyin the ~~~)sitl~)l~ ctccupied by the final IC‘ marked h> i in Fig. l(C). The transform;iti~~n can bc accomplished h! an equivalent decrease of both parameters from ,$ to /& I\ ~7 1. 2 [Fig. 3(A)] due to the reciprocal central influences on the antagonistic motoneurones. Besides. the slopr: of the new characttristic (0’) can be increased right up to the firnit. coinciding with the tinal characteristic 1 (F-i&. 3(Bj). h! ;t change of the parameters from /j; to & due to the joint central influences on the antagonistic motoncurones. Thus. the superposition of two central commands can lead to the transformation of the initial IC into the final one. Tho possibility of the superposition of the central commands can be also explained by using their vector symbols. To accomplish this, the area of the normalized meanings (n, and j7?) of the respecticc parameters should be considered (see also FI:LDMAN. 1979n). The area is a square (Fig. 4). The points p and cf symbolize the initial and final combinations of the parameters. A vector prj symbolizes the central program of rapid change of posture. The projections of the vector on the diagonals of the square p,> and pi represent the central programs of pure reciprocal and coactivating influences correspondingly. The data available do not allow one to judge whether two central programs are accomplished simultaneously or in series, However. the fulfilment of the programs strictly in series does not seem to be expedient. For instance, if the program of the coactivation develops at first, the forearm is rigidly fixed in the initial position. i.e. the subseyuent program of the reciprocal activation proceeds against the background
I
MAN, 1979~)
P,
0
B, FIG. 4. Vector representation of the motor programs. The square is an area of the normalized meanings of the parameters PI and pz designating the tonic stretch reflex thresholds of the elbow flexors and extensors, respectively. Initial (p) and final (q) combinations of their meanings are
shown. The vector pq symbolizes the central program of the rapid change of the forearm position. Projections of the vector, ps and pr, symbolize the programs of the pure reciprocal
and
joint
influences motoneurones.
on
the
antagonistic
Control of rapid change of posture of large resistance.
If these programs develop in reverse order the final equilibrium position is achieved after a marked overshoot because the program of the coactivation extinguishing velocity due to
9s
stiffness of the muscles is switched on too late. Therefore, it would be useful if both the programs were carried out with a very short delay if not simultaneously. increasing
REFERENCES AIZERMAN M. A.. ANDREEVA E. A., KANDELE. I. & TEHNENBAUM L. A. (1974)Mechanisms o/the Control of Musclr Actkit? (Morm and Fathobg_y). Publ. House ‘Nauka*, Moscow. (In Russian.) ASATRYAND. G. & FELDMANA. G. (1965) Functional tuning of the nervous system with control of movement or maintenance of a steady posture--I. Mechanographic anatysis of the work of the joint on execution of a postural task. Biophysics
10. 925-935.
B~zzt E.. POL~TA. & M~RAW P. f 1976) Mechanisms underlying achievement of tinal head position. J. /V~,t~rop~~sjo~. 39, 435 444. FELDMANA. G. (1966~) Functional tuning of the nervous system during control of movement or maintenance of a steady posture-II. Controllable parameters of the muscle. Biophysics 1 I, 565-578. FELDMANA. G. (1966h) Functional tuning of the nervous system during control of movement or maintenance of a stead} posture--III. Mechanographic analysis of the execution by man of a simplest motor tasks. Biophysics II. 76G.775. FELDMANA. G. (1974) Control of the length of the muscle. Biophysics 19, 760-771. FELDMANA. G. (1979) Central and Refkx Mechanisms in t/u> Control o/Movements. Pub]. House ‘Nauka‘. Moscow. (In Russian.) FELDMAKA. G. (1980) Superposition of motor programs--f. Rhythmic ,forearm mnrements in morn. R’c~ltrosc.ic~tl1.e 5, 81-90. HALLETM.. SHAHANIE. T. & YOUNGR. R. (1975) EMG analysis of stereotyped voiuntary movements in man. J. Xt~oi. Neurusurg. Psychiut. 38, t 154. f 162. HUFSCHWX H. 3. & HL.F.WHMIDT T. (1954) Antagonist inhibition as the earliest sign of a sensory-motor reaction. Sarure, Land. 174, W-61 9. KOTS Y. M. (1975) Organization 01 Volunr~r~ Mooemenr. Publ. House ‘Nauka’. Moscow. (In Russian.) LEST~ENNE F. & BOUIWT S. (1972) Role played by the antagonist in the control of a voluntary movement. Symposia! pupers of the Fowrh International Biophysics Congress, Moscow. POLITA. & BWZIE. (1978)Processes controlling arm movements in monkeys. Science. h’.Y. 201, 1235 1237. TANAKAR. (1974) Reciprocal Ia inhibition during voluntary movements in man. Espl Bruin Res. 21. 529-540.
(Accepted 21
May
1979)