Brain Research, 132 (1977) 153-158 © Elsevier/North-Holland Biomedical Press
153
The influence of Group II muscle afferents and low threshold skin afferents on dynamic fusimotor neurones to the triceps surae of the cat
B. APPELBERG, H. JOHANSSON and G. KALISTRATOV* Department of Physiology, University of Umed, S-901 87 Umed (Sweden)
(Accepted May l lth, 1977)
Eccles and Lundberg 5 studied synaptic actions in motoneurones evoked by Group II and Group III muscle and cutaneous afferents. Closely similar actions by the three different types of fibres were revealed and Group II afferents as well as all cutaneous afferents have since come to be included in the flexor reflex afferent (FRA) concept. The majority of Group II afferents in the nerve from the triceps surae seem to be secondary muscle spindle afferentsa, 15, and so these afferents from a highly sophisticated sense organ came to be looked upon as merely subserving the flexor reflex. Matthews 25 heavily criticized this view and Lundberg in recent reviews 1a,19 stated that though, according to his opinion, Group II afferents are part of the FRA, this does not exclude the possibility that these afferents may also have other reflex lines. Indirect evidence to this effect was obtained 21,22 when it was shown that effects from Group II afferents from the extensor digitorum brevis nerve conforming to the FRA-pattern were indeed caused mainly by afferents of non-spindle origin. Furthermore, the use of a new method recently indicated monosynaptic actions from spindle secondary afferents on motoneurones16,17. Such a finding, recently confirmed 28,27, does not seem compatible with a view on the secondary spindle afferents as merely being part of the FRA. That low threshold skin afferents do not exclusively belong to the FRA is more clear. Such afferents from the plantar surface of the foot do, for instance, evoke plantar reflexes6. Strong arguments for the existence of other special reflex pathways for low threshold cutaneous afferents have been given 2A2,18. Interneurones activated from very low threshold cutaneous afferents were then actually found 13. Very recently also 2° such afferents have been shown to converge to the Ib pathway to motoneurones. It is clear from what has been said above that our knowledge concerning the functional role of Group II muscle and low threshold skin afferents is still meager. The findings to be presented below will further strengthen the notion that pathways separate from the FRA ones do exist from the two types of afferents in question. It is made likely that secondary afferents from muscle spindles project to dynamic ~-
* Current address: Biruzov str. 43-164, Moscow, 123060, U.S.S.R.
154 motoneurones. The functional implications of such an organization will be discussed. The results to be described were obtained within the framework of a long series of experiments aimed at studies of reflex pathways to ;v-motoneurones. The experiments were performed on cats anaesthetized with chloralose (60 mg/kg) and paralyzed with Flaxedil. The preparation was similar to the one recently describedL The technique of distinguishing between static and dymamic y-motoneurones with the aid of central stimulation within a certain area of the mid-brain (the MesADC-region, known to selectively influence muscle spindle dynamic sensitivity 1) was utilized also in the present experiments. All roots were left intact, and a variety of hind limb nerves were dissected and mounted for stimulation. The following abbreviations will be used : ABSm, anterior biceps-semimembranosus; EPSP, excitatory postsynaptic potential; FRA, flexor reflex afferents, GS, gastrocnemius-soleus (.triceps surae); IPSP, inhibitory postsynaptic potential: MesADC, mesencephalic area controlling dynamic spindle sensitivity; NR, nucleus ruber; PBSt, posterior biceps-semitendinosus; Q, quadriceps; SP, superficial peroneal ; Su, sural; T, threshold for detectable incoming volley in L7 dorsal root entry zone. So far, 18 triceps surae cells have been studied. Twelve of these cells were classified as dynamic, the others as static. As judged by the stimulating strength used and the resulting volley recorded in the dorsal root entry zone, Group III effects were seen in all these cells, excitatory (9 cells) or inhibitory (9 cells). Among the Group III inhibited cells, 8 were of the dynamic type. Group III excitations was thus seen in only 4 dynamic cells, while it was seen in all but one of the cells classified as static. Within the population of cells classified as dynamic and receiving Group II1 inhibition (8 cells), Group H muscle afferents caused excitation in 4 cells'. This was revealed by intracellularly recorded PSPs. In two cells, inhibition was seen instead in the form of a pause in the spontaneous extracellularly recorded discharge of these cells. In one intracellularly recorded cell Group II PSPs were not observed, but instead this cell received a clearcut Group I excitation at monosynaptic latency from its own nerve. The last cell within this group was so badly damaged by the intracellular electrode that Group II effects could not be seen. Typically also, dynamic cells received low threshold excitation from at least one of the three cutaneous nerves used (Su, SP and Tib) although stronger stimuli of cutaneous nerves also usually brought about inhibitory effects. The pattern of effects evoked by Group lI muscle and by cutaneous nerve stimulation is illustrated in Fig. 1. The cell is identified in Fig. 1A by being antidromically invaded from its own nerve. A long train of impulses at 600 Hz in the red nucleus inhibited the cell (Fig. 1B), while, on the other hand, a weak and slowly rising excitation was evoked from the MesADC (Fig. 1C). This together with the observation of MesADC driving of the celt while the electrode was still in a juxtacellular position (Fig. 1D) classified the cell as a dynamic y-motoneurone of the triceps surae. In Fig. I E-H, different muscle nerves were stimulated at 5T. Note that the GS stimulus evoked a late IPSP in the cell. This was correlated to a weak Group llI volley in the dorsal root recording (Fig. I E). Stimulation of all the muscle nerves caused initial EPSPs which, according to the analysis at faster sweep speed in Fig. 1, records
155
A
asY
B
NR
C
.,,ADC
D
E
Gs 5
F
PBSt s
G
0 s
H
A.S~5
K
cs5
L
PBSt 5
M
0 s
N
sP5
O
Su~.=
p
Gs2
R
pest2
S
Q2
T
sP2
U
Sul.~
,
I
Su 2
•
Fig. 1. Intracellular recording from dynamic GS 7-cell. A: antidromic identification; B: stimulation of NR at 600 Hz, 60/~A during time indicated by horizontal bar; C: stimulation of MesADC at 600 Hz, 70 pA; D: as C but slower sweep speed and obtained just before penetration; E-U: stimulation of peripheral nerves as indicated. Figures indicate stimulating strengths in multiples of threshold. Upper records in E-U obtained from dorsal root entry. Lower records in E-H and P-U are extracellular recordings obtained at 50 T. In all records positivity is signalled upwards. Horizontal calibration bar is 4 msec in A and I-U, 10 msec in B, C and E-H, and 20 msec in D. Vertical calibration bar is 20 mV in A, 10 mV in D, and 4 mV in B, C and E-U.
K - M and P-S, had in all cases a central latency close to 2 msec. The threshold for their appearance was a r o u n d 2T f r o m GS, PBSt and Q, slightly higher f r o m A B S m (not illustrated) and they were thus likely to be caused by G r o u p II afferents. The late inhibition evoked f r o m the quadriceps nerve (Fig. 1G, M and S) is likely to be a G r o u p Ib effect, since it had a lower threshold than the excitatory effect, and thus tended to override the G r o u p II excitation at 2T (Fig. IS). A strong inhibition, which is p r o b a b l y a F R A effect, was evoked from the SP nerve at 5T (Fig. IN). The threshold for this effect was just below 2T (Fig. IT). On the other h a n d the Su nerve, t h o u g h also causing some late inhibition a r o u n d and above 2T (Fig. 1I), in addition excited the cell at low stimulating strength (Fig. 10). Even at 1.1T in Fig. 1U, a single liminal E P S P may be observed. The central latency of this low threshold cutaneous excitation was 1.8 msec as measured at 2T in Fig. 1I f r o m the very beginning o f the recorded incoming volley. It should be added that stimulating
156 muscle nerves at Group I1 strength has been observed also to excite GS y-cells classified as static (data only from two cells, both receiving Group !II excitation). Three static ABSm cells, on the other hand, all receiving Group I11 inhibition, were inhibited also at Group 1I strength. It is fully clear from the results presented that Group ll muscle afferents as welt as low threshold cutaneous afferents may evoke effects in dynamic 7-motoneurones distinctly separate from the effects evoked in these cells by higher threshold afferents. That such low threshold afferents have segmental pathways separate from the FRA pathways may therefore be looked upon as further established. Clearly, however, this still does not exclude the participation of Group II muscle afferents also in flexor reflex mechanisms. The functional implication of specific Group 1I pathways to dynamic fusimotor neurones is a subject of considerable interest. At least the GS and PBSt nerves are known to contain few afferents of non-spindle origin within the Group ii range 3. The excitatory effects studied were also evoked close to Group II threshold. It seems likely, therefore, that they depended upon stimulation of muscle spindle secondary afferents. The latency of the synaptic effect is similar to that observed in a-motoneurones 21 and indicates a disynaptic linkage. If muscle spindles via their secondary afferents feed back information to ),-motoneurones, the conceptual handling of the stretch reflex and its role in motor control has to be somewhat modified. It seems rather easy to incorporate a finding of secondary spindle afferent excitation of dynamic fusimotor neurones into the widely accepted framework of ideas concerning a-y-linkage and stretch reflex support of movement. A motor act aiming at, for example, lifting a subject is likely to be started by higher centres appreciating the weight of what is going to be lifted. A motor command is then sent to a- and both functional clssses of 7-motoneurones. if, when movement begins, the weight turns out to be heavier than anticipated, extrafusal shortening will lag behind intrafusal shortening. This results in a reflex support from spindle primaries to a-motoneurones 26. It seems clear, however, that such 'load compensation '7,8, at least in situations where increased load changes direction of muscle movement, will fulfill its purpose only if the primary endings of the spindles are set at a dynamic sensitivity related to the amount of load which has to be overcome. This might be achieved by the secondaries influencing the dynamic fusimotor neurones. An automatic adjustment of spindle sensitivity directly related to the load (or rather to the resulting misalignment between extra- and intrafusal muscle fibres) will be the result. The arrangement is close to a positive feedback, though directed from an intrafusal receptor to motoneurones not controlling this receptor, and will be automatically switched off when the reflex has become strong enough to allow the muscle to shorten again. Such an arrangement could be looked upon as an intrafusal stretch reflex supplying increased gain to the extrafusal stretch reflex in a situation where compensation is needed. A detailed discussion concerning the advantages associated with such an organization was recently given 14. Compensatory mechanisms triggered by mechanical disturbances injected into ongoing voluntary motor activity in man and monkey has been intensively studied
157 in recent years 4,9-11,24,2s. It seems to be well established that, in a muscle subjected to such a disturbance, two bursts o f myographic activity appear, none o f which is o f a voluntary character. It is generally agreed that the first burst, appearing after a b o u t 15 msec (in m a n as well as in monkey) is a m o n o s y n a p t i c stretch reflex. The second burst seen a b o u t 30 msec later has been attributed to a transcortical loop subserving load compensation. In the light o f the present findings it seems equally possible that this second sign o f muscle activity m a y be a second stretch reflex due to a segmentally evoked increase of dynamic muscle spindle sensitivity. The double segmental loop (secondary afferents ~ dynamic ),-cells -~ nuclear bag fibre contraction ~ primary afferents ~ a-motoneurones -+ main muscle activity) is likely to require a time compatible with the time lag actually observed. It seems quite clear that the projection f r o m low threshold cutaneous afferents described above m a y also be t h o u g h t o f as subserving load compensation. It is o f particular interest that such compensation has been f o u n d to disappear following a xylocaine block affecting the skin o f the t h u m b performing the m o v e m e n t 24. This work was supported by the Swedish Medical Research Council, Project No. 03873, and by G u n v o r and Josef An6rs Stiftelse. We wish to thank Mrs G e r d y Kristr6m for valuable technical assistance.
1 Appelberg, B., Jeneskog, T. and Johansson, H., Rubrospinal control of static and dynamic fusiomotor neurones, Acta physioL scand., 95 (1975) 431-440. 2 Baldissera, F., Ten Bruggencate, G. and Lundberg, A., Rubrospinal monosynaptic connexion with last-order interneurones of polysynaptic reflex paths, Brain Research, 27 (1971) 390-392. 3 Boyd, I. A. and Davey, M. R., Composition of Peripheral Nerves, Livingstone, Edinburgh, 1968, 57 pp. 4 Conrad, B., Meyer-Lohmann, J., Matsunami, K. and Brooks, V. B., Precentral unit activity following torque pulse injections into elbow movements, Brain Research, 94 (1975) 219-236. 5 Eccles, R. M. and Lundberg, A., Synaptic actions in motoneurones by afferents which may evoke the flexion reflex, Arch. ital. BioL, 97 (1959) 199-221. 6 Engberg, I., Reflexes to foot muscles in the cat, ActaphysioL scand., 62, Suppl. 235 (1964) 64 pp. 7 Euler, C., The control of respiratory movement. In J. B. L. Howell and E. J. M. Campbell (Eds.), Breathlessness, Blackwell Sci. Publ., Oxford, 1966, pp. 19-32. 8 Euler, C., Proprioceptive control in respiration. In R. Granit (Ed.), Muscular Afferents and Motor Control, Nobel Symposium I, Almqvist and Wiksell, Stockholm, 1966, pp. 197-207. 9 Evarts, E. V., Motor cortex reflexes associated with learned movement, Science, 179 (1973) 501-503. 10 Evarts, E. V. and Tanji, J., Gating of motor cortex reflexes by prior instruction, Brain Research, 71 (1974) 479-494. l 1 Hammond, P. H., Merton, P. A. and Sutton, C. G., Nervous gradation of muscular contraction, Brit. med. Bull., 12 (1956) 214-218. 12 Hongo, H., Jankowska, E. and Lundberg, A., The rubrospinal tract. II. Facilitation of interneuronal transmission in reflex paths to motoneurones, Exp. Brain Res., 7 (1969) 365-391. 13 Hongo, T., Jankowska, E. and Lundberg, A., The rubrospinal tract. IV. Effects on interneurones, Exp. Brain Res., 15 (1972) 54-78. 14 Houk, J. C., The Phylogeny of Muscular Control Configurations, Biocybernetics IF, VEB, Gustav Fischer Verlag, Jena, 1972, pp. 125-144. 15 Hunt, C. C., Relation of function to diameter in afferent fibres of muscle nerves, J. gen. PhysioL, 38 (1954) 117-131. 16 Kirkwood, P. A. and Sears, T. A., Monosynaptic excitation of motoneurones from secondary endings of muscle spindles, Nature (Lond.), 252 (1974) 243-244.
158 17 Kirkwood, P. A. and Sears, T. A., Monosynaptic excitation of motoneurones from muscle spindle secondary endings of intercostal and triceps surae muscles in the cat, J. Physiol. (Lond.), 245 (1975) 64-66P. 18 Lundberg, A., Integration in the reflex pathway. In R. Granit (Ed.), Muscular Afferents and Motor Control, Nobel Symposium 1, Almqvist and Wiksell, Stockholm, 1966, pp. 275- 305. 19 Lundberg, A., T h e significance of segmental spinal mechanisms in motor control, Symposial paper, 4th International Biophysics Congress, Moscow, 1972, 13 pp. 20 Lundberg, A., Malmgren, K. and Schomburg, E. D., Convergence from Ib, cutaneous and joint afferents in reflex pathways to motoneurones, Brain Research, 87 (1975) 81-84. 21 Lundberg, A., Malmgren, K. and Schomburg, E. D., Characteristics of the excitatory pathways from group II muscle afferents to alpha motoneurones, Brain Research, 88 (1975) 538-542. 22 Lundberg, A., Malmgren, K. and Schomburg, E. D., Group ii excitation in motoneurones and double sensory innervation of extensor digitorum brevis, Acta physiol, scand., 94 (1975) 398-400. 23 Lundberg, A., Malmgren, K. and Schomburg, E. D., Comments on reflex actions evoked by electrical stimulation of group 11 muscle afferents, Brain Research, 122 (1977) 551-555. 24 Marsden, C. D., Merton, P. A. and Morton, H. B., Servo action in human voluntary movement, Nature (Lond.), 238 (1972) 140-143. 25 Matthews, P. B. C., Mammalian Muscle Receptors and their Central Actions, Edward Arnold, London, 1972. 26 Phillips, C. G., The Ferrier lecture, 1968, Motor apparatus of the baboon's hand, Proe. roy. Soc. B, 173 (1969) 141-174. 27 Stauffer, E. K., Watt, D. G. D., Taylor, A., Reinking, R. M. and Stuart, D. G., Analysis of muscle receptor connections by spike-triggered averaging. 2. Spindle group II afferents, J. Neurophysiol., 39 (1976) 1393-1402. 28 Watt, D. G. D., Chan, C. W. Y. and Melvill Jones, G., Is the late response to muscle stretch in man mediated through a long-loop reflex pathway?, DBR aviat, med. Res. Unit Rep., 3 (1971 1973) 210-222.
153
The influence of Group II muscle afferents and low threshold skin afferents on dynamic fusimotor neurones to the triceps surae of the cat
B. APPELBERG, H. JOHANSSON and G. KALISTRATOV* Department of Physiology, University of Umed, S-901 87 Umed (Sweden)
(Accepted May l lth, 1977)
Eccles and Lundberg 5 studied synaptic actions in motoneurones evoked by Group II and Group III muscle and cutaneous afferents. Closely similar actions by the three different types of fibres were revealed and Group II afferents as well as all cutaneous afferents have since come to be included in the flexor reflex afferent (FRA) concept. The majority of Group II afferents in the nerve from the triceps surae seem to be secondary muscle spindle afferentsa, 15, and so these afferents from a highly sophisticated sense organ came to be looked upon as merely subserving the flexor reflex. Matthews 25 heavily criticized this view and Lundberg in recent reviews 1a,19 stated that though, according to his opinion, Group II afferents are part of the FRA, this does not exclude the possibility that these afferents may also have other reflex lines. Indirect evidence to this effect was obtained 21,22 when it was shown that effects from Group II afferents from the extensor digitorum brevis nerve conforming to the FRA-pattern were indeed caused mainly by afferents of non-spindle origin. Furthermore, the use of a new method recently indicated monosynaptic actions from spindle secondary afferents on motoneurones16,17. Such a finding, recently confirmed 28,27, does not seem compatible with a view on the secondary spindle afferents as merely being part of the FRA. That low threshold skin afferents do not exclusively belong to the FRA is more clear. Such afferents from the plantar surface of the foot do, for instance, evoke plantar reflexes6. Strong arguments for the existence of other special reflex pathways for low threshold cutaneous afferents have been given 2A2,18. Interneurones activated from very low threshold cutaneous afferents were then actually found 13. Very recently also 2° such afferents have been shown to converge to the Ib pathway to motoneurones. It is clear from what has been said above that our knowledge concerning the functional role of Group II muscle and low threshold skin afferents is still meager. The findings to be presented below will further strengthen the notion that pathways separate from the FRA ones do exist from the two types of afferents in question. It is made likely that secondary afferents from muscle spindles project to dynamic ~-
* Current address: Biruzov str. 43-164, Moscow, 123060, U.S.S.R.
154 motoneurones. The functional implications of such an organization will be discussed. The results to be described were obtained within the framework of a long series of experiments aimed at studies of reflex pathways to ;v-motoneurones. The experiments were performed on cats anaesthetized with chloralose (60 mg/kg) and paralyzed with Flaxedil. The preparation was similar to the one recently describedL The technique of distinguishing between static and dymamic y-motoneurones with the aid of central stimulation within a certain area of the mid-brain (the MesADC-region, known to selectively influence muscle spindle dynamic sensitivity 1) was utilized also in the present experiments. All roots were left intact, and a variety of hind limb nerves were dissected and mounted for stimulation. The following abbreviations will be used : ABSm, anterior biceps-semimembranosus; EPSP, excitatory postsynaptic potential; FRA, flexor reflex afferents, GS, gastrocnemius-soleus (.triceps surae); IPSP, inhibitory postsynaptic potential: MesADC, mesencephalic area controlling dynamic spindle sensitivity; NR, nucleus ruber; PBSt, posterior biceps-semitendinosus; Q, quadriceps; SP, superficial peroneal ; Su, sural; T, threshold for detectable incoming volley in L7 dorsal root entry zone. So far, 18 triceps surae cells have been studied. Twelve of these cells were classified as dynamic, the others as static. As judged by the stimulating strength used and the resulting volley recorded in the dorsal root entry zone, Group III effects were seen in all these cells, excitatory (9 cells) or inhibitory (9 cells). Among the Group III inhibited cells, 8 were of the dynamic type. Group III excitations was thus seen in only 4 dynamic cells, while it was seen in all but one of the cells classified as static. Within the population of cells classified as dynamic and receiving Group II1 inhibition (8 cells), Group H muscle afferents caused excitation in 4 cells'. This was revealed by intracellularly recorded PSPs. In two cells, inhibition was seen instead in the form of a pause in the spontaneous extracellularly recorded discharge of these cells. In one intracellularly recorded cell Group II PSPs were not observed, but instead this cell received a clearcut Group I excitation at monosynaptic latency from its own nerve. The last cell within this group was so badly damaged by the intracellular electrode that Group II effects could not be seen. Typically also, dynamic cells received low threshold excitation from at least one of the three cutaneous nerves used (Su, SP and Tib) although stronger stimuli of cutaneous nerves also usually brought about inhibitory effects. The pattern of effects evoked by Group lI muscle and by cutaneous nerve stimulation is illustrated in Fig. 1. The cell is identified in Fig. 1A by being antidromically invaded from its own nerve. A long train of impulses at 600 Hz in the red nucleus inhibited the cell (Fig. 1B), while, on the other hand, a weak and slowly rising excitation was evoked from the MesADC (Fig. 1C). This together with the observation of MesADC driving of the celt while the electrode was still in a juxtacellular position (Fig. 1D) classified the cell as a dynamic y-motoneurone of the triceps surae. In Fig. I E-H, different muscle nerves were stimulated at 5T. Note that the GS stimulus evoked a late IPSP in the cell. This was correlated to a weak Group llI volley in the dorsal root recording (Fig. I E). Stimulation of all the muscle nerves caused initial EPSPs which, according to the analysis at faster sweep speed in Fig. 1, records
155
A
asY
B
NR
C
.,,ADC
D
E
Gs 5
F
PBSt s
G
0 s
H
A.S~5
K
cs5
L
PBSt 5
M
0 s
N
sP5
O
Su~.=
p
Gs2
R
pest2
S
Q2
T
sP2
U
Sul.~
,
I
Su 2
•
Fig. 1. Intracellular recording from dynamic GS 7-cell. A: antidromic identification; B: stimulation of NR at 600 Hz, 60/~A during time indicated by horizontal bar; C: stimulation of MesADC at 600 Hz, 70 pA; D: as C but slower sweep speed and obtained just before penetration; E-U: stimulation of peripheral nerves as indicated. Figures indicate stimulating strengths in multiples of threshold. Upper records in E-U obtained from dorsal root entry. Lower records in E-H and P-U are extracellular recordings obtained at 50 T. In all records positivity is signalled upwards. Horizontal calibration bar is 4 msec in A and I-U, 10 msec in B, C and E-H, and 20 msec in D. Vertical calibration bar is 20 mV in A, 10 mV in D, and 4 mV in B, C and E-U.
K - M and P-S, had in all cases a central latency close to 2 msec. The threshold for their appearance was a r o u n d 2T f r o m GS, PBSt and Q, slightly higher f r o m A B S m (not illustrated) and they were thus likely to be caused by G r o u p II afferents. The late inhibition evoked f r o m the quadriceps nerve (Fig. 1G, M and S) is likely to be a G r o u p Ib effect, since it had a lower threshold than the excitatory effect, and thus tended to override the G r o u p II excitation at 2T (Fig. IS). A strong inhibition, which is p r o b a b l y a F R A effect, was evoked from the SP nerve at 5T (Fig. IN). The threshold for this effect was just below 2T (Fig. IT). On the other h a n d the Su nerve, t h o u g h also causing some late inhibition a r o u n d and above 2T (Fig. 1I), in addition excited the cell at low stimulating strength (Fig. 10). Even at 1.1T in Fig. 1U, a single liminal E P S P may be observed. The central latency of this low threshold cutaneous excitation was 1.8 msec as measured at 2T in Fig. 1I f r o m the very beginning o f the recorded incoming volley. It should be added that stimulating
156 muscle nerves at Group I1 strength has been observed also to excite GS y-cells classified as static (data only from two cells, both receiving Group !II excitation). Three static ABSm cells, on the other hand, all receiving Group I11 inhibition, were inhibited also at Group 1I strength. It is fully clear from the results presented that Group ll muscle afferents as welt as low threshold cutaneous afferents may evoke effects in dynamic 7-motoneurones distinctly separate from the effects evoked in these cells by higher threshold afferents. That such low threshold afferents have segmental pathways separate from the FRA pathways may therefore be looked upon as further established. Clearly, however, this still does not exclude the participation of Group II muscle afferents also in flexor reflex mechanisms. The functional implication of specific Group 1I pathways to dynamic fusimotor neurones is a subject of considerable interest. At least the GS and PBSt nerves are known to contain few afferents of non-spindle origin within the Group ii range 3. The excitatory effects studied were also evoked close to Group II threshold. It seems likely, therefore, that they depended upon stimulation of muscle spindle secondary afferents. The latency of the synaptic effect is similar to that observed in a-motoneurones 21 and indicates a disynaptic linkage. If muscle spindles via their secondary afferents feed back information to ),-motoneurones, the conceptual handling of the stretch reflex and its role in motor control has to be somewhat modified. It seems rather easy to incorporate a finding of secondary spindle afferent excitation of dynamic fusimotor neurones into the widely accepted framework of ideas concerning a-y-linkage and stretch reflex support of movement. A motor act aiming at, for example, lifting a subject is likely to be started by higher centres appreciating the weight of what is going to be lifted. A motor command is then sent to a- and both functional clssses of 7-motoneurones. if, when movement begins, the weight turns out to be heavier than anticipated, extrafusal shortening will lag behind intrafusal shortening. This results in a reflex support from spindle primaries to a-motoneurones 26. It seems clear, however, that such 'load compensation '7,8, at least in situations where increased load changes direction of muscle movement, will fulfill its purpose only if the primary endings of the spindles are set at a dynamic sensitivity related to the amount of load which has to be overcome. This might be achieved by the secondaries influencing the dynamic fusimotor neurones. An automatic adjustment of spindle sensitivity directly related to the load (or rather to the resulting misalignment between extra- and intrafusal muscle fibres) will be the result. The arrangement is close to a positive feedback, though directed from an intrafusal receptor to motoneurones not controlling this receptor, and will be automatically switched off when the reflex has become strong enough to allow the muscle to shorten again. Such an arrangement could be looked upon as an intrafusal stretch reflex supplying increased gain to the extrafusal stretch reflex in a situation where compensation is needed. A detailed discussion concerning the advantages associated with such an organization was recently given 14. Compensatory mechanisms triggered by mechanical disturbances injected into ongoing voluntary motor activity in man and monkey has been intensively studied
157 in recent years 4,9-11,24,2s. It seems to be well established that, in a muscle subjected to such a disturbance, two bursts o f myographic activity appear, none o f which is o f a voluntary character. It is generally agreed that the first burst, appearing after a b o u t 15 msec (in m a n as well as in monkey) is a m o n o s y n a p t i c stretch reflex. The second burst seen a b o u t 30 msec later has been attributed to a transcortical loop subserving load compensation. In the light o f the present findings it seems equally possible that this second sign o f muscle activity m a y be a second stretch reflex due to a segmentally evoked increase of dynamic muscle spindle sensitivity. The double segmental loop (secondary afferents ~ dynamic ),-cells -~ nuclear bag fibre contraction ~ primary afferents ~ a-motoneurones -+ main muscle activity) is likely to require a time compatible with the time lag actually observed. It seems quite clear that the projection f r o m low threshold cutaneous afferents described above m a y also be t h o u g h t o f as subserving load compensation. It is o f particular interest that such compensation has been f o u n d to disappear following a xylocaine block affecting the skin o f the t h u m b performing the m o v e m e n t 24. This work was supported by the Swedish Medical Research Council, Project No. 03873, and by G u n v o r and Josef An6rs Stiftelse. We wish to thank Mrs G e r d y Kristr6m for valuable technical assistance.
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