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Fusimotor reflexes to antagonistic muscles simultaneously assessed by multi-afferent recordings from muscle spindle afferents
Brain Research. 435 (1987) 337-342
337
Elsevier BRE 22604
Fusimotor reflexes to antagonistic muscles simultaneously assessed by multi-afferent recordings from muscle spindle afferents H h k a n J o h a n s s o n l, P e r S j 6 1 a n d e r 2, P e t e r S o j k a I a n d I n g e r W a d e l l 1 Departments of IPhysiology and 2Zooph ysiology , University of Umed, (Sweden)
(Accepted 18 August 1987) Key words: F-Motoneuron; Motor control; Spinal cord; Reflex; Muscle afferent;
Muscle spindle afferent; Cutaneous afferent; Movementsense
Several singleagonist/antagonistprimary muscle spindle afferents were simultaneouslyrecorded in chloraloseanaesthetized cats. It was shownthat their dynamic and static sensitivityto sinusoidalmusclestretches could be increased or decreasedvia the fusialotor system by extensionand flexionof the contralateral hind limb as well as by stretch of ipsilatcrai musclesand stimulationof ipsilateral skin nerves. The resultsseem to support the hypothesisthat the primary musclespindle afferents conveycomplexmultisensorymessagesto the central nervoussystem (CNS).
The segmental and supraspinal control of y-motoneurones have been thoroughly investigated during the last decades, in our laboratory, the contribution from activity in ipsi- and contralateral hind limb muscle, skin and joint afferents to the segmental control of lumbar y..motoneurones has, so far, been studied with intra- and extracellular recordings directly from y-cells (classified as static or dynamic) 3-5't6'i7, and with indirect evaluation of fusimotor activity from recordings of muscle spindle afferent discharge 2'6'7. A prominent finding in these investigations was the great amount of variation in effects on the individual y-cells, indicating a remarkably complex organization of segmental reflexes to y-motoneurones. However, since these studies were performed on single ycells or on single spindle afferent units, recorded one at a time, the diversity in type and size of fusimotor reflex effects observed might have been due to spontaneous variations of descending fusimotor drive, and/or to changes in the 'setting' of the spinal interneuronal network, during the time interval between the recordings. Therefore, in order to settle this issue and in order to further clarify the functional organi-
zation of interneuronal network projecting to the fusimotor system, we have developed a new technique which permits us to simultaneously assess changes in fusimotor activity to several single muscle spindle afferent units. The experiments were performed on five cats lightly anaesthetized with a-chloralose, h, :he ipsilateral hind limb conventional nerve-mt~scle pteparations were made for posterior biceps and semitendinosus (PBSt) and for lateral gastrocnemius, plantaris and soleus (GS). The rest of the ipsilateral hind limb was denervated and the sural nerve (Su) was prepared for electrical stimulation. The GS and PBSt tendons were disconnected from their distal points of insertion, and tied to two separate electromagnetic pullers (stiffness: 0.06 mm/N). The muscles were continuously stretched and released between -10 and -2 mm (maximum physiological length settled in situ = 0 mm) at a velocity of 10 mm/s and wLh a plateau duration of 15 s. Repetitive sinusoidal stretches at 1 Hz for the GS muscle and at 0.9 Hz for the PBSt muscles, with a half peakqo-peak amplitude of 1 ram, were superimposed on the ramp-and-hold stretches.
Correspondence: H. Johansson, Department of Physiology,Universityof Ume~, S-901 87 Umeh, Sweden.
0006-8993/87/$03.50© 1987Elsevier SciencePublishersB.V. (BiomedicalDivision)
338 In all experiments, and for both muscles, the occurrence of any skeletomotor activity was detected by observing the display of the muscle force (tension) signals (recorded via the pullers: lowermost detection limit = 0.01 N) on the oscilloscope. In addition, during one experiment, the electromyographic activity was recorded via needle eJectrodes inserted into the muscle bellies. The contralateral hind limb was always left intact. Contralateral reflex stimulation consisted of manually performed extensions (up to the maximum physiological joint angles) of the hip, knee and ankle joints simultaneously (in some cases only the ankle joint), and full flexion of the knee and/or ankle joints. Also, in one experiment, the contralateral knee joint was stimulated by tonic pressure applied (one of the experimentators used his thumb and index finger) to the frontal part of the knee joint distally to the patella. The activity of 2-4 single GS and/or PBSt primary muscle spindle afferents was recorded in parallel from dissected and thinly cut dorsal root filaments. The responses or' each primary spindle afferent (conduction velocity > 72 m/s), to 10 successive sinusoidal stretches of the receptor bearing muscle, were averaged on-line to give cycle histograms showing the probability density of firing. Simple ~inusoids were then fitted to the histograms using a leastsquare algorithm method which ignored periods of afferent silence tt. Parameters of the fitted sines (i.e. 'fitted mean' = mean rate of discharge, and 'depth of modulation' = the amplitude of the fitted sine) were taken as quantitative estimates of the afferent unitresponses. Each set of units (pairs, triplets, quadruplets) was studied with a number of pairs of control (in absence of any reflex stimulation) and test (during ongoing reflex stimulation) responses, The occurrence of dynamic, static and mixed (static and dynamic) fusimotor activity was inferred from compar:son of the induced changes in fitted sine characteristics (tests minus controls) to the sine changes known to be evoked by selective electrical stimulation of dynamic, static or both dynamic and static fusimotor fibres projecting to the GS muscle tin2. For a detailed description of the criteria for assessment of occurrence of fusimotor activation, see Appeiberg et al. ~,2 Details about anaesthesia, preoperative care, set-up etc. have been given in previous papers 1.z.6.7.
Fig. 1 shows the assessments of reflex effects on GS and PBSt fusimotor neurones evoked simultaneously by full extension of the intact contralateral hind limb. Simultaneously recorded responses of one primary muscle spindle afferent from GS (in A ) and one from PBSt (in B) to 10 successive cycles of sinusoidal stretching were averaged and are displayed as cycle histograms. The data of the control responses (dotted lines) were obtained when the contralateral hind limb was in approximately resting position. During test measurements (continuous lines) the contralateral hind limb was fully extended, with the 3 joints close to their maximal physiological angles (onset 10 s before the start of the data collection). A comparison of control and test responses elicited in the GS primary spindle afferent (A), shows that contr,,ateral whole limb extension clearly produced changes in the sinusoidal response of this unit. Thus, the quantitative analysis revealed that an increase in fitted mean (from 52.9 to 61.5 impulses/s) was accompanied by an increase in depth of modulation (from 88.1 to 92.4 impulses/s). Also, there was a short period of silence in the afferent discharge during the release of the sinusoidai stretch (which began at 90°). All these findings indicate that extension of the contralateral hind limb provoked reflex excitation of predominantly dynamic fusimotor neurones, to this particular GS unit. In contrast, in the simultaneously recorded PBSt primary spindle afferent (B),, inhibition, predominantly of dynamic fusimotor drive, seemed to be evoked, since both the induced changes in fitted mean (from 31.2 to 16.5 impulses/s) and in depth of ;undulation (from 29.0 to 19.5 impulses/s) were negative. Neither increased force signals (cf. above) from the GS and PBSt muscles nor visible muscle twitches were observed during ongoing reflex stimulations. Therefore, the reflex effects observed were tentatively attributed to activity in ~,-motoneurones rather than in//-motoneurones or in tt-motoneurones. In this investigation each set of muscle spindle afferents was studied with 7-16 pairs of control and test measurements, so that the consistency and tl~e degree of stability of the fusimotor reflex effects could be settled. The scatter diagram of Fig. 1C shows the result when the simultaneously recorded afferent units of Fig. 1A,B were investigated with 10 control and test sequences (each being the result of 10 averaged consecutive cycles). The diagram dis-
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Fig. 1. Simultaneouslyrecorded responses of primary muscle spindle afferent units from GS and PBSt during full extension of the contralaterai hind limb. A and B: cycle histograms showing single simultaneously recorded control and test pairs for the GS afferent (A) and the PBSt afferent (B). Averaged responses to 10 sinusoidalstretching cyclesat 1 Hz, 1 mm of the GS muscleand at 0.9 Hz, 1 mm of the PBSt muscles (mean muscle length -2 ram). The probability density of firing (ordinate) is plotted against the phase of the stretch cycle (abscissa), which began at 0°, and a simple sinusoid is fitted to each histogram. Dotted lines, control responses (eontralaterai hind limb in resting position); continuous lines, test responses (contralateral hip, knee and ankle joint fully extended). C: scatter diagram showingchanges in sinusoidal response for each one of the 10 control and test pairs, both for the GS afferent (&) and the PBSt afferent (O). For each of the 10 pairs the change (i.e. test minus control value) in depth of modulation (the amplitude of the curves in A and B) is plotted against the change in fitted mean (mean level of discharge). The average difference in sinusoidal responses for the whole series of control and test pairs is illustrated by filled symbols, connected with a line. The symbols marked by arrows in C corresponds to the control and test pairs shown in A and B. The slope of the line labelled )'D gives the ratio of mean change in modulation/ mean change in fitted mean (1.07), which has been found with electrical stimulation of dynamic fusimotor fibres projecting to the GS muscle. The slope of the line labelled ?s (ratio 0.47) corresponds to changes found with selective stimulation of static fnsimotor fibres projecting to the GS muscle and the line labelled 7s + 7o (ratio 0.24) to changes obtained with combined stimulation of static and dynamic fusimotor fibres (see Appelberg et al.-"where data from Hulliger et al. i."were recalculated and replotted).
plays the changes in responses (i.e. test minus control) elicited by the test (contralateral whole limb extension), rather than the absolute size of the test respouses 1'2's. For both the GS unit ( & ) and the PBSt unit (O) the change in modulation, of each control and test pair, is plotted against the corresponding change in fitted mean. The average changes for the whole series of control and test pairs are shown by filled symbols, connected by a line. It can be seen that for the GS primary muscle spindle afferent there was a parallel increase in dynamic sensitivity (measured by the change in modulation) and in fitted mean. However, the PBSt primary afferent simultaneously recorded from, exhibited clear-cut decreases in fitted mean as well as in depth of modulation. For the GS unit the symbols, representing the changes in modulation and fitted mean of each control-test measurement, are all scattered around the reference line labelled YD, the slope of which gives the ratio (1.07) of mean change in modulation/mean change in fitted mean obtained by selective stimulation of dynamic fusimotor fibres projecting to the GS muscle mr2. For
the PBSt unit, on the other hand, the location of the symbols indicate primarily inhibition of dynamic fusimotor neurones, but a small contribution of inhibition of static fusimotor neurones cannot be excluded. Thus, for the two units illustrated in Fig. 1, the same type of stimulus (contralateral whole limb extension) most probably elicited opposite types of respnnses, excitation predominantly of dynamic furlmotor neurones (the GS unit) and inhibition of both dynamic and static fusimotor neurones (the PBSt unit). So far 3 afferent pairs (consisting of one GS and one PBSt primary spindle afferent unit), one afferent triplet (consisting of two GS and one PBSt primary spindle afferent unit) and one afferent quadruplet (consisting of two GS and two PBSt primary spindle afferent units) have been studied with different ipsiand contralateral stimulations. The scatter diagrams in Fig. 2 show the size of the reflex effects for the afferent pairs and the afferent triplet induced by full extension of the contralateral hind limb (A) and by flexion of the contralateral knee and ankle joints (B).
34O
feet on the fusimotor drive to the PBSt unit and a statistically insignificant (open symbol) effect on the GS unit. For set no. 2, on the other hand, both types of stimuli caused a small predominantly static reflex effect on the GS unit, while for th:: PBSt unit the effect changed character from mixed (A, contralateral whole limb extension) to dynamic (B, contralateral knee and ankle flexion). With the triplet (set 3), one of the GS units exhibited a more pronounced dynamic effect for flexion (B) than for extension (A), while the other GS unit showed a dynamic response to extension but only a statistically insignificant response to flexion. The PBSt unit in the triplet showed predominantly static responses to both stimuli. In general, the GS units seemed to be less responsive to contralateral knee and ankle flexion than to contralateral whole limb extension, while no such tendency could be seen for the PBSt units. Fusimotor effects of different types (i.e. excitation and inhibition of static and dynamic fusimotor neu-
For each unit the average change (average values of 7-16 control-test pairs, each control and test value being the result of l0 averaged consecutive cycles) in modulation is plotted against the average change in fitted mean. Note that simultaneously recorded units are connected with lines, and that responses recorded from the same sets of units are labelled with the same numbers in A and B. Perhaps the most striking feature of the set of diagrams in Fig. 2A,B is that the two different stimuli zometimes influenced the individual afferents in each set of agonist-antagonist afferents in a similar way and sometimes very differently. Also, it should be observed that a change in stimuli sometimes resulted in similar changes in effects for the individual afferents in a set, but frequently it resulted in different changes. Thus, for set 1, both afferents showed clearcut static reflex effects in respons e to contralateral whole limb extension (A), while contralateral knee and ankle flexion (B) gave a very small inhibitory ef-
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Fig. 2. Scatter diagrams showing the average changes in sinusoidal rcsn..-,nses for simultaneously recorded sets of primary muscle spindle afferent units front tile (iS muscle (&) and the PBSt muscles (@), induced by fuU extension of tile contralateral hind limb (in A) and by contralateral knee and ankle flex,on (in B). Sialultaneously recorded units are connected with lines. For each unit tile average change in modulation (test trlinus control values) is plotted against tile average change ill fitted m e a n . "l'he average values are the resuits of 7-16 co=,trol and test pairs, and each control and test pair is the average response to 10 sinustfidal cycles. All units iUustrated by filled symbols exhibited statistically significant (paired t-test: P < 0.05) reflex eft'tots, while the open symbols (B) represent statistically insignificant reflt:x effects (i.e P > 0,0S). Note that the numbers in the diagrams label tile same sets of afferent units. The slopes of the reference lines (same its in Figs. I and 3) give tile ratios found with electrical stimulation of fusimotor fibres projecting to the GS muscle. Preparations with intact spinal cord. Fat' further details, see text.
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Fig. 3. Scatter diagrams showing the average changes in sinusoidal responses for two primary muscle spindle affercnts from GS ( A ,ffi) and two prinlary muscle spindle affcrcnts from PBSt (0,~), simultaneously recorded, with use of different test stimuli. For each unit the average ch~mgc in modulation (test minus control wducs) is ploucd against the average change in fitted mean, the average values being tile results of 7-10 control and lest pairs. The lusts were in A fall extension of tile conIralateral hind limb, in B contralateral ankle extension, ill C cont,ah::eral kllee pressure, ill I) conlrahll~ral knee and ankle flexion, in E contralateral ankle flexion, in F contralalcral knee flexion, in G totlic stretch of ipsilateral PBSI muscles, in I I tonic stretch of ipsilateral GS muscle, in I electrical stinlul:llion of ipsilateral Su nerve at 5T (40 Hz), and in J electrical stimulation of ipsilatcral Su nerve at 10T (,Ill Hz) (xT = times the threshold fi~r the most excitahle fii~r,:s). Filled symbols illustrate statistically significant reflex effects (paired t.tcst: P < 1).|15), while open symbols illustrate reflex effects whicl: were not statistically significant (i.e. P > {I.05). Note that the reference lines are the same as in Figs. I and 2. Preparation with intact spinal cord. For further details, see text.
rones) and size, observed in afferent units recorded at the same time, are even more clearly demonstrated when the results obtained with many different reflex stimulations are taken into consideration. The scatter diagrams in Fig. 3 show the average changes in depth of modulation and fitted mean for 4 primary muscle spindle afferent units (two from GS and two from PBSt) recorded in parallel using 10 different test stimuli. In this figure it can be seen that one of the GS units f A / exhibited clearcut excitatory dy-
namic fusimotor reflexes to most of the stimulations used, Insignificant changes in the sinusoidal response were elicited by contralateral knee pressure (C) and by contralateral ankle flexion (E). In contrast, the other GS unit (ffi) was significantly influenced only when different contralateral joints were extended (A,B) and when the ipsilateral skin or muscle afferents were stimulated (G,I,J). One of the simultaneously recorded PBSt afferent units (~¢) exhibited predominantly dynamic, or mixed dynamic and static, fusimotor effects as a re_-ult of most of the different contralateral hind limb manipulations, while, in the other PBSt unit (O), inhibition of the fusimotor drive was evoked. On the other hand, when electrical stimulation of the ipsilateral Su nerve (l,J) and tonic stretch of the ipsilateral GS muscle (H) were used as stimuli, small excitatory static fusimotor reflexes were elicited in both PBSt units. In this context it is of interest to note that natural stimulation of the GS muscle elicited most probably pure or predominantly static fusimotor reflexes in the two PBSt units (Fig. 3H), and that stretching of the PBSt muscles evoked mainly dynamic fusimotor effects in the GS pair (Fig. 3G). On account of the wide range of different reflex effects elicited in a given fusimotorneurone pool, by activity in ipsi- and contralateral hind limb muscle, skin and joint afferents, we have proposed a complementary view on the role of the y-motor-spindle system in motor acts, 'the final common input hypothesis ''~'14. This hypothesis implies that each y-motoneurone and each primary muscle spindle afferent can be regarded as having a multisensory and very individualized receptive field. However, most of the investigations on reflex control of the fusimotor system have so far been performed with single unit recordings (i.e. from y-cells, y-efferents or muscle spindle afferents) m. 111this context it should be remembered that the reflex effects from a specific type of afferent can be transmitted to the motoneurones via a number of alternative pathways TM,i.e. the type of effects elicited depend on which of the paths in the interneuronal network are open, closed, facilitated or inhibited (i.e. the 'setting' of the network) due to variations (e.g. spontaneous) in descending or afferent drive. Since changes in these conditions obviously can occur during the time intervals between single unit recordings, the new method with simultaneous assessments of changes in fusimotor activity to several single
342 agonist or antagonist muscle spindle afferent units may be a more useful tool in the investigation of functional organization of the interneuronai reflex networks controlling the ?'-motoneurones and the muscle spindles. So far, oe!y a few sets of simultaneously recorded afferent units have been investigated. Yet, the results indicate a great variability in type and size of the fusimotor effects elicited in primary muscle spindle afferents from the homonymous muscle as well as from antagonistic muscles, and it is tentatively concluded that they reflect the individualized receptive profiles of the fusimotor neurones hypothesized in our earlier papers s.~'*-17. The observation of a high degree of individuality in the reflex responses of primary muscle spindle afferents also agrees well with the finding of Inbar et al.]3 that 7'-activity seems to decorrelate the muscle spindle response. It has been suggested 17 that the individualized reflex profiles of the y-cells and the complex multisensory messages in ",he prim?ry muscle spindle afferents might partly explain why these afferents can provide the central nervous system with information relevant for movement i Appelbcrg, B,, Hulligcr, M,, Johansson, H. and Sojka, P., Reflex activation of dynamic fusimotor neurones by natural stimulation of muscle and joint receptor afferent units. In A. Taylor and A. Prt~dlazka (Eds.), Muscle Receptors and Movement, Macmillan, London, 198!, pp, 149-161. 2 Appelberg, B., Flulliger, M,, Johansson, H. and Sojka, P., Fusimotor reflexes in triceps surae muscle elicited by natu. ral stimulation of muscle afi'erents from the cat ipsilateral hind limb, J, Physiol, (London), 329 (1982) 211-229. 3 Appelberg, B., Hulliger, M., Johansson, H. and Sojka, P., Actions on y-motoneurones elicited by electrical stimula. tion of group I muscle afferent fibres in the hind limb of the cat, J. Physiol. (London), 335 (1983)237-253. 4 Appelberg, B., Hulliger, M., Johansson, H. and Sojka, P., Actions on },-motoneurones elicited by electricai stimula. tion of group I[ muscle afferent fibres in the hind limb of the cat, J. Physiol. (London), 335 (1983) 255-273. 5 Appelberg, B., Hulliger, M., Johan~son, H. and Sojka, P., Actions on y-motoneurones elicited by electrical stimulation of group Ill muscle afferent fibres in the hind limb of the cat, J. Physiol. (London), 335 (1983) 275-292. 6 Appelberg, B., Hulliger, M., Johansson. H. and Sojka, P., Fusimotor reflexes in triceps surae muscle elicited by extension of the contralateral hind limb in the cat, I. Physiol. (London), 355 (1984) 99-117. 7 Appelberg, B., Johansson, H. and Sojka, P., Fusimotor reflexes in triceps surae elicited by stretch of muscles in the contralateral hind limb in tile cat, J. Physiol. (London), 373 (1986) 419-441. 8 Crowe, A. and Matthews, P.B.C., Further studies of static and dynamic fusimotor fibres, J. Physiol. (London), 174 (1964) 132-152. 9 Goodwin, G.M., McCloskey, D.I. and Matthews, P.B.C., The contribution of muscle afferents to kinaesthesia shown
and position sense (cf. ref. 9). However, since the information transmitted by a spindle afferent depends on both the reflex input to the ?'-cells and the localization of the spindle, it is not likely that a single afferent can convey complete and unambiguous information about ongoing movements. Instead, the central nervous system (CNS) probably derives this information from a large number of spindle afferents. This and the results of the present study indicate that it is necessary to use multi-afferent recordings in the search for the pattern of and the functional organization of the reflexes on the ?'-motor-spindle system. The authors wish to thank Dr. T. Jeneskog for valuable comments on the manuscript. This work was supported by the Swedish Medical Research Council. Project 07915, by Ingabritt och Arne Lundbergs forskningsstiftelse (H.J.) and by Gunvor och Josef An6rs Stiftelse. Support was also provided by the Medical Faculty of Ume~ from Fonden f6r medicinsk forskning (H.J. and P.S.) and in the form of Anslag f f r ograduerade forskares vetenskapliga verksamhet (I.W.). by vibration induced illusion of movement and by the effects of paralyzing joint afferents, Brain, 95 (1972)
705-748. I0 Hulliger, M., The mammalian intlsclc spindle and its cen-
tral control, Rev. PhysioL Biochem. Pharmacol., 101 (1984) 1-1 I0. II ltulligcr, M., Matthews, P.B.C. and Noth, J., Static and dynamic fusimotor action on the response of [a fibres to low frequency sinusoidal stretching of wide amplitudes, J. Physiol. fLondon), 267 (1977) 81 !-838. 12 Hulliger, M., Matthews, P.B.C. and Noth, J., Effects of combining static and dynamic fusimotor stimulation on the response of muscle primary endings to sinusoidai stretching, J. Physiol. (London), 267 (1977) 839-856. 13 Inbar, G., Madrid, J. and Rudomin, P., The influence of the gamma system on cross-correlated activity of Ia muscle spindles and its relation to information transmission, Neu. rosci. Lett., 13 (1979) 73-78. 14 Johansson, H., Reflex Control of y-Motoneurones, Umefi University Medical Dissertations, New Series no. 72, 1981. 15 Johansson, H., Reflex integration in the ),-motor system, in [.A. Boyd and M.H. Gladden (Eds.), The Muscle Spindle, Macmillan, London, 1985, pp. 297-301. 16 Johansson, H., SjOlander, P. and Sojka, P., Actions on )'motoneurones elicited by electrical stimulation of joint afferent fibres in the hind limb of the cat, J. Physiol. (London), 375 (1986) 137-152. 17 Johansson, H. and Sojka, P., Actions on )'-motoneurones elicited by electrical stimulation o[ cutaneous afferent fibres in the hind limb of the cat, Z Physiol. (London), 366 (1985) 343-363. 18 Lundberg, A., Multisensory control of spinal reflex pathways, Progr. Brain Res., 50 (1979) 11-28.
337
Elsevier BRE 22604
Fusimotor reflexes to antagonistic muscles simultaneously assessed by multi-afferent recordings from muscle spindle afferents H h k a n J o h a n s s o n l, P e r S j 6 1 a n d e r 2, P e t e r S o j k a I a n d I n g e r W a d e l l 1 Departments of IPhysiology and 2Zooph ysiology , University of Umed, (Sweden)
(Accepted 18 August 1987) Key words: F-Motoneuron; Motor control; Spinal cord; Reflex; Muscle afferent;
Muscle spindle afferent; Cutaneous afferent; Movementsense
Several singleagonist/antagonistprimary muscle spindle afferents were simultaneouslyrecorded in chloraloseanaesthetized cats. It was shownthat their dynamic and static sensitivityto sinusoidalmusclestretches could be increased or decreasedvia the fusialotor system by extensionand flexionof the contralateral hind limb as well as by stretch of ipsilatcrai musclesand stimulationof ipsilateral skin nerves. The resultsseem to support the hypothesisthat the primary musclespindle afferents conveycomplexmultisensorymessagesto the central nervoussystem (CNS).
The segmental and supraspinal control of y-motoneurones have been thoroughly investigated during the last decades, in our laboratory, the contribution from activity in ipsi- and contralateral hind limb muscle, skin and joint afferents to the segmental control of lumbar y..motoneurones has, so far, been studied with intra- and extracellular recordings directly from y-cells (classified as static or dynamic) 3-5't6'i7, and with indirect evaluation of fusimotor activity from recordings of muscle spindle afferent discharge 2'6'7. A prominent finding in these investigations was the great amount of variation in effects on the individual y-cells, indicating a remarkably complex organization of segmental reflexes to y-motoneurones. However, since these studies were performed on single ycells or on single spindle afferent units, recorded one at a time, the diversity in type and size of fusimotor reflex effects observed might have been due to spontaneous variations of descending fusimotor drive, and/or to changes in the 'setting' of the spinal interneuronal network, during the time interval between the recordings. Therefore, in order to settle this issue and in order to further clarify the functional organi-
zation of interneuronal network projecting to the fusimotor system, we have developed a new technique which permits us to simultaneously assess changes in fusimotor activity to several single muscle spindle afferent units. The experiments were performed on five cats lightly anaesthetized with a-chloralose, h, :he ipsilateral hind limb conventional nerve-mt~scle pteparations were made for posterior biceps and semitendinosus (PBSt) and for lateral gastrocnemius, plantaris and soleus (GS). The rest of the ipsilateral hind limb was denervated and the sural nerve (Su) was prepared for electrical stimulation. The GS and PBSt tendons were disconnected from their distal points of insertion, and tied to two separate electromagnetic pullers (stiffness: 0.06 mm/N). The muscles were continuously stretched and released between -10 and -2 mm (maximum physiological length settled in situ = 0 mm) at a velocity of 10 mm/s and wLh a plateau duration of 15 s. Repetitive sinusoidal stretches at 1 Hz for the GS muscle and at 0.9 Hz for the PBSt muscles, with a half peakqo-peak amplitude of 1 ram, were superimposed on the ramp-and-hold stretches.
Correspondence: H. Johansson, Department of Physiology,Universityof Ume~, S-901 87 Umeh, Sweden.
0006-8993/87/$03.50© 1987Elsevier SciencePublishersB.V. (BiomedicalDivision)
338 In all experiments, and for both muscles, the occurrence of any skeletomotor activity was detected by observing the display of the muscle force (tension) signals (recorded via the pullers: lowermost detection limit = 0.01 N) on the oscilloscope. In addition, during one experiment, the electromyographic activity was recorded via needle eJectrodes inserted into the muscle bellies. The contralateral hind limb was always left intact. Contralateral reflex stimulation consisted of manually performed extensions (up to the maximum physiological joint angles) of the hip, knee and ankle joints simultaneously (in some cases only the ankle joint), and full flexion of the knee and/or ankle joints. Also, in one experiment, the contralateral knee joint was stimulated by tonic pressure applied (one of the experimentators used his thumb and index finger) to the frontal part of the knee joint distally to the patella. The activity of 2-4 single GS and/or PBSt primary muscle spindle afferents was recorded in parallel from dissected and thinly cut dorsal root filaments. The responses or' each primary spindle afferent (conduction velocity > 72 m/s), to 10 successive sinusoidal stretches of the receptor bearing muscle, were averaged on-line to give cycle histograms showing the probability density of firing. Simple ~inusoids were then fitted to the histograms using a leastsquare algorithm method which ignored periods of afferent silence tt. Parameters of the fitted sines (i.e. 'fitted mean' = mean rate of discharge, and 'depth of modulation' = the amplitude of the fitted sine) were taken as quantitative estimates of the afferent unitresponses. Each set of units (pairs, triplets, quadruplets) was studied with a number of pairs of control (in absence of any reflex stimulation) and test (during ongoing reflex stimulation) responses, The occurrence of dynamic, static and mixed (static and dynamic) fusimotor activity was inferred from compar:son of the induced changes in fitted sine characteristics (tests minus controls) to the sine changes known to be evoked by selective electrical stimulation of dynamic, static or both dynamic and static fusimotor fibres projecting to the GS muscle tin2. For a detailed description of the criteria for assessment of occurrence of fusimotor activation, see Appeiberg et al. ~,2 Details about anaesthesia, preoperative care, set-up etc. have been given in previous papers 1.z.6.7.
Fig. 1 shows the assessments of reflex effects on GS and PBSt fusimotor neurones evoked simultaneously by full extension of the intact contralateral hind limb. Simultaneously recorded responses of one primary muscle spindle afferent from GS (in A ) and one from PBSt (in B) to 10 successive cycles of sinusoidal stretching were averaged and are displayed as cycle histograms. The data of the control responses (dotted lines) were obtained when the contralateral hind limb was in approximately resting position. During test measurements (continuous lines) the contralateral hind limb was fully extended, with the 3 joints close to their maximal physiological angles (onset 10 s before the start of the data collection). A comparison of control and test responses elicited in the GS primary spindle afferent (A), shows that contr,,ateral whole limb extension clearly produced changes in the sinusoidal response of this unit. Thus, the quantitative analysis revealed that an increase in fitted mean (from 52.9 to 61.5 impulses/s) was accompanied by an increase in depth of modulation (from 88.1 to 92.4 impulses/s). Also, there was a short period of silence in the afferent discharge during the release of the sinusoidai stretch (which began at 90°). All these findings indicate that extension of the contralateral hind limb provoked reflex excitation of predominantly dynamic fusimotor neurones, to this particular GS unit. In contrast, in the simultaneously recorded PBSt primary spindle afferent (B),, inhibition, predominantly of dynamic fusimotor drive, seemed to be evoked, since both the induced changes in fitted mean (from 31.2 to 16.5 impulses/s) and in depth of ;undulation (from 29.0 to 19.5 impulses/s) were negative. Neither increased force signals (cf. above) from the GS and PBSt muscles nor visible muscle twitches were observed during ongoing reflex stimulations. Therefore, the reflex effects observed were tentatively attributed to activity in ~,-motoneurones rather than in//-motoneurones or in tt-motoneurones. In this investigation each set of muscle spindle afferents was studied with 7-16 pairs of control and test measurements, so that the consistency and tl~e degree of stability of the fusimotor reflex effects could be settled. The scatter diagram of Fig. 1C shows the result when the simultaneously recorded afferent units of Fig. 1A,B were investigated with 10 control and test sequences (each being the result of 10 averaged consecutive cycles). The diagram dis-
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Fig. 1. Simultaneouslyrecorded responses of primary muscle spindle afferent units from GS and PBSt during full extension of the contralaterai hind limb. A and B: cycle histograms showing single simultaneously recorded control and test pairs for the GS afferent (A) and the PBSt afferent (B). Averaged responses to 10 sinusoidalstretching cyclesat 1 Hz, 1 mm of the GS muscleand at 0.9 Hz, 1 mm of the PBSt muscles (mean muscle length -2 ram). The probability density of firing (ordinate) is plotted against the phase of the stretch cycle (abscissa), which began at 0°, and a simple sinusoid is fitted to each histogram. Dotted lines, control responses (eontralaterai hind limb in resting position); continuous lines, test responses (contralateral hip, knee and ankle joint fully extended). C: scatter diagram showingchanges in sinusoidal response for each one of the 10 control and test pairs, both for the GS afferent (&) and the PBSt afferent (O). For each of the 10 pairs the change (i.e. test minus control value) in depth of modulation (the amplitude of the curves in A and B) is plotted against the change in fitted mean (mean level of discharge). The average difference in sinusoidal responses for the whole series of control and test pairs is illustrated by filled symbols, connected with a line. The symbols marked by arrows in C corresponds to the control and test pairs shown in A and B. The slope of the line labelled )'D gives the ratio of mean change in modulation/ mean change in fitted mean (1.07), which has been found with electrical stimulation of dynamic fusimotor fibres projecting to the GS muscle. The slope of the line labelled ?s (ratio 0.47) corresponds to changes found with selective stimulation of static fnsimotor fibres projecting to the GS muscle and the line labelled 7s + 7o (ratio 0.24) to changes obtained with combined stimulation of static and dynamic fusimotor fibres (see Appelberg et al.-"where data from Hulliger et al. i."were recalculated and replotted).
plays the changes in responses (i.e. test minus control) elicited by the test (contralateral whole limb extension), rather than the absolute size of the test respouses 1'2's. For both the GS unit ( & ) and the PBSt unit (O) the change in modulation, of each control and test pair, is plotted against the corresponding change in fitted mean. The average changes for the whole series of control and test pairs are shown by filled symbols, connected by a line. It can be seen that for the GS primary muscle spindle afferent there was a parallel increase in dynamic sensitivity (measured by the change in modulation) and in fitted mean. However, the PBSt primary afferent simultaneously recorded from, exhibited clear-cut decreases in fitted mean as well as in depth of modulation. For the GS unit the symbols, representing the changes in modulation and fitted mean of each control-test measurement, are all scattered around the reference line labelled YD, the slope of which gives the ratio (1.07) of mean change in modulation/mean change in fitted mean obtained by selective stimulation of dynamic fusimotor fibres projecting to the GS muscle mr2. For
the PBSt unit, on the other hand, the location of the symbols indicate primarily inhibition of dynamic fusimotor neurones, but a small contribution of inhibition of static fusimotor neurones cannot be excluded. Thus, for the two units illustrated in Fig. 1, the same type of stimulus (contralateral whole limb extension) most probably elicited opposite types of respnnses, excitation predominantly of dynamic furlmotor neurones (the GS unit) and inhibition of both dynamic and static fusimotor neurones (the PBSt unit). So far 3 afferent pairs (consisting of one GS and one PBSt primary spindle afferent unit), one afferent triplet (consisting of two GS and one PBSt primary spindle afferent unit) and one afferent quadruplet (consisting of two GS and two PBSt primary spindle afferent units) have been studied with different ipsiand contralateral stimulations. The scatter diagrams in Fig. 2 show the size of the reflex effects for the afferent pairs and the afferent triplet induced by full extension of the contralateral hind limb (A) and by flexion of the contralateral knee and ankle joints (B).
34O
feet on the fusimotor drive to the PBSt unit and a statistically insignificant (open symbol) effect on the GS unit. For set no. 2, on the other hand, both types of stimuli caused a small predominantly static reflex effect on the GS unit, while for th:: PBSt unit the effect changed character from mixed (A, contralateral whole limb extension) to dynamic (B, contralateral knee and ankle flexion). With the triplet (set 3), one of the GS units exhibited a more pronounced dynamic effect for flexion (B) than for extension (A), while the other GS unit showed a dynamic response to extension but only a statistically insignificant response to flexion. The PBSt unit in the triplet showed predominantly static responses to both stimuli. In general, the GS units seemed to be less responsive to contralateral knee and ankle flexion than to contralateral whole limb extension, while no such tendency could be seen for the PBSt units. Fusimotor effects of different types (i.e. excitation and inhibition of static and dynamic fusimotor neu-
For each unit the average change (average values of 7-16 control-test pairs, each control and test value being the result of l0 averaged consecutive cycles) in modulation is plotted against the average change in fitted mean. Note that simultaneously recorded units are connected with lines, and that responses recorded from the same sets of units are labelled with the same numbers in A and B. Perhaps the most striking feature of the set of diagrams in Fig. 2A,B is that the two different stimuli zometimes influenced the individual afferents in each set of agonist-antagonist afferents in a similar way and sometimes very differently. Also, it should be observed that a change in stimuli sometimes resulted in similar changes in effects for the individual afferents in a set, but frequently it resulted in different changes. Thus, for set 1, both afferents showed clearcut static reflex effects in respons e to contralateral whole limb extension (A), while contralateral knee and ankle flexion (B) gave a very small inhibitory ef-
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Fig. 2. Scatter diagrams showing the average changes in sinusoidal rcsn..-,nses for simultaneously recorded sets of primary muscle spindle afferent units front tile (iS muscle (&) and the PBSt muscles (@), induced by fuU extension of tile contralateral hind limb (in A) and by contralateral knee and ankle flex,on (in B). Sialultaneously recorded units are connected with lines. For each unit tile average change in modulation (test trlinus control values) is plotted against tile average change ill fitted m e a n . "l'he average values are the resuits of 7-16 co=,trol and test pairs, and each control and test pair is the average response to 10 sinustfidal cycles. All units iUustrated by filled symbols exhibited statistically significant (paired t-test: P < 0.05) reflex eft'tots, while the open symbols (B) represent statistically insignificant reflt:x effects (i.e P > 0,0S). Note that the numbers in the diagrams label tile same sets of afferent units. The slopes of the reference lines (same its in Figs. I and 3) give tile ratios found with electrical stimulation of fusimotor fibres projecting to the GS muscle. Preparations with intact spinal cord. Fat' further details, see text.
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Fig. 3. Scatter diagrams showing the average changes in sinusoidal responses for two primary muscle spindle affercnts from GS ( A ,ffi) and two prinlary muscle spindle affcrcnts from PBSt (0,~), simultaneously recorded, with use of different test stimuli. For each unit the average ch~mgc in modulation (test minus control wducs) is ploucd against the average change in fitted mean, the average values being tile results of 7-10 control and lest pairs. The lusts were in A fall extension of tile conIralateral hind limb, in B contralateral ankle extension, ill C cont,ah::eral kllee pressure, ill I) conlrahll~ral knee and ankle flexion, in E contralateral ankle flexion, in F contralalcral knee flexion, in G totlic stretch of ipsilateral PBSI muscles, in I I tonic stretch of ipsilateral GS muscle, in I electrical stinlul:llion of ipsilateral Su nerve at 5T (40 Hz), and in J electrical stimulation of ipsilatcral Su nerve at 10T (,Ill Hz) (xT = times the threshold fi~r the most excitahle fii~r,:s). Filled symbols illustrate statistically significant reflex effects (paired t.tcst: P < 1).|15), while open symbols illustrate reflex effects whicl: were not statistically significant (i.e. P > {I.05). Note that the reference lines are the same as in Figs. I and 2. Preparation with intact spinal cord. For further details, see text.
rones) and size, observed in afferent units recorded at the same time, are even more clearly demonstrated when the results obtained with many different reflex stimulations are taken into consideration. The scatter diagrams in Fig. 3 show the average changes in depth of modulation and fitted mean for 4 primary muscle spindle afferent units (two from GS and two from PBSt) recorded in parallel using 10 different test stimuli. In this figure it can be seen that one of the GS units f A / exhibited clearcut excitatory dy-
namic fusimotor reflexes to most of the stimulations used, Insignificant changes in the sinusoidal response were elicited by contralateral knee pressure (C) and by contralateral ankle flexion (E). In contrast, the other GS unit (ffi) was significantly influenced only when different contralateral joints were extended (A,B) and when the ipsilateral skin or muscle afferents were stimulated (G,I,J). One of the simultaneously recorded PBSt afferent units (~¢) exhibited predominantly dynamic, or mixed dynamic and static, fusimotor effects as a re_-ult of most of the different contralateral hind limb manipulations, while, in the other PBSt unit (O), inhibition of the fusimotor drive was evoked. On the other hand, when electrical stimulation of the ipsilateral Su nerve (l,J) and tonic stretch of the ipsilateral GS muscle (H) were used as stimuli, small excitatory static fusimotor reflexes were elicited in both PBSt units. In this context it is of interest to note that natural stimulation of the GS muscle elicited most probably pure or predominantly static fusimotor reflexes in the two PBSt units (Fig. 3H), and that stretching of the PBSt muscles evoked mainly dynamic fusimotor effects in the GS pair (Fig. 3G). On account of the wide range of different reflex effects elicited in a given fusimotorneurone pool, by activity in ipsi- and contralateral hind limb muscle, skin and joint afferents, we have proposed a complementary view on the role of the y-motor-spindle system in motor acts, 'the final common input hypothesis ''~'14. This hypothesis implies that each y-motoneurone and each primary muscle spindle afferent can be regarded as having a multisensory and very individualized receptive field. However, most of the investigations on reflex control of the fusimotor system have so far been performed with single unit recordings (i.e. from y-cells, y-efferents or muscle spindle afferents) m. 111this context it should be remembered that the reflex effects from a specific type of afferent can be transmitted to the motoneurones via a number of alternative pathways TM,i.e. the type of effects elicited depend on which of the paths in the interneuronal network are open, closed, facilitated or inhibited (i.e. the 'setting' of the network) due to variations (e.g. spontaneous) in descending or afferent drive. Since changes in these conditions obviously can occur during the time intervals between single unit recordings, the new method with simultaneous assessments of changes in fusimotor activity to several single
342 agonist or antagonist muscle spindle afferent units may be a more useful tool in the investigation of functional organization of the interneuronai reflex networks controlling the ?'-motoneurones and the muscle spindles. So far, oe!y a few sets of simultaneously recorded afferent units have been investigated. Yet, the results indicate a great variability in type and size of the fusimotor effects elicited in primary muscle spindle afferents from the homonymous muscle as well as from antagonistic muscles, and it is tentatively concluded that they reflect the individualized receptive profiles of the fusimotor neurones hypothesized in our earlier papers s.~'*-17. The observation of a high degree of individuality in the reflex responses of primary muscle spindle afferents also agrees well with the finding of Inbar et al.]3 that 7'-activity seems to decorrelate the muscle spindle response. It has been suggested 17 that the individualized reflex profiles of the y-cells and the complex multisensory messages in ",he prim?ry muscle spindle afferents might partly explain why these afferents can provide the central nervous system with information relevant for movement i Appelbcrg, B,, Hulligcr, M,, Johansson, H. and Sojka, P., Reflex activation of dynamic fusimotor neurones by natural stimulation of muscle and joint receptor afferent units. In A. Taylor and A. Prt~dlazka (Eds.), Muscle Receptors and Movement, Macmillan, London, 198!, pp, 149-161. 2 Appelberg, B., Flulliger, M,, Johansson, H. and Sojka, P., Fusimotor reflexes in triceps surae muscle elicited by natu. ral stimulation of muscle afi'erents from the cat ipsilateral hind limb, J, Physiol, (London), 329 (1982) 211-229. 3 Appelberg, B., Hulliger, M., Johansson, H. and Sojka, P., Actions on y-motoneurones elicited by electrical stimula. tion of group I muscle afferent fibres in the hind limb of the cat, J. Physiol. (London), 335 (1983)237-253. 4 Appelberg, B., Hulliger, M., Johansson, H. and Sojka, P., Actions on },-motoneurones elicited by electricai stimula. tion of group I[ muscle afferent fibres in the hind limb of the cat, J. Physiol. (London), 335 (1983) 255-273. 5 Appelberg, B., Hulliger, M., Johan~son, H. and Sojka, P., Actions on y-motoneurones elicited by electrical stimulation of group Ill muscle afferent fibres in the hind limb of the cat, J. Physiol. (London), 335 (1983) 275-292. 6 Appelberg, B., Hulliger, M., Johansson. H. and Sojka, P., Fusimotor reflexes in triceps surae muscle elicited by extension of the contralateral hind limb in the cat, I. Physiol. (London), 355 (1984) 99-117. 7 Appelberg, B., Johansson, H. and Sojka, P., Fusimotor reflexes in triceps surae elicited by stretch of muscles in the contralateral hind limb in tile cat, J. Physiol. (London), 373 (1986) 419-441. 8 Crowe, A. and Matthews, P.B.C., Further studies of static and dynamic fusimotor fibres, J. Physiol. (London), 174 (1964) 132-152. 9 Goodwin, G.M., McCloskey, D.I. and Matthews, P.B.C., The contribution of muscle afferents to kinaesthesia shown
and position sense (cf. ref. 9). However, since the information transmitted by a spindle afferent depends on both the reflex input to the ?'-cells and the localization of the spindle, it is not likely that a single afferent can convey complete and unambiguous information about ongoing movements. Instead, the central nervous system (CNS) probably derives this information from a large number of spindle afferents. This and the results of the present study indicate that it is necessary to use multi-afferent recordings in the search for the pattern of and the functional organization of the reflexes on the ?'-motor-spindle system. The authors wish to thank Dr. T. Jeneskog for valuable comments on the manuscript. This work was supported by the Swedish Medical Research Council. Project 07915, by Ingabritt och Arne Lundbergs forskningsstiftelse (H.J.) and by Gunvor och Josef An6rs Stiftelse. Support was also provided by the Medical Faculty of Ume~ from Fonden f6r medicinsk forskning (H.J. and P.S.) and in the form of Anslag f f r ograduerade forskares vetenskapliga verksamhet (I.W.). by vibration induced illusion of movement and by the effects of paralyzing joint afferents, Brain, 95 (1972)
705-748. I0 Hulliger, M., The mammalian intlsclc spindle and its cen-
tral control, Rev. PhysioL Biochem. Pharmacol., 101 (1984) 1-1 I0. II ltulligcr, M., Matthews, P.B.C. and Noth, J., Static and dynamic fusimotor action on the response of [a fibres to low frequency sinusoidal stretching of wide amplitudes, J. Physiol. fLondon), 267 (1977) 81 !-838. 12 Hulliger, M., Matthews, P.B.C. and Noth, J., Effects of combining static and dynamic fusimotor stimulation on the response of muscle primary endings to sinusoidai stretching, J. Physiol. (London), 267 (1977) 839-856. 13 Inbar, G., Madrid, J. and Rudomin, P., The influence of the gamma system on cross-correlated activity of Ia muscle spindles and its relation to information transmission, Neu. rosci. Lett., 13 (1979) 73-78. 14 Johansson, H., Reflex Control of y-Motoneurones, Umefi University Medical Dissertations, New Series no. 72, 1981. 15 Johansson, H., Reflex integration in the ),-motor system, in [.A. Boyd and M.H. Gladden (Eds.), The Muscle Spindle, Macmillan, London, 1985, pp. 297-301. 16 Johansson, H., SjOlander, P. and Sojka, P., Actions on )'motoneurones elicited by electrical stimulation of joint afferent fibres in the hind limb of the cat, J. Physiol. (London), 375 (1986) 137-152. 17 Johansson, H. and Sojka, P., Actions on )'-motoneurones elicited by electrical stimulation o[ cutaneous afferent fibres in the hind limb of the cat, Z Physiol. (London), 366 (1985) 343-363. 18 Lundberg, A., Multisensory control of spinal reflex pathways, Progr. Brain Res., 50 (1979) 11-28.