REVIEW / SYNTHÈSE

Direct and indirect assessment of �-motor firingpatterns1

A. Taylor, R. Durbaba, and P.H. Ellaway

Abstract: The study of the patterns of γ-motor activity which accompany natural contractions has been long and diffi-cult, and has not as yet led to general agreement. In this review we have simplified matters by considering the case oflocomotion in the cat only, and we have avoided discussion of the various hypotheses which have been advanced toprovide general schemes of γ control for a wide range of movements. The development of the subject is shown to de-pend very much on devising ingenious methods applicable to reduced and intact animals. Direct recording from γ-motoneurones has only been possible in reduced preparations, whereas indirect assessment of γ activity from spindleafferent recordings was used in these and in intact animals. At this point in time, we still have no direct recordingsfrom γ-motoneurones in normally behaving animals, but those obtained in decerebrate animals show distinct patterns ofmodulation for static and dynamic types with particular temporal relation to the stepping movements. The spindle re-cordings in intact animals potentially provide the most important information, and the problems of interpretation, whichhave previously caused difficulties, are beginning to be solved through the insights obtained from the reduced prepara-tions.

Key words: locomotion, gamma motoneurons, muscle spindles.

Résumé : L’étude des patrons d’activité motrice � qui accompagnent les contractions naturelles a été longue et difficileet n’a pas encore fait l’unanimité. Dans la présente synthèse, nous avons simplifié les choses en considérant unique-ment le cas de la locomotion chez le chat, et nous avons évité de discuter des diverses hypothèses de modèles géné-raux de contrôle γ pour une vaste gamme de mouvements. Nous montrons que le développement du sujet a étéétroitement lié à la mise au point de méthodes ingénieuses applicables à des préparations animales réduites ou intactes.L’enregistrement direct des motoneurones � n’a été possible que dans les préparations animales réduites, alors quel’évaluation indirecte de l’activité � à partir d’enregistrements au niveau des afférences fusoriales a été utilisée chez cesanimaux et chez les animaux intacts. À ce stade-ci, nous n’avons toujours pas d’enregistrement direct des motoneuro-nes � chez les animaux intacts, mais ceux obtenus chez les animaux décérébrés montrent des patrons de modulationdistincts pour les types statiques et dynamiques ainsi qu’une relation temporelle spécifique aux mouvements de marche.Les enregistrements au niveau des fuseaux musculaires chez les animaux intacts fournissent probablement l’informationla plus importante, et les problèmes d’interprétation, qui posaient des difficultés, commencent à être résolus grâce auxrévélations obtenues des préparations réduites.

Mots clés : locomotion, motoneurones gamma, fuseaux musculaires.

[Traduit par la Rédaction] Taylor et al. 802

It is fortunate for studies of posture, gait, and movementthat the activity of skeletal muscles is so easily monitored byelectromyographic recording. The rectified and filtered masssignals yield information on both the timing and the relativestrength of contraction of muscles. Single motor unit record-

ing is also possible, and gives detailed insights into the be-haviour of individual α-motoneurones. It is evident,however, that the α-motor activity is just the final output ofthe system — Sherrington’s “final common path”. To under-stand the neural control mechanisms that result in this output

Can. J. Physiol. Pharmacol. 82: 793–802 (2004) doi: 10.1139/Y04-053 © 2004 NRC Canada

793

Received 10 February. Accepted 5 June 2004. Published on the NRC Research Press Web site at http://cjpp.nrc.ca on 28 October2004.

A. Taylor,2 R. Durbaba, and P.H. Ellaway. Department of Movement and Balance, Division of Neuroscience and PsychologicalMedicine, Faculty of Medicine, Imperial College London, Charing Cross Hospital Campus, St. Dunstans Road, London, W6 8RP,UK.

1This paper is one of a selection of papers published in this Special Issue entitled Nerve, muscle, and beyond: the R.B. SteinSymposium.2Corresponding author (e-mail: t.taylor@imperial.ac.uk).

requires knowledge of the sensory feedback signals, espe-cially from the muscle proprioceptors. The importance ofthis feedback is attested to by the gross impairment that re-sults from the loss of large-diameter afferents (Hulliger et al.1998). The muscle spindles and Golgi tendon organs thusassume particular importance, with attention focussed on thespindles because of the existence of the complex form ofcentrifugal control of their behaviour via the γ-motor sys-tem. Unfortunately, because the γ-motoneurones innervateonly the minute intrafusal muscle fibres, there is no γ-motorrecording method equivalent to electromyography that canbe applied to freely moving animals. This has always placeda restriction on a full understanding of control strategies ofmovement. The purpose of this review is to consider theproblems that arise in trying to work out how the γ-motorsystem is employed, specifically in the control of locomo-tion, and to describe the development of suitable experimen-tal methods and the main conclusions that can be drawn atthe present time. Substantial work has also been done on re-spiratory and masticatory and human limb movements, but acomplete review would be too long and would inevitably re-peat much of what has appeared before (Prochazka 1981,1996; Hulliger 1984). We have chosen to concentrate on lo-comotion and to emphasise the way in which the develop-ment of understanding in this area has depended on thesuccessive refinement of experimental methods.

The ideal situation for understanding γ-efferent activityduring natural behaviour is to make direct recordings fromsingle γ-motoneurones or their axons, identified as static ordynamic, during such behaviour. The realisation of this idealinvolves as-yet unsolved technical difficulties. Nevertheless,some direct γ recordings have been made by working on re-duced preparations, such as the decerebrate cat; these studieswill be reviewed later, but first we shall consider indirectmethods in which recordings from muscle spindle afferentsare combined with movement records to deduce the underly-ing fusimotor patterns.

Early observations in reduced preparationsSeverin et al. (1967) conducted the first studies of afferent

activity during locomotion. Their preparation was the pre-collicular decerebrate cat with stimulation in the midbrainlocomotor region. The animal walked, with support, with all4 feet on a moving belt, and movement at 1 ankle joint wasrecorded, together with electromyography (EMG), from me-dial gastrocnemius (MG) and tibialis anterior (TA). Singlespindle or Golgi tendon organ afferents were recorded fromdorsal root filaments, leaving the hindlimb innervation virtu-ally intact. The striking finding was that spindle afferents inboth muscles increased their firing frequency, not only dur-ing the periods of muscle lengthening, but also during peri-ods of active contraction. It was concluded that the increasesduring active contraction were due to fusimotor activation ofthe intrafusal muscle fibres. The interpretations possible fromthis pioneering work were naturally limited because therewas no distinction made between primary and secondaryspindle afferents, or between static and dynamic fusimotoreffects, however the principle of indirect deduction offusimotor patterns from spindle recordings was well estab-lished. Severin (1970) subsequently extended these observa-tions by showing that blocking conduction in small-diameter

axons with local anaesthetic considerably reduced the risesin spindle frequency in both lengthening and shorteningphases. Interpretations were limited, as in the earlier experi-ments, but in retrospect it can be suggested that the reduc-tion in response to lengthening indicated removal of dynamicfusimotor influence, whereas the reduction during shorteningwas consistent with removal of static fusimotor action.

In similarly inspired experiments on decorticate cats,Perret and Buser (1972) recorded separately from primaryand secondary afferents in MG and TA. In their study,uncalibrated frequency records showed increases in bothtypes of afferent in time with muscle contraction, which sup-ported the proposal that static fusimotor discharge increasesduring active contraction. However, the potential effective-ness of this fluctuating static fusimotor discharge in counter-acting the effect of active shortening could not be assessedbecause the muscle contracted against an isometric straingauge. Deafferentation of the hindlimb ensured that noipsilateral reflex influences contributed to the fusimotor dis-charge. It is likely, therefore, that the patterned staticfusimotor discharge is generated autonomously within thecentral nervous system (CNS). In an extension of this work,Perret and Berthoz (1973) confirmed the existence of modu-lated static fusimotor activity. From records of movementsof the opposite limb, it can be deduced that TA staticfusimotor firing increased in phase with contraction,whereas in MG it was clearly phase-advanced (see Fig. 1).The additional technique used was to apply continuous sinu-soidal stretches to the MG or TA while recording from a pri-mary or secondary spindle afferent. Increases in the dynamicsensitivity of a primary, but not of a secondary, ending in TAwere seen during the period in which contraction of TAcould be inferred from extension of the contralateral ankle.This implies that an increase in dynamic fusimotor activityto TA occurs during the locomotor cycle sometime during itscontraction, though the timing could not be estimated withany precision. The data did not allow any clear interpretationin the case of MG. Evidence supporting the generation ofrhythmic fusimotor patterns within the spinal cord was pro-vided by Sjöström and Zangger (1975, 1976). They showedthat gastrocnemius γ-motoneurones in the spinal-curarisedcat treated with DOPA and nialamide fire with a locomotorrhythm and sometimes starts 150 ms in advance of the α-motoneurones.

Cabelguen (1981) continued studies in decorticate catsand observed changes in spindle responses to sinusoidal andramp-muscle stretches throughout the locomotor cycle.Afferents from a flexor (TA) and an extensor (triceps surae)were recorded simultaneously (13 TA and 14 tricepsafferents, both primary and secondary). With TA, there wasclear evidence of strong phasic static fusimotor activity dur-ing muscle contraction, and increased sensitivity to stretchindicated the presence of dynamic fusimotor action duringthe same period. In triceps spindles, the signs of phasicstatic drive were less clear, but the stretch responses indi-cated that dynamic effects were stronger than in TA. Furtherobservations (Cabelguen et al. 1984) on forelimb muscleswere notable for the very clear illustrations showing evi-dence of phasic static fusimotor drive approximately in timewith the parent muscle EMG activity, and the lack of anysign of difference between flexors and extensors. The data

© 2004 NRC Canada

794 Can. J. Physiol. Pharmacol. Vol. 82, 2004

presented in these papers were more detailed than in previ-ous reports, but were still simple descriptions that permittedonly general statements about static and dynamic fusimotoractivity. One must also admit the limitations of such experi-ments in that the extensive denervations carried out and fix-ation of the limb removed afferent influences that may beimportant in determining the normal fusimotor patterns.However, the findings seemed to support the “hypothesis ofa tight coupling between skeletomotor and fusimotorneurones as to their driving by the locomotor command.”This is a disappointing hypothesis, in that it fails to suggestany evolutionary advantage for the emergence of 2fusimotor systems distinct from the skeletomotor innervation(see Taylor et al. 1999).

The methods introduced by Cabelguen (1981) of applyingstretches throughout the stepping cycle were further devel-oped, with much greater instrumental sophistication, inStein’s laboratory (Taylor et al. 1985), where effective usewas made of computer analysis. The test stretches were usu-ally 4-Hz or 10-Hz sinusoids of intermediate amplitude(0.1 mm to 1.0 mm). In control experiments, these stretcheswere shown to be most appropriate for revealing an in-creased sensitivity of primary afferents, resulting from dy-namic fusimotor stimulation, and a decrease from staticstimulation. It was demonstrated (in cats decerebrated at apremammillary level) that stretch sensitivity of primaryafferents varied systematically during the step cycle, withmaximum sensitivity toward the end of active muscle con-traction. This implied that dynamic γ-activity is highest dur-ing that period, in agreement with results of the authors’direct recordings from γ-axons, which were designated asphasically modulated and identified as dynamic (reviewedbelow) (Murphy et al. 1984). There was also evidence, par-ticularly from the secondary afferents, of a high level oftonic static γ activity. The surprising feature of the data wasthat the spindle discharge was most prominent in the musclerelaxation phase, and showed minimal increase in associa-tion with active contraction. This was very different from theresults of the other studies mentioned, in which there was aconspicuous increase in afferent firing when the muscle con-

tracted in near-isometric conditions and very low frequen-cies during relaxation. However, the static pattern deducedby Taylor et al. (1985) was in accordance with what theyhad previously found for their tonically modulated γ-axons,and was designated as static. The direct γ recordings will beconsidered later, after completing an account of the rest ofthe indirect studies. At this stage, we can see that there wasreasonable agreement that dynamic γ firing increasesphasically during muscle contraction in flexors and exten-sors to increase the spindle responses to the lengtheningphase. It was not clear why phasic static γ firing in time withflexor contraction and with some phase advance relative toextensor contraction was so clear in the earlier experimentsand overshadowed by tonic static firing in the later ones.

Chronic recordings in normal locomotionA striking advance was made when methods were devel-

oped for recording single hindlimb spindle afferents in catsafter recovery from an operation to implant microelectrodesin dorsal roots (Prochazka et al. 1976, 1977) or in dorsalroot ganglia (Loeb et al. 1977). Length gauges were eitherattached externally or implanted in parallel with the muscleof interest, and EMG electrodes were implanted in pairs ofmuscles. Both groups took considerable care with unit iden-tification, including testing with succinylcholine (Prochazkaet al. 1976) and measuring conduction velocity (Loeb et al.1977). In Prochazka’s group, the 15 spindle afferents re-corded were all primaries, 5 of them in triceps surae. Widevariations in behaviour were observed (Fig. 2), but in mostcases the highest firing frequencies occurred during the mus-cle’s rapid lengthening (F) phase. Nevertheless, signs offusimotor activity were evident, as judged by afferent firing(in one case up to 200 Hz) during muscle shortening (E2),and it was concluded that “the basic pattern of fusimotordrive to primaries during stepping in the mesencephalicpreparation is basically similar to that in the conscious ani-mal.” One presumes that the principal fusimotor activity re-sponsible for the afferent firing during E2 must have beenstatic. No conclusions regarding dynamic activity were pos-sible. In a related study (Prochazka et al. 1977), the similar-

© 2004 NRC Canada

Taylor et al. 795

Fig. 1. Spindle afferent discharge showing locomotor rhythm in decerebrate cat. Records of instantaneous frequency from primaryafferents ((A) from TA, (C) from MG) and from a secondary afferent from TA (B). Parent muscle length is kept constant (upper linein each record), while movement of the contralateral hindlimb occurred (flexion upwards in each record). TA, tibialis anterior; MG,medial gastrocnemius. From Perret and Berthoz (1973), with permission.

ity of the timing of fusimotor drive in conscious anddecerebrate cats was again emphasised. When active move-ments of the ankle were simulated passively by hand, afterfusimotor activity was suppressed with deep anaesthesia, thefiring normally seen during the E1 phase was abolished, andduring E2 and E3 was greatly diminished.

In the work of Loeb and Duysens (1979), the most easilyinterpreted data came from 3 MG secondaries, one primaryin TA and one primary in peroneus longus (another ankleflexor). The MG secondary firing most closely reflectedmuscle length changes, though there were signs of staticfusimotor firing during the stance phases. The lack of pri-mary recordings precluded any comments about dynamic ac-tion. Both ankle flexor primaries had peak activity duringmuscle shortening, with a second, smaller peak duringlengthening. The net excitation during active shorteningcould only be accounted for by a fluctuating static output in-

creasing in that phase, but again, there was no useful evi-dence regarding dynamic action. However, in a later study(Loeb and Hoffer 1985), recordings from spindle primaryafferents of knee extensor muscles showed that, when smallaxons in the muscle nerve were selectively blocked by localanaesthetic, there were changes indicating the loss of staticfusimotor effects in the near isometric stance phase and theloss of dynamic effects in the passive stretch of the flexionphase.

It is evident from the above that normally locomoting catsshow some definite signs of static fusimotor drive that is en-hanced in close association with contraction in ankle flexorsand extensors and knee extensors. However, the exact pat-terns could not be identified, nor was there any clear evi-dence regarding dynamic fusimotor involvement. The needfor direct recordings from γ-axons was obvious, and the onlyway to achieve this was to go back to the decerebratelocomoting cat. Such experiments were carried out in Stein’slaboratory (Murphy et al. 1984), and involved dissecting sin-gle γ-axons from triceps muscle nerve filaments from onehindlimb, which was denervated (save for triceps), and rig-idly fixed, allowing the other 3 legs to walk on the treadmillbelt. The denervation and limb fixation, with muscle con-traction recorded isometrically, meant that γ patterns re-corded were centrally generated and would not be modifiedby afferent influences. Two distinct patterns of γ-motor dis-charge were observed (Fig. 3). In one, the firing frequencywas low at rest, but rose with the onset of walking, and wasmaintained with a very modest cyclic modulation. Frequencystarted to rise just after the end of MG contraction, andreached a maximum just before the onset of EMG activity,falling again through the contraction period. The second pat-tern was characterised by a higher resting frequency andvery strong modulation, in which frequency dropped to zeroin the periods of minimal triceps EMG. Units of the first

© 2004 NRC Canada

796 Can. J. Physiol. Pharmacol. Vol. 82, 2004

Fig. 2. Spindle primary recording from ankle extensors of nor-mally walking cat. (B) and (C) Spindle behaviour during threematched steps. In each case, the top record is lateral gastrocne-mius electromyography (EMG), the middle record is musclelength (increase upward), and the lower record is afferent instan-taneous frequency. In (A), the result of manually simulating theobserved ankle movements after arresting fusimotor output bydeep anaesthesia is shown below the step-cycle diagram. FromProchazka et al. (1977), with permission.

Fig. 3. Two patterns of γ-motoneuron firing to triceps surae ob-served in decerebrate locomoting cat. (A) The tonically modu-lated efferent has a high mean frequency (bottom panel), and isweakly modulated out of phase with the muscle force (middlepanel) and EMG (top panel). (B) The phasically modulated effer-ent falls silent during muscle relaxation, and is strongly modu-lated in phase with muscle contraction. Records averaged from15 steps in (A) and from 10 steps in (B). From Murphy et al.(1984), with permission.

type were referred to as tonically modulated (γt), and thoseof the second as phasically modulated (γp). Separate experi-ments were then performed, in which the resting firing fre-quency of γ-axons recorded in continuity in small naturalmuscle nerve filaments was observed. The effect of stimulat-ing the same axon in a ventral root filament was then deter-mined to be static or dynamic by its effects on spindlesensitivity to stretch. It was concluded that a low resting fre-quency was characteristic of static γ-efferents, whereas ahigh resting frequency indicated dynamic γ-efferents. Withthese identification criteria, it appeared that, in triceps surae,both types of γ-motoneurones were modulated in a firingfrequency approximately in parallel with α-motor activity,but the dynamic was much stronger than the static. Further γrecordings were reported (Murphy and Hammond 1990), inwhich any afferent influences were removed by paralysiswith curare. The 2 patterns of firing were the same as in ear-lier experiments, in which some afferent innervation hadbeen preserved. This supported the view that the output ofdistinct profiles of activation of static and dynamic γ-motoneurones was an inherent property of the central patterngenerator (see Sjöström and Zangger 1975, 1976). On thebasis of their resting frequencies, the identification of staticand dynamic types cannot be regarded as reliable; in view ofrecent experiments in which independently identified staticand dynamic γ units were recorded simultaneously (Tayloret al. 2000b; Figs. 1 and 2).

Simulation of the �-motor patternsThe apparently weak modulation of static γ firing, ob-

served by Murphy et al. (1984), was surprising in that previ-ous work on decerebrate locomotion had indicated that itwas often strong enough to more than compensate for activeshortening, although it is true that this effect had generallybeen stronger in flexors than in extensors. A powerful cyclicmodulation of dynamic fusimotor discharge had certainlynot been predicted from chronic recordings in normallywalking cats, although some dynamic modulation in thedecerebrate had been diagnosed from spindle recordings byCabelguen (1981), and was subsequently confirmed by Tay-lor et al. (1985). The time had come for a more detailedanalysis of the chronic spindle recording data, to see if evi-dence could be found for the occurrence in the intact animalof the modulated patterns seen in the decerebrate animal. Aningenious method was devised by Hulliger and Prochazka(1983), in which attempts were made to simulate the chronicspindle recordings in separate acute experiments on anaes-thetized cats with cut ventral roots. Spindle afferents wererecorded from dorsal root filaments, and one was selectedfor the similarity of its stretch responses to those of a chron-ically recorded unit. The original movement records werethen reproduced by stretching the muscle with a servo whilevarious patterns of fusimotor drive were applied by stimulat-ing identified static or dynamic γ-axons in ventral root fila-ments. The resulting spindle discharge pattern was comparedwith that recorded in the chronic cat, and the fusimotor pat-terns were progressively modified to give the best simulationpossible. This method was applied to recordings made in avariety of circumstances, but the main results in triceps re-lating to locomotion (Hulliger et al. 1989) can be brieflysummarised as follows. (i) Passive movements without ac-

companying fusimotor stimulation could not simulate thechronic records; (ii) the initial increase in afferent firing (inpreparation for walking) could be explained by an increasein static firing; (iii) and the high sensitivity to stretch in theflexion phases required the addition of dynamic fusimotorstimulation. In what was considered to be an example of asatisfactory simulation, both static and dynamic stimulusrates were determined to have risen abruptly in preparationfor walking, and then to have declined somewhat, with slowfluctuations unrelated to the individual steps. In summary,“the fusimotor activation profiles bore no resemblance to thetime course of the EMG” (Hulliger et al. 1989). This resultis so different from what has been found in the decerebratestate that one must examine it in more detail; for that pur-pose, we show part of the relevant figure from Hulliger et al.(1989), with an expanded time scale, in Fig. 4. The impor-tant point to notice is that, whereas in the original chronic Iarecording (shaded points), the frequency reaches a maximumduring muscle shortening (solid cursor); in the simulatedpattern, the maximum occurs at the time of maximum veloc-ity of lengthening (dashed cursor). This problem seems to

© 2004 NRC Canada

Taylor et al. 797

Fig. 4. Result of simulation of afferent activity during naturalstepping, by combining the observed movement with various pat-terns of static and dynamic γ stimulation. A section from Fig. 3bin Hulliger et al. (1989) has been reproduced in expanded form.(A) Triceps muscle length record (lengthening upward). (B) Sim-ulated Ia discharge frequency record (solid symbols) superim-posed on the naturally observed pattern (stippled symbols). Notethat the peak frequency in the simulation occurs at the maximumvelocity of muscle lengthening (dashed vertical lines), whereas inthe original data, the peak occurs during muscle shortening(solid vertical lines). From Hulliger et al. (1989), with permis-sion.

have been overlooked because of the rather cramped timescale in the original. The original Ia record could only havebeen produced if there had been a powerful increase in staticdrive during each shortening of the parent muscle. Thisproblem of interpretation inevitably raises doubts regardingthe prediction of a relatively constant dynamic fusimotordrive.

ModellingA new phase in handling data from chronic recordings

started with an attempt to generalise the descriptions by ac-cumulating ensemble averages of spindle-firing profilesfrom many experiments (Prochazka et al. 1989). The aver-ages allow much more confident interpretation than individ-ual unit records, but it is still not easy to be sure about thecontribution of fusimotor activity by simple inspection. Ithelps to make direct comparisons with responses caused bymovement in the absence of fusimotor activity. Fig. 2ashows a simple attempt to achieve this by imposing anklemovements by hand in the anaesthetised animal. This princi-ple was first applied to jaw muscles, by playing back a re-cording of active movements through a servo (Taylor andDavey 1968). This method was also used by Loeb andHoffer (1985) in studies of thigh muscle spindles. Its poten-tial usefulness is illustrated by Fig. 5. Here published musclelength records during locomotion (Prochazka et al. 1989)have been reproduced with a servo apparatus in acute experi-ments, with fusimotor activity suppressed. An ensemble ofresponses from soleus Ia afferents to such passive move-ments is compared with the ensemble of Ia responses re-corded during normal walking. It is clear from thiscomparison that, in the natural state, there must be some on-going static fusimotor activity to maintain the backgroundfiring. Also, the onset of natural Ia firing at the end of E3 oc-curs earlier than in the passive case, which indicates a rise instatic drive in advance of muscle shortening. Furthermore,the burst of firing early in E2 in normal walking is not pres-ent in the passive case. This may indicate increased dynamicsensitivity in this phase caused by increased dynamic γ ac-tivity.

Some ten years later, Prochazka’s group reviewed a largebody of ensemble data accumulated from chronic spindle re-cordings in locomotion and produced updated “look-up ta-bles” that provided easy access to the results from variousmuscles (Prochazka and Gorassini 1998a, 1998b; Prochazka1999). They carried the analysis much further, by attemptingto design mathematically based models that related musclelength changes and afferent firing patterns. For hamstringmuscles, several simple models were quite satisfactory, withan important common feature being the dominance of thevelocity component in the relatively large, fast movementsof normal walking. A minor improvement in fit was ob-tained by adding a small element proportional to the EMGsignal. In triceps spindle recordings, this contribution neededto be larger, but the dominant feature was still the sensitivityto stretch, which was high and indicated the presence of dy-namic fusimotor sensitisation of primary afferents. The mod-elling was carried further by using the inverse of theestimated transfer characteristic of length to frequency to de-rive predicted muscle length changes from observed afferentdischarge profiles. In some cases, the goodness of the fits

obtained seem to justify the methods, but there are reasonsto believe that great caution should be excercised before ac-cepting the overall interpretation of constant dynamic driveand a modest EMG-linked contribution from static fusimotoractivity. For example, Fig. 6 in Prochazka and Gorassini(1998), the predictions of muscle-length profiles for TA andperoneus longus, implies that muscle lengthening accompa-nies the EMG activity, which is certainly not what is ob-served in reality. The observed large rises in afferentfrequency in these cases during EMG activity must havebeen occurring during muscle shortening, and hence mustindicate a powerful period of static fusimotor output. It isalso evident that simple models of spindle properties did notpredict triceps spindle behaviour at all well, even with anadded EMG-linked static γ effect (Prochazka 1999).

Further spindle and �-motor recordings in thedecerebrate cat

Taking into account the strong evidence for cyclicallymodulated firing in both static and dynamic γ-motoneurones,from direct and indirect observations in the decerebrate catand from some of the chronic spindle recordings (Loeb and

© 2004 NRC Canada

798 Can. J. Physiol. Pharmacol. Vol. 82, 2004

Fig. 5. Comparison of triceps surae primary spindle afferent be-haviour during natural walking, with MG primary response tothe same movements applied passively. (A–D) Data taken fromFig. 4 of Prochazka et al. (1989), with permission, to show anensemble average of nine Ia afferents in triceps surae of nor-mally locomoting cats. Below the step diagram (A), are shownsmoothed rectified EMG of gastrocnemius (B), muscle lengthwith increase upward (C), and ensemble afferent firing rate (D).(E) Data obtained in this study show an ensemble average from10 soleus primary afferents from fully anaesthetised cats, withthe muscle exposed to stretch taken from (C). Note that the af-ferent firing in the natural steps starts earlier than in the simu-lated movements. Also, in the natural records there is a markedburst early in E2 and background firing, which are not seen inthe passive movements in (E).

Duysens 1979), it becomes essential to investigate the wholematter further. To this end, we made observations duringdecerebrate locomotion of TA and MG spindle activity(Taylor et al. 2000a) and have compared the resulting pre-dictions of γ-motor firing with direct recordings from MG γ-motor axons (Taylor et al. 2000b). A floating electrode ar-rangement was used to record from a number of single spin-dle afferents in dorsal root filaments during active walking.The afferents were characterised both by conduction veloc-ity and by their responses to succinylcholine (see Taylor etal. 1992). The latter test shows which intrafusal musclefibres are contacted by each afferent and identifies primaryafferents with no contacts on bag1 fibres (b2c primaries). Af-ter making recordings during locomotion, fusimotor activitywas completely suppressed by i.v. pentobarbitone, the previ-ously recorded active ankle movements were reproducedpassively by means of an electromagnetic servo, and thespindle responses were again recorded. Similar locomotorcycles were then chosen, and responses were averaged sothat the firing profiles in passive conditions could be sub-tracted from those recorded in the presence of fusimotor ac-tivity to yield difference records. The difference recordsfrom secondary afferents (Fig. 6a and 6c) and from b2c pri-mary afferents (not shown) were taken to represent the pro-file of static fusimotor activity that existed in the activelocomotion. This indicated an increase before the onset oflocomotion, followed by a strongly modulated discharge inparallel with muscle shortening. The modulation profilesmatched the record of muscle shortening very closely in thecase of TA, but were phase-advanced with respect to short-ening in MG. The same effects were observed in primaryafferents, but with primaries there was also an afferent burst

during muscle lengthening (Fig. 6b and 6d). By subtractingan ensemble average of the difference signal for the b2c pri-mary afferents from the difference signal for b1b2c prima-ries, a burst of firing was revealed that was very similar inform to the stretch velocity profile. This clearly indicated theoccurrence of dynamic fusimotor activity during locomotion,but there was no way of knowing whether the dynamicfusimotor firing was continuous (tonic) or whether it variedduring the step cycle. This had to be decided by direct γ-axon recordings (Taylor et al. 2000b). The experiments wereessentially the same, but with the additional isolation of oneor more γ-axons in a filament of the MG muscle nerve.Static and dynamic efferents were identified by correlatingvariations in spontaneously occurring firing, or in responseto stimulation of the brainstem, with concurrent changes inthe responses of spindle afferents to ramp-muscle stretches.Static γ-axons, identified in this way, increased their firingat the onset of walking, and were then modulated in one oftwo patterns (Figs. 7a and 7b). In one group (type 1), firingwas strongly modulated, with the profile of rising frequencymatching precisely that predicted by the difference signal forsecondaries, as reported above. In the second group (type 2),the frequency rose slowly throughout the muscle-lengthening period, then fell back during active shortening.Type 1 units were twice as plentiful as, and were morestrongly modulated than, type 2 units. Their firing patterncould fully explain the fact that spindle afferents can actu-ally increase their frequency during active muscle shorten-ing, especially with secondaries. Whether or not a primaryfires during this period evidently depends on the speed ofshortening. It has been shown that, if shortening is fasterthan 0.2 resting lengths per second, afferent discharge can-

© 2004 NRC Canada

Taylor et al. 799

Fig. 6. Cycle average firing frequencies for spindle afferents during decerebrate locomotion. (A) Ensemble means for two TA second-ary afferents (!). The passive response to the imposed active movement has been subtracted from the active response to give a differ-ence record. Continuous line, ankle angle with TA shortening upwards. (B) Difference record for a TA b1b2c primary afferent.(C) Difference record for an MG b2c secondary afferent. (D) Ensemble average difference record for four b1b2c MG primaries. The ar-row head on the movement trace in each case shows the direction of muscle lengthening. Assembled from Figs. 4, 6, and 9 from Tay-lor et al. (2000a), with permission.

not be sustained (Prochazka et al. 1979; Prochazka 1981).The significance of the type 2 units is not yet clear, althoughone suggestion is that they may be providing innervationprincipally to the slow bag2 intrafusal fibres, whereas type 1may act via chain or chain plus bag2 fibres, which, in eithercase, can modulate afferent discharge strongly and rapidly(Durbaba et al. 2001). It is curious that, in the direct γ-axonrecordings by Murphy et al. (1984), the static units all ap-peared to show the type 2 firing pattern, that is, they wereonly weakly modulated (and hence referred to as tonicallymodulated). The chief experimental differences, whichmight have influenced the results, were that in the experi-ments of Murphy et al. (1984), the limb was deafferented,except for MG and soleus, and the muscle contraction oc-curred isometrically. In the experiments of Taylor et al.(2000b), the ankle was free to rotate, and the innervation ofTA and most of MG was retained.

Another surprising feature of the recent γ recordings is thepattern observed in dynamic axons (Fig. 7c). As Murphy etal. (1984) described, these were very strongly modulated,

and when their firing is recorded as instantaneous frequency,rather than by a heavily filtered ratemeter (Murphy andHammond 1990), they operate in an almost on–off manner.The onset of a high frequency discharge occurred abruptly,just before muscle shortening commenced, and continuedinto about the first 10% of lengthening before more slowlyfalling silent again. In separate experiments in which dy-namic γ-axons were stimulated for various periods during si-nusoidal stretch, the naturally observed timing ensured highsensitivity to the first part of muscle lengthening. In the lightof this, it may be that the natural pattern is best suited to de-riving a sharp afferent timing signal to indicate the onset ofthe muscle-lengthening phase.

With regard to γ-motor behaviour in flexor muscles,Murphy and Hammond (1993) argued that the different tasksfaced by TA and MG might be reflected in different γ pat-terns. It was found that TA γ-motoneurones had no back-ground discharge, but during locomotion, they dischargedwith 1 of the 2 patterns previously described (now desig-nated as phasic or tonic). In the absence of any means of

© 2004 NRC Canada

800 Can. J. Physiol. Pharmacol. Vol. 82, 2004

Fig. 7. Patterns of static and dynamic motoneurone firing in MG γ-axons during locomotion in decerebrate cat. (A) Top panel, anklerotation; middle panel, type 2 static unit; lower panel, type 1 static unit. (B) Averages from the 14 cycles of records illustrated in (A).Top: TA and MG smoothed rectified EMG; type 1 unit (!); type 2 unit (o); continuous line, ankle angle with MG shortening upwards.Time is normalyzed with respect to cycle duration, mean period 0.65 s. (C) Two dynamic γ-axons recorded simultaneously. Top panel,15 movement cycles superimposed (MG shortening upwards); middle panels, dot raster displays of the timing of γ-axon firing in suc-cessive cycles; bottom panel, ensemble mean for these two units. From Figs. 3 and 8 of Taylor et al. (2000b), with permission.

identifying the γ units as dynamic or static, they argued that,because previous spindle recordings (Perret and Berthoz1973; Cabelguen 1981; Taylor et al. 1985) had shown evi-dence of static γ drive during active contraction, the γ pat-terns observed in TA should be opposite to those for MG.The conclusion was that for TA, static γ-neurones were pha-sic and dynamic neurones were tonic during locomotion.The same 2 patterns of tonic and phasic modulation have re-cently been described in γ recordings in flexor digitorumlongus (FDL) and flexor hallucis longus (FHL) (Murphy2002). Some differences in phasing relative to alpha activitywere taken to suggest a task-dependent use of the γ output ofthese muscles, but no further evidence was advanced toidentify the two patterns. In related work on FHL and FDL(Murphy et al. 2002), an attempt was made to identify theunderlying static and dynamic patterns using intermediateamplitude 4–5 Hz sinusoidal stretches. In FHL, the evidencewas in favour of the tonic-static, phasic-dynamic concept. InFDL, there seemed be signs that static might be phasic ortonic.

The obvious need for a more satisfactory identification inTA has led us to recently extend the γ recordings to thismuscle, using the same identification methods used in MG(Taylor et al. 2004). In the case of TA, access to small mus-cle nerve filaments is more difficult, and single γ units aremore difficult to retain in the face of the vigorous MG andTA contractions. Nevertheless, data analysed so far from 30units, including 5 dynamics, strongly supports the existenceof patterns of activity entirely comparable with those de-scribed for MG. The main differences are (i) the lack ofbackground γ firing in TA (Murphy and Hammond 1993),and (ii) the fact that there is no phase advance in the TAstatic firing pattern with respect to the muscle shortening. Infact, the instantaneous firing frequency of the static γ-motoneurones matches the muscle-shortening record in de-tail. This fully justifies the deductions from previous TAspindle records (Taylor et al. 2000a).

Summary

Attempts to identify the natural firing patterns of γ-motoneurones have been made with a variety of techniquesfor some 40 years. There is still no way of obtaining the cru-cial direct γ recordings during normal movements; we mustrely either on indirect deduction from spindle afferent re-cordings in intact or reduced preparations, or on direct re-cordings in reduced preparations. The difficulties involved inthe experiments have meant that the amount of data avail-able has been limited and has been derived from rather di-verse approaches. The consequence has been that a clear andgenerally accepted account of the way in which the γ-motorsystem is used has not emerged. Various guiding principleshave been advanced, notably the follow-up servo, alpha-gamma coactivation or linkage, servo-assistance, fusimotorset, and temporal template, but none have proven entirelysatisfactory. In this review, we chose to avoid these terms,because they might introduce an element of pre-judgement,and to simplify matters by keeping strictly to studies of lo-comotion in the cat.

The outcome is that, from the work on decerebrate prepa-rations with unloaded ankle movements, the static γ moto-

neurones show a strong and continuous pattern of modula-tion, which is in time with flexor muscle shortening, butphase-advanced with respect to extensor shortening. Staticfiring also increases in mean frequency during locomotion,especially in extensors. There is some evidence that there isa minority population of static γ-motoneurones with aweaker and differently phased firing profile. Dynamic γ-motoneurones are also strongly modulated, but with a differ-ent pattern. Their firing starts at a high frequency very sud-denly at the onset of muscle shortening, is maintained intothe early part of lengthening, and then ceases firing lessabruptly. This activity seems well-adapted to preparing themuscle spindle primaries to signal the onset of lengthening.From the work on normal locomotion, there is some evi-dence that static γ firing is modulated, but it is often ob-scured by the unloading effects of rapid muscle shortening.Dynamic γ activity seems to be increased, but there is no ev-idence of a modulated pattern.

These findings still have to be clarified, but methods areconstantly being refined, so a concensus on natural γ-motorpatterns may soon be reached. Then the serious business ofexplaining the strategy of this aspect of motor control canbegin.

References

Cabelguen, J.-M. 1981. Static and dynamic fusimotor controls invarious hindlimb muscles during locomotion activity in thedecorticate cat. Brain Res. 213: 83–97.

Cabelguen, J.-M., Orsal, D., and Perret, C. 1984. Discharges offorelimb spindle primary afferents during locomotor activity inthe decorticat cat. Brain Res. 306: 359–364.

Hulliger, M. 1984. The mammalian muscle spindle and its centralcontrol. Rev. Physiol. Biochem. Pharmacol. 101: 1–110.

Hulliger, M., and Prochazka, A. 1983. A new simulation method todeduce fusimotor activity from afferent discharge recorded infreely moving cats. J. Neurosci. Methods, 8: 197–204.

Hulliger, M., Dürmüller, N., Prochazka, A., and Trend, P. 1989.Flexible fusimotor control of muscle spindle feedback during avariety of natural movements. Prog. Brain Res. 80: 87–101.

Hulliger, M., Bishop, G.M., Djupsjöbacka, M., and Zanussi, A.1998. Large fibre sensory contribution to the control of locomo-tion studied by non-invasive deafferentation. Gait Posture, 8:226–233.

Loeb, G.E., and Duysens, J. 1979. Activity patterns in individualhindlimb primary and secondary afferents during normal move-ments in unrestrained cats. J. Neurophysiol. 42: 420–440.

Loeb, G.E., and Hoffer, J.A. 1985. Activity of spindle afferentsfrom cat anterior thigh muscles. II. Effects of fusimotor block-ade. J. Neurophysiol. 54: 565–577.

Loeb, G.E., Bak, M.J., and Duysens, J. 1977. Long-term unit re-cording from somatosensory nerons in the spinal ganglia of thefreely walking cat. Science, 197: 1192–1194.

Murphy, P.R. 2002. Tonic and phasic discharge patterns in toeflexor γ-motoneurons during locomotion in the decerebrate cat.J. Neurophysiol. 87: 286–294.

Murphy, P.R., and Hammond, G.R. 1990. γ-motoneurone dischargepatterns during fictive locomotion in the decerebrate cat. Exp.Physiol. 75: 107–110.

Murphy, P.R., and Hammond, G.R. 1993. The locomotor dischargecharacteristics of ankle flexor γ-motoneurones in the decerebratecat. J. Physiol. 462: 59–70.

© 2004 NRC Canada

Taylor et al. 801

Murphy, P.R., Stein, R.B., and Taylor, J. 1984. Phasic and tonicmodulation of impulse rates in γ-motoneurones during locomo-tion in premammillary cats. J. Neurophysiol. 52: 228–243.

Murphy, P.R., Pearson, K., and Stein, R.B. 2002. Toe flexor musclespindle discharge and stretch modulation during locomotor ac-tivity in the decerebrate cat. J. Physiol. 542: 939–949.

Perret, C., and Berthoz, A. 1973. Evidence of static and dynamicfusimotor actions on the spindle response to sinusoidal stretchduring locomotor activities in the cat. Exp. Brain Res. 18: 178–188.

Perret, C., and Buser, P. 1972. Static and dynamic fusimotor activ-ity during locomotor movements in the cat. Brain Res. 40: 165–169.

Prochazka, A. 1981. Muscle spindle function during normal move-ment. In Neurophysiology IV. International review of physiol-ogy. Edited by R. Porter. University Park Press, Baltimore, Md.pp. 47–90.

Prochazka, A. 1996. Proprioceptive feedback and movement regu-lation. In Handbook of physiology: section 12. Exercise: regula-tion and integration of multiple systems. Edited by L.B. Rowelland J.T. Sheperd. American Physiological Society, New York,N.Y., pp. 89–127.

Prochazka, A. 1999. Quantifying proprioception. Prog. Brain Res.123: 133–142.

Prochazka, A., and Gorassini, M. 1998a. Models of ensemble fir-ing of muscle spindle afferents recorded during normal locomo-tion in cats. J. Physiol. 507: 277–292.

Prochazka, A., and Gorassini, M. 1998b. Ensemble firing of mus-cle afferents recorded during normal locomotion in cats. J.Physiol. 507: 293–304.

Prochazka, A., Westerman, R.A., and Ziccone, S.P. 1976. Dis-charges of single hindlimb afferents in the freely moving cat. J.Neurophysiol. 39: 1090–1104.

Prochazka, A., Westerman, R.A., and Ziccone, S.P. 1977. Ia affer-ent activity during a variety of voluntary movements in the cat.J. Physiol. 268: 423–448.

Prochazka, A., Stephens, J.A., and Wand, P. 1979. Muscle spindledischarge in normal and obstructed movements. J. Physiol. 287:57–66.

Prochazka, A., Trend, P., Hulliger, M., and Vincent, S. 1989. En-semble proprioceptive activity in the cat step cycle: towards arepresentative look-up chart. Prog. Brain Res. 80: 61–74.

Severin, F.V. 1970. The role of the gamma motor system in the ac-tivation of the extensor alpha motor neurones during controlledlocomotion. Biofizika, 15: 1096–1102.

Severin, F.V., Orlovskii, G.N., and Shik, M.L. 1967. Work of themuscle spindle receptors during controlled locomotion.Biofizika, 12: 502–511.

Sjöström, A and Zangger, P. 1975. α-γ-linkage in the spinal gener-ator for locomotion in the cat. Acta Physiol. Scand. 94: 130–132.

Sjöström, A and Zangger, P. 1976. Muscle spindle control duringlocomotor movements generated by the deafferented spinal cat.Acta Physiol. Scand. 97: 281–291.

Taylor, A., and Davey, M.R. 1968. Behaviour of jaw muscle stretchreceptors during active and passive movements in the cat. Na-ture, 220: 301–302.

Taylor, J., Stein, R.B., and Murphy, P.R. 1985. Impulse rates andsensitivity to stretch of soleus muscle spindle afferent fibers dur-ing locomotion in premammillary cats. J. Neurophysiol. 53:341–360.

Taylor, A., Rodgers, J.F., Fowle, A.J., and Durbaba, R. 1992. Theeffect of succinylcholine on cat gastrocnemius muscle spindleafferents of different type. J. Physiol. 456: 629–644.

Taylor, A., Ellaway, P.H., and Durbaba, R. 1999. Why are therethree types of intrafusal muscle fibers? Prog. Brain Res. 123:121–131.

Taylor, A., Durbaba, R., Ellaway, P.H., and Rawlinson, S. 2000a.Patterns of fusimotor activity during locomotion in thedecerebrate cat deduced from recordings from hindlimb musclespindles. J. Physiol. 522: 515–532.

Taylor, A., Ellaway, P.H., Durbaba, R., and Rawlinson, S. 2000b.Distinctive patterns of static and dynamic gamma motor activityduring locomotion in the decerebrate cat. J. Physiol. 529: 825–836.

Taylor, A., Durbaba, R., Ellaway, P.H., and Rawlinson, S. 2004.Flexor γ-motor patterns during locomotion. J. Physiol. In press.

© 2004 NRC Canada

802 Can. J. Physiol. Pharmacol. Vol. 82, 2004