3 - Features of the system for movement production

1. Histological and histochemical studies suggest that each tendon organ in a mixed mammalian muscle should be particularly responsive to the contraction of a discrete number of motor units (ca. ten to fifteen), each with differing mechanical properties. This report describes physiological experiments that demonstrate this arrangement for the tendon organs of cat medial gastrocnemius. 2. No correlations could be found between the intensity of discharge of a single tendon organ and the contraction strengths of motor units whose contraction excited the receptor. Tendon organs were found to be as responsive to contraction of small slow twitch units as they were to contraction of larger fast twitch units. Taking the data as a whole, the apparent sensitivity of the receptors during motor unit contractions (pps/force recorded at the tendon) was inversely related to the contraction strengths of the motor units. 3. These findings are discussed in relation to recent evidence on the territory of single motor units in medial gastrocnemius and the force producing capabilities of their individual muscle fibres. It is concluded that in general each motor unit, whose contraction excites a given receptor, contributes one muscle fibre to the receptor capsule. Further, it appears that the various excitatory effects of those muscle fibres inserting into a given receptor capsule are not simply related to their relative contraction strengths but also depend on the details of the mechanical coupling between each fibre and the Ib afferent receptor endings. 4. The results of an ensemble analysis show that despite the lack of correlation between the intensity of tendon organ discharge and the force developed at the tendon during contraction of different motor units, a correlation does appear when the responses of several tendon organs and the forces developed by the motor units which excite them are summed progressively. This finding has implications for the recruitment order of motor units in that the profile of the collective Ib response is shown to differ according to whether motor unit forces are summed randomly or in order of increasing contraction strengths.

1. The responses of individual tendon organs of the cat peroneus tertius muscle to motor-unit contractions were recorded in anesthetized cats during experiments in which all the Ib-afferent fibers from the muscle had been prepared for recording in dorsal root filaments. This was possible because the cat peroneus tertius only contains a relatively small complement of approximately 10 tendon organs. 2. Motor units of different physiological types were tested for their effects on the whole population of tendon organs in the muscle. Effects of unfused tetanic contractions were tested under both isometric and anisometric conditions. Each motor unit activated at least one tendon organ, and each tendon organ was activated by at least one motor unit. Individual slow-type units were found to act on a single or two receptors, whereas a fast-type unit could activate up to six tendon organs. 3. In one experiment, the effects of 8 motor units on 10 tendon organs were examined. One fast-twitch, fatigue resistant (FR)-type unit acted on six tendon organs, of which four were also activated by another FR unit. The contraction of each unit, on its own, elicited a range of individual responses, from weak to strong. The discharge frequencies of individual responses displayed no clear relation with the strength of contraction, nor did they accurately represent the shape of force profiles. But when all the discharges were pooled, a fairly good correspondence appeared between variations of contractile force and variations of averaged discharge frequencies.(ABSTRACT TRUNCATED AT 250 WORDS)

1. The discharges from individual Golgi tendon organs of peroneus tertius and brevis muscles were recorded in anesthetized cats. Responses to unfused isometric contractions of single motor units and combinations of motor units were compared with responses to contractions eliciting muscle shortening (i.e., shortening contractions). 2. In 75% of the examined instances, the effect of muscle shortening during unfused contractions was a slight decrease in tendon organ activation, in keeping with the reduction of contractile tension recorded at the muscle tendon. In other instances there was either no change in tendon organ response or, in less than 10% of instances, a slight increase For two motor units eliciting similar activation of a given tendon organ under isometric conditions, the effect of shortening contraction was not necessarily the same. 3. The reductions observed in tendon organ discharges upon muscle shortening were less than proportional to the reductions of contractile tension and difficult to correlate with the properties of motor units, as determined under isometric conditions. The present observations suggest three main reasons for this lack of relation. 4. The first reason depended on the properties of motor units, in that the relation between length changes and tension changes was not the same for all units. Two motor units developing similar isometric tensions did not necessarily produce the same degree of muscle shortening. Some units produced relatively significant shortening without much loss of tension. 5. Second, the dynamic sensitivity of tendon organs is known to exert a major influence on their responses to isometric unfused contractions, accounting for 1:1 driving of discharge during tension oscillations and high frequency bursts upon abrupt increase of tension. Although less tension was produced and the rate of tension development was slower in shortening contractions, similar manifestations of the dynamic sensitivity of tendon organs were observed. In such cases, the responses of tendon organs were the same whether or not the muscle shortened during contraction. 6. Third, when several motor units were stimulated in combination, the unloading influences of in-parallel units were facilitated by muscle shortening so that unloading effects, which were hardly visible under isometric conditions became evident during shortening contractions.

The responses of 13 Golgi tendon organs to graded force development of 29 motor units in medial gastrocnemius of the cat have been studied in five experiments. Of the 13 tendon organs, 11 were responsive to passive stretch within the physiological range of muscle length and 5 were "spontaneously" active at very short lengths where no passive tension could be recorded. The relationship between passive force and the firing rates of the various afferents ranged from a linear one to a power relation (Y = Axb + c) with b, a widely varying exponent. Results support the general conclusion that although many Ib afferents respond to passive force within the physiological range of muscle stretch, this form of stimulus is not a particularly effective one. The statis responses of Golgi tendon organs to active force development produced by single motor units was studied at different muscle lengths. In all cases the apparent sensitivity (change in firing rate per active force developed) decreased as muscle length approached Lo. The static responses of Golgi tendon organs to force developed by single motor units were also studied during fatiguing contractions. The data suggest a sigmoid relationship between force developed at the tendon and the Ib response. The collective response of all 13 tendon organs to active and passive forces at different muscle lengths was also examined. This analysis offered further support for the viewpoint that active motor unit contractions provide themost significant excitatory input to tendon organs and that changes in passive force during muscle stretch have comparatively little effect on the collective tendon organ response. The interaction between active and passive force inputs to the Golgi tendon organs is discussed in relation to the complicated nature of the relationship between forces measured at the tendon and those acting within the receptor capsule. When these complications were taken into account it was possible to explain the differences in responsiveness of a given tendon organ to active contraction of several motor units and to passive force in terms of a single force-firing rate curve for the receptor. It is concluded that changes in the force of contraction of single motor units result in relatively small changes in Ib afferent firing and that during normal muscle contractions, changes in the number of motor units acting on a single receptor must produce far more significant changes in firing rate than changes in the amount of force developed by any single unit. Changes in dynamic Ib sensitivity to single motor unit contractions are also shown to depend on length and in a similar way to the changes in static Ib sensitivity. During fatiguing contractions, a sigmoid relation was found between the dynamic Ib response and the rate of force development by single motor units.

The discharges of individual tendon organs of peroneus longus and tertius muscles were examined in anesthetized cats during stimulation of single motor units at frequencies that elicit unfused contraction (5-50/s). At these frequencies nearly all the fast-contracting motor units activating a tendon organ elicited responses whose discharge rates reproduced the stimulation frequency ("1:1 driving"), whereas slow-contracting motor units elicited responses in which the discharge rate was higher than the stimulation frequency. When a motor unit stimulated at 40/s developed a gradually potentiating tension, the tendon organ discharge could remain locked on stimulation frequency over an appreciable range of the increasing tension as if the receptor responded to the tension oscillations rather than to the mean level of tension. The only visible effect of the gradual increase in mean tension on the tendon organ response was a gradual decrease of the delay between each stimulus and the corresponding impulse. Driving of tendon organ discharge at the stimulation frequency occurred not only when relatively large oscillations were superimposed on a low level of static tension but also when the static component of the tension was quantitatively preponderant. These observations suggest that during unfused contractions the dynamic component of the stimulus (i.e., oscillation of tension) exerts a prevailing influence on the discharge pattern of tendon organs. Computed simulations of tendon organ responses confirmed that a relatively strong dynamic sensitivity could account for the observed behavior of the receptor.

The model of tendon organ activation proposed by Houk and Henneman (1967) has been tested by considering two of its implicit predictions: (1) that only a select group of motor units within a muscle can provide an adequate stimulus to a given tendon organ; and (2) that due to the presence of motor units that can “unload” a given tendon organ, its response to whole muscle contraction can be less vigorous than that to contraction of just the excitatory motor units alone. Tendon organ afferents from the soleus muscle of the cat were functionally isolated from dorsal root filaments. The L7 and S1 ventral roots were split into 25 to 50 “natural” subdivisions, each of which was stimulated at 50 to 100 Hz for 1.5 s. The subdivided filaments were segregated into two groups; those which when stimulated elicited discharge from the Ib afferent (“excitatory” filaments) and those which did not (“non-excitatory” filaments). In ten of eleven experiments, it was found that when all the excitatory filaments were separated out, concurrent stimulation of all the non-excitatory filaments failed to excite the tendon organ, even when these filaments generated over 90% of the muscle's peak tetanic tension. The response of a tendon organ to stimulation of just its excitatory filaments often exceeded its response to whole muscle stimulation. However, several exceptions to this finding were observed, indicating that some tendon organs are affected by “off-line” forces. In general, the present results lend strong support to the Houk and Henneman model.

Golgi tendon organ (GTO) responses reveal pronounced non-linearities in that excitation by combined action of several motor units (MU) is less than the sum of the excitatory effects elicited by the individual MUs (see Jami, 1992; review). Such sub-linear summation is not caused by simple receptor saturation since the degree of non-linearity is independent of the level of firing rate (Gregory & Proske, 1979). It has been suggested that unloading effects elicited by MUs located in parallel to a GTO might account for the nonlinear summation (Fukami, 1981) and, implicitly, for the gain compression in the firing rate-force relation. Another possibility is that the non-linearity results from interactions between multiple transducers and/or encoders within the receptor (Gregory, Morgan & Proske, 1985). The aim of the present study was to clarify the role of different receptor mechanisms in non-linear summation.

The structure and response properties of Golgi tendon organs in control and hypodynamia–hypokinesia rats

Golgi tendon organs from human, cat and rat extensor digitorum brevis muscles are compared in structural design. Microscopic studies reveal that these receptors appear to be very similar in structure, suggesting close functional similarities even though they are largest in man, intermediate size in cats and smallest in rats. This contrasts with similar observations on the structure of muscle spindles which show strong differences in respect to the insertion of intrafusal muscle fibers thereby implying species specialization of response characteristics to intramuscular tensions and pressures.Reconstructive drawings of human tendon organs from serial sections suggest how sensory endings may be affected by tensions at the musculotendinous junctions due to stretch or contraction of motor units. Finely divided collagen bundles appear to compress and distort nerve endings lying between them, thus inducing the generation of spike discharges.

Henneman's size principle relates the input and output properties of motoneurons and their muscle fibers to size and is the basis for size-ordered activation or recruitment of motor units during movement. After nerve injury and surgical repair, the relationship between motoneuron size and the number and size of the muscle fibers that the motoneuron reinnervates is initially lost but returns with time, irrespective of whether the muscles are self- or cross-reinnervated by the regenerated axons. Although the return of the size relationships was initially attributed to the recovery of the cross-sectional area of the reinnervated muscle fibers and their force per fiber, direct enumeration of the innervation ratio and the number of muscle fibers per motoneuron demonstrated that a size-dependent branching of axons accounts for the size relationships in normal muscle, as suggested by Henneman and his colleagues. This same size-dependent branching accounts for the rematching of motoneuron size and muscle unit size in reinnervated muscles. Experiments were carried out to determine whether the daily amount of neuromuscular activation of motor units accounts for the size-dependent organization and reorganization of motor unit properties. The normal size-dependent matching of motoneurons and their muscle units with respect to the numbers of muscle fibers per motoneuron was unaltered by synchronous activation of all of the motor units with the same daily activity. Hence, the restored size relationships and rematching of motoneuron and muscle unit properties after nerve injuries and muscle reinnervation sustain the normal gradation of muscle force during movement by size-ordered recruitment of motor units and the process of rate coding of action potentials. Dynamic modulation of size of muscle fibers and their contractile speed and endurance by neuromuscular activity allows for neuromuscular adaptation in the context of the sustained organization of the neuromuscular system according to the size principle.

Tendon organs respond preferentially to contractions of a select set of motor units. If a tendon organ is given a resting discharge by raising the passive tension in the muscle, other motor units can be identified which on contraction interrupt the discharge, presumably by unloading the passive tension. These experiments investigate the possibility that stimulation of motor units with unloading effects can reduce the response of a tendon organ to a loading contraction. We find that over most of the range of muscle lengths the unloading contraction produces only a transient lowering of the firing rate. Only at short muscle lengths where further shortening is accompanied by a steep fall in tension is the unloading contraction able to induce a sustained reduction of afferent discharge.

Motor unit synchronization refers to temporal associations among action potentials of the active motor units in a muscle contraction. A method developed by Milner-Brown et al. (1973; 1975) has been widely cited for assessing short-term synchronization in a population of motor units. A major limitation of this method, however, is its inability to accurately distinguish synchronization from methodological artifact related to signal rectification (Yue et al., 1995). The purpose of this study was to examine the effectiveness of an alternative assessment, a Stochastic Method (Xiong et al., 2000), for quantifying synchrony in a population of motor units. Surface EMG was simulated at 4 levels of excitation: 10%, 30%, 50%, and 70% of the maximum level. It was simulated by generating muscle fiber action potentials; acquiring motor unit action potentials; and specifying motor unit discharge times. The level of synchrony among the simulated motor units was determined by adjusting the timing of the occurrence of the selected motor unit action potentials. The synchronization index (SI) was calculated by the stochastic method. To test the efficacy of the stochastic method in assessing motor unit synchronization, the SI determined by the stochastic method was compared to a recently published SI (Yao et al., 2000). The method by Yao et al. requires to dividing the entire simulation period into separated 1-ms bins and enumerating the action potentials of the active motor units in each bin. Thus, this method is highly accurate in determining synchronization in a population of motor units from simulated EMG. By comparing the SI of the stochastic method to that of Yao et al., the accuracy of the stochastic method SE can be determined. Pearson Correlation Coefficient calculated by using the indexes determined by the two different methods was 0.8149, and p < .001. This result suggests that the stochastic method is a fairly accurate method in determining synchronization in a population of motor units. Unlike the method of Yao et al., which cannot be used for synchronization measurements based on real EMG data, the stochastic method is fully applicable for synchronization measurements using real EMG data because all parameters needed for the synchronization calculation are directly measurable. This advantage enables evaluations of motor unit synchronization by the stochastic method in a variety of experimental and clinical situations, in which determining synchrony with accuracy among a motor unit population was not previously possible.

POINT-COUNTERPOINTRebuttal from FarinaPublished Online:01 Nov 2008https://doi.org/10.1152/japplphysiol.90598.2008cMoreSectionsPDF (36 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInEmailWeChat Although von Tscharner and Nigg (8) focus on the time-frequency analysis of the surface EMG and the results obtained in a number of experimental studies (e.g., Refs. 6, 7), their point of view illustrates the general issues that I outlined in my Counterpoint (1). A fundamental confusion is apparent in one of the opening statements of my colleagues: “A refined subdivision of fibers was proposed correlating fiber types with EMG spectral properties” (8). According to this statement, slow and fast fibers are defined as fibers with surface action potentials with relative energy mainly at low and high frequencies, respectively, and this definition is considered more appropriate (“refined”) than the schemes based on histochemistry (type I and II) and physiology (slow and fast twitch). Surface EMG spectral properties are thus used to directly define, rather than indirectly identify, muscle fiber types, which is the central issue in this debate. Consistent with this perspective, the main evidence that my colleagues present to illustrate their Point (8) consists in the wavelet transform of surface EMG signals recorded during running. They associate high (low) frequencies in the surface EMG to recruitment of fast (slow) motor units, although they do not provide a direct measure or a theoretical rationale to prove this association when a histochemical or physiological definition of fiber type is used.In response to the unequivocal experimental evidence of inconsistency of surface EMG spectral properties with motor unit recruitment strategies in simple cases when these strategies are predictable (e.g., 2, 3, 10), my colleagues reply that when studying “single-task experiments such as isometric ramped increase in force…substantial changes in the power spectra should not be expected.” However, surprisingly, they support their own interpretations with results reported for this type of contraction (4, 5, 9). While my colleagues consider the lack of consistency of the association between EMG spectral analysis and recruitment strategies irrelevant because it comes from “single-task experiments”), the occasional observation of this association during the same type of “single-ask experiments” is used as the basis for a “refined subdivision” of fiber types.The assertion by von Tscharner and Nigg (8) that surface EMG spectral properties provide information about recruitment strategies and fiber-type proportions is based on distinguishing between surface motor unit action potentials and not on the physiological properties of the motor units.REFERENCES1 Farina D. Counterpoint: Spectral properties of the surface EMG do not provide information about motor unit recruitment and muscle fiber type. J Appl Physiol; doi:10.1152/japplphysiol.90598.2008a.Link | ISI | Google Scholar2 Gabriel DA, Kamen G. Experimental and modeling investigation of spectral compression of biceps brachii SEMG activity with increasing force levels. J Electromyogr Kinesiol. 2007 Dec 11. [Epub ahead of print].Google Scholar3 Gerdle B, Karlsson S, Crenshaw AG, Fridén J. The relationships between EMG and muscle morphology throughout sustained static knee extension at two submaximal force levels. Acta Physiol Scand 160: 341–351, 1997.Crossref | PubMed | Google Scholar4 Karlsson S, Gerdle B. Mean frequency and signal amplitude of the surface EMG of the quadriceps muscles increase with increasing torque—a study using the continuous wavelet transform. J Electromyogr Kinesiol 11: 131–140, 2001.Crossref | ISI | Google Scholar5 Solomonow M, Baten C, Smit J, Baratta R, Hermens H, D'Ambrosia R, Shoji H. Electromyogram power spectra frequencies associated with motor unit recruitment strategies. J Appl Physiol 68: 1177–1185, 1990.Link | ISI | Google Scholar6 von Tscharner V, Goepfert B. Estimation of the interplay between groups of fast and slow muscle fibers of the tibialis anterior and gastrocnemius muscle while running. J Electromyogr Kinesiol 16: 188–197, 2006.Crossref | ISI | Google Scholar7 von Tscharner V, Goepfert B, Nigg BM. Changes in EMG signals for the muscle tibialis anterior while running barefoot or with shoes resolved by non-linearly scaled wavelets. J Biomech 36: 1169–1176, 2003.Crossref | ISI | Google Scholar8 von Tscharner V, Nigg BM. Point: Spectral properties of the surface EMG provide information about motor unit recruitment and muscle fiber type. J Appl Physiol; doi:10.1152/japplphysiol.90598.2008.Link | ISI | Google Scholar9 Wakeling JM, Syme DA. Wave properties of action potentials from fast and slow motor units of rats. Muscle Nerve 26: 659–668, 2002.Crossref | PubMed | ISI | Google Scholar10 Westbury JR, Shaughnessy TG. Associations between spectral representation of the surface electromyogram and fiber type distribution and size in human masseter muscle. Electromyogr Clin Neurophysiol 27: 427–435, 1987.Google Scholar Download PDF Previous Back to Top Next FiguresReferencesRelatedInformation More from this issue > Volume 105Issue 5November 2008Pages 1675-1675 Copyright & PermissionsCopyright © 2008 the American Physiological Societyhttps://doi.org/10.1152/japplphysiol.90598.2008cHistory Published online 1 November 2008 Published in print 1 November 2008 Metrics

12 - Electrodiagnostic Examination

The cat step cycle: hind limb joint angles and muscle lengths during unrestrained locomotion.