BACKGROUND:The distribution of muscle spindles (Sps) in a small muscle of simple architecture, the capsularis at the cat's hip joint, was quantified to reveal the patterns of proprioceptive representation in the transverse and sagittal planes as well as to model the effect a local disturbance in muscle length would have on total Sp discharge.METHODS:Locations in serial cross-sections of the 32 and 38 Sps in 2 muscles, 1 perfused with the hip joint flexed and the other extended, were plotted, and their patterns of integrated sensitivity calculated assuming that (1) the discharge rate of a Sp afferent varies linearly with change in length along the Sp's axis, and (2) that within a local disturbance produced by contraction of a motor unit (MU), lengths decrease either linearly or as the square of the distance from its center.RESULTS:The isomeric pattern of "integrated, total Sp representation on cross-section" showed two peaks of sensitivity in the half of the muscle that had been next to the joint capsule, offset by low representation in a small, central area and along the extensive zone bordering the laterally facing "superficial surface." The equivalent radius of an idealized symmetrical MU territory was estimated from distributions of the few fast, oxidative-glycolytic fibers found in two muscles, and the effect of a MU's contraction on net Sp discharge predicted when the unit was positioned at distinctive sites within the pattern. As an index of Ia and II afferent representation in the sagittal plane, the distribution of the nucleated regions of Sps and the summed lengths of segments of Sp axial bundles and capsules, respectively, within successive 1-mm segments of the muscle were graphed.CONCLUSIONS:The longitudinal representation and structure of the muscle are not suited for reflex adjustment of differences in length along the muscle. The isomeric pattern of high relief in the transverse plane suggests that in this approximately 0.2 g muscle, the localization of myotatic reflexes might be accommodated but the need for adjustment in activation of MUs seems minimal. This is because the muscle is not compartmentalized, its fibers extend between the muscle's origin and insertion, their angle of pinnation is low, and greater than 90% are of slow type. The distribution of Sps is consistent with gauging length of the entire muscle and hence angulation at the hip joint.

The spatial representation of muscle spindles (Sps) in the small (approximately 0.2 g), simply structured capsularis muscle that crosses anterior to the cat's hip joint was compared with the distribution of the slow oxidative (SO) and few (< 10%) fast oxidative-glycolytic (FOG) fibers of which it is composed to see if their distributions were consistent with a hypothesis that sensory input from Sps influences the incidence of extrafusal fiber types. In frozen sections from 4 muscles, FOG fibers were enumerated along 1-mm strips across the muscle's maximum width, and between the 'superficial' surface and the 'deep' one that contacts the joint. The locations of Sps in complete serial sections of 2 paraffin-embedded muscles, one perfused with the hip joint flexed and the other with it extended, were plotted on an outline of each muscle at its midlength, and their numbers and density in horizontal and sagittal 'strata' determined. In general, the incidence of Sps increased down the superficial-to-deep axis, while FOG fibers became fewer, as is consistent with support of SO status by Sp input. Along the craniocaudal axis, i.e. width, the numbers of FOG fibers rose toward the hip joint, but this was not associated with a monomodal gradient of Sps. In the extended muscle, however, the lengths of the axial bundle and capsular space of Sps in the half of the muscle next to the joint exceeded those in the longer, cranial half, implying that under stretch the input from Sps became higher toward the joint. In the non-extended muscle these lengths did not differ, although the lengths of extrafusal fibers isolated from 2 macerated muscles and normalized according to sarcomere length decreased linearily by approximately 50% along craniocaudal axis. It is explained that if elastic resistance of a Sp's sensory region exceeded that of an equivalent length of septal tissue in-series, the progressive shift in the ratio of compliances across this trapezoidally-shaped muscle should result in relatively greater lengthening of Sps at the shorter border as the muscle was extended. Levels of discharge conducive to transition of some motor units to the FOG type might be attained. Thus, gradients in the discharge of Sps (but not necessarily incidence) along both transverse and superficial-to-deep axes may be consistent with Sp sensory input influencing the distribution of at least these types of motor units.

The physiological cross-sectional area (CSA) of a motor unit (MU), taken as the sum of fiber areas measured on a single section through the approximate midlength of the MU, has been compared with the physiological CSA more strictly defined as the sum of the maximal areas to be found anywhere along the length of each of the MU fibers. The CSA at intervals along the fiber length was measured in fibers selected from four glycogen-depleted, isolated MUs in the cat tibialis anterior (TA), and profiles of the summed areas made. In one MU, measurements were also taken on all the MU's fibers at less frequent intervals. The profiles demonstrate that the summed CSA based on each fiber's maximum CSA may exceed that derived from observation on any single section by as much as 20%. As a consequence, values that have been reported for specific tension (force per unit area) of MUs in the TA and probably other muscles may have been overestimated, especially for those MUs of fast type. Estimates were also made of the share of the MU's total force transmitted directly to the tendons of origin and insertion via endings of the blunt musculotendinous type as distinct from tapering intrafascicular endings acting through in-series connective tissue and non-MU fibers. In two MUs of slow type in which most fibers ran from tendon to tendon, "partial tapering" extending over 1 cm of the fiber length accounted for a third of the total physiological CSA, and indicated yet another mode for relay of the MU's force to the tendon.

The geometric shape of the filamentous, intrafascicular type of muscle fiber ending was reconstructed as a basis for understanding the pattern in relay of the fiber's force to the muscle tendon. Single motor units (MUs) identified physiologically as being fast and slow, respectively, were isolated in cat tibialis muscles and glycogen-depleted for recognition in cross sections of the muscle frozen at its Lo. Serial measurements of cross-sectional area (CSA) using an image processing system were made along 14 intrafascicular endings of MU fibers and an additional seven, non-depleted fibers identified histochemically as slow. Comparison of coefficients of variation for the linear relation of the CSAs and of the equivalent diameters with length along the taper indicated that in both fast and slow fibers the areas bore a closer relationship, that is, the taper had the equivalent of a parabolic, rather than a conical outline. The implications of these two conformations to relay of the fiber's contractile force to surrounding structures are displayed graphically.

There is increasing evidence that the architectural design and arrangement of the fibers within a motor unit have important physiological and developmental ramifications. Limited data, however, are available to directly address this issue. In the present study the physiological properties of one motor unit in each of seven cat tibialis anterior (TA) muscles were determined. Each of these units then was repetitively stimulated to deplete the glycogen in all muscle fibers within the unit. Subsequently, the length, type of ending, and spatial distribution of fibers sampled from these physiologically and histochemically typed motor units were determined. Four fast fatigable (FF), one fast, fatigue resistant (FR), and two slow (S) motor units (MU) were studied. The samples consisted of all those glycogen-depleted fibers (9-27) contained within a single fascicle or a circumscribed area of each of the motor unit territories. The mean fiber lengths for the two slow motor units were 35.9 and 45.5 mm. The mean fiber lengths for the fast motor unit samples ranged from 8.8 to 48.5 mm. Some fibers of both the fast and slow units reached lengths of 58 mm. Most of the fibers in the slow units extended the entire distance between the proximal and distal musculotendinous planes, had relatively constant cross-sectional areas, and terminated at the tendon as blunt endings. In contrast, the majority of the fibers in the fast units terminated intrafascicularly at one end, and the cross-sectional area decreased progressively along their lengths, that is, showed a tapering pattern for a significant proportion of their lengths. Therefore, the force generated by units that end midfascicularly would appear to be transmitted to connective tissue elements and/or adjacent fibers. All fibers of a fast unit within a fascicle were located at approximately the same proximo-distal location. Thus, developmentally the selection of muscle fibers by a motoneuron would seem to be influenced by their spatial distribution. The architectural complexities of motor units also have clear implications for the mechanical interactions of active and inactive motor units. For example, the tension capabilities of a motor unit may be influenced not only by the spatial arrangement of its own fibers, but also by the level of activation of neighboring motor units.

Estimates were made of the changing volumes of discharge arising from the total populations of Ia and II spindle afferent fibers in the cat's deefferented medial gastrocnemius as the muscle was extended stepwise over its excursion range. The estimates were based on values reported elsewhere for (i) the incidence of active units and (ii) their rates of discharge at static muscle lengths normalized against the excursion range of the particular muscle, together with (iii) the numbers of Ia and II afferent fibers in the medial gastrocnemius as derived from a critical review of published information. Curves representing the total discharge of the two afferent types are similar and show three phases: an initial level of spontaneous activity, a somewhat curvilinear rise associated with early recruitment of units during stretch, and rectilinear increase after full recruitment. There was no appearance of saturation. Completion of recruitment of both types of units occurred about halfway in the extension range of the passive muscle. Over most of the excursion range, inflow from the group II population was about one-third greater than that from the Ia units.

The static discharge characteristics of deefferented Ia and II spindle afferents in the cat medical gastrocnemius muscle have been compared with respect to incidence and firing rate of spontaneously firing units, length threshold of non spontaneous units, linearity of the response to stretch, and position sensitivity. Measurements of the stretch response were taken 20 s after each step increase in length so as to obtain the nearly fully adapted rate. Under this condition the frequency-length relationship was quite linear, especially for group II units. The mean position sensitivity of group II fibers exceeded that of I a fibers in the ratio of 1.5∶1.0. The incidence of spontaneously discharging units was about 20% for both types of unit.

Characteristics of soleus (SOL) and medial gastrocnemius (MG) muscles in cats cordotomized at either 2 or 12 weeks of age, some of which were exercised on a treadmill during the following 11 to 19 weeks, were compared to see if age at spinalization or if enforced exercise on a treadmill had any differential effects. In non-exercised animals, SOL weights in both 2-week and 12-week groups were less than in 14-week intact controls, but MG weights were equal or greater. Muscles in general were moderately heavier in exercised animals, the MG values in the 12-week animals equalling those in intact adults. The effect of transection was an increase in percent of fast-twitch oxidative-glycolytic fibers in the SOL at the expense of slow-twitch oxidative fibers, and contraction times were shortened. In the MG only a slight shift in fiber-type complement was suggested. Both muscles demonstrated large increases in biochemically determined ATPase activity, without relation to age at cordotomy. Only a modest increase in the myosin ATPase activity as shown biochemically or histochemically was associated with a marked reduction in contraction time in the SOL, whereas in the MG increases in ATPase activity occurred in the absence of a change in contraction time. Because the exercise potentiated the shortening of contraction time in the SOL, characteristic of slow muscle in chronically transected cats, it appears that absence of neuromuscular activity of spinalized cats cannot explain the development of contractile, histochemical, and biochemical properties characteristic of “faster” muscles.

To see if the discharge behavior of muscle spindles is altered in glucocorticoid-induced muscle atrophy, the firing of Ia and II afferent units in deefferented medial gastrocnemius muscles of male cats given triamcinolone (4 mg/kg) for 10 to 12 days was monitored under static conditions of stretch and compared with results from untreated controls. No difference in mean rate of discharge from spontaneously firing units nor of nonspontaneous units at their length threshold was found. However, the incidence of spontaneous units in the treated animals was greater, and consistent with this the length threshold for nonspontaneous units was less. Position sensitivities were significantly reduced. Estimates made of volumes of discharge arising from total muscle populations of Ia and II afferent fibers indicated that they were increased throughout the range of muscle lengthening. In contrast with the control muscles, there was a greater volume of discharge from Ia than group II afferent fibers for most of the lengthening range. It is considered that these alterations were due to mechanical factors, rather than any direct effect on the sensory terminal.

The effects on the Hoffmann reflex and tendon tap responses in the human soleus and medial gastrocnemius muscles of a brief conditioning volitional contraction have been compared with the objective of distinguishing contributions from the central nervous system and the periphery. The H-wave on successive trials over a 50 sec period following contraction for the most part demonstrated a depression, especially upon the initial trial. The T-wave responses in the first few trials were greater than those in the control period. Using the assumption that responses to tendon taps had been reduced by the amounts reflected in the excitability curve for H-response, it was deducted that a marked enhancement in T-wave excitability had been present at the initial tendon tap and more moderate facilitation thereafter. This is consistent with the post-contraction discharge and increase in stretch sensitivity of spindle receptors seen after contraction of a muscle in experimental animals. It is concluded that such effects on spindles may occur in man, maybe of such force as to detectably influence dynamic movements.

The susceptibility of fast- and slow-twitch hind limb muscles to glucocorticoid-induced atrophy was investigated in adult male cats treated for 10 to 14 days with triamcinolone (4 mg/kg/day), using several histochemical, biochemical, and functional indices. After treatment, muscle weight loss in the fast-twitch muscles (medial gastrocnemius and vastus medialis) occurred to a greater extent than in the slow-twitch muscles (soleus and vastus intermedius), with the latter muscles decreasing in weight proportional to the body weight. Fast-twitch glycolytic (FG) fibers responded with similar degrees of atrophy in the muscles examined; however, slow-twitch oxidative (SO) and fast-twitch oxidative glycolytic (FOG) fibers atrophied more in the fast-twitch compared to the slow-twitch muscles. Phosphofructokinase and NADP+-linked isocitrate dehydrogenase specific activities decreased similarly in the fast-twitch muscles, while no change occurred in the slow-twitch muscles. Functionally, the soleus and medial gastrocnemius remained unchanged in abilities to generate tension tetanically, when this was expressed per unit muscle mass or per unit contractile protein. As a result of the treatment, however, the medial gastrocnemius fatigued faster in response to repetitive stimulation in the glucocorticoid-treated animals. The results suggest that the response of muscle to glucocorticoid-induced atrophy is not regulated by the primary metabolic pathways used for energy production. The differences in response of the SO and FOG fiber types in fast- versus slow-twitch muscles suggest basic differences in metabolic and activity profiles of the same fiber types in different muscles, which may influence susceptibility to atrophy.

This chapter discusses the nature of the persisting canges in afferent discharge from muscle following its contraction. In an experiment presented in the chapter, the postcontraction increase in sensory discharge is observed to study the effects of tenotomy. Several conclusions are drawn from these observations—a persisting increase in discharge at a maintained muscle length and in response to stretch appears after a muscle has undergone contraction, under the condition that the efferent background is otherwise quiet; fusimotor activation alone—that is, contraction of intrafusal fibers, can produce this effect, though extrafusal contraction also seems to contribute; the enhanced discharge, as it is recorded, arises to a major extent in Ia afferent fibers; and the cause of the effect is probably of a mechanical nature. It is believed that the cause of the postcontraction effect is mechanical, rather than due to the sensory ending being affected by a contraction-induced change in the metabolic milieu. Momentary stretch of the muscle results in an immediate disappearance of the postcontraction effect; it is unlikely that this action would rapidly dispel an excess accumulation of metabolite that is capable of such long-lasting effect. The duration of stimulus needed for the response is a few tenths of a second; excitatory levels of K+ would probably not build up in this time.

The effect of long-term stretch on the discharge of muscle spindles was studied by placing a cast on one hindlimb of cats so as to keep the calf region under moderate extension and after 2 to 6 weeks comparing responses of gastrocnemius afferents on casted and unrestrained sides to step wise extension of the muscle. The mean slope of the frequency-length relationship for populations of afferent fibers from immobilized limbs showed mixed effects. The slope was less in three animals, greater in three, and not significantly different in four. Three cats in which the calf region had been under stretch for only 3 to 5 days also demonstrated reduced sensitivity. In contrast, all cats in an earlier series in which the leg had been casted for 2 to 7 weeks with the calf muscles at resting length, showed greater stretch sensitivity. It is concluded that the spindle receptor adapts to long-term stretch of the muscle with a decrease in stretch sensitivity.

A study was made to see if contractions induced by reflex action were followed by an elevation in muscle afferent activity comparable to the postcontraction sensory discharge (PCSD) that occurs after stimulation of the ventral roots. In lightly anesthetized cats, extension reflexes of the triceps surae muscle in the otherwise denervated leg were induced by contralateral stimulation of the popliteal nerve or footpad. The reflex response was followed by an elevated afferent discharge, which disappeared after a brief stretch, as is characteristic also of the PCSD. Crossed-extension responses in fusimotor activity unaccompanied by contraction of the gross muscle were also succeeded by an elevation in sensory discharge and an increased sensitivity to a vibratory stimulus applied to the tendon. Pinna reflexes had a similar effect. In the presence of the elevated discharge, α-motoneurons demonstrated increased sensitivity to vibration stimuli. It is suggested that the increase in spindle sensitivity may help stabilize the muscle against minor perturbations in length, at least when background fusimotor activity is relatively quiet.

The intrafusal fiber content observed in 850 spindles from seven kinds of limb muscles of the cat are presented. The tenuissimus had the smallest content, 6.14 fibers per spindle, and the extensor digitorum longus the largest, 7.91. Gastrocnemius spindles had more fibers than those in the soleus. The differences were attributable primarily to variation in number of nuclear chain fibers. No infallible correlation with anatomical or functional characteristics of the muscles was evident, although greater fiber content seemed to be associated with flexor action and fast contractility. The possible consequences of the spindle content of intrafusal fibers on static and dynamic sensitivity of its afferents are discussed in relation to available data on stretch sensitivity.

The effects on dynamic and static components of the afferent stretch response from a muscle were examined in the period after a brief tetanus, which previous study has shown is marked by a persisting elevation in sensory discharge. Afferent activity of the cat's triceps surae or medial gastrocnemius muscle was monitored as integrated multiunit discharge in a whole dorsal root, and the ventral roots were stimulated to produced a tetanus. The levels of activity at a static muscle length were found to be elevated in decreasing degree over several millimeters of lengthening beyond that at which the muscle was held during tetanus. During a ramp stretch, the velocity-related overshoot in dorsal root activity was also increased. Such changes were still detected after the elevated discharge had been made to disappear by momentary limited extension of the muscle. They are consistent with the hypothesis of residual effect on the intrafusal fibers, perhaps in the form of persisting actin-myosin crossbridges.

The effect on muscle spindle development of multiple exposure to x-irradiation was studied in the soleus and plantaris muscles of young rats. Growth in muscle volume and extrafusal fiber cross-sectional area was strongly reduced following exposures of 2400 to 4100 rad given within two weeks after birth. Spindles also demonstrated reduction in size of the nuclear bag and chain intrafusal fibers in the irradiated as compared to the contralateral muscle, but the difference was relatively less than that of the extrafusal fibers. The intracapsular space was reduced in some heavily irradiated spindles to the point where virtually no space was seen beneath the capsule wall. The number of clearly recognizable spindles was less in the heavily irradiated muscles. Essentially similar results were found in one rat given a single exposure to 4000 rad. The effects on the fibers are interpreted to indicate relative resistance to irradiation in development of the intrafusal musculature as compared to extrafusal fibers.

ArticlesPostcontraction sensory discharge from muscle and its sourceR. S. Hutton, J. L. Smith, and E. EldredR. S. Hutton, J. L. Smith, and E. EldredPublished Online:01 Nov 1973https://doi.org/10.1152/jn.1973.36.6.1090MoreSectionsPDF (2 MB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInEmailWeChat Previous Back to Top Next Download PDF FiguresReferencesRelatedInformationCited ByKinesthetic Senses18 June 2018Fusimotor-induced changes in muscle spindle outflow and responsiveness in muscle fatigue in decerebrate catsNeuroscience, Vol. 63, No. 1Thixotropy in skeletal muscle and in muscle spindles: A reviewProgress in Neurobiology, Vol. 41, No. 6Role of ia muscle spindle afferents in post-contraction and post-vibration motor effect genesisNeuroscience Letters, Vol. 135, No. 2Measurements of muscle stiffness, the electromyogram and activity in single muscle spindles of human flexor muscles following conditioning by passive stretch or contractionBrain Research, Vol. 493, No. 1Effects of muscle thixotropy on spindle afferent activity in the hindlimb of the ratH-reflex changes during static stretching and two variations of proprioceptive neuromuscular facilitation techniquesElectroencephalography and Clinical Neurophysiology, Vol. 63, No. 2Can Ib axons be selectively activated by electrical stimuli in human subjects?Experimental Neurology, Vol. 86, No. 3Activation history and constant errors in human force productionBrain Research, Vol. 307, No. 1-2Electromyographic and mechanical characteristics of human skeletal muscle during fatigue under voluntary and reflex conditionsElectroencephalography and Clinical Neurophysiology, Vol. 55, No. 4EMG activity and kinematics of human cycling movements at different constant velocitiesBrain Research, Vol. 240, No. 2Changes in excitability of tendon tap and hoffmann reflexes following voluntary contractionsElectroencephalography and Clinical Neurophysiology, Vol. 48, No. 6Postcontraction discharge of motor neurons in spinal animalsExperimental Neurology, Vol. 64, No. 3Changes in the pause in muscle spindle discharge during a sequence of twitchesExperimental Neurology, Vol. 60, No. 2Supplement to bibliography on muscle receptors: Their morphology, pathology, physiology, and pharmacologyExperimental Neurology, Vol. 55, No. 3Effects of skin cooling on stretch reflex activity in triceps surae of the decerebrate catExperimental Neurology, Vol. 49, No. 1Postcontraction changes in sensitivity of muscle afferents to static and dynamic stretchBrain Research, Vol. 78, No. 2 More from this issue > Volume 36Issue 6November 1973Pages 1090-1103 Copyright & PermissionsCopyright © 1973 the American Physiological Societyhttps://doi.org/10.1152/jn.1973.36.6.1090PubMed4271542History Published online 1 November 1973 Published in print 1 November 1973 Metrics