Segmental and supraspinal control of synaptic effectiveness of functionally identified muscle afferents in the cat

The present investigation documents the patterns of primary afferent depolarization (PAD) of single, functionally identified muscle afferents from the medial gastrocnemius nerve in the intact, anesthetized cat. Classification of the impaled muscle afferents as from muscle spindles or from tendon organs was made according to several criteria, which comprised measurement of conduction velocity and electrical threshold of the peripheral axons, and the maximal frequency followed by the afferent fibers during vibration, as well as the changes in discharge frequency during longitudinal stretch, the projection of the afferent fiber to the motor pool, and, in unparalyzed preparations, the changes in afferent activity during a muscle twitch. In confirmation of a previous study, we found that most muscle spindle afferents (46.1–66.6%, depending on the combination of criteria utilized for receptor classification) had a type A PAD pattern. That is, they were depolarized by stimulation of group I fibers of the posterior biceps and semitendinosus (PBSt) nerve, but not by stimulation of cutaneous nerves (sural and superficial peroneus) or the bulbar reticular formation (RF), which in many cases inhibited the PBSt-induced PAD. In addition, we found a significant fraction of muscle spindle primaries that were depolarized by stimulation of group I PBSt fibers and also by stimulation of the bulbar RF. Stimulation of cutaneous nerves produced PAD in 9.1–31.2% of these fibers (type B PAD pattern) and no PAD in 8.2–15.4% (type C PAD pattern). In contrast to muscle spindle afferents, only the 7.7–15.4% of fibers from tendon organs had a type A PAD pattern, 23–46.1% had a type B and 50–61.5% a type C PAD pattern. These observations suggest that the neuronal circuitry involved in the control of the synaptic effectiveness of muscle spindles and tendon organs is subjected to excitatory as well as to inhibitory influences from cutaneous and reticulospinal fibers. As shown in the accompanying paper, the balance between excitation and inhibition is not fixed, but can be changed by crushing the afferent axons in the peripheral nerve and allowing subsequent reconnection of these afferent fibers with muscle receptors.     

PAD patterns of physiologically identified afferent fibres from the medial gastrocnemius muscle

Summary Intracellular recordings were made in the barbiturate-anesthetized cat from single afferent fibres left in continuity with the medial gastrocnemius muscle to document the transmembrane potential changes produced in functionally identified fibres by stimulation of sensory nerves and of the contralateral red nucleus (RN). Fifty five fibres from muscle spindles had conduction velocities above 70 m/s and were considered as from group Ia. Stimulation of group I afferent fibres of the posterior biceps and semitendinosus nerve (PBSt) produced primary afferent depolarization (PAD) in 30 (54%) Ia fibres. Stimulation of the sural (SU) nerve produced no transmembrane potential changes in 39 (71%) group Ia fibres and dorsal root reflex-like activity (DRRs) in 16 (29%) fibres. In 17 out of 28 group Ia fibres (60.7%) SU conditioning inhibited the PAD generated by stimulation of the PBSt nerve. Facilitation of the PBSt-induced PAD by SU conditioning was not seen. Repetitive stimulation of the RN had mixed effects: it produced PAD in 1 out of 8 fibres and inhibited the PAD induced by PBSt stimulation in 2 other fibres. Nine fibres connected to muscle spindles had conduction velocities below 70 m/s and were considered to be group II afferents. No PAD was produced in these fibres by SU stimulation but DRRs were generated in 5 of them. In 23 out of 31 fibres identified as from tendon organs group I PBSt volleys produced PAD. However, stimulation of the SU nerve produced PAD only in 3 out of 34 fibres, no transmembrane potential changes in 30 fibres and DRRs in 1 fibre. The effects of SU conditioning on the PAD produced by PBSt stimulation were tested in 19 Ib fibres and were inhibitory in 12 of them. In 9 of these fibres SU alone produced no transmembrane potential changes. Repetitive stimulation of the RN produced PAD in 3 out of 9 Ib fibres. SU conditioning inhibited the RN-induced PAD. The present findings support the existence of an alternative inhibitory pathway from cutaneous to Ib fibres, in addition to the well known excitatory pathway producing PAD. Possible functional implications of inhibitory actions of cutaneous fibres with the pathways mediating the PAD of group Ia and Ib fibres are discussed.     

Selective cortical and segmental control of primary afferent depolarization of single muscle afferents in the cat spinal cord

 This study was primarily aimed at investigating the selectivity of the cortico-spinal actions exerted on the pathways mediating primary afferent depolarization (PAD) of muscle spindle and tendon organ afferents ending within the intermediate nucleus at the L6–L7 segmental level. To this end we analyzed, in the anesthetized cat, the effects produced by electrical stimulation of sensory nerves and of the cerebral cortex on (a) the intraspinal threshold of pairs of single group I afferent fibers belonging to the same or to different hindlimb muscles and (b) the intraspinal threshold of two collaterals of the same muscle afferent fiber. Afferent fibers were classified in three categories, according to the effects produced by stimulation of segmental nerves and of the cerebral cortex. Twenty-five of 40 fibers (62.5%) were depolarized by stimulation of group I posterior biceps and semitendinosus (PBSt) or tibialis (Tib) fibers, but not by stimulation of the cerebral cortex or of cutaneous and joint nerves, which instead inhibited the PBSt- or Tib-induced PAD (type A PAD pattern, usually seen in Ia fibers). The remaining 15 fibers (37.5%) were all depolarized by stimulation of the PBSt or Tib nerves and the cerebral cortex. Stimulation of cutaneous and joint nerves produced PAD in 10 of those 15 fibers (type B PAD pattern) and inhibited the PBSt- or Tib-induced PAD in the 5 remaining fibers (type C PAD pattern). Fibers with a type B or C PAD pattern are likely to be Ib. Not all sites in the cerebral cortex inhibited with the same effectiveness the segmentally induced PAD of group I fibers with a type A PAD pattern. With the weakest stimulation of the cortical surface, the most effective sites that inhibited the PAD of individual fibers were surrounded by less effective sites, scattered all along the motor cortex (area 4γ and 6) and sensory cortex (areas 3, 2 and 1), far beyond the area of projection of group I fibers from the hindlimb. With higher strengths of cortical stimulation, the magnitude of the inhibition was also increased, and previously ineffective or weakly effective sites became more effective. Maps obtained when using the weakest cortical stimuli have indicated that the most effective regions that produced PAD of group I fibers with a type B or type C PAD pattern were also scattered throughout the sensory-motor cortex, in the same general area as those that inhibited the PAD of group I afferents with a type A PAD pattern. In eight fibers with a type A PAD pattern it was possible to examine the intraspinal threshold of two collaterals of the same single afferent fiber ending within the intermediate nucleus at the L7 segmental level. In six fibers, stimulation of the PBSt nerve with trains of pulses between 1.5 and 1.86 times threshold (×T) produced a larger PAD in one collateral than in the other. In seven fibers, stimulation of the sensory-motor cortex and of cutaneous nerves produced a larger inhibition of the PBSt-induced PAD in one collateral than in the other. The ratio of the cortically induced inhibition of the PAD elicited in the two collaterals could be modified by changing the strength of cortical and of PBSt stimulation. In three fibers it was possible to inhibit almost completely the background PAD elicited in one collateral while having little or no effect on the PAD in the other collateral. Changes in the intraspinal threshold of pairs of collaterals following electrical stimulation of segmental nerves and of the somato-sensory cortex were examined in three fibers with a type B and two fibers with a type C PAD pattern. In four fibers the PAD elicited by stimulation of cutaneous (4–20×T) and muscle nerves (1.54–3.7×T), or by stimulation of the sensory-motor cortex, was of different magnitude in the two collaterals. In two experiments it was possible to find cortical sites in which weak surface stimulation produced PAD in one collateral only. The magnitude of the PAD elicited in pairs of collaterals of group I afferents with a type B or C PAD pattern, or the inhibition of the PAD in pairs of collaterals of fibers with a type A PAD pattern, appeared not to be topographically related to the site of spinal projection of the cutaneous and cortico-spinal fibers used for conditioning stimulation. The present demonstration of a differential control of the PAD exerted on two collaterals of the same afferent fiber suggests that the profuse intraspinal branching of muscle spindle and tendon organs is a potentially rich substrate for information transmission. By means of presynaptic control mechanisms, the terminal arborizations of the afferent fibers could function either as a simple unit or in a fractionated manner, allowing funneling of information to selected groups of central neurons. Received: 18 April 1996 / Accepted: 5 September 1996     

Patterns of connectivity of spinal interneurons with single muscle afferents

 A technique was developed to measure, in the anesthetized and paralyzed cat under artificial ventilation, changes of excitability to intraspinal stimulation simultaneously in two different afferent fibers or in two collaterals of the same afferent fiber. Intraspinal stimulation reduced the threshold of single muscle afferent fibers ending in the intermediate nucleus. This effect was seen with strengths below those required to activate the afferent fiber tested (1.5–12 μA), occurred at a short latency (1.5–2.0 ms), reached a maximum between 15 and 30 ms, and lasted up to 100 ms. The effects produced by graded stimulation applied at the shortest conditioning-testing stimulus time intervals increased by fixed steps, suggesting recruitment of discrete elements, most likely of last-order interneurons mediating primary afferent depolarization (PAD). The short-latency increases in excitability produced by the weakest effective intraspinal stimuli were usually detected only in the collateral closest to the stimulating micropipette, indicating that the stimulated interneurons mediating PAD have spatially restricted actions. The short-latency PAD produced by intraspinal stimuli, as well as the PAD produced by stimulation of the posterior biceps and semitendinosus (PBSt) nerve or by stimulation of the bulbar reticular formation (RF), was depressed 19–30 min after the i.v. injection of 0.5 mg/kg of picrotoxin, suggesting that all these effects were mediated by GABAergic mechanisms. The PAD elicited by stimulation of muscle and/or cutaneous nerves was depressed following the i.v. injection of (–)-baclofen, whereas the PAD elicited in the same collateral by stimulation of the RF was baclofen-resistant. The short-latency PAD produced by intraspinal stimulation was not always depressed by i.v. injections of (–)-baclofen. Baclofen-sensitive and baclofen-resistant monosynaptic PADs could be produced in different collaterals of the same afferent fiber. The results suggest that the intraspinal terminals of single muscle afferents receive synapses from more than one PAD-mediating GABAergic interneuron and that a single last-order interneuron has synaptic connections with a restricted number of intraspinal terminals and/or collaterals of the same afferent fiber. In addition, they support the existence of separate subsets of last-order baclofen-sensitive and baclofen-resistant interneurons that respond predominantly to segmental and to descending inputs. It is suggested that the restricted nature of the PAD plays an important role in the central control of the synaptic effectiveness of group I muscle afferents. Received: 10 October 1996 / Accepted: 10 December 1996     

Muscle spindle discharge in response to contraction of single motor units

1. In human subjects, microelectrode recordings were made from 25 muscle spindle afferents and two tendon organ afferents coming from muscles innervated by the peroneal nerve. 2. Stimulation at low intensity through the recording microelectrode activated efferent axons innervating motor units in close proximity to the muscle spindle or tendon organ. There was a clear alteration in the discharge of 17 afferents (15 muscle spindle, 2 tendon organ) in response to twitch contractions that involved only one, two, or three motor units. With three other afferents there was a less overt but statistically significant alteration in discharge rate by the twitch contraction of a single motor unit. 3. The sensitivity of 21 receptors (20 spindles, 1 tendon organ) to twitch contractions of anatomically close motor units was contrasted with their sensitivity to twitches of more remote motor units in the muscle. In no instance was the sensitivity to the contraction of remote motor units greater than that to the contraction of local motor units stimulated through the microelectrode; with remote stimulation many units usually had to be activated before the resulting twitch contraction altered the discharge of an afferent. 4. It is concluded that muscle spindles as well as tendon organs can play a role in monitoring the activity of motor units anatomically close to the receptor.     

Reticulospinal actions on primary afferent depolarization of cutaneous and muscle afferents in the isolated frog neuraxis

The effects of the brainstem reticular formation on the intraspinal excitability of low threshold cutaneous and muscle afferents were studied in the frog neuraxis isolated together with the right hindlimb nerves. Stimulation of low threshold fibers (less than two times threshold) in cutaneous nerves produced short latency, negative field potentials in the ipsilateral dorsal neuropil (200–400 m depth) that reversed to positivity at deeper regions (500–700 m). Stimulation of low threshold fibers (less than two times threshold) in muscle nerves produced, instead, negative responses that acquired their maximum amplitude in the ventral neuropil (700–900 m depth). These electrophysiological findings suggest, in agreement with observations in the cat, that low threshold cutaneous and muscle afferents end at different sites in the spinal cord. Intraspinal microstimulation applied within the dorsal neuropil produced antidromic responses in low threshold cutaneous afferents that were increased in size following stimulation of the dorsal or ventral roots, as well as of the brainstem reticular formation. This increase in excitability is interpreted as being due to primary afferent depolarization (PAD) of the intraspinal terminals of cutaneous fibers. Antidromic responses recorded in muscle nerves following intraspinal stimulation within the ventral neuropil were also increased following conditioning stimulation of adjacent dorsal or ventral roots. However, stimulation of the bulbar reticular formation produced practically no changes in the antidromic responses, but was able to inhibit the PAD of low threshold muscle afferents elicited by stimulation of the dorsal or ventral roots. It is suggested that the PAD of low threshold cutaneous and muscle afferents is mediated by independent sets of interneurons. Reticulospinal fibers would have excitatory connections with the interneurons mediating the PAD of cutaneous fibers and inhibitory connections with the interneurons mediating the PAD of muscle afferents. Although our results provide no direct information on whether the reticulospinal depression of the PAD elicited in low threshold muscle afferents is due to inhibition along the pathways producing PAD of muscle spindle or of tendon organ afferents, it seems likely — by analogy with what has been seen in the cat spinal cord — that these inhibitory actions are mostly restricted to the pathways producing PAD in the terminal arborizations of muscle spindle afferents. These results emphasize the specificity of the descending control of the synaptic efficacy of low threshold cutaneous and muscle afferents which could be of importance for motor performance.     

Patterns of primary afferent depolarization of segmental and ascending intraspinal collaterals of single joint afferents in the cat

We have examined in the anesthetized cat the threshold changes produced by sensory and supraspinal stimuli on intraspinal collaterals of single afferents from the posterior articular nerve (PAN). Forty-eight fibers were tested in the L3 segment, in or close to Clarke’s column, and 70 fibers in the L6–L7 segments within the intermediate zone. Of these, 15 pairs of L3 and L6–L7 collaterals were from the same afferent. Antidromically activated fibers had conduction velocities between 23 and 74 m/s and peripheral thresholds between 1.1 and 4.7 times the threshold of the most excitable fibers (xT), most of them below 3 xT. PAN afferents were strongly depolarized by stimulation of muscle afferents and by cutaneous afferents, as well as by stimulation of the bulbar reticular formation and the midline raphe nuclei. Stimulation of muscle nerves (posterior biceps and semitendinosus, quadriceps) produced a larger PAD (primary afferent depolarization) in the L6–L7 than in the L3 terminations. Group II were more effective than group I muscle afferents. As with group I muscle afferents, the PAD elicited in PAN afferents by stimulation of muscle nerves could be inhibited by conditioning stimulation of cutaneous afferents. Stimulation of the cutaneous sural and superficial peroneal nerves increased the threshold of few terminations (i.e., produced primary afferent hyperpolarization, PAH) and reduced the threshold of many others, particularly of those tested in the L6–L7 segments. Yet, there was a substantial number of terminals where these conditioning stimuli had minor or no effects. Autogenetic stimulation of the PAN with trains of pulses increased the intraspinal threshold in 46% and reduced the threshold in 26% of fibers tested in the L6–L7 segments (no tests were made with trains of pulses on fibers ending in L3). These observations indicate that PAN afferents have a rather small autogenetic PAD, particularly if this is compared with the effects of heterogenetic stimulation. Therefore, the depression of the PAN intraspinal fields produced by autogenetic stimulation described by Rudomin et al. (Exp Brain Res DOI 10.1007/s00221-006-0600-x, 2006) may be ascribed to other mechanisms besides a GABAa PAD. It is suggested that the small or no autogenetic PAD displayed by the examined joint afferents prevents presynaptic filtering of their synaptic actions and preserves the original information generated in the periphery. This could be important for proper adjustment of limb position.     

PAD and PAH response patterns of group Ia- and Ib-fibers to cutaneous and descending inputs in the cat spinal cord

The characteristics of the primary afferent depolarization (PAD) of Ia- and Ib-fibers generated by segmental and descending inputs have been analyzed in the spinal cord of anesthetized cats. The PAD was inferred from the changes produced by conditioning inputs on the intraspinal stimulus current required to produce a constant antidromic firing of single group I afferent fibers from the gastrocnemius (GS) or posterior biceps and semitendinosus (PBSt) nerves. Group I GS and PBSt fibers ending in the intermediate nucleus could be classified in three different types according to their PAD patterns in response to stimulation of cutaneous nerves and of descending fibers. In one set of group I fibers stimulation of cutaneous nerves and of the ipsilateral brain stem reticular formation, or the contralateral red nucleus, produced no PAD, but was able to inhibit the PAD generated by stimulation of group I fibers from flexors (type A PAD pattern). PBSt nerve fibers with this PAD pattern had peripheral thresholds and conduction velocities between 1.01 and 1.56 times threshold and 76.3 to 118 m/s, respectively. A second set of group I fibers was found to be depolarized by cutaneous nerves as well as by stimulation of rubrospinal and reticulospinal fibers (type B PAD pattern). The peripheral thresholds and conduction velocities of PBSt afferent fibers with a type B PAD pattern were of 1.66-2.03 times threshold and 71-83 m/s, respectively. We found a third set of group I fibers that were also depolarized by reticulospinal and rubrospinal inputs, but not by cutaneous nerves that instead inhibited the PAD elicited by group I volleys in flexor nerves (type C PAD pattern). All PBSt afferent fibers with a type C PAD pattern, with the exception of two, had peripheral thresholds and velocities between 1.46 and 2.16 times threshold and between 72 and 89 m/s, respectively. Stimulation of the Deiter's nucleus was found to depolarize the intraspinal terminals of a small fraction of group I GS fibers with a type A PAD pattern and of all group I GS and PBSt fibers with type B and C PAD patterns. The PAD produced by vestibulospinal stimulation in fibers with type A and C PAD patterns could be inhibited by conditioning volleys applied to cutaneous nerves. It is suggested that group I afferent fibers from flexors and extensors with a type A PAD pattern are group Ia, and that most fibers with type B and type C PAD patterns are group Ib.(ABSTRACT TRUNCATED AT 400 WORDS)     

Differential action of (−)-baclofen on the primary afferent depolarization produced by segmental and descending inputs

Summary The purpose of the present series of experiments was to analyze, in anesthetized and paralyzed cats, the effects of (-)-baclofen and picrotoxin on the primary afferent depolarization (PAD) generated in single Ib afferent fibers by either intraspinal microstimulation or stimulation of the segmental and descending pathways. PAD was estimated by recording dorsal root potentials and by measuring the changes in the intraspinal activation threshold of single Ib muscle afferent fibers. The PAD elicited by stimulation of group I muscle or cutaneous afferents was readily depressed and often abolished 20–40 min after the intravenous injection of 1–2 mg/kg (-)-baclofen. In contrast, the same amounts of (-)-baclofen produced a relatively small depression of the PAD elicited by stimulation of the brainstem reticular formation (RF). The monosynaptic PAD produced in single Ib fibers by intraspinal microstimulation within the intermediate nucleus was depressed and sometimes abolished following the i.v. injections of 1–2 mg/kg (-)-baclofen. Twenty to forty minutes after the i.v. injection of picrotoxin (0.5–1 mg/kg), there was a strong depression of the PAD elicited by stimulation of muscle and cutaneous afferents as well as of the PAD produced by stimulation of the RF and the PAD produced by intraspinal microstimulation. The results obtained suggest that, in addition to its action on primary afferents, (-)-baclofen may depress impulse activity and/or transmitter release in a population of last-order GABAergic interneurons that mediate the PAD of Ib fibers. The existence of GABA_b autoreceptors in last-order interneurons mediating the PAD may function as a self-limiting mechanism controlling the synaptic efficacy of these interneurons.     

Organization of group I activated cells in the main and external cuneate nuclei of the cat: Identification of muscle receptors

Summary Extracellular recording was made from 77 primary afferent fibres, 106 cells in the external cuneate nucleus, and 60 cells in the main cuneate nucleus, all activated by slowly adapting muscle stretch receptors. The nature of the muscle receptors responsible for the activation was determined by various types of receptor stimulation.Primary group I afferents from muscle spindles and tendon organs in distal forelimb muscles showed complete overlap of conduction velocities and thresholds to electrical stimulation. Both types of group I afferents as well as group II muscle spindle afferents were shown to ascend through the dorsal funiculus to the level of the cuneate nuclei.Three groups of cells were identified in the external cuneate nucleus, activated by group I muscle spindle afferents, tendon organ afferents and group II muscle spindle afferents, respectively.Almost all group I activated cells in the main cuneate nucleus, including all 34 cells identified as cuneo-thalamic relay cells, received their afferent input from muscle spindle afferents. Three cells were activated by tendon organ afferents.     

Effects upon spindle discharges of electrical stimulation of static fusimotor fibers with concomitant application of muscle vibration.

Discharges of single afferent fibers from the primary endings of the soleus muscle spindles were recorded from thin dorsal root filaments in cats anesthetized with urethane and chloralose. The distal cut end of the ventral root was split into fine filaments to obtain functionally single fusimotor fibers. The fusimotor fibers obtained in this study were of the static type. The soleus muscle was sinusoidally stretched at 70 Hz with various amplitude concurrently with 100 Hz electric stimulation of fusimotor fiber. The spindle afferent discharges were analysed by compiling inter-spike interval histograms and cross-correlograms between the afferent spikes and the stimulus pulses applied to the fusimotor fiber. The same analysis was also made between the afferent spikes and peak extensions of muscle yielded by vibratory stimulation. One-third of the fusimotor fibers were capable of driving the spindle afferents. The driving of fusimotor stimulation was replaced by driving by muscle dibration of more than 10 mum amplitude applied concurrently with fusimotor stimulation. The remaining two-thirds of the fusimotor fibers could not drive the spindle afferents. In this case, the driving by muscle vibration was obtained when vibration of more than 5 mum amplitude was applied concurrently with fusimotor stimulation. It was suggested that fusimotor fibers which produced driving of the spindle afferents would terminate on nuclear chain fibers and those not producing driving on nuclear bag fibers, or the latter would terminate relatively distant from the primary ending as compared with the former.     

Effects of temperature on the discharges of muscle spindles and tendon organs

1. In anaesthetized cats the effects of temperature on the nervous outflow from skeletal muscle via thick myelinated afferent fibres were studied. Single unit recordings were made from afferents of muscle spindles and tendon organs during slow and fast temperature changes of the medial gastrocnemius muscle which was deefferented by ventral root section and prestretched to a tension of 100 p.
2. Group I afferent units from muscle spindles were activated by warming and depressed by cooling, the effect of warming being much more pronounced than that of cooling. Afferents from secondary spindle endings with a high background discharge behaved similar to Ia fibres, whereas those with a low initial discharge rate showed an activation by cooling and a depression (mostly to cessation of firing) by warming. The discharges of group I afferents from tendon organs varied; an activation by warming was the most frequently observed reaction.
3. Some of the afferents from muscle spindles and tendon organs showed signs of a dynamic sensitivity to thermal stimulation, but in general the dynamic component in the responses to temperature changes was only small.
4. The results suggest that the afferent outflow via thick myelinated fibres from a resting, moderately prestretched muscle strongly depends on temperature. At raised intramuscular temperatures (about 42°C) the nervous outflow is characterized by an increased activity in all of the I a and many of the I b afferents, while the majority of group II spindle afferents will be depressed. In contrast, in a cold muscle (about 29°C) the nervous outflow via afferents from primary spindle endings will be reduced, while the net activity from secondary spindle endings will be increased and no marked changes are expected to occur in the discharges of I b fibres.

     

Axotomy induces fusimotor-free muscle spindles in neonatal rats.

Crushing the nerve to the medial gastrocnemius (MG) muscle at birth and administering nerve growth factor to rats afterwards results in a reinnervated muscle with supernumerary muscle spindles, some of which must have formed de novo. Structure and innervation of spindles in the reinnervated MG muscles were studied in serial 1 micron transverse sections. Two types of spindle-like encapsulations were observed. The prevalent type consisted of one to three small diameter intrafusal fibers with features of nuclear chain fibers or infrequently a nuclear bag fiber. The second type of encapsulation consisted of the small-diameter fibers located in a compartment which abutted a compartment containing a large diameter extrafusal fiber. All intrafusal fibers in spindles of the experimental muscles were innervated by afferents, but most of them (85%) were devoid of efferent innervation. Thus, immature fusimotor neurons may be more susceptible than spindle afferents to cell death after axotomy at birth.     

Reduction of Ib autogenetic inhibition in motoneurons during contractions of an ankle extensor muscle in the cat

1. Triceps surae and plantaris (Pl) motoneurons were recorded intracellularly in chloralose or pentobarbital sodium (Nembutal)-anesthetized cats during unfused tetanic contractions of gastrocnemius medialis muscle (GM) produced by stimulating either a cut branch of the GM nerve or the muscle directly. 2. In alpha-motoneurons, during a series of GM twitches at 10/s, contraction-induced inhibitory potentials, probably the result of input from Golgi tendon organs (autogenetic inhibition), rapidly subsided before the end of the series. In contrast, excitatory potentials, probably the result of the activation of spindle primary endings during relaxation from contraction, persisted. 3. In gastrocnemius lateralis-soleus (GL-S) and Pl motoneurons lacking an excitatory connection with Ia afferents from GM, the sustained contraction of this muscle also elicited a declining inhibition. Rapid reduction of contraction-induced autogenetic inhibition was also observed in homonymous gamma-motoneurons. During unfused tetanic contractions lasting 0.5-4s, inhibitory potentials quickly subsided, but an abrupt increase in contractile force elicited a new series of decreasing inhibitory potentials. 4. The assumption that the inhibition induced by GM unfused tetanic contractions was due to activation of homonymous Ib afferents was supported by observations of the effects of electrical stimulation of the GM nerve. In Pl motoneurons lacking an excitatory connection with Ia afferents from GM, repetitive trains applied to the GM nerve, at a strength just above threshold for group I fibers, elicited rapidly declining inhibitory potentials similar to those produced by GM contraction. It was verified that during such stimulation, the amplitude of the group I afferent volleys did not decrease. 5. Reduction of contraction-induced Ib inhibition during sustained GM contraction was still present after a low spinalization of the preparation. As GM tendon organ discharges were verified to persist throughout prolonged contractions, the observed decline of autogenetic inhibition is likely to depend on a spinal mechanism, possibly involving presynaptic inhibition of Ib afferents and/or mutual inhibition of Ib-inhibitory interneurons.     

Afferent fibres from muscle receptors in the posterior nerve of the cat's knee joint

Summary The properties of some receptors with afferent fibres in the cat's posterior knee joint nerve have been examined, especially those discharging tonically with the joint in intermediate positions between full flexion and extension. Some of these receptors behave like muscle spindles, and respond to manoeuvres which stretch popliteus muscle. Both in single unit and whole nerve recordings their discharge pauses during a popliteus twitch, and can be strikingly augmented by tetanic stimulation of a number of popliteus fusimotor fibres isolated from ventral root filaments. The action of succinylcholine on these receptors closely resembles its effect on popliteus spindle units with fibres sited normally in the popliteus nerve. Other units with properties suggesting origin from popliteus tendon organs were also observed; their fibres and those of the spindle units conducted at Group I velocity. It is concluded that some afferent fibres from popliteus spindles and possibly tendon organs commonly pursue an aberrant course in the posterior articular nerve of the knee joint.     

A comparative analysis of the encapsulated end-organs of mammalian skeletal muscles and of their sensory nerve endings

The encapsulated sensory endings of mammalian skeletal muscles are all mechanoreceptors. At the most basic functional level they serve as length sensors (muscle spindle primary and secondary endings), tension sensors (tendon organs), and pressure or vibration sensors (lamellated corpuscles). At a higher functional level, the differing roles of individual muscles in, for example, postural adjustment and locomotion might be expected to be reflected in characteristic complements of the various end‐organs, their sensory endings and afferent nerve fibres. This has previously been demonstrated with regard to the number of muscle‐spindle capsules; however, information on the other types of end‐organ, as well as the complements of primary and secondary endings of the spindles themselves, is sporadic and inconclusive regarding their comparative provision in different muscles. Our general conclusion that muscle‐specific variability in the provision of encapsulated sensory endings does exist demonstrates the necessity for the acquisition of more data of this type if we are to understand the underlying adaptive relationships between motor control and the structure and function of skeletal muscle. The present quantitative and comparative analysis of encapsulated muscle afferents is based on teased, silver‐impregnated preparations. We begin with a statistical analysis of the number and distribution of muscle‐spindle afferents in hind‐limb muscles of the cat, particularly tenuissimus. We show that: (i) taking account of the necessity for at least one primary ending to be present, muscles differ significantly in the mean number of additional afferents per spindle capsule; (ii) the frequency of occurrence of spindles with different sensory complements is consistent with a stochastic, rather than deterministic, developmental process; and (iii) notwithstanding the previous finding, there is a differential distribution of spindles intramuscularly such that the more complex ones tend to be located closer to the main divisions of the nerve. Next, based on a sample of tendon organs from several hind‐foot muscles of the cat, we demonstrate the existence in at least a large proportion of tendon organs of a structural substrate to account for multiple spike‐initiation sites and pacemaker switching, namely the distribution of sensory terminals supplied by the different first‐order branches of the Ib afferent to separate, parallel, tendinous compartments of individual tendon organs. We then show that the numbers of spindles, tendon organs and paciniform corpuscles vary independently in a sample of (mainly) hind‐foot muscles of the cat. Grouping muscles by anatomical region in the cat indicated the existence of a gradual proximo‐distal decline in the overall average size of the afferent complement of muscle spindles from axial through hind limb to intrinsic foot muscles, but with considerable muscle‐specific variability. Finally, we present some comparative data on muscle‐spindle afferent complements of rat, rabbit and guinea pig, one particularly notable feature being the high incidence of multiple primary endings in the rat.     

Inhibition of muscle spindle afferent activity during masseter muscle fatigue in the rat

The influence of muscle fatigue on the jaw-closing muscle spindle activity has been investigated by analyzing: (1) the field potentials evoked in the trigeminal motor nucleus (Vmot) by trigeminal mesencephalic nucleus (Vmes) stimulation, (2) the orthodromic and antidromic responses evoked in the Vmes by stimulation of the peripheral and central axons of the muscle proprioceptive afferents, and (3) the extracellular unitary discharge of masseter muscle spindles recorded in the Vmes. The masseter muscle was fatigued by prolonged tetanic masseter nerve electrical stimulation. Pre- and postsynaptic components of the potentials evoked in the Vmot showed a significant reduction in amplitude following muscle fatigue. Orthodromic and antidromic potentials recorded in the Vmes also showed a similar amplitude decrease. Furthermore, muscle fatigue caused a decrease of the discharge frequency of masseter muscle spindle afferents in most of the examined units. The inhibition of the potential amplitude and discharge frequency was strictly correlated with the extent of muscle fatigue and was mediated by the group III and IV afferent muscle fibers activated by fatigue. In fact, the inhibitory effect was abolished by capsaicin injection in the masseter muscle that provokes selective degeneration of small afferent muscle fibers containing neurokinins. We concluded that fatigue signals originating from the muscle and traveling through capsaicin-sensitive fibers are able to diminish the proprioceptive input by a central presynaptic influence. In the second part of the study, we examined the central projection of the masseter small afferents sensitive to capsaicin at the electron-microscopic level. Fiber degeneration was induced by injecting capsaicin into the masseter muscle. Degenerating terminals were found on the soma and stem process in Vmes and on the dendritic tree of neurons in Vmot. This suggests that small muscle afferents may influence the muscle spindle activity through direct synapses on somata in Vmes and on dendrites of neurons in Vmot.     

The afferent innervation of two infrahyoid muscles of the cat

1. The afferent innervation of the straplike muscles of the infrahyoid region were investigated in two ways. The morphology of spindles and counts of tendon organs were investigated by the gold chloride technique in ten muscles. Spindle counts were made in forty pairs of thyrohyoid and infrahyoid muscles. De-efferenting of the nerves to these muscles was done in three cats and the calibre spectra of the afferent innervation investigated. These were compared with the total counts of fibres in intact nerves.2. In the thyrohyoid, spindles are frequently absent. No tendon organs were seen. In the large infrahyoid (combined sternohyoid and sternothyroid), spindle counts varied from 0 to 20 and the mean spindle count per gram of muscle was 3.5. A maximum of five tendon organs were seen in the muscle. Both spindle and tendon organ counts are low when compared with a limb muscle of similar weight and size.3. In the infrahyoid muscle complex spindles were about equal in number to simple spindles.4. Counts of spindles in the infrahyoid muscle in families of three or more siblings suggest that some families of kittens tend to have higher spindle counts than other families.5. The afferent innervation of the two muscles varied between 21 and 42% of the total fibre population and the fibre diameter spectrum is in keeping with the low counts of encapsulated endings.     

Rat muscle spindles deficient in elements of the static system

Motor nerve supplies to 15 poles of rat lumbrical spindle were reconstructed from serial, 1-micron transverse sections of muscle embedded in resin. Neural and muscular elements associated with the modulation of static sensitivity of afferents were deficient in these spindles relative to cat tenuissimus and rat soleus spindles. Rat lumbrical spindles contained fewer static fusimotor axons, fewer static chain intrafusal fibers, fewer motor-innervated static bag2 and chain fibers and fewer secondary afferents. The sparsity of static elements in spindles of the rat lumbrical muscle may correlate with the distal location or with the delicate motor tasks performed by the muscle.