Changes in PAD patterns of group I muscle afferents after a peripheral nerve crush

In the anesthetized cat we have analyzed the changes in primary afferent depolarization (PAD) evoked in single muscle spindle and tendon organ afferents at different times after their axons were crushed in the periphery and allowed to regenerate. Medial gastrocnemius (MG) afferents were depolarized by stimulation of group I fibers in the posterior biceps and semitendinosus nerve (PBSt), as soon as 2 weeks after crushing their axons in the periphery, in some cases before they could be activated by physiological stimulation of muscle receptors. Two to twelve weeks after crushing the MG nerve, stimulation of the PBSt produced PAD in all MG fibers reconnected with presumed muscle spindles and tendon organs. The mean amplitude of the PAD elicited in afferent fibers reconnected with muscle spindles was increased relative to values obtained from Ia fibers in intact (control) preparations, but remained essentially the same in fibers reconnected with tendon organs. Quite unexpectedly, we found that, between 2 and 12 weeks after crushing the MG nerve, stimulation of the bulbar reticular formation (RF) produced PAD in most afferent fibers reconnected with muscle spindle afferents. The mean amplitude of the PAD elicited in these fibers was significantly increased relative to the PAD elicited in muscle spindle afferents from intact preparations (from 0.08–0.4 to 0.47-0.34 mV). A substantial recovery was observed between 6 months and 2.5 years after the peripheral nerve injury. Stimulation of the sural (SU) nerve produced practically no PAD in muscle spindles from intact preparations, and this remained so in those afferents reconnected with muscle spindles impaled 2–12 weeks after the nerve crush. The mean amplitude of the PAD produced in afferent fibers reconnected with tendon organs by stimulation of the PBSt nerve and of the bulbar RF remained essentially the same as the PAD elicited in intact afferents. However, SU nerve stimulation produced a larger PAD in afferents reconnected with tendon organs 2–12 weeks after the nerve crush (mean PAD changed from 0.05-0.04 to 0.32-0.17 mV). The results obtained indicate that the PAD patterns of the afferent fibers reconnected with muscle spindle and tendon organ afferents are changed after crushing their axons in the periphery: stimulation of the bulbar RF appears to produce larger PAD in fibers reconnected with muscle spindles, and stimulation of cutaneous afferents produces larger PAD in fibers reconnected with tendon organs. It is suggested that these alterations in the patterns of PAD of muscle afferents result from central changes in the balance of excitatory and inhibitory influences acting on the segmental pathways mediating the PAD. Although the functional role of these changes has not been established, they may reflect compensatory changes aimed to adjust information arising from damaged afferents.     

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     

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.     

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)     

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.     

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.     

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     

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.     

Convergence onto interneurons subserving primary afferent depolarization of group I afferents

The aim of the study was to investigate whether common or independent neuronal pathways are used to evoke primary afferent depolarization (PAD) from selectively activated group Ia and Ib afferents of different muscles. To this end, the spatial facilitation of effects of various afferents, indicating convergence on the same interneurons, was used as a test. Its occurrence was assessed on dorsal root potentials (DRPs) evoked in unspecified fibers or using intra-axonal recording from identified group Ia muscle spindle afferents or group Ib tendon organ afferents. Spatial facilitation has been found in PAD pathways a) from various Ia-afferents, whether of flexors or extensors; b) from various Ib-afferents, whether of flexors or extensors; and c) from flexor Ib-afferents and flexor or extensor Ia-afferents. In contrast, no indications have been found for common pathways from extensor Ib- and any Ia-afferents under conditions that proved effective in other combinations. Latencies of those components of PAD that appeared as a result of the spatial facilitation ranged from 2 to more than 7 ms, indicating that the convergence occurred in the shortest (trisynaptic) as well as longer pathways. The same patterns of convergence have been found in PAD pathways to extensor and flexor Ia-afferents (in experiments with intraaxonal recording from these afferents). The possibility might thus be considered that some neuronal pathways are used to modulate transmission via Ia-afferents independently of their muscle origin. The same might hold true for extensor and flexor Ib-afferents. Generally, it is concluded that the minimal number of distinct neuronal populations subserving PAD of group I afferents may be two to six. Additionally, actions of cutaneous, joint, and interosseous afferents on DRPs from Ia-afferents were reexamined to further the comparison between neurons mediating PAD and those mediating postsynaptic excitation or inhibition of motoneurons. Only depression of Ia DRPs followed stimulation of these afferents at intensities of 1.5-2.0 times threshold and higher; lower threshold afferents were apparently ineffective. On the basis of lack of convergence of extensor Ib and Ia muscle afferents and of low-threshold cutaneous afferents, interneurons mediating PAD may thus be distinguished from the interneurons subserving Ib and Ia-like-Ib postsynaptic actions in motoneurons. The latter are coexcited by these three groups of afferents.     

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.     

Sites of action of segmental and descending control of transmission on pathways mediating PAD of Ia- and Ib-afferent fibers in cat spinal cord

The present series of investigations was aimed to disclose the possible sites of action of excitatory and inhibitory inputs on tho-interneuron pathway mediating the primary afferent depolarization (PAD) of group I afferents of extensor muscles in the cat spinal cord. To this end we compared the effects produced by stimulation of segmental and descending pathways on the PAD generated either by stimulation of group I fibers of flexor muscles or by intraspinal microstimulation. It was assumed that under the appropriate conditions the PAD produced by intraspinal microstimulation results from the activation of the last-order interneurons in the PAD pathway and may, therefore, allow detection pathway. The PAD of single group I afferent fibers was determined in barbiturate-anesthetized preparations by measuring the test stimulus current required to maintain a constant probability of antidromic firing. This was achieved by means of a feedback system that continuously adjusted the test stimulus current to the required values. The PAD of individual group Ia gastrocnemius soleus (GS) fibers that is produced by activation of the low-threshold afferents of the posterior biceps and semitendinosus nerve was found to be inhibited by conditioning stimulation of the relatively low-threshold cutaneous fibers and also by stimulation of supraspinal structures such as the ipsilateral brain stem reticular formation, the contralateral red nucleus, and the contralateral pyramidal tract. In contrast, the PAD of group Ia fibers produced by microstimulation applied in the intermediate nucleus could be inhibited only by stimulation of the brain stem reticular formation but not by stimulation of the other descending inputs presently tested or by stimulation of cutaneous nerves. PAD of group Ia fibers was produced also by microstimulation applied within the motor nucleus. However, in most fibers the resulting PAD could not be inhibited either by stimulation of the brain stem reticular formation, the red nucleus, the pyramidal tract, or cutaneous nerves. Stimulation of cutaneous and of flexor muscle nerves of the brain stem reticular formation, the red nucleus, and the pyramidal tract all produced PAD of the group Ib GS fibers.(ABSTRACT TRUNCATED AT 400 WORDS)     

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.

     

Tonic suppression of reflex transmission in low spinal cats

Summary Transmission in various spinal hindlimb reflex pathways arising from muscle, cutaneous and joint afferents, was investigated in acute low spinal (Th10) cats before and after lesions at more caudal levels in the lumbar segments. Lesions of the ipsilateral dorsolateral funiculus (DLF) resulted in increased mono- and polysynaptic ventral root discharges. With conditioning of monosynaptic reflexes it was demonstrated that the DLF lesion enhanced transmission in reflex pathways from group II and III muscle afferents. The DLF lesion also resulted in increased dorsal root potentials from cutaneous, joint and group III muscle afferents. These reflex enhancements could not be obtained with lesions rostral to L2, but developed with lesions in L2 and to some extent in L3, but no further effect was obtained by adding lesions caudal to L3. Ventral extension of the DLF lesion gave hardly any increase of reflex transmission. It is postulated that the investigated reflex pathways may be tonically inhibited in the acute low spinal state by propriospinal neurones with cell bodies in the L2–L3 segments and with axons descending in the dorsolateral funiculus.Abbreviations LF Lateral funiculus - DLF dorsolateral funiculus - FRA flexor reflex afferents - DRP dorsal root potential - PAD primary afferent depolarization - PBSt Nerves: posterior biceps and semitendinosus - ABSm anterior biceps and semimembranosus - Sur sural - G-S gastrocnemius and soleus - Pl plantaris - FDHL flexor digitorum and hallucis longus - j posterior knee joint - DP deep peroneus - SP superficial peroneus - Sart sartorius - Q quadriceps     

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.     

Differential modulation of primary afferent depolarization of segmental and ascending intraspinal collaterals of single muscle afferents in the cat spinal cord

We examined primary afferent depolarization (PAD) in the anesthetized cat elicited in 109 pairs of intraspinal collaterals of single group I afferents from the gastrocnemius nerve, one of the pair ending in the L3 segment, around the Clarkes column nuclei, and the other in the L6 segment within the intermediate zone. Tests for refractoriness were made to assess whether the responses produced by intraspinal stimulation in the L3 and L6 segments were due to activation of collaterals of the same afferent fiber. PAD in each collateral was estimated by independent computer-controlled measurement of the intraspinal current required to maintain a constant probability of antidromic firing. In most fibers, stimulation of the ipsilateral posterior biceps and semitendinosus (PBSt) nerve with trains of pulses maximal for group I afferents had a qualitatively similar effect but produced a larger PAD in the L6 than in the L3 collaterals. Stimulation of cutaneous nerves (sural and superficial peroneus) with single pulses and of the posterior articular nerve, the ipsilateral reticular formation, nucleus raphe magnus and contralateral motor cortex with trains of pulses often had qualitatively different effects. They could produce PAD and/or facilitate the PBSt-induced PAD in one collateral, and produce PAH and/or inhibit the PAD in the other collateral. These patterns could be changed in a differential manner by sensory or supraspinal conditioning stimulation. In summary, the present investigation suggests that the segmental and ascending collaterals of individual afferents are not fixed routes for information transmission, but parts of dynamic systems in which information transmitted to segmental reflex pathways and to Clarkes column neurons by common sources can be decoupled by sensory and descending inputs and funneled to specific targets according to the motor tasks to be performed.     

Effects of pad on conduction of action potentials within segmental and ascending branches of single muscle afférents in the cat spinal cord

In anesthetized and paralyzed cats under artificial respiration, we examined the extent to which primary afferent depolarization (PAD) might affect invasion of action potentials in intraspinal axonal and/or terminal branches of single muscle afferents. To this end, one stimulating micropipette was placed at the L6 spinal level within the intermediate or motor nucleus, and another one at the L3 level, in or close to Clarke's column. Antidromically conducted responses produced in single muscle afferents by stimulation at these two spinal levels were recorded from fine lateral gastrocnemius nerve filaments. In all fibers examined, stimulation of one branch, with strengths producing action potentials, increased the intraspinal threshold of the other branch when applied at short conditioning testing stimulus intervals (<1.5-2.0 ms), because of the refractoriness produced by the action potentials invading the tested branch. Similar increases in the intraspinal threshold were found in branches showing tonic PAD and also during the PAD evoked by stimulation of group I afferent fibers in muscle nerves. It is concluded that during tonic or evoked PAD, axonal branches in the dorsal columns and myelinated terminals of muscle afferents ending deep in the L6 and L3 segmental levels continue to be invaded by action potentials. These findings strengthen the view that presynaptic inhibition of muscle afferents produced by activation of GABAergic mechanisms is more likely to result from changes in the synaptic effectiveness of the afferent terminals than from conduction failure because of PAD.     

Correlation analysis of muscle receptor discharge during active contractions of the cat medial gastrocnemius muscle

The spike trains of afferent fibers innervating muscle spindles and Golgi tendon organs in the medial gastrocnemius muscle were recorded during spontaneous contractions in either decerebrate cats or decapitate cats treated with L-dopa. For each afferent fiber, the approximate location of its receptor within the muscle was determined. Cross-correlation histograms were compiled from the simultaneously recorded spike trains of pairs of afferent fibers (Ia, Ib, spindle II) to determine if the degree of temporal correlation in their discharge was related to the mutual proximity of the receptors they innervated within the muscle. The frequency of occurrence and degree of correlated activity between pairs of muscle afferents, regardless of receptor type, was much greater in the decerebrate preparations than in the decapitate-L-dopa preparations. However, in all cases, the extent of correlated activity appeared to be unrelated to the relative locations of the receptors. The results suggest that the degree to which the discharge patterns of muscle receptors display temporal correlations and thereby potentially reinforce the "sensory partitioning" (5) of their parent muscle is strongly dependent on the type of preparation used, and thus by inference, dependent on the central state of the animal.     

Bulbospinal inhibition of PAD elicited by stimulation of afferent and motor axons in the isolated frog spinal cord and brainstem

Summary 1. In the isolated spinal cord and brainstem of the frog, stimulation of the brainstem (BS) with trains of 3–4 pulses at 60–400 Hz produced dorsal root potentials (DRPs). The lowest threshold sites eliciting DRPs were located at the level of the obex up to about 2.5 mm rostrally, 0.5–1.2 mm laterally, between 0.5 and 1.6 mm depth. This region corresponds to the bulbar reticular formation (RF). 2. Stimulation of the RF with strengths below those required to produce DRPs, very effectively inhibited the DRPs produced by stimulation of a neighboring dorsal root (DR-DRPs) as well as the DRPs produced by antidromic stimulation of the central end of motor nerves (VR-DRPs). The inhibition was detectable 20 ms after the first pulse of the conditioning train, attained maximal values between 50 and 100 ms and lasted more than 250ms. 3. Stimulation of the bulbar RF increased the negative response (N₁ response) produced in the motor pool by antidromic activation of motoneurons. The time course of the facilitation of the N₁ response resembled that of the reticularly-induced inhibition of the VR-DRPs and DR-DRPs. 4. The present series of observations supports the existence of reticulospinal pathways that are able to inhibit the depolarization elicited in afferent fibers by stimulation of other afferent fibers or by antidromic activation of motor axons. This inhibition appears to be exerted on the PAD mediating interneurons and is envisaged as playing an important role in motor control.     

Differential effects of hindlimb peripheral afferents on motoneurons innervating different parts of longissimus muscle in cats

Previous studies (Wada and Kanda 2001, Exp Brain Res 136:263–263; Wada et al. 1999, Exp Brain Res 128:543–549) demonstrated that input patterns from hindlimb muscles and cutaneous afferents vary among individual trunk muscle motoneurons. The purpose of the present study was to examine the relationship between the synaptic pattern from hindlimb afferents and the area innervated by motoneurons. Histologic study of m. longissimus lumborum (Long) indicated that the distribution of different fiber types (slow-twitch oxidative, SO; fast-twitch oxidative glycolytic, FOG; fast-twitch glycolytic, FG) depends on the area of the Long cross-section. The ventromedial area and dorsolateral area of the cross-section possess a high content of SO and FG, respectively. The motoneurons innervating the dorsolateral area receive muscle afferent inputs mainly from the ipsilateral side, while the motoneurons innervating the ventromedial area often receive bilateral afferent inputs. The motoneurons innervating the dorsolateral area receive excitatory post-synaptic potentials from cutaneous nerves on both sides. These findings indicate that the effects of afferent inputs from the hindlimbs are related to motoneuron type or the area innervated by the motoneurons.