Regenerating sprouts of axotomized cat muscle afferents express characteristic firing patterns to mechanical stimulation

1991 ◽  
Vol 66 (6) ◽  
pp. 2155-2158 ◽  
Author(s):  
R. D. Johnson ◽  
J. B. Munson

1. In cats, we studied the physiological properties of regenerating sprouts of muscle afferent fibers and compared them with sprouts from cutaneous afferent fibers. 2. Muscle nerves to the triceps surae and cutaneous sural nerves were axotomized in the popliteal fossa, and the proximal ends were inserted into nerve cuffs. Six days later, we recorded action potentials from single Groups I and II muscle and mostly Group II cutaneous afferents driven by mechanostimulation of the cuff. 3. Most muscle afferent sprouts (91%) had a regular slowly adapting discharge in response to sustained mechanical displacement of the cuff, particularly to sustained stretch stimuli, whereas most cutaneous afferents (92%) did not. Muscle afferents were more likely to have a spontaneous discharge and afterdischarge. 4. Group II muscle afferent sprouts had lower stretch thresholds and a higher incidence of spontaneous discharge compared with Group I fiber sprouts, whereas Group I fibers had a higher incidence of high-frequency afterdischarge to mechanical stimuli. 5. We conclude that, 6 days after axotomy, regenerating sprouts of muscle afferents, particularly Group II afferents, have become mechanosensitive in the absence of a receptor target and exhibit physiological properties similar to those found when innervating their native muscle but significantly different from sprouts of cutaneous afferents. Expression of these native muscle afferent firing patterns after the inappropriate reinnervation of hairy skin may be due to inherent properties of the muscle afferent fiber.

1987 ◽  
Vol 57 (5) ◽  
pp. 1288-1313 ◽  
Author(s):  
P. Rudomin ◽  
M. Solodkin ◽  
I. Jimenez

Spike-triggered averaging of dorsal and ventral root potentials was used in anesthetized cats to disclose possible synaptic connections of spinal interneurons in the intermediate nucleus with afferent fibers and/or motoneurons. With this method we have been able to document the existence of a distinct group of interneurons whose activity was associated with the recording of inhibitory potentials in the ventral roots (iVRPs), but not with negative dorsal root potentials (nDRPs). The iVRPs had mean durations of 60.8 +/- 22.1 ms and latencies between 1.7 and 5.1 ms relative to the onset of the interneuronal spikes. Within this group of neurons it was possible to characterize two categories depending on their responses to segmental inputs. Most type A interneurons were mono- or disynaptically activated by group I muscle afferents and polysynaptically by low threshold (1.08-1.69 X T) cutaneous fibers. Type B interneurons were instead polysynaptically activated by group II muscle and by cutaneous fibers with thresholds ranging from 1.02 to 3.1 X T. Whenever tested, both type A and B interneurons could be antidromically activated from Clarke's columns. There was a second group of interneurons whose activity was associated with the generation of both iVRPs and nDRPs. These potentials had mean durations of 107.5 +/- 35.6 and 131.5 +/- 32 ms, respectively, and onset latencies between 1.7 and 6.1 ms. The interneurons belonging to this group, which appear not to send axonal projections to Clarke's column, could be classified in three categories depending on their responses to peripheral inputs. Type C interneurons responded mono- or disynaptically to group I muscle volleys and polysynaptically to intermediate threshold (1.22-2.7 X T) cutaneous afferents. Type D interneurons were polysynaptically activated by group II muscle afferents (2.3-8.5 X T) and by intermediate threshold (1.4-3 X T) cutaneous fibers and type E interneurons only by group I muscle afferents with mono- or disynaptic latencies. A third group of interneurons produced nDRPs without iVRPs. The nDRPs had onset latencies varying from 1.9 to 6.2 ms and mean durations of 130.0 +/- 34.6 ms. These neurons (type F) showed spontaneous and evoked bursts of activity and were not antidromically activated from Clarke's column. They responded to stimulation of low- and intermediate-threshold cutaneous fibers (1.04-2.9 X T) with mono- and polysynaptic latencies, but not by group I muscle fibers. Type F interneurons appear to be located in more superficial layers than all the other interneurons.(ABSTRACT TRUNCATED AT 400 WORDS)


1986 ◽  
Vol 56 (5) ◽  
pp. 1268-1283 ◽  
Author(s):  
R. E. Fyffe ◽  
S. S. Cheema ◽  
A. Rustioni

The terminal arborizations of single identified cutaneous hair follicle and slowly adapting type I receptors and muscle (Ia) afferents have been studied in the cuneate nucleus of cats after intra-axonal injection of horseradish peroxidase. Penetrations were mainly at the middle and caudal levels of the nucleus--i.e., from obex to approximately 7 mm caudal to it. Following histochemical processing, the injected axons, along with their collateral branches and synaptic terminals, were visualized and examined with light and electron microscopy. Cutaneous afferents in middle cuneate (from obex to approximately 4 mm caudal to it) issued collateral branches, along the rostrocaudal axis of the nucleus, at intervals between 100 and 1,000 microns. The terminal field of each collateral's branches encompassed an area elongated largely rostrocaudally and virtually confined to the dorsal part of the middle cuneate. Although adjacent collaterals had nonoverlapping terminal arborizations, each one could give rise to separate foci of terminations. Muscle afferents differed, on the whole, from cutaneous afferents in the location and extent of collateral branching and terminal arborizations. However, because muscle fibers terminated primarily in the ventral region of the cuneate, but nevertheless exhibited sparser terminations in the dorsal part of the middle cuneate, there was some spatial overlap between zones of muscle and cutaneous projection. Synaptic boutons of cutaneous afferent fibers contained round clear vesicles, contacted dendritic profiles (sometimes more than one), and were postsynaptic to small boutons containing polymorphic vesicles. In contrast, boutons of muscle afferent fibers contacted somatic and dendritic profiles and were not postsynaptic to other boutons. The results are in general agreement with previous anatomical and electrophysiological work; however, the extent of the terminal field of single collateral branches may provide for a greater convergence of different receptor classes and of receptive fields on neurons in the middle cuneate than estimated by previous electrophysiological investigations.


1976 ◽  
Vol 39 (3) ◽  
pp. 484-500 ◽  
Author(s):  
J. Hore ◽  
J. B. Preston ◽  
P. D. Cheney

1. A study was made of the response of single cortical units in areas 3a and 4 to electrical stimulation of hindlimb muscle nerves and to ramp stretch of hindlimb muscles in baboons anesthetized with chloralose.2. Stimulation of hindlimb muscle nerves revealed a group I projection primarily to area 3a but with some input into adjacent area. 4. A major group II projection was found in area 4 adjacent to area 3a. A small number of area 3a neurons receive convergence from both group I and group II muscle afferents.3a. On the basis of their response pattern to ramp stretch, units were classified into one of six categories and their cytoarchitectonic location was determined. Units in area 3a had hynamic sensitivities equivalent to that of the primary spindle afferents. Although the discharge of some area 3a neurons also reflected differences in muscle length, most area 3a neurons had low position sensitivities. One unit type in area 3a did not respond to maintained muscle stretch and signaled only velocity of stretch.4. Units in area 4 had position sensitivities equivalent to that of primary and secondary spindle afferents. Although the discharge of some area 4 units reflected different velocities of muscle stretch, these units had dynamic sensitivities similar to those of secondary spindle afferents rather than those of primary afferents. One type of unit in area 4 had no dynamic component to muscle stretch and signaled only muscle length.5. The results demonstrate that there is a transfer of dynamic and position sensitivity from spindle afferents to cortical neurons. Furthermore, data processing has occurred because some units respond only to the steady-state length of muscle, while other units encode only the dynamic phase of stretch. This behavior is different from the responses to ramp stretch of either group I or group II muscle afferents in the baboon.6. The results demonstrate that single units in cerebral cortex can encode the information transmitted to the central nervous system by muscle spindle afferents. The purpose for which this information is used remains undetermined.


1995 ◽  
Vol 73 (2) ◽  
pp. 651-661 ◽  
Author(s):  
R. D. Johnson ◽  
J. S. Taylor ◽  
L. M. Mendell ◽  
J. B. Munson

1. In this study we investigate the peripheral receptive field properties and spinal cord connections of low-threshold muscle afferent fibers cross-regenerated into the skin to determine whether a cutaneous target can rescue physiological functions lost after chronic axotomy. 2. In adult cats the medial gastrocnemius (MG) muscle nerve was coated with the distal cut end of either the caudal or lateral cutaneous sural nerves and allowed to regenerate into the hairy skin (postoperative period 6-30 mo). During terminal acute experiments we made recordings of single MG afferent fibers in dorsal root filaments and peripheral nerve. Conduction velocity and receptive field characteristics were determined for each fiber. In addition, the MG nerve was stimulated to elicit cord dorsum potentials and monosynaptic excitatory postsynaptic potentials (EPSPs) in heteronymous motoneurons. As controls, studies were carried out after MG nerve axotomy (postoperative period 2.5-12 mo). 3. After innervation of the skin, MG muscle afferent fibers exhibited firing characteristics and proximal segment conduction velocities like those of normal MG afferents. Responses to skin and hair stimulation consisted primarily of slowly adapting, stretch-sensitive, and steady discharge patterns, all common in normal muscle afferents but not in cutaneous afferents. These properties were observed despite the innervation of touch domes and single hairs, suggesting that the peripheral physiology of muscle afferents is a function of the axonal membrane and is not respecified by a cutaneous target and/or receptors. 4. Cord dorsum potentials were characteristic of those elicited by intact muscle afferents rather than skin afferents and showed recovery of configurations lost after chronic axotomy. 5. The monosynaptic EPSPs elicited in lateral gastrocnemius-soleus motoneurons also recovered from the reduction in amplitude observed after chronic axotomy. The configurations of these EPSPs were characteristic of muscle afferents rather than skin afferents. 6. These experiments demonstrate that the peripheral and central physiological properties of muscle afferents are rescued from the axotomy state if the afferents are allowed to reinnervate skin. We found no evidence that respecification had occurred to bring the function of muscle afferents into accord with the new cutaneous target.


1993 ◽  
Vol 70 (5) ◽  
pp. 1805-1810 ◽  
Author(s):  
J. Lafleur ◽  
D. Zytnicki ◽  
G. Horcholle-Bossavit ◽  
L. Jami

1. The aim of the present experiments was to verify whether group II inputs from gastrocnemius medialis (GM) muscle could elicit declining inhibitions similar to those observed during GM contractions in a variety of lumbar motoneurons of the cat spinal cord. Motoneurons were recorded intracellularly in chloralose- or pentobarbitone-anesthetized preparations during electrical stimulation of GM nerve with repetitive trains. 2. With strengths in the group I range, repetitive stimulation evoked the usual Ia excitation in homonymous motoneurons and excitatory postsynaptic potential (EPSP) amplitudes remained constant throughout the stimulation sequence. In synergic plantaris motoneurons lacking an excitatory connection with Ia afferents from GM, the same stimulation, kept at a constant strength throughout the stimulation sequence, elicited rapidly decreasing inhibitory potentials reminiscent of those evoked by GM contractions. 3. In motoneurons of pretibial flexors, quadriceps, and posterior biceps-semitendinosus, the stimulation strength required to observe declining inhibitions resembling those produced by GM contractions was 4-8 times group I threshold, engaging group II in addition to group I fibers. 4. These results show that input from GM group II plus group I afferents can elicit inhibitory effects in a variety of motoneurons. Such observations support the hypothesis that messages from spindle secondary endings and/or nonspecific muscle receptors activated during contraction might contribute to the widespread inhibition caused by GM contractions. 5. Inasmuch as constant input in group II and group I afferents evoked declining inhibitory potentials, the origin of the decline must be central, which suggests that the rapid reduction of contraction-induced inhibitions also depended on a central mechanism.


2012 ◽  
Vol 108 (4) ◽  
pp. 1176-1185 ◽  
Author(s):  
Rinaldo André Mezzarane ◽  
André Fabio Kohn ◽  
Erika Couto-Roldan ◽  
Lourdes Martinez ◽  
Amira Flores ◽  
...  

Crossed effects from group I afferents on reflex excitability and their mechanisms of action are not yet well understood. The current view is that the influence is weak and takes place indirectly via oligosynaptic pathways. We examined possible contralateral effects from group I afferents on presynaptic inhibition of Ia terminals in humans and cats. In resting and seated human subjects the soleus (SO) H-reflex was conditioned by an electrical stimulus to the ipsilateral common peroneal nerve (CPN) to assess the level of presynaptic inhibition (PSI_control). A brief conditioning vibratory stimulus was applied to the triceps surae tendon at the contralateral side (to activate preferentially Ia muscle afferents). The amplitude of the resulting H-reflex response (PSI_conditioned) was compared to the H-reflex under PSI_control, i.e., without the vibration. The interstimulus interval between the brief vibratory stimulus and the electrical shock to the CPN was −60 to 60 ms. The H-reflex conditioned by both stimuli did not differ from that conditioned exclusively by the ipsilateral CPN stimulation. In anesthetized cats, bilateral monosynaptic reflexes (MSRs) in the left and right L7 ventral roots were recorded simultaneously. Conditioning stimulation applied to the contralateral group I posterior biceps and semitendinosus (PBSt) afferents at different time intervals (0–120 ms) did not have an effect on the ipsilateral gastrocnemius/soleus (GS) MSR. An additional experimental paradigm in the cat using contralateral tendon vibration, similar to that conducted in humans, was also performed. No significant differences between GS-MSRs conditioned by ipsilateral PBSt stimulus alone and those conditioned by both ipsilateral PBSt stimulus and contralateral tendon vibration were detected. The present results strongly suggest an absence of effects from contralateral group I fibers on the presynaptic mechanism of MSR modulation in relaxed humans and anesthetized cats.


1961 ◽  
Vol 200 (4) ◽  
pp. 679-684 ◽  
Author(s):  
K. Koizumi ◽  
J. Ushiyama ◽  
C. McC. Brooks

Respiratory effects of stimulating afferent fibers of muscle, skin and mixed nerve were determined in Nembutal-anesthetized cats. Repetitive stimuli which produced only monosynaptic reflex actions caused augmentation of respiration. When stronger stimuli also activated fibers of a smaller diameter than group I afferents, polysynaptic reflexes were evoked and greater changes in respiration resulted. Volume rather than rate changes were induced by stimulation of these muscle afferents. Microelectrodes were used to record from respiratory neurons of the medulla and pons. Most neurons fired in conjunction with inspiration; stimulation of muscle afferents advanced time of firing and increased frequency of discharge. Neurons firing in conjunction with expiration were inhibited by muscle afferents. A few neurons of the pons showed respiration-linked activity modified by afferent nerve stimulation. Segmental reflex discharges, out intercostal nerves, elicited by dorsal root stimulation were found to be inhibited by stimulation of muscle afferents. Discharges from muscle receptors affect ventilatory volumes and activities of medullary neurons which seemingly participate in the control of respiration.


1985 ◽  
Vol 53 (2) ◽  
pp. 518-529 ◽  
Author(s):  
R. K. Powers ◽  
M. D. Binder

In the experiments described in the preceding paper electrical stimulation of the quadriceps (QUAD), medial tibial (MTIB), and flexor digitorum and hallucis longus (FDHL) muscle nerves was used to evoke oligosynaptic group I postsynaptic potentials (PSPs) in medial gastrocnemius (MG) motoneurons. In the present study, we attempted to specify the types of afferent fibers which mediate that oligosynaptic activity (FDHL to MG only). In one series of experiments, isolated single flexor digitorum longus (FDL) and flexor hallucis longus (FHL) afferents were identified as Ia, Ib, or group II fibers according to their conduction velocities, responses to muscle contraction, and mechanical thresholds to small amplitude triangular stretches applied to the parent muscles. We also determined the electrical thresholds of the identified afferent fibers by applying graded electrical stimulation to their muscle nerve. These results were used as criteria to define the types of afferents that mediated the electrically and stretch-evoked FDHL oligosynaptic PSPs recorded in MG motoneurons during a second series of experiments. The amplitudes of the oligosynaptic PSPs evoked in MG motoneurons increased as the strength of the electrical stimuli applied to the FDHL muscle nerves was raised to activate greater numbers of Ia- and Ib-fibers, but showed little or no additional increase when the stimulus intensity was raised further to include the majority of group II fibers. On this basis, a significant contribution by group II fibers to these oligosynaptic PSPs was considered unlikely. Simultaneous electrical activation of both Ia- and Ib-fibers produced distinct oligosynaptic PSPs in MG motoneurons, but these were likely due primarily to Ib-afferent activity, since selective activation of Ia-afferents (by stretch) rarely produced oligosynaptic PSPs in the same motoneurons. There was, however, evidence for some Ia contribution to these oligosynaptic PSPs. This is consistent with the demonstration that Ia- and Ib-afferent fibers converge onto common interneurons and that selective activation of Ia-fibers can produce PSPs similar to those evoked by concurrent stimulation of Ia- and Ib-fibers. On the basis of the present results and those of several related studies it is argued that the oligosynaptic PSPs evoked in MG motoneurons by submaximal group I stimulation of the FDHL, MTIB, or QUAD muscle nerves can be ascribed predominantly to the activation of Ib-afferent fibers, with only minimal Ia and probably no group II contribution.


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