Synaptic organization of defined motor-unit types in cat tibialis anterior

1980 ◽  
Vol 43 (6) ◽  
pp. 1631-1644 ◽  
Author(s):  
R. P. Dum ◽  
T. T. Kennedy

1. Synaptic potentials were recorded intracellularly in tibialis anterior (TA) motoneurons following stimulation of a descending brain stem pathway, the medial longitudinal fasciculus (MLF), and three segmental inputs, the homonymous and heteronymous group Ia afferents, the group I afferents from the antagonist, and the cutaneous and muscle afferents. Intracellular stimulation of the motoneurons was used to classify them, based on the properties of the innervated muscle units, into types FF, F(int), FR, and S (6, 16). 2. The sum of the monosynaptic EPSP amplitudes resulting from stimulation of homonymous and heteronymous group Ia afferents (summed group Ia EPSP) was inversely related to motoneuron size, as assessed by motoneuron input resistance, and was inversely related to motor-unit tetanic tension. Type-FF, -FR, and -S motoneurons showed significant differences in the mean amplitude of their summed group Ia EPSPs. 3. The amplitudes of disynaptic IPSPs resulting from stimulation of group I afferents in the antagonist muscle also showed an inverse relationship to motoneuron size. The observed relationships between motoneuron size and the monosynaptic group Ia EPSP amplitude or the disynaptic group I IPSP amplitude are compatible with the “size principle” of motor-unit recruitment (26). 4. The amplitudes of the monosynaptic EPSPs evoked in TA motoneurons by stimulation of the MLF were distributed rather randomly among all types of TA motoneurons. A slight tendency of larger monosynaptic EPSPs to occur in motoneurons with larger tetanic tensions was observed. 5. The polysynaptic effects from cutaneous and muscle afferents in sural and gastrocnemius-soleus nerves were frequently excitatory on type-FF motoneurons, but were primarily inhibitory on type-FR and -S motoneurons. Clearly, the polysynaptic cutaneous and muscle inputs and the monosynaptic MLF input onto TA motoneurons show a different pattern of synaptic organization than the group I inputs. 6. In general, the synaptic organization of the TA motor nucleus is similar to that of its extensor antagonist, medial gastrocnemius (MG) (2--5, 7, 8), when analogous neural circuits are compared. This parallel organization suggests a commonality of motor-control systems for both flexor and extensor muscles.

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.


1984 ◽  
Vol 51 (3) ◽  
pp. 432-449 ◽  
Author(s):  
E. Brink ◽  
E. Jankowska ◽  
B. Skoog

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.


1990 ◽  
Vol 64 (2) ◽  
pp. 637-647 ◽  
Author(s):  
A. Mailis ◽  
P. Ashby

1. The hypothesis that the exaggerated tendon jerks and stretch reflexes that follow chronic spinal cord lesions in humans result from alterations in transmission from group I muscle afferents to motoneurons was tested by making observations on nine normal subjects and 25 patients with spinal cord lesions. All the patients had increased tendon jerks, one-third of them had both increased tendon jerks and increased, velocity-dependent stretch reflexes (i.e.g spasticity). 2. Changes in the firing probability of single, voluntary-activated soleus or tibialis anterior motor units during stimulation of the muscle nerve below the threshold of the alpha-motoneuron axons were used to derive the characteristics of the postsynaptic potentials produced by group I volleys in single motoneurons. Paired stimuli were used to test how multiple volleys in group I muscle afferents were transmitted to motoneurons. 3. Stimulation of the posterior tibial nerve produced a short-latency period of increased firing probability representing the homonymous composite Ia excitatory postsynaptic potential (EPSP) in all soleus motoneurons tested. There was no detectable alteration in the magnitude, duration, or profile of the short-latency facilitation in the patients with spinal lesions when compared with normal subjects. 4. In patients with traumatic spinal cord lesions less than 8 wk in duration the magnitude of the facilitation representing the composite Ia EPSP was significantly larger than normal, although only one out of the four patients in this group had spasticity. 5. In the patients with the greatest spasticity, group I volleys produced a second period of facilitation 11-15 ms after the facilitation representing the composite Ia EPSP. This is presumed to represent enhanced transmission through polysynaptic pathways from group I afferents to motoneurons. 6. In normal subjects the facilitation of motoneurons produced by the second of two group I volleys is greater 5 and 10 ms after the first volley and less 20, 30, and 50 ms after the first volley. These changes involve at least two factors: 1) changes in excitability of peripheral nerves and 2) changes in transmission at the Ia-motoneuron synapse. 7. In patients with spinal lesions the facilitation produced by the second of two muscle-afferent volleys was less depressed at the 30-ms interstimulus interval. 8. Thus two separate abnormalities have been uncovered in human subjects with chronic spinal lesions: 1) a change in the transmission of multiple volleys from muscle afferents to motoneurons and 2) an increase in transmission through polysynaptic pathways from Ia afferents to motoneurons. Both could contribute to the increased tendon jerks and exaggerated stretch reflexes.


1976 ◽  
Vol 39 (3) ◽  
pp. 447-458 ◽  
Author(s):  
R. E. Burke ◽  
W. Z. Rymer

1. Intracellular recording and stimulation techniques were used in anesthetized cats to study the interrelations between amplitudes of PSPs produced by electrical stimulation of several short-latency pathways to MG alpha motoneurons and the mechanical properties of muscle units innervated by the same cells. Motor-unit types were identified by muscle-unit properties.2. The maximum amplitudes of monosynaptic EPSPs produced in MG motoneurons by activation of homonymous (MG) and heteronymous (LGS) group Ia afferents were clearly related to motor-unit type, being, on the average, largest in type S units, somewhat smaller in type FR and F(int) units, and smallest in type FF units. Correspondingly, group Ia EPSP amplitudes were inversely correlated with muscle-unit tension production and directly correlated with resistance to fatigue. The same input distribution was true for disynaptic IPSPs produced by group Ia afferents from antagonist ankle flexors.3. The amplitudes of monosynaptic EPSPs produced by fibers descending in the ipsilateral ventral funiculi of the low thoracic cord were not clearly related to MG motor-unit type or (therefore) to muscle-unit properties.4. A quantitative input-output model of the MG motor-unit pool, based in part on the present results, suggests that overall characteristics of MG motor units, and their relative numbers in the MG pool, reflect functional specializations determined by specific mechanical demands placed on the MG muscle by the usual motor behavior of the animal.


1990 ◽  
Vol 63 (3) ◽  
pp. 395-403 ◽  
Author(s):  
T. M. Hamm

1. Recurrent inhibitory postsynaptic potentials (IPSPs) to and from motoneurons innervating the flexor digitorum longus (FDL) and flexor hallucis longus (FHL) muscles of the cat were investigated to determine whether recurrent inhibitory projections involving these motoneurons are similar--as would be consistent with the Ia and anatomic synergism of FDL and FHL--or are dissimilar, as are the activities of these muscles during locomotion (O'Donovan et al. 1982). 2. Composite recurrent IPSPs were recorded in several species of motoneurons innervating hindlimb muscles in response to stimulation of a number of muscle nerves in cats allowed to become unanesthetized after ischemic decapitation. 3. No recurrent IPSPs from stimulation of the FDL nerve were observed in motoneurons innervating FDL, FHL, lateral gastrocnemius-soleus (LG-S), medial gastrocnemius (MG), plantaris (Pl), tibialis anterior (TA), or extensor digitorum longus (EDL). 4. The recurrent IPSPs produced by stimulation of FHL were larger and found more frequently in LG-S than in FDL motoneurons. Recurrent inhibition from FHL was also greater in Pl than in FDL motoneurons. 5. The recurrent IPSPs produced by stimulation of LG-S, PL, and MG were larger in FHL than in FDL motoneurons, and those from LG-S and MG were found more frequently in FHL than in FDL motoneurons. 6. Stimulation of the TA nerve produces recurrent IPSPs in FDL but not in FHL motoneurons. A few FDL and FHL cells (6 of 23 and 9 of 34, respectively) received small (less than 0.5 mV) recurrent IPSPs from stimulation of the EDL nerve.(ABSTRACT TRUNCATED AT 250 WORDS)


1985 ◽  
Vol 53 (2) ◽  
pp. 497-517 ◽  
Author(s):  
R. K. Powers ◽  
M. D. Binder

To characterize the oligosynaptic group I afferent input to the cat medial gastrocneumius (MG) motoneuron pool, the medial branch of the tibial nerve (MTIB: flexor digitorum and hallucis longus, popliteus, tibialis posterior and interosseous nerves), the nerves to flexor digitorum and hallucis longus (FDHL), or the nerves to the quadriceps muscles (QUAD) were stimulated at submaximal group I strength while recording intracellularly from MG motoneurons. Since previous work indicates that stimulation of these nerves at group I strength produces no significant monosynaptic Ia excitation or Renshaw inhibition of MG motoneurons, group I effects were assumed to be predominantly, though not exclusively, due to the action of Ib-fibers. Evidence supporting this assumption is presented in the following paper. MTIB, FDHL, and QUAD postsynaptic potentials (PSPs) were most commonly inhibitory. Since the MTIB, FDHL, and QUAD nerves are composed predominantly of fibers innervating muscles with extensor action, their inhibitory effect on MG motoneurons is consistent with previous findings that stimulation of Ib-afferents in nerves to extensor muscles produces di- and trisynaptic inhibition of extensor motoneurons. However, excitatory effects were observed in about one third of the motoneurons, indicating that oligosynaptic group I input is not homogeneously distributed within the MG motoneuron pool. Variations in QUAD, FDHL, and MTIB PSP pattern and amplitude were correlated with variations in the PSP pattern evoked by stimulation of the sural nerve: excitatory oligosynaptic group I PSPs generally appeared in motoneurons receiving excitatory cutaneous (sural nerve) input, whereas inhibitory PSPs generally appeared in motoneurons receiving some inhibitory cutaneous input and were largest in motoneurons receiving predominantly inhibition from the sural nerve. These variations in QUAD, FDHL, and MTIB PSP pattern and amplitude were not due to variations in resting potential and were only partly due to variations in intrinsic motoneuron properties or motoneuron "type." Our results indicate that activation of these cutaneous and group I muscle afferents can exert similar effects on the MG motoneuron pool. Moreover, the presence of a strong correlation between the distributions of cutaneous and oligosynaptic group I PSPs within a single motoneuron pool is consistent with the results of previous studies that have shown that some of the input to motoneurons from these peripheral afferents is mediated through common interneurons.


1996 ◽  
Vol 75 (3) ◽  
pp. 1126-1137 ◽  
Author(s):  
G. W. Hiebert ◽  
P. J. Whelan ◽  
A. Prochazka ◽  
K. G. Pearson

1. In this investigation, we tested the hypothesis that muscle spindle afferents signaling the length of hind-leg flexor muscles are involved in terminating extensor activity and initiating flexion during walking. The hip flexor muscle iliopsoas (IP) and the ankle flexors tibialis anterior (TA) and extensor digitorum longus (EDL) were stretched or vibrated at various phases of the step cycle in spontaneously walking decerebrate cats. Changes in electromyogram amplitude, duration, and timing were then examined. The effects of electrically stimulating group I and II afferents in the nerves to TA and EDL also were examined. 2. Stretch of the individual flexor muscles (IP, TA, or EDL) during the stance phase reduced the duration of extensor activity and promoted the onset of flexor burst activity. The contralateral step cycle also was affected by the stretch, the duration of flexor activity being shortened and extensor activity occurring earlier. Therefore, stretch of the flexor muscles during the stance phase reset the locomotor rhythm to flexion ipsilaterally and extension contralaterally. 3. Results of electrically stimulating the afferents from the TA and EDL muscles suggested that different groups of afferents were responsible for the resetting of the step cycle. Stimulation of the TA nerve reset the locomotor step cycle when the stimulus intensity was in the group II range (2-5 xT). By contrast, stimulation of the EDL nerve generated strong resetting of the step cycle in the range of 1.2-1.4 xT, where primarily the group Ia afferents from the muscle spindles would be activated. 4. Vibration of IP or EDL during stance reduced the duration of the extensor activity by similar amounts to that produced by muscle stretch or by electrical stimulation of EDL at group Ia strengths. This suggests that the group Ia afferents from IP and EDL are capable of resetting the locomotor pattern generator. Vibration of TA did not affect the locomotor rhythm. 5. Stretch of IP or electrical stimulation of TA afferents (5 xT) during the flexion phase did not change the duration of the flexor activity. Stimulation of the EDL nerve at 1.8-5 xT during flexion increased the duration of the flexor activity. In none of our preparations did we observe resetting to extension when the flexor afferents were activated during flexion. 6. We conclude that as the flexor muscles lengthen during the stance phase of gait, their spindle afferents (group Ia afferents for EDL and IP, group II afferents for TA) act to inhibit the spinal center generating extensor activity thus facilitating the initiation of swing.


1991 ◽  
Vol 66 (4) ◽  
pp. 1127-1138 ◽  
Author(s):  
T. C. Cope ◽  
B. D. Clark

1. Recruitment order was studied in pairs of motor units of the medial gastrocnemius (MG) muscle of decerebrate cats with the use of dual microelectrode recording from intact ventral root filaments. Excitation was provided by stretch of MG, stretch of synergists [lateral gastrocnemius (LG), plantaris (PL), and soleus (SOL) muscles] or electrical stimulation of the caudal cutaneous sural (CCS) nerve. Motor units were characterized by axonal conduction velocity (CV), tetanic tension (Pmax), twitch contraction time (CT), and fatigue index (FI). 2. Consistent with the recruitment pattern described by others, most often in relation to either CV or Pmax, the first unit of a pair to be recruited by MG stretch was typically the one with the lower CV and Pmax, and the higher FI and CT. The proportion of pairs that agreed in rank order of each property and recruitment order was as follows: for CT, 94%; for CV, 87%; for Pmax, 84%; and for FI, 75%. With a single marginal exception (CT vs. FI), no motor-unit property proved to be significantly better than the others at predicting recruitment (G test; P greater than 0.05). 3. In all 11 tested pairs containing one slow (type S) and one fast (type F) unit, the S was more easily recruited by stretch. Type F units divided into groups with high (type FR), low (type FF), and intermediate (type FInt) values for FI were recruited in order from FR to FInt to FF in 8/11 pairs. Thus our findings were similar to earlier demonstrations that recruitment proceeds in order by type. 4. Stretch of MG synergists usually recruited units in the same order as MG stretch. In two S-S pairs, recruitment order was switched with synergist stretch. 5. Stimulation of the CCS nerve was generally excitatory to the MG units sampled. Most unit pairs were recruited by CCS stimulation in the same order as by MG stretch, but, for 6 of 39 pairs, CCS stimulation switched the order produced by stretch. Thus, whereas sural afferent input can preferentially excite some units over others as suggested by Kanda et al., that effect is not widespread or selective for unit type under these conditions. 6. Assuming that all MG motor units cooperate as a single functional pool in homonymous stretch reflexes, we support others in concluding that a motoneuron's recruitment threshold is not strictly determined by its size. However, our data do not distinguish other schemes that predict recruitment order more accurately than the size principle.(ABSTRACT TRUNCATED AT 400 WORDS)


1982 ◽  
Vol 48 (2) ◽  
pp. 419-430 ◽  
Author(s):  
J. A. Flatman ◽  
I. Engberg ◽  
J. D. Lambert

1. Cat lumbosacral motoneurons were impaled by two individually advanced microelectrodes: one to record membrane potential (EM), the second to pass depolarizing currents. 2. During the passage of depolarizing current ramps the repetitive action-potential firing and the later high conductance (GM) state obscured and distorted Ia excitatory postsynaptic potentials (EPSPs) evoked by electrical stimulation of hindlimb muscle afferents. 3. Intracellular iontophoresis of QX-222 (a trimethyl analogue of lignocaine) or methylxylocholine, prevented action-potential generation and reduced the GM increase during current depolarization so that positive levels of EM could be reached. 4. Following QX-222 treatment it was possible to demonstrate a reversal of the Ia EPSP including its first part, at EM values between -13 and +32 mV. Reversal was seen in 13 of the 22 motoneurons tested. 5. Reversal was easiest to obtain in motoneurons of the deep peroneal group. More positive levels of EM were needed to show a reversal in neurons of the gastrocnemius-so-leus group. (The 10-90% rise times of the EPSPs were rather similar for both groups.) 6. In a few motoneurons the initial part of the Ia EPSP reversed at a more negative EM than a later part. This was best seen after subtraction of the extracellular field potentials from the records.


2012 ◽  
Vol 108 (11) ◽  
pp. 3034-3042 ◽  
Author(s):  
D. A. E. Bolton ◽  
J. E. Misiaszek

Electrical stimulation of the lateral gastrocnemius-soleus (LGS) nerve at group I afferent strength leads to adaptations in the amplitude and timing of extensor muscle activity during walking in the decerebrate cat. Such afferent feedback in the stance leg might result from a delay in stance onset of the opposite leg. Concomitant adaptations in hip abductor and adductor activity would then be expected to maintain lateral stability and balance until the opposite leg is able to support the body. As many hip abductors and adductors are also hip extensors, we hypothesized that stimulation of the LGS nerve at group I afferent strength would produce increased activation and prolonged burst duration in hip abductor and adductor muscles in the premammillary decerebrate walking cat. LGS nerve stimulation during the extensor phase of the locomotor cycle consistently increased burst amplitude of the gluteus medius and adductor femoris muscles, but not pectineus or gracilis. In addition, LGS stimulation prolonged the burst duration of both gluteus medius and adductor femoris. Unexpectedly, long-duration LGS stimulus trains resulted in two distinct outcomes on the hip abductor and adductor bursting pattern: 1) a change of burst duration and timing similar to medial gastrocnemius; or 2) to continue rhythmically bursting uninterrupted. These results indicate that activation of muscle afferents from ankle extensors contributes to the regulation of activity of some hip abductor and adductor muscles, but not all. These results have implications for understanding the neural control of stability during locomotion, as well as the organization of spinal locomotor networks.


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