Topography of recurrent inhibitory postsynaptic potentials between individual motoneurons in the cat

1994 ◽  
Vol 72 (1) ◽  
pp. 214-226 ◽  
Author(s):  
M. L. McCurdy ◽  
T. M. Hamm

1. The amplitude of recurrent inhibitory postsynaptic potentials (RIPSPs) was examined in pairs of lumbosacral motoneurons that were separated by a known distance and were identified by antidromic stimulation of muscle nerves. One motoneuron was stimulated by injecting depolarizing current pulses, and postsynaptic responses were recorded and averaged in the second motoneuron. Input resistance, rheobase, and conduction velocity were determined for many motoneurons. Most motoneurons innervated extensor muscles. 2. RIPSP values as large as -283 microV were recorded, but most were between -10 and -40 microV. RIPSPs from individual motoneurons of a pool are distributed to several heteronymous motor nuclei and have a range of amplitudes comparable with homonymous RIPSPs. 3. A specific spatial distribution of RIPSP amplitudes was found whereby the largest RIPSP amplitudes (> 40 microV) occurred in motoneurons located within +/- 1.4 mm of the stimulated motoneuron. A significant correlation was found between RIPSP amplitude and the distance between motoneurons for all motoneuron pairs. This correlation was also found within individual groups of motoneuron pairs that innervate the lateral gastrocnemius, medial gastrocnemius, anterior-middle biceps femoris, or soleus muscles. 4. The dependency of RIPSP amplitude on the motoneuron species, which is the particular muscle a motoneuron innervates, is less distinct than the dependency of RIPSP amplitude on topography. Pooling all motoneuron species of close motoneuron pairs indicated that RIPSPs measured in homonymous motoneuron pairs were greater in amplitude than RIPSPs measured in heteronymous pairs. In addition, homonymous RIPSPs of anterior middle biceps femoris or lateral gastrocnemius motoneurons were greater than heteronymous RIPSPs of those motoneurons in all heteronymous combinations. However, homonymous and heteronymous RIPSPs were not significantly different when heteronymous pairs were restricted to individual combinations of species. These findings indicate that RIPSP amplitudes within a set of motor nuclei interconnected by recurrent inhibition are dependent in some cases on the species of motoneurons, but this effect is less important than the effect of topography on RIPSP amplitude. 5. These results indicate that recurrent inhibition in motoneuron pools that innervate hindlimb extensor muscles has a strong topographic organization, such that the strongest recurrent inhibition is produced by each motoneuron in a restricted rostrocaudal zone that includes both homonymous and heteronymous motor nuclei. This suggests that recurrent inhibition is organized for the control of several motor nuclei engaged in common motor activity as well as regulation of activity within individual motor pools.

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)


1999 ◽  
Vol 81 (5) ◽  
pp. 2485-2492 ◽  
Author(s):  
Alan J. Sokoloff ◽  
Sondra G. Siegel ◽  
Timothy C. Cope

Recruitment order among motoneurons from different motor nuclei. The principles by which motoneurons (MNs) innervating different multiple muscles are organized into activity are not known. Here we test the hypothesis that coactivated MNs belonging to different muscles in the decerebrate cat are recruited in accordance with the size principle, i.e., that MNs with slow conduction velocity (CV) are recruited before MNs with higher CV. We studied MN recruitment in two muscle pairs, the lateral gastrocnemius (LG) and medial gastrocnemius (MG) muscles, and the MG and posterior biceps femoris (PBF) muscles because these pairs are coactivated reliably in stretch and cutaneous reflexes, respectively. For 29/34 MG-LG pairs of MNs, the MN with lower CV was recruited first either in all trials (548/548 trials for 22 pairs) or in most trials (225/246 trials for 7 pairs), whether the MG or the LG MN in a pair was recruited first. Intertrial variability in the force thresholds of MG and LG MNs recruited by stretch was relatively low (coefficient of variation = 18% on average). Finally, punctate stimulation of the skin over the heel recruited 4/4 pairs of MG-LG MNs in order by CV. By all of these measures, recruitment order is as consistent among MNs from these two ankle muscles as it is for MNs supplying the MG muscle alone. For MG-PBF pairings, the MN with lower CV was recruited first in the majority of trials for 13/24 pairs and in reverse order for 9/24 pairs. The recruitment sequence of coactive MNs supplying the MG and PBF muscles was, therefore, random with respect to axonal conduction velocity and not organized as predicted by the size principle. Taken together, these findings demonstrate for the first time, that the size principle can extend beyond the boundaries of a single muscle but does not coordinate all coactive muscles in a limb.


1987 ◽  
Vol 57 (4) ◽  
pp. 1227-1245 ◽  
Author(s):  
R. C. Foehring ◽  
G. W. Sypert ◽  
J. B. Munson

We tested whether the muscle innervated may influence the expression of motoneuron electrical properties. Properties of individual motor units were examined following cross-reinnervation (X-reinnervation) of cat lateral gastrocnemius (LG) and soleus muscles by the medial gastrocnemius (MG) nerve. We examined animals at two postoperative times: 9-10 wk (medX) and 9-11 mo (longX). For comparison, normal LG and soleus motoneuron properties were also studied. Motor units were classified on the basis of their contractile responses as fast contracting fatigable, fast intermediate fast contracting fatigue resistant, and slow types FF, FI, FR, or S, respectively) (9, 21). Motoneuron electrical properties (rheobase, input resistance, axonal conduction velocity, afterhyperpolarization) were measured. After 9-11 mo, MG motoneurons that innervated LG muscle showed recovery of electrical properties similar to self-regenerated MG motoneurons. The relationships between motoneuron electrical properties were largely similar to self-regenerated MG. For MG motoneurons that innervated LG, motoneuron type (65) predicted motor-unit type in 74% of cases. LongX-soleus motoneurons differed from longX-LG motoneurons or self-regenerated MG motoneurons in mean values for motoneuron electrical properties. The differences in overall means reflected the predominance of type S motor units. The relationships between motoneuron electrical properties were also different than in self-regenerated MG motoneurons. In all cases, the alterations were in the direction of properties of type S units, and the relationship between normal soleus motoneurons and their muscle units. Within motor-unit types, the mean values were typical for that type in self-regenerated MG. Motoneuron type (65) was a fairly strong predictor of motor-unit type in longX soleus. MG motoneurons that innervated soleus displayed altered values for axonal conduction velocity, rheobase, and input resistance, which could indicate incomplete recovery from the axotomized state. However, although mean afterhyperpolarization (AHP) half-decay time was unaltered by axotomy (25), this parameter was significantly lengthened in MG motoneurons that innervated soleus muscle. There were, however, individual motoneuron-muscle-unit mismatches, which suggested that longer mean AHP half-decay time may also be due to incomplete recovery of a subpopulation of motoneurons. Those MG motoneurons able to specify soleus muscle-fiber type exhibited motoneuron electrical properties typical of that same motoneuron type in self-regenerated MG.(ABSTRACT TRUNCATED AT 400 WORDS)


1993 ◽  
Vol 70 (4) ◽  
pp. 1585-1592 ◽  
Author(s):  
J. S. Carp

1. Homonymous and heteronymous monosynaptic composite excitatory postsynaptic potentials (EPSPs) were evaluated by intracellular recordings from 89 motoneurons innervating triceps surae (n = 59) and more distal (n = 30) muscles in 14 pentobarbital-anesthetized monkeys (Macaca nemestrina). 2. Homonymous EPSPs were found in all motoneurons tested. The mean values +/- SD for maximum EPSP amplitude of triceps surae motoneurons were 2.5 +/- 1.3, 1.8 +/- 1.3 and 4.5 +/- 2.0 mV for medial gastrocnemius, lateral gastrocnemius, and soleus motoneurons, respectively. Heteronymous EPSPs were almost always smaller than their corresponding homonymous EPSPs. 3. Triceps surae EPSP amplitude was larger in motoneurons with higher input resistance. However, this relationship was weak, suggesting that factors related to input resistance play a limited role in determining the magnitude of the EPSP. 4. The mean ratio +/- SD of the amplitude of the EPSP elicited by combined stimulation of all triceps surae nerves to the amplitude of the algebraic sum of the three individual EPSPs was 0.95 +/- 0.05. This ratio was greater in motoneurons with lower rheobase. 5. Some patterns of synaptic connectivity in the macaque are consistent with previously reported differences between primates and cat (e.g., heteronymous EPSPs elicited by medial gastrocnemius nerve stimulation in soleus motoneurons are small in macaque and other primates but large in cat). However, no overall pattern emerges from a comparison of the similarities and differences in EPSPs among species in which they have been studied (i.e., macaque, baboon, and cat). That is, there are no two species in which EPSP properties are consistently similar to each other, but different from those of the third species.(ABSTRACT TRUNCATED AT 250 WORDS)


2001 ◽  
Vol 281 (4) ◽  
pp. R1283-R1289 ◽  
Author(s):  
Lu-Ning Cui ◽  
Elaine Coderre ◽  
Leo P. Renaud

We used patch-clamp recordings in slice preparations from Sprague-Dawley rats to evaluate responses of 20 spinal-projecting neurons in the dorsal paraventricular nucleus (PVN) to electrical stimulation in suprachiasmatic nucleus (SCN). Neurons containing a retrograde label transported from the thoracic (T1-T4) intermediolateral column displayed three intrinsic properties that collectively allowed distinction from neighboring parvocellular or magnocellular cells: a low-input resistance, a hyperpolarization-activated time-dependent inward rectification, and a low-threshold calcium conductance. Twelve of fifteen cells tested responded to electrical stimulation in SCN. All of 10 cells tested in media containing 2,3,-dioxo-6-nitro-1,2,3,4-tetrahydrobenzo[f]quinoxaline-7-sulfonamide disodium (5 μM) andd(−)-2-amino-5-phosphonopentanoic acid (20 μM) responded with constant latency (11.4 ± 0.7 ms) inhibitory postsynaptic potentials, able to follow 20- to 50-Hz stimulation and blockable with bicuculline (20 μM). By contrast, all eight cells tested in the presence of bicuculline demonstrated constant latency (9.8 ± 0.6 ms) excitatory postsynaptic potentials that followed at 20–50 Hz and featured both non- N-methyl-d-aspartate (NMDA) and NMDA receptor-mediated components. We conclude that both GABAergic and glutamatergic neurons in SCN project directly to spinal-projecting neurons in the dorsal PVN.


1995 ◽  
Vol 74 (6) ◽  
pp. 2782-2787 ◽  
Author(s):  
P. J. Whelan ◽  
G. W. Hiebert ◽  
K. G. Pearson

1. This study examines whether the efficacy of polysynaptic group I excitatory pathways to extensor motoneurons are modified after axotomy of a synergistic nerve. Previously, it has been shown that stimulation of extensor nerves at group I strength can extend the stance phase and delay swing. Stimulation of the lateral gastrocnemius and soleus (LG/S) nerve prolongs stance for the duration of the stimulus train, whereas stimulation of the medial gastrocnemius (MG) nerve moderately increases stance. Our hypothesis was that after axotomy of the LG/S nerve the efficacy of the MG group I input would increase. 2. This idea was tested in 10 adult cats that had their left LG/S nerves axotomized for 3-28 days. On the experimental day the cats were decerebrated and the left (experimental) and right (control) LG/S and MG nerves were stimulated during late stance as the animals were walking on a motorized treadmill. A significant increase in the efficacy of the left MG nerve occurred 5 days after axotomy of the LG/S nerve when compared with the control response. By contrast, the previously cut LG/S nerve showed a reduction in efficacy after 3 days compared with the control limb. 3. Functionally, this plasticity may be an important mechanism by which the strength of the group I pathway is calibrated to different loads on the extensor muscles.


2015 ◽  
Vol 113 (7) ◽  
pp. 2769-2777 ◽  
Author(s):  
P. Krutki ◽  
A. Hałuszka ◽  
W. Mrówczyński ◽  
P. F. Gardiner ◽  
J. Celichowski

The aim of the study was to determine whether chronic muscle overload has measurable effect on electrophysiological properties of motoneurons (MNs), and whether duration of this overload influences intensity of adaptations. The compensatory overload was induced in the rat medial gastrocnemius (MG) by bilateral tenotomy of its synergists (lateral gastrocnemius, soleus, and plantaris); as a result, only the MG was able to evoke the foot plantar flexion. To assure regular activation of the MG muscle, rats were placed in wheel-equipped cages and subjected to a low-level treadmill exercise. The intracellular recordings from MG motoneurons were made after 5 or 12 wk of the overload, and in a control group of intact rats. Some of the passive and threshold membrane properties as well as rhythmic firing properties were considerably modified in fast-type MNs, while remaining unaltered in slow-type MNs. The significant changes included a shortening of the spike duration and the spike rise time, an increase of the afterhyperpolarization amplitude, an increase of the input resistance, a decrease of the rheobase, and a decrease of the minimum current necessary to evoke steady-state firing. The data suggest higher excitability of fast-type MNs innervating the overloaded muscle, and a shift towards electrophysiological properties of slow-type MNs. All of the adaptations could be observed after 5 wk of the compensatory overload with no further changes occurring after 12 wk. This indicates that the response to an increased level of chronic activation of MNs is relatively quick and stable.


1989 ◽  
Vol 61 (2) ◽  
pp. 291-301 ◽  
Author(s):  
L. A. LaBella ◽  
J. P. Kehler ◽  
D. A. McCrea

1. Postsynaptic potentials (PSPs) were recorded in 115 triceps surae motoneurons of 10 chloralose-anesthetized adult cats (spinal cord intact), upon electrical stimulation of the caudal and lateral cutaneous sural nerve branches (CCS and LCS, respectively). 2. With twice threshold (2T) stimulation of CCS, excitatory PSPs (EPSPs) were the predominant effect in 95% of all medial gastrocnemius (MG) motoneurons tested (min. central latency 1.5 ms; mean 2.4 ms). In only a few MG cells was the EPSP followed by an inhibitory postsynaptic potential (IPSP) and in only one cell was an IPSP the sole effect. Increasing the stimulus intensity to 5T tended to enhance both the later EPSP and IPSP components, with less change in the amplitude or latency of the earliest EPSPs. 3. In lateral gastrocnemius (LG) and soleus (SOL) motoneurons, 2T CCS stimulation led to either inhibition or no potential change in the majority of cells tested: EPSPs were the predominant effect in only 15 and 30% of LG and SOL cells, respectively (min. central latency 2.5 ms; mean 3.0 ms) and rarely occurred without subsequent inhibition. Again, increasing the stimulus intensity to 5T had more of an effect on later rather than earlier PSP components. 4. A predominance of depolarization in MG motoneurons but not in SOL motoneurons is in agreement with previous findings that CCS excitation is more powerful in "fast type" triceps surae motoneurons. However, the strong predominance of hyperpolarizing effects of CCS stimulation in the present LG population is evidence that such an organization does not transcend triceps surae motor nuclei as a whole. 5. Postsynaptic effects of LCS stimulation at 2T were frequently weak or absent but increasing the stimulus intensity to 5T produced predominant inhibition in 71% of all triceps surae motoneurons studied (n = 107). Of the few cells which did receive excitation from this nerve, most were MG, a few were SOL, and none were LG. These EPSPs occurred more frequently at 5T than at lower stimulation strengths. 6. The results indicate that excitation produced by electrical stimulation of the ipsilateral CCS nerve occurs preferentially in the MG portion of triceps surae and with the shortest central latencies. Effects of LCS stimulation are largely inhibitory throughout the motor nuclei comprising triceps surae but even here, the presence of excitation occurs more frequently in MG. A comparison of these results with those in other reports is discussed.


1991 ◽  
Vol 65 (2) ◽  
pp. 168-177 ◽  
Author(s):  
A. D. Lindsay ◽  
M. D. Binder

1. Steady-state recurrent (Renshaw) inhibitory postsynaptic potentials (RIPSPs) were evoked in cat triceps surae motoneurons by stimulating the heteronymous muscle nerve at 100 Hz after dorsal root section. The effective synaptic currents (i.e., the net synaptic current measured at the soma, IN) underlying these inhibitory potentials were measured with a modified voltage-clamp technique. 2. The average value of the effective synaptic currents measured in medial gastrocnemius (MG) motoneurons was 0.4 nA. There was no significant correlation between the IN measured in individual cells and motoneuron input resistance (RN), rheobase (IR), duration of the spike afterhyperpolarization (AHPt1/2), or putative motor-unit type, although the steady-state inhibitory post-synaptic potential (IPSP) amplitudes were correlated with all of these parameters. 3. Steady-state recurrent inhibition was accompanied by a small (3.5%, on average) decrease in the resting input resistance of the motoneurons. The small magnitude of this measured change supports the hypothesis of Burke et al. that the site of synaptic contact between Renshaw cells and motoneurons is somewhat distal to the cell soma. 4. The absence of a differential distribution of the effective synaptic currents generated by Renshaw cells within the MG pool does not support the idea that recurrent inhibition mediates a selective reduction of the firing of small, low-threshold motoneurons by large, high-threshold motoneurons. The small amplitude of the effective synaptic currents we measured suggests that the contribution of recurrent inhibition to the direct modulation of motoneuron firing rate is subtle and that it is perhaps principally involved in the fine control and smooth production of muscle force.


1998 ◽  
Vol 79 (2) ◽  
pp. 848-858 ◽  
Author(s):  
E. P. Zehr ◽  
K. Fujita ◽  
R. B. Stein

Zehr, E. P., K. Fujita, and R. B. Stein. Reflexes from the superficial peroneal nerve during walking in stroke subjects. J. Neurophysiol. 79: 848–858, 1998. The function of ipsilateral cutaneous reflexes was studied with short trains of stimuli presented pseudorandomly to the superficial peroneal nerve (SP; innervates the top of the foot) during treadmill walking in neurologically intact (NI) subjects and subjects who had had a stroke. Ankle and knee joint angles together with electromyograms (EMG) of tibialis anterior (TA), soleus (SOL), medial gastrocnemius (MG), vastus lateralis (VL), and biceps femoris (BF) muscles were recorded. Net reflex EMG and kinematic responses to stimulation were quantified in each of the 16 parts of the step cycle and responses compared between the stroke and NI subjects. Stimulation strongly suppressed extensor muscles throughout stance in the stroke subjects. TA muscle showed a significant suppression during swing phase that was correlated with reduced ankle dorsiflexion in both stroke and NI subjects. BF reflexes were facilitatory during parts of swing and VL reflexes were suppressive throughout stance in the stroke subjects. There was a significant correlation between BF facilitation and knee flexion during swing, which was stronger in NI subjects. We conclude that only part of the stumble correction to foot dorsum electrical stimulation observed in NI subjects is maintained after stroke, and that new, suppressive responses are seen.


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