Long-lasting excitability changes of soleus alpha-motoneuron induced by midpontine stimulation in decerebrate, standing cat

1986 ◽  
Vol 55 (3) ◽  
pp. 449-468 ◽  
Author(s):  
T. Sakamoto ◽  
Y. Atsuta ◽  
S. Mori

Stimulation of the dorsal portion of the caudal tegmental field (DTF) in the pons resulted in hyperpolarization of extensor alpha-motoneurons (alpha-MNs) that persisted for several minutes after cessation of the stimulation. The resulting inhibition of alpha-MN discharge led to a progressive reduction in the number of active motor units. Renshaw cells, persistently active at high levels of extensor muscle tone, were abruptly silenced by DTF stimulation. Active discharge was renewed at the time of cessation of the stimulation but at a frequency reduced in proportion to the persistently lowered level of extensor muscle tone. Ia primary afferents were tonically active during the high extensor tonus of reflex standing. DTF stimulation was accompanied by a brief, slight increase in Ia discharge frequency followed by a reduction in frequency variably correlated to the magnitude of extensor force reduction. Orthodromically elicited Ia EPSPs in the soleus alpha-MNs were reduced in peak voltage, time to peak, and half width during the hyperpolarization accompanying DTF stimulation. All of these parameters recovered beyond their prestimulus values with the cessation of DTF stimulation in spite of the persisting hyperpolarization. Antidromically initiated invasion of the somatodendritic (SD) segment of the motoneuron membrane was delayed and sometimes blocked during DTF stimulation. At the same time, the peak voltage of the SD action potential was reduced. There was an immediate recovery of these changes on termination of DTF stimulation, although the poststimulus hyperpolarization persisted. Intracellular injection of depolarizing current steps during DTF stimulation revealed a depression of membrane excitability that persisted during the hyperpolarization that followed the termination of the DTF stimulation. Depolarizing and hyperpolarizing steps of intracellular current were used to demonstrate a reduction of cellular input resistance during DTF stimulation. The resistance values rapidly returned to prestimulus levels following the cessation of DTF stimulation. It was demonstrated that the degree of resistance change is greater and that the magnitude of DTF-induced hyperpolarization is smaller for low-resistance cells than for high-resistance cells. Iontophoretically induced increase in intracellular Cl- resulted in a reversal of both Ia IPSPs and the hyperpolarization induced by DTF stimulation. The hyperpolarization enduring after DTF stimulation was not affected by the Cl- injection.

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)


1997 ◽  
Vol 77 (5) ◽  
pp. 2605-2615 ◽  
Author(s):  
John B. Munson ◽  
Robert C. Foehring ◽  
Lorne M. Mendell ◽  
Tessa Gordon

Munson, John B., Robert C. Foehring, Lorne M. Mendell, and Tessa Gordon. Fast-to-slow conversion following chronic low-frequency activation of medial gastrocnemius muscle in cats. II. Motoneuron properties. J. Neurophysiol. 77: 2605–2615, 1997. Chronic stimulation (for 2–3 mo) of the medial gastrocnemius (MG) muscle nerve by indwelling electrodes renders the normally heterogeneous MG muscle mechanically and histochemically slow (type SO). We tested the hypothesis that motoneurons of MG muscle thus made type SO by chronic stimulation would also convert to slow phenotype. Properties of all single muscle units became homogeneously type SO (slowly contracting, nonfatiguing, nonsagging contraction during tetanic activation). Motoneuron electrical properties were also modified in the direction of type S, fatigue-resistant motor units. Two separate populations were identified (on the basis of afterhyperpolarization, rheobase, and input resistance) that likely correspond to motoneurons that had been fast (type F) or type S before stimulation. Type F motoneurons, although modified by chronic stimulation, were not converted to the type S phenotype, despite apparent complete conversion of their muscle units to the slow oxidative type (type SO). Muscle units of the former type F motor units were faster and/or more powerful than those of the former type S motor units, indicating some intrinsic regulation of motor unit properties. Experiments in which chronic stimulation was applied to the MG nerve cross-regenerated into skin yielded changes in motoneuron properties similar to those above, suggesting that muscle was not essential for the effects observed. Modulation of group Ia excitatory postsynaptic potential (EPSP) amplitude during high-frequency trains, which in normal MG motoneurons can be either positive or negative, was negative in 48 of 49 chronically stimulated motoneurons. Negative modulation is characteristic of EPSPs in motoneurons of most fatigue-resistant motor units. The general hypothesis of a periphery-to-motoneuron retrograde mechanism was supported, although the degree of control exerted by the periphery may vary: natural type SO muscle appears especially competent to modify motoneuron properties. We speculate that activity-dependent regulation of the neurotrophin-(NT) 4/5 in muscle plays an important role in controlling muscle and motoneuron properties.


1979 ◽  
Vol 79 (1) ◽  
pp. 169-190 ◽  
Author(s):  
MICHAEL O'SHEA ◽  
PETER D. EVANS

1. Spikes in the octopaminergic dorsal unpaired median (DUM) neurone which innervates the extensor tibiae muscle of the locust metathoracic leg (DUMETi) produce direct and indirect effects on muscle tension. 2. Direct effects include a slowing of an intrinsic rhythm of contraction and relaxation, a relaxation of muscle tone and a small hyperpolarization of the muscle membrane potential. The latter two effects are weak and variable. All three effects are mimicked by superfusion of octopamine and are mediated by octopamine receptors on the muscle fibres. 3. Indirect effects are found when the DUMETi neurone is stimulated at the same time as the motoneurones innervating the extensor muscle. They include (a) potentiation of tension generated in the extensor muscle by spikes in the slow excitatory motoneurone (SETi), (b) reduction in duration of each twitch contraction generated by SETi due to an increase in the rate at which the muscle relaxes, (c) increase in the amplitude of the synaptic potential generated by SETi. These various effects have a time course of several minutes and far outlast the duration of DUMETi stimulation. They can be mimicked by superfusion of octopamine. 4. The effect of DUMETi on neuromuscular transmission is mediated by receptors with a high affinity for octopamine located both on the muscle and on the terminals of the slow motoneurone. The presence of the presynaptic receptors is revealed by the increase in the frequency of spontaneous miniature end plate potentials recorded in the muscle in the presence of octopamine. 5. DUMETi is a member of a group of similar aminergic neurones and it is suggested that they may share a role in modulating transmission at peripheral neuromuscular synapses, and possibly central synapses.


1997 ◽  
Vol 77 (1) ◽  
pp. 236-246 ◽  
Author(s):  
Xiang Q. Gu ◽  
Sulayman Dib-Hajj ◽  
Marco A. Rizzo ◽  
Stephen G. Waxman

Gu, Xiang Q., Sulayman Dib-Hajj, Marco A. Rizzo, and Stephen G. Waxman. TTX-sensitive and -resistant Na+ currents, and mRNA for the TTX-resistant rH1 channel, are expressed in B104 neuroblastoma cells. J. Neurophysiol. 77: 236–246, 1997. To examine the molecular basis for membrane excitability in a neuroblastoma cell line, we used whole cell patch-clamp methods and reverse transcription-polymerase chain reaction (RT-PCR) to study Na+ currents and channels in B104 cells. We distinguished Tetrodotoxin (TTX)-sensitive and -resistant Na+ currents and detected the mRNA for the cardiac rH1 channel in B104 cells. Na+ currents could be recorded in 65% of cells. In the absence of TTX, mean peak Na+ current density was 126 ± 19 pA/pF, corresponding to a channel density of 2.7 ± 0.4/μ2 (mean ± SE). Time-to-peak (t-peak), activation (τm), and inactivation time constants (τh) for Na+ currents in B104 cells were 1.0 ± 0.04, 0.4 ± 0.06, and0.9 ± 0.04 ms at −10 mV. The peak conductance-voltage relationship had a V 1/2 of −39.8 ± 1.5 mV. V 1/2 for steady-state inactivation was −81.6 ± 1.5 mV. TTX-sensitive and -resistant components of the Na current had half-maximal inhibitions (IC50), respectively, of 1.2 nM and, minimally, 575.5 nM. The TTX-sensitive and-resistant Na+ currents were kinetically distinct; time-to-peak, τm, and τh for TTX-sensitive currents were shorter than for TTX-resistant currents. Steady-state voltage dependence of the two currents was indistinguishable. The presence of TTX-sensitive and-resistant Na+ currents, which are pharmacologically and kinetically distinct, led us to search for mRNAs known to be associated with TTX-resistant channels, in addition to the α subunit mRNAs, which have previously been shown to be expressed in these cells. Using RT-PCR and restriction enzyme mapping, we were unable to detect αSNS, but detected mRNA for rH1, which is known to encode a TTX-resistant channel, in B104 cells. B104 neuroblastoma cells thus express TTX-sensitive and -resistant Na+ currents. These appear to be encoded by neuronal-type and cardiac Na+ channel mRNAs including the RH1 transcript. This cell line may be useful for studies on the rH1 channel, which is known to be mutated in the long-QT syndrome.


1990 ◽  
Vol 258 (1) ◽  
pp. C62-C70 ◽  
Author(s):  
G. Desypris ◽  
D. J. Parry

Contractile and histochemical properties of reinnervated motor units in soleus muscles of C57BL/6J mice were examined 1 mo after sectioning the soleus nerve. Fifty-one motor units were isolated by the technique of ventral root splitting. Their sizes ranged from 0.4 to 13.6% of whole muscle tetanic tension (Po) with a mean size of 5.3% Po corresponding to 19 motor units. In control unoperated mice, the range was 2.2-8.6% Po, with a mean size of 4.8% Po corresponding to 22 motor units. Although no clear relationship between unit time to peak tension and size was seen in control units, it appeared that in the reinnervated muscle the large units were also slow contracting, whereas the smaller units were predominantly fast contracting. Adenosinetriphosphatase (ATPase) staining revealed an increase in the proportion of muscle area occupied by type I fibers in reinnervated soleus compared with control soleus. Immunohistochemical staining of reinnervated soleus with monoclonal antibodies against type I and IIa myosin showed the presence of hybrid fibers containing both myosins. It is concluded that during reinnervation most motoneurons reinnervate the soleus muscle of the mouse. The hypothesis that slow motoneurons are more adept at expanding their innervating field than fast motoneurons is also supported by the data.


1989 ◽  
Vol 67 (5) ◽  
pp. 1835-1842 ◽  
Author(s):  
C. K. Thomas ◽  
J. J. Woods ◽  
B. Bigland-Ritchie

With fatigue, force generation may be limited by several factors, including impaired impulse transmission and/or reduced motor drive. In 5-min isometric maximal voluntary contraction, no decline was seen in the peak amplitude of the tibialis anterior compound muscle mass action potential (M wave) either during or immediately after the voluntary effort, provided maximal nerve stimulation was retained. For first dorsal interosseous (FDI) muscle, M wave amplitudes declined by 19.4 +/- 1.6% during the first 2 min but did not change significantly thereafter, despite the continued force reduction (up to 94% in 5 min for both muscles). The duration of the FDI M waves increased (greater than 30%), suggesting that the small decline in amplitude was the result of increased dispersion between the responses of different motor units. Some subjects kept FDI maximally activated throughout, but when they used tibialis anterior, twitch occlusion and tetanic muscle stimulation showed that most subjects were usually only able to do so for the first 60 s and thereafter only during brief “extra efforts.” Thus force loss during isometric voluntary contractions sustained at the highest intensities results mainly from failure of processes within the muscle fibers.


1986 ◽  
Vol 55 (5) ◽  
pp. 947-965 ◽  
Author(s):  
R. C. Foehring ◽  
G. W. Sypert ◽  
J. B. Munson

This study tested the hypothesis that functional connection to muscle is necessary for expression of normal motoneuron electrical properties. Also examined was the time course of self-reinnervation. Properties of individual medial gastrocnemius (MG) motor units were examined following section and reanastomosis of the MG nerve. Stages examined were 3-5 wk (prior to reinnervation, no-re), 5-6 wk (low-re), 9-10 wk (med-re), and 9 mo (long-re, preceding paper) after nerve section. Motor units were classified on the basis of their mechanical response as type fast twitch, fast fatiguing (FF), fast twitch with intermediate fatigue resistance (FI), fast twitch, fatigue resistant (FR), or slow twitch, fatigue resistant (S) (11, 24). Motoneuron electrical properties were measured. Muscle fibers were classified using histochemical methods as type fast glycolytic (FG), fast oxidative glycolytic (FOG), or slow oxidative (SO) (60). Prior to functional reinnervation, MG motoneurons exhibited increased input resistance, decreased rheobase, decreased rheobase/input resistance, and decreased axonal conduction velocity. There was no change in mean afterhyperpolarization (AHP) half-decay time. Normal relationships between motoneuron electrical properties were lost. These data are consistent with dedifferentiation of motoneuron properties following axotomy (35, 47). At 5-6 wk after reanastomosis, motor-unit tensions were small, and motoneuron membrane electrical properties were unchanged from the no-re stage. There were no differences in motoneuron electrical properties between cells that elicited muscle contraction and those that did not. Motor-unit types were first recognizable at the med-re stage. The proportions of fast and slow motor units were similar to normal MG. Within the fast units, there were fewer type-FF units and more type-FI and type-FR units than normal, reflecting a general increase in fatigue resistance at this stage. Neither motoneuron membrane electrical properties nor muscle contractile properties had reached normal values, although both were changed in that direction from the low-re stage. Normal relationships between muscle properties, between motoneuron properties, and between motoneuron and muscle properties were re-established. The correspondence between motor-unit type and motoneuron type was similar to normal or 9 mo reinnervated MG. Muscle-unit tetanic tensions became larger with time after reinnervation. Most of the increase in muscle tension beyond the med-re stage could be accounted for by increase in muscle fiber area. There was an increased proportion of SO muscle fibers observed in the med-re muscles, as at the long-re stage.(ABSTRACT TRUNCATED AT 400 WORDS)


1978 ◽  
Vol 234 (3) ◽  
pp. C90-C95 ◽  
Author(s):  
J. Grossie

Basic mechanical and electrical properties of rat extensor muscle were analyzed 4--6 wk after thyroid removal. Isometric twitch tensions in thyroidectomized (Tx) rat muscle varied considerably, with over 60% of the muscles showing abnormally low values and the remainder showing a high twitch force. The duration of the twitch was significantly increased from 137 to 245 ms but contraction and half-relaxation times were not significantly changed. Tetanic force was not effected by thyroidectomy. Electrical properties of the muscle fiber membranes were made exclusively via intracellular techniques. The resting membrane potential was slightly higher in thyroidectomized rats (-79 mV) as compared to sham controls (-78 mV). Both direct and indirect action potentials showed higher overshoots, amplitudes, and rates of depolarization in thyroidectomized rats. The threshold of the indirect action potential appeared at a higher transmembrane potential as compared to sham-operated controls. The input resistance, space constant, time constant, and specific membrane resistance were all significantly increased in thyroidectomized rat extensor muscle, whereas fiber diameter and capacitance were significantly decreased. Estimates of specific ionic conductance show that both potassium and chloride conductance are decreased in thyroidectomized rat muscle.


2016 ◽  
Vol 116 (3) ◽  
pp. 1208-1217 ◽  
Author(s):  
Zhen Yang ◽  
Fidel Santamaria

Coding in cerebellar Purkinje cells not only depends on synaptic plasticity but also on their intrinsic membrane excitability. We performed whole cell patch-clamp recordings of Purkinje cells in sagittal cerebellar slices in mice. We found that inducing long-term depression (LTD) in the parallel fiber to Purkinje cell synapses results in an increase in the gain of the firing rate response. This increase in excitability is accompanied by an increase in the input resistance and a decrease in the amplitude of the hyperpolarization-activated cyclic nucleotide-gated (HCN) channel-mediated voltage sag. Application of a HCN channel blocker prevents the increase in input resistance and excitability without blocking the expression of synaptic LTD. We conclude that the induction of parallel fiber-Purkinje cell LTD is accompanied by an increase in excitability of Purkinje cells through downregulation of the HCN-mediated h current. We suggest that HCN downregulation is linked to the biochemical pathway that sustains synaptic LTD. Given the diversity of information carried by the parallel fiber system, we suggest that changes in intrinsic excitability enhance the coding capacity of the Purkinje cell to specific input sources.


Sign in / Sign up

Export Citation Format

Share Document