Robert M. Reinking

Localization of monosynaptic Ia excitatory post‐synaptic potentials in the motor nucleus of the cat biceps femoris muscle.

Evidence is presented for the existence of a localization of monosynaptic Ia excitatory post‐synaptic potentials (e.p.s.p.s) in the motor nucleus of a cat hind limb muscle. Intracellular recordings from biceps femoris motoneurones were made in anaesthetized low spinal cats of the effects of stimuli to the nerve branches supplying the anterior, middle, and posterior portions of the biceps femoris muscle. Recordings were also made during stimulation of nerves to semimembranosus and semitendinosus in order to provide a means of categorizing middle biceps cells as ‘extensors’ (middle biceps‐extensor; i.e. like anterior biceps cells) or as ‘flexors’ (middle biceps‐flexor; like posterior biceps). Homonymous nerve‐branch (i.e. from anterior, middle or posterior biceps) monosynaptic Ia e.p.s.p.s were compared within unifunctional (flexor or extensor) groups of motoneurones. In three of four comparisons (anterior biceps nerve branch onto anterior and middle biceps‐extensor cells, middle biceps onto middle biceps‐flexor and posterior biceps, posterior biceps onto middle biceps‐flexor and posterior biceps) the anterior, middle and posterior biceps nerve branches contributed larger e.p.s.p.s to their ‘own’ motoneurones than to motoneurones supplying other ‘compartments’ of the muscle. In the fourth case, middle bicepss input appeared to have similar effects onto anterior biceps and middle biceps‐extensor cells. A normalization was performed to eliminate the possibility that the differences in e.p.s.p. sizes were due to differences in cell type within the four cell groupings (i.e. differences in the number of cells supplying FF, F(int.), FR and S muscle units). This normalization confirmed that the localization in the first three comparisons was not a consequence of differences in motoneurone type and, in addition, suggested that middle biceps may indeed have greater effects on middle biceps‐extensor than anterior biceps cells. In addition to the asymmetrical effects of anterior and middle biceps nerve branches onto anterior biceps and middle biceps‐extensor motoneurones, it was shown that while semitendinosus and posterior biceps contributed larger e.p.s.p.s to middle biceps‐flexor than to middle biceps‐extensor cells, the anterior biceps nerve branch and semimembranosus nerve contributed equally to the two middle biceps groups. Analysis of cell location in the spinal cord and rostro‐caudal differences in group I volley sizes gave evidence of a topographic organization of the biceps femoris motor nucleus which could contribute to the observed localization. However, localization was also evident when comparing e.p.s.p. amplitudes in pairs of neighbouring cells of different category, indicating a role for neuronal recognition factors.

Distribution of monosynaptic Ia excitatory post‐synaptic potentials in the motor nucleus of the cat semitendinosus muscle.

Evidence is presented for a lack of localization of monosynaptic Ia excitatory post‐synaptic potentials (e.p.s.p.s) in the motor nucleus supplying the atypical cat hind limb muscle semitendinosus, which has anatomically distinct in‐series compartments. Recordings were made from dorsal root filaments containing functionally isolated Ia, spindle group II and Ib axons from the proximal and distal compartments of semitendinosus. Twitch of either of these in‐series compartments resulted in accelerated discharge of Ia and spindle group II fibres in the other compartment. Ib fibres of either compartment showed an in‐series response to twitch of a single compartment which was weaker than twitch of the whole muscle, a finding which was consistent with the diminished force produced by twitch of either compartment alone. In addition, intracellular recordings were made from semitendinosus motoneurones in anaesthetized low‐spinal cats during electrical stimulation of the nerve branches to proximal semitendinosus and distal semitendinosus. Comparison of proximal semitendinosus and distal semitendinosus motoneurones failed to reveal any difference between the two cell groups with respect to the average Ia e.p.s.p. amplitude produced by either the proximal or distal semitendinosus nerve branch. However, e.p.s.p.s due to stimulation of distal semitendinosus were approximately 65% larger, on average, than those due to stimulation of proximal semitendinosus in either motoneurone group. Analysis of cell location along the rostro‐caudal axis of the spinal cord indicated that the proximal and distal semitendinosus cell groups are largely co‐extensive. Recordings of volleys in the proximal and distal semitendinosus nerve branches in response to stimulation of the L6, L7 and S1 dorsal roots showed that group I afferents from the proximal semitendinosus compartment tend to have a more rostral entry point to the spinal cord than do distal semitendinosus afferents. E.p.s.p. amplitude in either cell group due to stimulation of either nerve branch showed little dependence on cell location in the spinal cord. The results are discussed with respect to the relation between muscle function and the distribution of monosynaptic Ia connexions.

Adaptation of cat motoneurons to sustained and intermittent extracellular activation.

1. The main purpose of this study was to quantify the adaptation of spinal motoneurons to sustained and intermittent activation, using an extracellular route of stimulating current application to single test cells, in contrast to an intracellular route, as has been used previously. In addition, associations were tested between firing rate properties of the tested cells and other type (size)‐related properties of these cells and their motor units. 2. Motoneurons supplying the medial gastrocnemius muscle of the deeply anaesthetized cat were stimulated for 240 s with microelectrodes which passed sustained extracellular current at 1.25 times the threshold for repetitive firing. Many cells were also tested following a rest period with intermittent 1 s current pulses (duration 600 ms) at the same relative stimulus strength. Cell discharge was assessed from the EMG of the motor unit innervated by the test neuron. The motoneurons and their motor units were assigned to four categories (i.e. types FF, FR, S and F; where F = FF + FR) based on conventional criteria. In all, twenty F (16 FF, 4 FR) and fourteen S cells were studied with sustained stimulation. Thirty of these cells (17 F, 13 S) and an additional two cells (1 F, 1 S) were studied with intermittent stimulation. 3. The mean threshold current required for sustained firing for a period of > or = 2 s was not significantly different for F and S cells. However, most of the other measured parameters of motoneuron firing differed significantly for these two cell groups. For example, at 1.25 times the threshold current for repetitive firing, the mean firing duration in response to 240 s of sustained activation was 123 +/‐ 88 s (+/‐ S.D.) for F cells vs. 233 +/‐ 19 s for S cells. These values were significantly longer than those from a comparable, previously reported study that employed intracellular stimulation. With intermittent stimulation, the firing durations of F and S cells were not significantly different from each other. 4. All cells exhibited a delay from the onset of current to the first spike, followed by a brief accelerating discharge that was followed by a slower drop in firing rate. Some cells (21 of 34 with sustained activation; 20 of 32 with intermittent) exhibited doublet discharges (interspike intervals < or = 10 ms) that were intermingled with the more predominant singlet discharges. Doublets were more common in the S cell type.(ABSTRACT TRUNCATED AT 400 WORDS)

The effect of the stimulation pattern on the fatigue of single motor units in adult cats.

1. The main purpose of this study was to examine the effects of two subtly different stimulus patterns on the force developed by fast‐twitch, fatiguable motor units in a cat hindlimb muscle during control (pre‐fatigue) and fatiguing contractions. 2. The peak force and the force‐time integral responses of nineteen high fatigue (FF) and three intermediate fatigue (FI) motor units of the tibialis posterior muscle in five deeply anaesthetized adult cats were measured at selected times during the course of a 360‐s fatigue test. 3. The fatigue test involved a pseudo‐random alternation of two patterns of stimulation. One pattern (regular) was composed of a train of stimuli with constant interpulse intervals, set at 1.8 x the twitch contraction time of each unit (interval range, 27‐51 ms), and delivered for 500 (or 400) ms. For the total (FF + FI) motor‐unit sample, the mean (+/‐ S.D.) stimulation frequency was 26 +/‐ 4 Hz (range, 19‐37 Hz). The other stimulus pattern (optimized) consisted of three initial stimuli with short (10 ms) interpulse intervals, followed by a constant interpulse‐interval train that was adjusted (interval range, 29‐62 ms; frequency, 23 +/‐ 5 Hz; frequency range, 16‐36 Hz) such that the total train had the same number of pulses, and the same average frequency and duration as the regular train. 4. The stimulus trains were delivered at 1 s‐1 for 360 s, using three‐train sequences of each pattern, randomly alternating with one another. The response of the third train in each sequence was selected for the force measurements. The force profile obtained from the fatigue test was subsequently decomposed into two profiles: one attributable to regular and one to optimized stimulation. 5. During the initial responses to the fatigue test, the optimized stimulus pattern produced significantly more force than the regular stimulus pattern. For FF units, the mean increase in peak force (141%) was significantly greater than the increase in the force‐time integral (59%). 6. All motor units exhibited an initial potentiation of peak force with the regular stimulation pattern, whereas peak force declined monotonically with the optimized pattern. In contrast, the force‐time integral potentiated in the first 30 s for both regular and optimized stimulus patterns. 7. Each motor unit maintained an increased force response to optimized stimulation during the fatigue test, with the greatest relative increase occurring about 120 s into the test, well after the potentiation effect had subsided.(ABSTRACT TRUNCATED AT 400 WORDS)

The motor units of cat medial gastrocnemius: Problem of their categorisation on the basis of mechanical properties

SummaryThe mechanical properties of 126 motor units from medial gastrocnemius muscle have been studied in 12 adult cats.Units with long contraction times (>45 msec) were non fatigable (24 out of 26 units) and small (25 out of 26 units with <0.3% of the parent whole muscle tetanic tension) thus forming a very homogeneous population. In contrast, fast twitch units (contraction time <45 msec) exhibited a very broad range of tetanic tensions and fatigability. Significant correlations were found, however, within the fast contracting population which indicate a tendency for the more fatigable units to develop more tetanic tension and to be faster contracting.These findings are discussed in relation to the problems associated with using the interrelationships between twitch contraction time, tetanic tension and fatigue resistance to classify motor units into subpopulations sharing similar mechanical properties.

Mechanical arrangement and transducing properties of Golgi tendon organs

Summary1.The mechanical arrangement and transducing properties of Golgi tendon organs in soleus and anterior tibial muscles of anesthetized cats have been studied by noting responses of their Ib afferents to muscle stretch (passive force) and contraction (active force) of small portions of the muscle including functionally isolated motor units.2.Tendon organs were shown to be arranged both in-series and in-parallel with adjacent muscle fibers. There were gradations in these relations, the tightest arrangements involving the response to contraction of a single motor unit, brisk discharge from an in-series receptor and pause in the stretch-activated firing of an in-parallel receptor. Other arrangements included those in which groups of muscle fibers neither directly in-series nor in-parallel with a receptor were still found capable of influencing its firing pattern. If in-series muscle fibers maintained their contraction while in-parallel fibers were also contracting, the receptor usually responded slightly less actively than it did to the in-series force alone.3.Tendon organs were found to have a very low threshold to in-series force developed by muscle contraction. Responses were observed to as little as 0.5 gm of twitch tension. Minimum active force thresholds were similar for the two muscles studied, but thresholds to dynamic stretch were lower for anterior tibial receptors. Division of the dynamic stretch threshold by the minimum active force threshold gave a measure of the extent to which each tendon organ was more sensitive to active than passive force. These values (generally less than 50) did not negate the physiological significance of responses to passive stretch.4.The present data, together with those of Houk and his co-workers (1967, 1971) emphasize that tendon organs can participate in the moment to moment reflex control of normal muscle activity.

Motoneurons: A preferred firing range across vertebrate species?

The term “preferred firing range” describes a pattern of human motor unit (MU) unitary discharge during a voluntary contraction in which the profile of the spike‐frequency of the MUs compound action potential is dissociated from the profile of the presumed depolarizing pressure exerted on the units spinal motoneuron (MN). Such a dissociation has recently been attributed by inference to the presence of a plateau potential (PP) in the active MN. This inference is supported by the qualitative similarities between the firing pattern of human MUs during selected types of relatively brief muscle contraction and that of intracellularly stimulated, PP‐generating cat MNs in a decerebrate preparation, and turtle MNs in an in vitro slice of spinal cord. There are also similarities between the stimulus‐response behavior of intracellularly stimulated turtle MNs and human MUs during the elaboration of a slowly rising voluntary contraction. This review emphasizes that there are a variety of open issues concerning the PP. Nonetheless, a rapidly growing body of comparative vertebrate evidence supports the idea that the PP and other forms of non‐linear MN behavior play a major role in the regulation of muscle force, from the lamprey to the human.

Motor unit - muscle spindle interactions in active muscles of decerebrate cats

Single muscle spindle afferent and motor unit EMG spike trains have been recorded simultaneously during periods of spontaneous motor activity in triceps surae muscles of decerebrate cats. The approximate time course and magnitude of the motor unit contractions were extracted from the whole muscle force record by spike-triggered averaging, and the functional interactions between motor unit contractions and spindle discharge were assessed by cross-correlating their respective spike trains. We have found that both spindle group Ia and II afferents are responsive to the contractions of single motor units in the presence of spontaneous motor activity, being strongly coupled to the activity of some motor units and indifferent to the contractions of others. Moreover, the cross-correlation analysis revealed modulation of a single motor units discharge pattern by the input of a single Ia afferent.

Selective activation of Ia afferents by transient muscle stretch

Summary1.This report extends the work of Lundberg and Winsbury (1960a and 1960b) in emphasizing the usefulness of brief muscle stretch for selective activation of the primary endings of muscle spindles.2.In 36 experiments on anesthetized cats a distribution of rhomboid stretch (20 msec duration) thresholds was obtained for activation of 393 stretch receptors from de-efferented soleus muscles maintained at comparable degrees of initial tension by setting length to give a peak of active tension during an isometric twitch. These receptors included 153 Ia afferents with conduction velocities greater than 75 m/sec, 127 Ib afferents and 97 group II afferents with conduction velocities below 65 m/sec. A pull of 60 μ or less activated 95% of the Ia fibers in contrast to 41% of the group II fibers and only 3% of the Ib fibers. At threshold the mean latency (normalized) between the onset of stretch and impulse arrival at the spinal cord (recording electrodes) was 5.4 msec for the Ia fibers (S.D.±1.7 msec), 10.6 (± 3.9) msec for the group II fibers, and 9.1 (± 3.3) msec for the Ib afferents. In all cases only one impulse was initiated by the test stretch and no significant differences were encountered in the responses of receptors located in proximal, middle and distal portions of the muscle.3.In 7 experiments soleus nerve volleys were recorded at nerve-muscle and spinal cord-dorsal root levels during similar stretching procedures. A stretch of 5 μ amplitude was sufficient to generate a group I volley. As stretch amplitude was raised to 60 μ this volley grew progressively in size and decreased in duration as well as in latency from stretch onset to volley formation. A second volley, 1.5 to 2.0 msec after the first, developed with a 30 μ stretch. At 60 μ stretch its size was approximately 30–50% that of the first volley. Conduction velocity for the first volley was 90–110 m/sec and was faster than the second volley by 5–10 m/sec. Our data on isolated afferents suggest that the first volley is of Ia origin while the second volley represents predominantly a second discharge from some Ia afferents plus a minor group II input. Significant Ib contribution is excluded since only 4 of the 127 Ib fibers responded within this stretch range and then at latencies beyond formation of either volley.

Stretch responsiveness of Golgi tendon organs

Summary1.This report describes experiments on Ib afferents from tendon organs of the de-efferented soleus in acutely prepared cats in which: a) contrast was made of responses to passive forces generated by a dynamic stretch and to active forces generated by stimulating either the muscle nerve or small ventral root filaments; and, b) responses to static and dynamic stretch were related to physiological extents and rates of movement.2.No significant differences were observed in tensions associated with threshold responses to active and passive inputs if rates of tension development were relatively similar and if the active force was generated by stimulation of the muscle nerve. Stimulation of small ventral rootlets revealed however that many motor units are “in parallel” and many “in series” with certain receptors. Thresholds of these receptors were much lower to active forces generated by “in series” motor units than to forces developed more randomly by graded stimulation of the muscle nerve. An absolute active force threshold was not gauged since it was estimated that at least some tendon organs can be driven by independent twitch contraction of 30–50 motor units.3.Threshold responses to static stretch indicated that gradual flexion of the ankle joint (as for example on slow assumption of a crouched posture) would involve progressive recruitment of soleus Ib discharge with over 2/3rds of the units firing by the extreme of dorsi-flexion. Responses to dynamic stretch suggested that an even greater percentage of soleus tendon organs would be fired during ankle flexions associated with walking. During galloping the triceps surae undergoes an eccentric (lengthening) contraction at one phase of the step cycle and soleus Ib input to the spinal cord would then become even more pronounced.4.In recent years the role of Golgi tendon organs in the reflex regulation of muscle has been reassessed with an emphasis on their ability to transmit continuously to the spinal cord information concerning the active force developed by muscle contraction and a de-emphasis of the significance of responses to muscle stretch. The present results emphasize however that soleus tendon organs are sufficiently sensitive to passive forces that muscle stretch can influence Ib input to the spinal cord in normal postural and locomotor activity. There is discussion of the functional significance of this finding and its relation to the central organization of Ib reflexes.