Douglas G. Stuart

Ensemble characterivstics ofcat locovmotionand its neural control

2.2.1. Schematics of gait: contact patterns 2.2.2. Contact patterns in walking, trotting, and galloping by the cat 2.2.3. Non-contact patterns of interlimb coordination 2.3. Gait conversion 2.3.1. Individuation of movements within gaits 2.3.2. Movement transitions with changes in speed and across gaits 2.3.3. Changes in mechanical events as a function of forward speed 2.4. Situational contributions to stepping 2.5. Synthesis of stepping pattern information: mathematical models 2.51. Historical development of models 2.5.2. The nature of energy and stability requirements 2.5.3. Stability and the analysis of gaits 2.5.4. Control theory and applications relevant to the nervous system 2.6. Summary 4 5 5 6 6 12 12 12 13 15 15 16 17 18 19 19 21 21 23 24

THE RESPONSE OF GOLGI TENDON ORGANS TO SINGLE MOTOR UNIT CONTRACTIONS

1. Cross‐correlation analysis has been used to quantify the responses of cat soleus tendon organs to repetitive twitch contractions of: (a) different motor units within the muscle, (b) single motor units at different muscle lengths, and (c) single motor units when the pulse‐train pattern of stimulation delivered to the motor unit axon was altered. 2. Ib afferents were observed which responded to each of several hundred successive motor unit twitches with identical numbers of spikes and with relatively invariant latencies. 3. The present results show that tendon organs are sensitive to subtle alterations in motor unit twitch wave form and amplitude, and that this sensitivity is reflected in the precise timings of their afferent discharge. 4. Examination of these tendon organ responses indicates that the forces produced by single motor units couples to the receptor capsule are well above threshold. Calculations based on these results, and earlier soleus motor unit and muscle fibre data, suggest that the absolute force threshold for tendon organs may be as little as 4 mg, which is less than the estimated minimum twitch force generated by individual soleus muscle fibres. 5. Considering the number of tendon organs in a muscle, and the likelihood that every motor unit is connected with at least one receptor, the sensitivity of tendon organs ensures that every twitch of every motor unit will be reflected in the population of afferent signals projecting to the spinal cord.

Correlation analysis of muscle spindle responses to single motor unit contractions.

1. Cross‐correlation techniques have been used to study the responses of muscle spindle afferents from the soleus muscle of the cat to twitch contractions of single motor units. 2. Cross‐correlograms (post‐stimulus time histograms) were used to give the frequency of occurrence of a receptor spike at various times following the initiation of a motor unit contraction together with a display of the average twitch tension wave form. 3. The cross‐correlograms revealed that the contraction of a single motor unit can be an effective stimulus to a spindle receptor and may induce afferent firing pattern alterations similar to those observed with whole muscle contraction. 4. The cross‐correlograms also revealed quantitative differences in the response of a receptor to contraction of different motor units and to contraction of the same motor unit at different lengths. These differences reflect subtle changes in receptor deformation developed by the twitch of a motor unit under different conditions and by the twitches of different motor units. The results are consistent with anatomical data on the number and distribution of motor units and receptor organs in cat soleus. 5. These findings emphasize that rather than simply acting as generalized force or length sensors for the muscle as a whole, each receptors spike train carries information about the state of a particular set of motor units.

Henneman's ‘size principle’: current issues

Despite initial formulation over a quarter of a century ago, Hennemans ‘size principle’ remains a provocative concept. Evaluation of the size principle has focused on testing the possibility that motoneuron size is the basis for orderly motor-unit recruitment during the graded development of muscle force. Although the results have been largely inconclusive, these efforts have been central to our understanding of motor-control mechanisms. This article provides an assessment of the relevance of the ‘size principle’ to our current understanding of motor control.

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)

Time Constraints for Inter-Limb Co-Ordination in the Cat During Unrestrained Locomotion

Unrestrained walking, trotting and galloping by adult cats is analyzed cinematographically. Classical models, which have previously characterized quadrupedal gait by “idealized” footfall formulas and support durations, can be revised from the present data to specifically describe cat locomotion. The number of limbs supporting the body weight and the sequence in which they are placed on the ground are largely a function of forward speed. Even within one gait and at a given speed, however, the same cat can be observed to vary its support pattern markedly in different strides, such as a transition in mid-flight from a rotatory to a transverse gallop. On the basis of these findings we then propose that, since locomotion can thrive under a variety of conditions both across and within gaits, the locomotor control program has facultative capability.

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.