Cat hindlimb motoneurons during locomotion. II. Normal activity patterns

Activity patterns were recorded from 51 motoneurons in the fifth lumbar ventral root of cats walking on a motorized treadmill at a range of speeds between 0.1 and 1.3 m/s. The muscle of destination of recorded motoneurons was identified by spike-triggered averaging of EMG recordings from each of the anterior thigh muscles. Forty-three motoneurons projected to one of the quadriceps (vastus medialis, vastus lateralis, vastus intermedius, or rectus femoris) or sartorius (anterior or medial) muscles of the anterior thigh. Anterior thigh motoneurons always discharged a single burst of action potentials per step cycle, even in multifunctional muscles (e.g., sartorius anterior) that exhibited more than one burst of EMG activity per step cycle. The instantaneous firing rates of most motoneurons were lowest upon recruitment and increased progressively during a burst, as long as the EMG was still increasing. Firing rates peaked midway through each burst and tended to decline toward the end of the burst. The initial, mean, and peak firing rates of single motoneurons typically increased for faster walking speeds. At any given walking speed, early recruited motoneurons typically reached higher firing rates than late recruited motoneurons. In contrast to decerebrated cats, initial doublets at the beginning of bursts were seen only rarely. In the 4/51 motoneurons that showed initial doublets, both the instantaneous frequency of the doublet and the probability of starting a burst with a doublet decreased for faster walking speeds. The modulations in firing rate of every motoneuron were found to be closely correlated to the smoothed electromyogram of its target muscle. For 32 identified motoneurons, the unit's instantaneous frequencygram was scaled linearly by computer to the rectified smoothed EMG recorded from each of the anterior thigh muscles. The covariance between unitary frequencygram and muscle EMG was computed for each muscle. Typically, the EMG profile of the target muscle accounted for 0.88-0.96 of the variance in unitary firing rate. The EMG profiles of the other anterior thigh muscles, when tested in the same way, usually accounted only for a significantly smaller fraction of the variance. Brief amplitude fluctuations observed in the EMG envelopes were usually also reflected in the individual motoneuron frequencygrams. To further demonstrate the relationship between unitary frequencygrams and EMG, EMG envelopes recorded during walking were used as templates to generate depolarizing currents that were applied intracellularly to lumbar motoneurons in an acute spinal preparation.(ABSTRACT TRUNCATED AT 400 WORDS)     

Cat hindlimb motoneurons during locomotion. III. Functional segregation in sartorius

Cat sartorius has two distinct anatomical portions, anterior (SA-a) and medial (SA-m). SA-a acts to extend the knee and also to flex the hip. SA-m acts to flex both the knee and the hip. The objective of this study was to investigate how a "single motoneuron pool" is used to control at least three separate functions mediated by the two anatomical portions of one muscle. Discharge patterns of single motoneurons projecting to the sartorius muscle were recorded using floating microelectrodes implanted in the L5 ventral root of cats. The electromyographic activity generated by the anterior and medial portions of sartorius was recorded with chronically implanted electrodes. The muscle portion innervated by each motoneuron was determined by spike-triggered averaging of the EMGs during walking on a motorized treadmill. During normal locomotion, SA-a exhibited two bursts of EMG activity per step cycle, one during the stance phase and one during the late swing phase. In contrast, every recorded motoneuron projecting to SA-a discharged a single burst of action potentials per step cycle. Some SA-a motoneurons discharged only during the stance phase, whereas other motoneurons discharged only during the late swing phase. In all cases, the instantaneous frequencygram of the motoneuron was well fit by the rectified smoothed EMG envelope generated by SA-a during the appropriate phase of the step cycle. During normal locomotion, SA-m exhibited a single burst of EMG activity per step cycle, during the swing phase. The temporal characteristics of the EMG bursts recorded from SA-m differed from the swing-phase EMG bursts generated by SA-a.(ABSTRACT TRUNCATED AT 250 WORDS)     

Effects of acute dorsal spinal hemisection on motoneuron discharge in the medial gastrocnemius of the decerebrate cat

1. The discharge of single alpha-motoneuron axons was recorded from small cut filaments of the medial gastrocnemius (MG) muscle nerve in the decerebrated cat preparation before and after a dorsal hemisection of the thoracic spinal cord. The remainder of the MG muscle nerve was left intact, and muscle force and multiunit electromyographic (EMG) activity were recorded along with alpha-motoneuron discharge, while motor output was varied by manual stimulation of the contralateral hindlimb. 2. We recorded activity in 32 motoneurons before and after the spinal lesion, and pre- and postlesion recruitment forces and minimum firing rates were determined for 30 of these. Postlesion decreases in minimum firing rates were observed in 25/30 motoneurons, and decreases in recruitment force were seen in 21/30 motoneurons. The remaining motoneurons, which generally had low presection recruitment forces and minimum rates, exhibited postlesion increases in both parameters (see below). 3. The effects of the spinal lesion on the recruitment force and minimum firing rate of a motoneuron were related to the prelesion values of these parameters; the largest postlesion decreases were seen in motoneurons with the highest prelesion rates and recruitment forces. Spinal lesions thus acted to shift and compress the range of recruitment forces and minimum firing rates, so that after the lesion all motoneurons tended to exhibit discharge behavior typical of that seen only in the lowest threshold motoneurons before the lesion. In addition, motoneurons with low prelesion recruitment forces (less than 1.0 N of active force) generally showed an increase in recruitment force after the lesion, indicating that the lesion may have led to changes in the prelesion recruitment order. Direct evidence of recruitment reversals was obtained in 4/14 experiments where two or more motoneurons were followed pre- and postlesion. 4. The lesion-induced changes in motoneuron discharge characteristics were associated with changes in the relations between muscle force, rectified EMG, and motoneuron rate. Postlesion discharge rates were always significantly lower than the prelesion rates when compared over the same range of EMG levels. This postlesion drop in discharge rates was generally associated with inefficient force production, as evidenced by a significant drop in muscle force for matched EMG levels. 5. The degree of discharge synchrony in MG motoneurons was assessed by calculating a spike-triggered average (STA) between axonal discharge and multiunit rectified EMG. Significant STA peaks were rare before the lesion (4/32 motoneurons) but were quite common after the lesion (29/32 motoneurons).(ABSTRACT TRUNCATED AT 400 WORDS)     

Functionally complex muscles of the cat hindlimb

Several cat hindlimb muscles that exhibit differential activation (activity that is restricted to a specific region of muscle) during natural movements were studied to determine the possible roles of 1) non-uniform distribution of histochemically-identified muscle fiber-types (semitendinosus, ST; tibialis anterior, TA) or 2) mechanical heterogeneity (biceps femoris, BF; tensor fasciae latae, TFL). Using chronic recording techniques, electromyographic (EMG) activity was recorded from multiple sites of each muscle during treadmill locomotion, ear scratch, and paw shake. Standard histochemical analysis was performed on each muscle to determine fiber-type distribution. The histochemically regionalized muscles (ST and TA) were differentially active during slow locomotion; the deep regions (high in type I [SO] fibers) were active, but the superficial regions (high in type IIB [FG] fibers) were inactive. Vigorous movements (fast locomotion, ear scratch, paw shake) produced additional, synchronous activation of the superficial regions. In all movements, ST and TA activation patterns were consistent with the existence of identically timed synaptic inputs to all motoneurons within each motoneuron pool, resulting in an orderly recruitment of each whole pool. The differential activation recorded from ST and TA during slow locomotion was presumably a consequence of the non-uniform distribution of the different muscle fiber types. In contrast, differential activation of the histochemically nonregionalized, mechanically heterogeneous muscles (BF and TFL) resulted from non-synchronous activation of different muscle regions. The selective activation of BF or TFL compartments was indicative of differential synaptic inputs to, and selective recruitment of, subpopulations of the motoneuron pool, with each motoneuron subpopulation exclusively innervating physically separate regions of the muscle consistent with the regions defined by the neuromuscular territories of the major nerve branches supplying each muscle. Individual neuromuscular compartments of BF and TFL differ in their mechanical arrangements to the skeleton and in their contribution to mechanical action(s) at the hip and knee joints. Selective neural activation of mechanically distinct compartments within a mechanically heterogeneous muscle can provide highly advantageous mechanical "options" for animals that perform kinematically diverse movements. With regard to EMG recording techniques, the results of this study emphasize the need for carefully chosen EMG sampling sites and the value of knowing the muscle histochemistry, neuromuscular and musculoskeletal anatomy and possible mechanical functions prior to recording EMG.     

Cat hindlimb motoneurons during locomotion. IV. Participation in cutaneous reflexes

The responses of 11 individual motoneurons, the muscle to which each projected, plus all other muscles in the anterior thigh of the cat, were recorded following single non-noxious electrical stimuli to cutaneous nerves while the intact animal walked on a treadmill. The various excitatory and/or inhibitory responses were qualitatively similar for stimuli within the range 1.1-10 times threshold for group I fibers in the stimulated nerve (usually saphenous). Monarticular knee extensor muscles in the vastus group and their motoneurons were usually inhibited in the period 10- to 25-ms poststimulus. The faster contracting vastus medialis and lateralis muscles tended to have an excitatory rebound at approximately 25- to 40-ms poststimulus that was confined to the stance phase of the step cycle when these muscles were normally active. Biarticular hip flexor muscles rectus femoris and both the anterior and medial parts of sartorius and their motoneurons all had similar bimodal excitatory responses, including an early period 3- to 18-ms poststimulus and a later period 20- to 35-ms poststimulus. The short-latency excitatory responses appeared to be proportional to the normal recruitment of the muscles in the step cycle, whereas the long-latency responses tended to be phase advanced with respect to normal recruitment. Motoneurons projecting to muscles with two excitatory peaks tended to have similar excitatory responses at both latencies and occasionally responded at both latencies to a single stimulus.     

Axon collaterals of anterior semicircular canal-activated vestibular neurons and their coactivation of extraocular and neck motoneurons in the cat

We studied the ascending and descending axonal trajectories of excitatory vestibular neurons related to the anterior semicircular canal, by means of local stimulation and spike-triggered signal averaging techniques in anesthetized cats. More than 200 vestibular neurons related to the ampullary nerve of the anterior semicircular canal (ACN) were identified as vestibulo-ocular neurons by antidromic stimulation of the contralateral inferior oblique (IO) muscle motoneuron pool. In the descending, medial and ventral lateral nuclei, about 60% of these vestibulo-ocular neurons were also activated antidromically by upper cervical spinal cord stimulation (vestibulo-ocular-collic (cervical) = VOC). These VOC neurons produced unitary EPSPs in the majority of neck extensor motoneurons located at the C₁ segment. None of the VOC neurons had axons descending as far as the thoracic level. Most of these VOC neurons were activated monosynaptically following stimulation of the ACN. The conduction velocity of the descending axons of VOC neurons was approximately 63 m/s, which was significantly faster than that of the ascending axons. The remaining 40% of the vestibulo-ocular neurons were not activated antidromically following spinal cord stimulation at intensities of 1 mA or more (vestibulo-ocular = VO). Most of the VO neurons were activated polysynaptically by ACN stimulation. The superior vestibular nucleus contained VO neurons that were activated mono- and polysynaptically following ACN stimulation.     

Relationships between motor unit size and recruitment threshold in older adults: implications for size principle

As a part of the aging process, motor unit reorganization occurs in which small motoneurons reinnervate predominantly fast-twitch muscle fibers that have lost their innervation. We examined the relationship between motor unit size and the threshold force for recruitment in two muscles to determine whether older individuals might develop an alternative pattern of motor unit activation. Young and older adults performed isometric contractions ranging from 0 to 50% of maximal voluntary contraction in both the first dorsal interosseous (FDI) and tibialis anterior (TA) muscles. Muscle fiber action potentials were recorded with an intramuscular needle electrode and motor unit size was computed using spike-triggered averaging of the global EMG signal (macro EMG), which was also obtained from the intramuscular needle electrode. As expected, older individuals exhibited larger motor units than young subjects in both the FDI and the TA. However, moderately strong correlations were obtained for the macro EMG amplitude versus recruitment threshold relationship in both the young and older adults within both muscles, suggesting that the size principle of motor unit recruitment seems to be preserved in older adults.     

Activity of spindle afferents from cat anterior thigh muscles. II. Effects of fusimotor blockade

Chronically implanted electrodes and nerve cuff catheters were used to record the activity of individual muscle spindle afferents during treadmill walking as low doses of lidocaine were infused around the femoral nerve to progressively block gamma motoneuron activity. Both primary and secondary endings from both the monarticular knee extensors and the biarticular hip/knee muscles of the anterior thigh showed large decreases in afferent activity, usually well before changes in the electromyographic activity, force output, or length and velocity were seen in the parent muscles. This decline in the proprioceptive signal feeding back onto the spinal cord, which we presume to have involved most of the spindles supplied by the femoral nerve, did not cause noticeable irregularities or instability of the walking gait. At the peak of the fusimotor blockade, spindle afferents from knee extensor muscles lost about half of their usually brisk activity during the near-isometric contraction of the stance phase. Significant decreases in the response to passive stretch during the flexion phase also occurred. At the peak of the fusimotor blockade, spindle afferents from the biarticular muscles lost all of their activity during the rapidly shortening swing phase and about half of their activity during the rapidly lengthening stance phase. For both monarticular and biarticular muscle spindles, the activity decreases in stance and swing phase often occurred at distinctly different stages of the progressive fusimotor blockade, indicating several different sources of fusimotor control. From these data, we infer that the sensitivity of most spindle afferents is substantially influenced by fusimotor activity during phases of both extrafusal activity and extrafusal silence. At least some of this influence appears to come from fusimotor neurons whose recruitment is independent of the extrafusal recruitment. The extent and type of fusimotor effects on spindle afferent sensitivity (dynamic or static) appear to be specialized for the mechanical events that tend to occur during those phases.     

Mechanism for activation of locomotor centers in the spinal cord by stimulation of the mesencephalic locomotor region

The synaptic pathways of mesencephalic locomotor region (MLR)-evoked excitatory and inhibitory postsynaptic potentials (EPSPs and IPSPs) recorded from lumbar motoneurons of unanesthetized decerebrate cats during fictive locomotion were analyzed prior to, during, and after cold block of the medial reticular formation (MedRF) or the low thoracic ventral funiculus (VF). As others have shown, electrical stimulation of the MLR typically evoked short-latency excitatory or mixed excitatory/inhibitory PSPs in flexor and extensor motoneurons. The bulbospinal conduction velocities averaged approximately 88 m/s (range: 62-145 m/s) and segmental latencies for EPSPs ranged from 1.2 to 10.9 ms. The histogram of segmental latencies showed three peaks, suggesting di-, tri-, and polysynaptic linkages. Segmental latencies for IPSPs suggested trisynaptic or polysynaptic transmission. Most EPSPs (69/77) were significantly larger during the depolarized phase of the intracellular locomotor drive potential (LDP), and most IPSPs (35/46) were larger during the corresponding hyperpolarized phase. Bilateral cooling of the MedRF reversibly abolished locomotion of both hindlimbs as measured from the electroneurogram (ENG) activity of muscle nerves and simultaneously abolished or diminished the motoneuron PSPs and LDPs. Unilateral cooling of the VF blocked locomotion ipsilaterally and diminished it contralaterally with concomitant loss or decrease the motoneuron PSPs and LDPs. Relative to the side of motoneuron recording, cooling of the ipsilateral VF sometimes uncovered longer-latency EPSPs, whereas cooling of the contralateral VF abolished longer-latency EPSPs. It is concluded that MLR stimulation activates a pathway that relays in the MedRF and descends bilaterally in the VF to contact spinal interneurons that project to motoneurons. Local segmental pathways that activate or inhibit motoneurons during MLR-evoked fictive locomotion appear to be both ipsilateral and contralateral.     

Voltage threshold and excitability among variously sized cat hindlimb motoneurons

Intracellular recording has been performed to examine whether any differences in apparent initial-segment voltage threshold exist between types F and S cat triceps surae motoneurons. Voltage threshold was estimated using orthodromic action potentials initiated by large, monosynaptic excitatory postsynaptic potentials (EPSPs) evoked by dorsal root stimulation. No significant differences in voltage threshold could be detected between types F and S motoneurons. Further, voltage thresholds did not covary with motoneuron input resistance, afterhyperpolarization duration, or the twitch contraction time of functionally isolated muscle units. Significant positive correlations were observed between voltage threshold and the motoneuron resting potential. Utilizing a compartmental neuron model, a theoretical analysis has been performed that examines the influence of specific passive membrane properties on current threshold for action potentials initiated by large, monosynaptic EPSPs. This analysis indicates that total membrane capacitance will be the primary determinant of these thresholds. Further analysis of available data suggests that active membrane properties will play a minimal role in setting these thresholds. Since specific membrane capacitance is likely to be similar among cat motoneurons, it is concluded that only size or surface area-related current threshold differences will exist among these cells for activation with brief currents such as those underlying large EPSPs. For motoneurons thus activated, it is suggested that variations in the excitatory/inhibitory balance or density of synaptic input would be the major mechanisms for producing differential recruitment thresholds among the motoneuron population. Other available evidence is discussed that indicates that factors intrinsic to the motoneurons themselves will contribute to the setting of functional recruitment thresholds for activation with longer duration currents.     

Increased c-fos gene expression in alpha motoneurons in rat loaded hindlimb muscles with inclined locomotion

The potential usefulness of c-fos gene expression as an indicator of the activity level of spinal alpha motoneurons was examined in loaded locomotive rats. The motor pools of the plantaris (PL) and soleus muscles (SOL), mainly composed respectively of fast- and slow-twitch muscle fibers, were investigated in rats under locomotion at 25 m/min on a 20% incline. We first labeled motoneurons with a retrograde tracer, Nuclear Yellow (NY), and then quantified the c-fos mRNA expression level in the NY-labeled alpha motoneurons by means of in situ hybridization. Electromyographic (EMG) activities were also recorded. The c-fos expression level per alpha motoneuron showed a greater increase in the PL (75%) than in the SOL motor pool (38%). EMG activities also showed a greater increase in the PL (159%) than in the SOL (43%). Taken together, these results suggest that c-fos expression levels in alpha motoneurons are associated with the activity levels of their corresponding muscle. This cytochemical method for identifying the c-fos expression level has potential for use as a tool for estimating the activity level of large populations of alpha motoneurons in unrestricted animals.     

Vertical eye movement-related secondary vestibular neurons ascending in medial longitudinal fasciculus in cat. II. Direct connections with extraocular motoneurons

1. The preceding study in the alert cat has shown that many secondary vestibular axons that ascend in the medial longitudinal fasciculus (MLF) increase their firing rate in proportion to downward eye position. In the present study, projection and termination of these downward-position-vestibular (DPV) neurons within extraocular motoneuron pools were studied electrophysiologically by spike-triggered averaging techniques and morphologically be reconstructing their axonal trajectory after intra-axonal injection of horseradish peroxidase (HRP). 2. Extracellular field potentials recorded within the trochlear nucleus and/or the inferior rectus subdivision of the oculomotor nucleus were averaged by the use of spike potentials of single DPV neurons as triggers. All the crossed-DPV axons tested induced negative unitary field potentials in the trochlear nucleus (n = 9) and in the inferior rectus subdivision of the oculomotor nucleus (n = 5), suggesting that they made monosynaptic excitatory connection with motoneurons in these nuclei. The four crossed-DPV axons tested in the two motoneuron pools induced unitary field potentials in both. The majority of crossed-DPV axons terminated in these nuclei were directly activated from the caudal MLF, indicating that they had descending collaterals projecting to the spinal cord as well. The uncrossed-DPV axons did not induce such unitary field potentials either in the trochlear nucleus (n = 4) or in the inferior rectus subdivision (n = 3). 3. All the uncrossed-DPV axons examined (n = 14) induced positive unitary field potentials in the superior rectus subdivision of the oculomotor nucleus, suggesting that they made monosynaptic inhibitory connections with motoneurons innervating the superior rectus muscle. These uncrossed-DPV axons displayed regular firing patterns and were not activated from the caudal MLF. None of the crossed-DPV axons tested (n = 4) induced unitary field potentials in the superior rectus subdivision. 4. Five crossed-DPV axons were injected with HRP. All these axons ascended in the MLF contralateral to their soma, gave off many collaterals to the trochlear nucleus, and projected more rostrally. For three well-stained axons, numerous terminal branches were also found in the rostroventral part of the contralateral oculomotor nucleus, the area corresponding to the inferior rectus subdivision. Some collaterals in the oculomotor nucleus recrossed the midline to terminate in the medial part of the ipsilateral oculomotor nucleus. Other terminations were observed in the interstitial nucleus of Cajal and in the periaqueductal gray adjacent to the oculomotor nucleus. The crossed axons injected included both regular and irregular types, and three of the four examined were activated from the caudal MLF.(ABSTRACT TRUNCATED AT 400 WORDS)     

Functionally complex muscles of the cat hindlimb

Similarities between the muscle synergies associated with the flexion reflex and locomotion in reduced preparations have suggested that spinal circuits subserving these two motor tasks might share common interneurons. To test this hypothesis in functionally complex muscles, we studied the interaction between low-threshold cutaneous afferents and the locomotor central pattern generator (CPG) during treadmill locomotion in awake, intact cats. Electrical stimuli were delivered via implanted nerve cuff electrodes at all phases of locomotion, and EMGs were recorded from fourteen intramuscular subregions in eight bifunctional thigh muscles (adductor femoris, biceps femoris, caudofemoralis, gracilis, semimembranosus, semitendinosus, tensor fasciae latae, and tenuissimus). In addition, the EMG patterns recorded during locomotion were compared with those recorded during two other centrally driven rhythmical behaviors, scratching and paw shaking, to determine whether the functional relationships among these intramuscular subregions were fixed or task dependent. Four of the five broad, bifunctional muscles studied (biceps femoris, gracilis, semimembranosus, and tensor fasciae latae) had functional subunits that could be differentially activated in one or more of the three movements studied; adductor femoris was consistently uniformly activated despite its distributed skeletal attachments. The pattern of recruitment of the intramuscular functional subunits was movement-specific. The locomotor CPG and cutaneous reflex pathways both similarly subdivided some bifunctional muscles, but not others, into intramuscular subregions. The results of the present study confirm that some combinations of muscle subregions and cutaneous nerves constitute simple reciprocal categories of flexors and extensors, as described originally by Sherrington (1910). "Typical" low threshold excitatory or inhibitory reflex responses were produced in muscles or muscle subregions that were recruited as "net" flexors of extensors, respectively. However, muscles with complex activation patterns during walking often had very individualized, complex reflex responses during locomotion that did not conform to the background locomotion synergies. All of the reflex responses observed were mediated by low threshold cutaneous afferents. These data indicate that there are multiple, low threshold, excitatory and inhibitory cutaneous reflex pathways that have highly specialized connections with flexor and extensor muscles and even their intramuscular subregions. It is also clear that the premotoneuronal circuits mediating these cutaneous reflex effects are not necessarily synonymous with those of the locomotor CPG. These two systems do interact powerfully, however, suggesting some convergence. The nature of the convergence between the CPG and the many independent subsets of spinal interneurons mediating cutaneous reflexes is specialized and muscle subregion-specific.     

Motor-unit properties following cross-reinnervation of cat lateral gastrocnemius and soleus muscles with medial gastrocnemius nerve. II. Influence of muscle on motoneurons

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)     

Properties of human motor units after prolonged activity at a constant firing rate

The primary purpose of this study was to examine if there are changes in the intrinsic properties of spinal motoneurons after prolonged submaximal contractions. To do this, we assessed whether or not the synaptic drive to motoneurons needs to increase in order to maintain a constant firing rate of a motor unit. Recruitment of new units and an increase in total electromyographic (EMG) activity of the muscle of interest were taken as estimates of an increase in synaptic drive. Subjects were asked to maintain a constant firing rate of a clearly identifiable (targeted) motor unit from the first dorsal interosseous muscle for approximately 10 min, while surface EMG and force were recorded simultaneously. For the 60 units studied, the duration of the constant-firing-rate period ranged from 73 to 1,140 s (448 ± 227 s; mean ± SD). There was a significant increase (t-test, p<0.001) in the magnitude of mean surface EMG, and DC force while the targeted motoneuron maintained a constant rate suggesting an increase in the net excitatory input to the motoneuron pool. Changes occurring simultaneously in other parameters, namely, variability in interspike interval, magnitude of force fluctuations, the duration of motor unit action potentials, and the median power frequency of surface EMG were also computed. The firing rates of 16 concurrently firing motoneurons, not controlled by the subject, remained constant. The key finding of this study is that after prolonged activity, a motoneuron requires a stronger excitatory input to maintain its firing rate. Additional results are indicative of significant changes in the characteristics of the synaptic inputs, changes at the neuromuscular junction (both pre- and postsynaptic regions) and the sarcolemma.     

Effects of preventing reinnervation on axotomized spinal motoneurons in the cat. I. Motoneuron electrical properties

1. The intent of this study was to determine the effect on the electrical properties of axotomized spinal motoneurons when motor axons are allowed to regenerate but are denied the opportunity to reinnervate muscle. 2. The nerve supplying the medial gastrocnemius (MG) muscle in cats was served close to its entry into the muscle and sutured onto the surface of the lateral gastrocnemius (LG) muscle. The MG muscle was excised to prevent availability of vacant end-plates to the regenerating MG axons. The electrical properties of antidromically identified MG motoneurons were studied using intracellular recording at various postoperative intervals. 3. In 9 of 12 experimental animals, no sign of functional innervation by MG axons of the LG muscle could be detected. In three experimental animals, electrical and contraction activity in the LG muscle was observed following electrical stimulation of the transplanted MG nerve. The observed electrical and contraction activity was, however, negligible compared to the effects of electrical stimulation of the intact LG-soleus nerve. 4. At the earliest postoperative interval studied (20 days), MG motoneuron electrical properties [input resistance, afterhyperpolarization (AHP) duration, conduction velocity, time constant, rheobase current, and sag] exhibited significant changes that were nearly identical to those described for spinal motoneurons following section of ventral roots or motor nerves or in the earliest stages of reinnervation. 5. At the 44-60 day postoperative (DPO) intervals, several motoneuron electrical properties showed signs of recovery to control levels. At 44 DPO, average values of input resistance, time constant, and AHP duration declined from the significant increases observed at 20 DPO and could not be distinguished statistically from control mean values. 6. These indications of an early recovery of normal electrical properties were not sustained. At subsequent postoperative intervals (90, 120, and 150-180 DPO), average values of motoneuron electrical properties tended to be similar to those observed at 20 DPO. 7. Correlations observed among control motoneuron electrical properties were weakened and the pattern of correlation was disrupted at all postoperative intervals. 8. In conjunction with previous results demonstrating recovery of normal electrical properties following reinnervation (Foehring et al. 1986b), our findings suggest that functional contact with muscle is required for the full expression of the normal range of motoneuron electrical properties.(ABSTRACT TRUNCATED AT 400 WORDS)     

Kinesiological studies of self- and cross-reinnervated FDL and soleus muscles in freely moving cats

The activity patterns in self- and cross-reinnervated flexor digitorum longus (FDL) and soleus (SOL) muscles were examined during natural movements in awake, unrestrained cats in which electromyographic (EMG) electrodes, tendon-force gauges, and muscle-length gauges had been chronically implanted under anesthesia and aseptic conditions. Kinesiological data were recorded between 13 and 22 mo after nerve surgery. Self-reinnervated FDL and SOL muscles (i.e., FDL----FDL and SOL----SOL, respectively) exhibited locomotor activity patterns that were the same as observed in normal, unoperated FDL and SOL muscles (26). FDL----FDL muscles exhibited primarily brief bursts of activity in early swing, just after the toes had left the ground, whereas SOL----SOL muscles showed bursts of activity just before and during stance. In contrast, the cross-reinnervated muscles (both SOL----FDL and FDL----SOL) that had little or no unwanted self-reinnervation showed the patterns of activity that are associated with the innervating foreign motoneurons. That is, cross-reinnervated SOL----FDL muscles were intensely active in quadrupedal standing and, during the stance phase of stepping, producing large force transients while actively lengthening. Conversely, cross-reinnervated FDL----SOL muscles were active mainly in short bursts at the onset of the swing phase of stepping, just after the foot had left the ground. There was considerable modulation of EMG and peak force output in FDL----SOL muscles with changing speed of locomotion, whereas little modulation was evident in SOL----FDL muscles. The activity patterns in self- and cross-reinnervated FDL and SOL muscles were also recorded during scratch and paw-shaking reflexes. As in locomotion, the observed patterns were in all cases consistent with those expected for the innervating motor pool rather than the innervated muscle. Muscles that had been dually reinnervated by both the original and foreign motor pools displayed activity patterns that were a mixture of the FDL and SOL activity patterns described above. The present results demonstrate that motoneuron activation patterns remain qualitatively unaltered when their motor axons reinnervate foreign muscles. In addition, the observations permit some quantitative estimates of the degree to which cross-reinnervated muscles are subjected to patterns of motoneuron activity and to conditions of mechanical loading that are markedly different from those in the self-reinnervated or normal conditions.     

Disynaptic excitation from the medial longitudinal fasciculus to lumbosacral motoneurons: modulation by repetitive activation,descending pathways,and locomotion

Summary Short-latency excitatory postsynaptic potentials (EPSPs) evoked by stimulation in the medial longitudinal fasciculus (MLF) were recorded intracellularly from motoneurons in the cat lumbosacral spinal cord. Monosynaptic and disynaptic EPSPs occurred in most flexor and extensor motoneurons studied. These EPSPs resulted from the activation of fast (> 100 m/s) descending axons from the MLF to the spinal cord. Several features distinguished monosynaptic and disynaptic MLF EPSPs. Disynaptic EPSPs exhibited temporal facilitation during short trains of stimulation, whereas monosynaptic EPSPs did not. Disynaptic EPSPs, but not monosynaptic EPSPs, were also facilitated by stimulation of the pyramidal tract and the mesencephalic locomotor region. However, disynaptic MLF EPSPs exhibited little or no facilitation when conditioned by short-latency cutaneous pathways. During fictive locomotion, the amplitude of disynaptic MLF EPSPs was modulated, with maximal amplitudes during the step cycle phase when the recorded motoneuron was active, resulting in reciprocal patterns of modulation of flexors and extensors. No comparable change was seen in the amplitude of monosynaptic MLF EPSPs during fictive stepping. These data suggest that the central pattern generator for locomotion modulates disynaptic MLF excitation at a premotoneuronal level in a phase-dependent manner. The effects of lesions made in the MLF and thoracic cord suggest that the interneurons in the disynaptic pathway from the MLF to motoneurons reside in the lumbosacral cord.     

Functionally complex muscles of the cat hindlimb

Summary The cat sartorius (SA) can be divided functionally into an anterior (SAa), knee extensor portion and a medial (SAm), knee flexor portion; it can be further subdivided anatomically by multiple nerve branches into parallel longitudinal columns that terminate in a distributed insertion at the knee with a continuous range of moment arms. Thus, SA may be controlled by a discrete number of motoneuron task groups reflecting a small number of central command signals or by a continuum of activation patterns associated with a continuum of moment arms. To resolve this question, the activation patterns across the width of the SA were recorded with an electrode array during three kinematically different movements — treadmill locomotion, scratching and paw shaking, in awake, unrestrained cats. Uniformity of activation along the longitudinal axis was also examined because individual muscle fibers do not extend the length of the SA. In addition, the cutaneous reflex responses were recorded throughout all regions of the SA during locomotion. Two fascial surface-patch arrays, each carrying 4–8 pairs of bipolar EMG electrodes, were sutured to the inner surface of the SA, one placed proximally and the other more distally. Each array sampled separate sites across the anterior to medial axis of SA. During locomotion, two basic EMG patterns were observed: the two burst-per-step-cycle pattern typical of SAa and the single burst pattern typical of SAm. There was an abrupt transition in the pattern of activation recorded in the two parts of SA during locomotion, and no continuum in the activation pattern was observed. Stimulation of both sural and saphenous cutaneous nerves during locomotion produced reflex responses that were uniformly distributed throughout SA, in contrast to the regional differences noted during unperturbed walking. Similarly, during scratching and paw shaking all parts of the SA were active simultaneously but with regional differences in EMG amplitude. The abrupt functional border between SAa and SAm coincided with the division of the SA into a knee flexor vs. a knee extensor. In all cases, the quantitative and qualitative differences in SAa and SAm EMGs were uniformly recorded throughout the entire extent of SAa or SAm; i.e., there was no segregation of activity within either SAa or SAm. Furthermore, the time course of EMG from each proximal recording site was nearly identical to the corresponding distal site, indicating no segregation of function along the longitudinal axis of SA. These results indicate that SAa and SAm constitute the smallest functional modules that can be recruited in SA. The functional subdivision of the SA motor nucleus is reflected in the central pattern generators for these movements to permit a task-dependent recruitment of any combination of SAa and SAm. Our data indicate that the number of task groups even in an anatomically and functionally complex muscle like the SA is small and appears to be related to the kinematic conditions under which the muscle operates.     

Firing rate modulation of motoneurons activated by cutaneous and muscle receptor afferents in the decerebrate cat

The aim of this study was to investigate whether activation of spinal motoneurons by sensory afferents of the caudal cutaneous sural (CCS) nerve evokes an atypical motor control scheme. In this scheme, motor units that contract fast and forcefully are driven by CCS afferents to fire faster than motor units that contract more slowly and weakly. This is the opposite of the scheme described by the size principle. Earlier studies from this lab do not support the atypical scheme and instead demonstrate that both CCS and muscle stretch recruit motor units according to the size principle. The latter finding may indicate that CCS and muscle-stretch inputs have similar functional organizations or that comparison of recruitment sequence was simply unable to resolve a difference. In the present experiments, we examine this issue using rate modulation as a more sensitive index of motoneuron activation than recruitment. Quantification of the firing output generated by these two inputs in the same pairs of motoneurons enabled direct comparison of the functional arrangements of CCS versus muscle-stretch inputs across the pool of medial gastrocnemius (MG) motoneurons. No systematic difference was observed in the rate modulation produced by CCS versus muscle-stretch inputs for 35 pairs of MG motoneurons. For the subset of 24 motoneuron pairs exhibiting linear co-modulation of firing rate (r > 0.5) in response to both CCS and muscle inputs, the slopes of the regression lines were statistically indistinguishable between the two inputs. For individual motoneuron pairs, small differences in slope between inputs were not related to differences in conduction velocity (CV), recruitment order, or, for a small sample, differences in motor unit force. We conclude that an atypical motor control scheme involving selective activation of typically less excitable motoneurons, if it does occur during normal movement, is not an obligatory consequence of activation by sural nerve afferents. On average and for both muscle-stretch and skin-pinch inputs, the motoneuron with the faster CV in the pair tended to be driven to fire at slightly but significantly faster firing rates. Computer simulations based in part on frequency-current relations measured directly from motoneurons revealed that properties intrinsic to motoneurons are sufficient to account for the higher firing rates of the faster CV motoneuron in a pair.