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1. Recurrent collaterals of motoneurons innervating muscles that have a role in control of the hindlimb digits were studied with neuroanatomic tracing methods to determine whether these motoneurons have simple recurrent collateral arbors in comparison with those of hip, knee, and ankle muscles. 2. Motoneurons innervating the hindlimb muscles plantaris (Pln), flexor hallucis longus (FHL), or flexor digitorum longus (FDL) were injected with 10% horseradish peroxidase. Recurrent collaterals were reconstructed from serial transverse sections. 3. No recurrent collaterals were observed in a sample of 10 FDL motoneurons. 4. FHL motoneurons had simple recurrent collateral arbors as assessed by number of first-order collaterals, number of collateral swellings, number of end branches, and the highest-order branch of individual collateral trees. Recurrent collateral arbors of Pln motoneurons were more complex than those of FHL motoneurons. Pln and FHL recurrent collateral arbors were less complex than those described for gastrocnemius-soleus, anterior tibial, and posterior biceps motoneurons. 5. These anatomic findings correspond well with electrophysiological results indicating that the recurrent inhibition produced by FHL motoneurons is weak and that FDL motoneurons do not produce recurrent inhibition. In addition, Pln motoneurons are reported to produce stronger recurrent inhibition than FHL motoneurons in many motor pools. 6. Consideration of these results with respect to the mechanical actions and patterns of motor activity observed in FDL, FHL, and Pln suggests that the complexity of recurrent collaterals of a motoneuron pool and the extent of its contribution to recurrent inhibition diminish with its involvement in the individualized control of the digits.

1. Recurrent inhibitory postsynaptic potentials (IPSPs) to and from motoneurons innervating the flexor digitorum longus (FDL) and flexor hallucis longus (FHL) muscles of the cat were investigated to determine whether recurrent inhibitory projections involving these motoneurons are similar--as would be consistent with the Ia and anatomic synergism of FDL and FHL--or are dissimilar, as are the activities of these muscles during locomotion (O'Donovan et al. 1982). 2. Composite recurrent IPSPs were recorded in several species of motoneurons innervating hindlimb muscles in response to stimulation of a number of muscle nerves in cats allowed to become unanesthetized after ischemic decapitation. 3. No recurrent IPSPs from stimulation of the FDL nerve were observed in motoneurons innervating FDL, FHL, lateral gastrocnemius-soleus (LG-S), medial gastrocnemius (MG), plantaris (Pl), tibialis anterior (TA), or extensor digitorum longus (EDL). 4. The recurrent IPSPs produced by stimulation of FHL were larger and found more frequently in LG-S than in FDL motoneurons. Recurrent inhibition from FHL was also greater in Pl than in FDL motoneurons. 5. The recurrent IPSPs produced by stimulation of LG-S, PL, and MG were larger in FHL than in FDL motoneurons, and those from LG-S and MG were found more frequently in FHL than in FDL motoneurons. 6. Stimulation of the TA nerve produces recurrent IPSPs in FDL but not in FHL motoneurons. A few FDL and FHL cells (6 of 23 and 9 of 34, respectively) received small (less than 0.5 mV) recurrent IPSPs from stimulation of the EDL nerve.(ABSTRACT TRUNCATED AT 250 WORDS)

This report describes the use of a synchronization index (Is; Hamm et al., 1985a) and its sensitivity to various forms and degrees of synchrony between spike trains. The dependence of the Is on signal-to-noise ratio, the number of synchronized spike trains and their degree of synchrony is shown in analog and digital simulations. These simulations and a comparison with peristimulus time histograms under conditions of induced synchrony reveal that the Is is a sensitive measure of synchronization in a population of spike trains.

A test for synchronization among the spike trains of muscle afferents or motor units is described which utilizes averages of neurograms and rectified neurograms. Synchronization is quantified by the increase of a synchronization index Is above a theoretical value for asynchrony. The dependence of the Is on signal amplitude and certain experimental conditions and a method of estimating confidence limits for the test are presented.

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 biceps's 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.

Experiments were conducted to test the hypothesis that a partitioning of Ia monosynaptic excitatory postsynaptic potentials (Ia EPSPs) is present in motor nuclei supplying muscles with regions capable of different mechanical actions. Intracellular recordings of synaptic potentials were made in lateral gastrocnemius (LG) motoneurons in anesthetized low-spinal cats. The effects were tested of stimuli (group I range) to the four primary nerve branches of the LG nerve supplying muscle compartments LGm, LG1, LG2, and LG3 (terminology of English, Ref. 26) and the nerve to a heteronymous muscle, soleus. Stimulation of a given LG nerve branch produced monosynaptic Ia EPSPs of greater amplitude in "own-branch" motoneurons than "other-branch" cells. A significant partitioning of mean Ia EPSPs was found in three (LG1, LG2, LG3) out of the four homonymous pathways studied. An EPSP normalization (7) was performed to eliminate potential differences in cell type that might affect the amplitudes of the EPSPs between these four cell groups (e.g., differences in the number of cells supplying FF, FR, and S muscle units). This normalization confirmed that the partitioning of monosynaptic Ia inputs upon stimulation of LG1, LG2, and LG3 could not be attributed to differences in cell type. In addition, the effects of LGm stimulation were found to be significantly greater in the LGm motoneurons compared with the other cell groups. Heteronymous input (from soleus) to the LG motor nucleus showed some partitioned effects. Motoneurons innervating compartment LG2 received larger EPSPs from soleus than did the cells supplying compartments LG1, LG3, and LGm. The contributions of location specificity and species specificity (terminology of Scott and Mendell, Ref. 55) in the establishment of these Ia-afferent-motoneuronal connections were examined. Cell location sites within the spinal cord were consistent with location specificity making some contribution to the observed pattern of homonymous Ia connections. A more prominent role for species specificity was indicated by species-dependent differences in EPSP amplitude in pairs of LG motoneurons (e.g., LGm vs. LG2) at similar rostrocaudal locations upon stimulation of a given homonymous or heteronymous nerve/branch.

In anesthetized cats 3 medial gastrocnemius (MG) motor units (MUs) were electrically activated with independent pseudorandom patterns at physiological mean rates. Recordings of isometric MG tension (T) and membrane potential changes (PSPs) in MG alpha-motoneurons (MNs) were averaged with respect to each stimulus train. The resulting T and PSP trajectories displayed the responses of each MN to the 3 average MU twitches. These responses could vary from no response to a sequence of depolarizing and hyperpolarizing waves in a PSP trajectory. The results are consistent with the known behavior of muscle stretch receptors to muscle and MU twitches and the receptors' connections to homonymous MNs.

An analysis is made of linear and non-linear summation of the motor unit (MU) tension and motoneuron (MN) membrane potential (PSP) trajectories evoked by stimulation of MUs as previously reported. In most cases, summation of both averaged responses was linear. Seldom, PSPs summed non-linearly, then usually coinciding with non-linear summation of the responsible MU twitches. The results suggest that the afferent pathways mediating the mechanical events in muscle to MNs behave rather linearly, at least in the small-signal range of interest here.

Intracellular recordings form biceps femoris (BF) motoneurons were made in anesthetized low spinal cats during periods of electrical stimulation of the nerve branches supplying the anterior, middle and posterior portions of the BF muscle and the nerves to semimembranosus and semitendinosus. Measurements were made of each cell's composite intrahomonymous and heteronymous monosynaptic Ia-EPSP responses to stimulation of the test nerves (branches). We have found evidence for an intramuscular localization of these monosynaptic Ia reflex effects not only when comparing responses between the two functional components of the BF muscle as is well established [6] but, in addition, when comparing responses between different parts of each functional (hip extensor and knee flexor) component as well. It is argued that both somatotopic and neuronal recognition factors may contribute to the localization of these monosynaptic reflex effects.

Motor units from the cat tibialis posterior muscle were examined for an association between physiological and biochemical properties. Functionally isolated motor units were categorized on the basis of their physiological properties. This was followed by quantitative microbiochemical analysis of single muscle fibers from each unit, identified in cross sections using the glycogen-depletion method. The activities of malate dehydrogenase and beta-hydroxyacyl-CoA dehydrogenase distinguished between fatigable (type FF) and fatigue-resistant (types FR and S) units. The activities of both lactate dehydrogenase and adenylokinase were higher in fast- than in slow-contracting units. Cluster analyses, based on both physiological and biochemical properties or on biochemical properties alone, produced groupings identical to types FF, FR, and S. The association between physiological and biochemical properties substantiates the idea that biochemically distinct groups of motor units correspond to physiologically identifiable groups.

Individual muscle fibers of 10 motor units from the tibialis posterior muscle of cat were identified by glycogen depletion techniques, characterized for histochemical type, diameter, and intramuscular locations, and analyzed by quantitative biochemical methods. Four enzymes, representing different energy-yielding pathways, were quantitatively assayed in muscle fibers belonging to motor units selected from each of the three major physiological types. All four enzymes demonstrated identical activities among fibers within a motor unit, while showing up to 11-fold differences among fibers belonging to different motor units. Moreover, fibers within a single motor unit, but of substantially different diameters, were nevertheless homogeneous in specific enzyme activities.

In anaesthetized low-spinal cats, intracellular recordings were made of the Ia excitatory post-synaptic potential (e.p.s.p.) responses of semimembranosus motoneurones to electrical stimulation (Group I range) of nerve branches supplying the anterior and posterior heads of semimembranosus, the anterior and posterior parts of biceps femoris, and the distal part of semitendinosus. Recordings were also made during stimulation of nerves to the gracilis muscle and to the vasti muscle group. Stimulation of the semimembranosus-anterior nerve branch produced Ia e.p.s.p.s. of greater amplitude in semimembranosus-anterior motoneurones than in semimembranosus-posterior cells; likewise, stimulation of the semimembranosus-posterior nerve branch produced larger e.p.s.p.s. in cells which supplied the posterior head than in those which supplied the anterior head. Stimulation of the nerve branches to components of two 'flexor' muscles (Sherrington, 1910), biceps-posterior and semitendinosus-distal, produced larger e.p.s.p.s in semimembranosus-posterior cells than in the anterior motoneurones. A tendency was found for stimulation of the nerve to biceps femoris-anterior (an 'extensor') to produce larger e.p.s.p.s in semimembranosus-anterior than in-posterior motoneurones. However, this effect was of borderline (0.06 greater than P greater than 0.05) significance. The limited monosynaptic input produced by stimulation of the nerves to the gracilis and vasti muscles showed that their Ia axons do not distinguish between the two semimembranosus cell groups. A slight topographic organization of motoneurones within the semimembranosus motor nucleus was found, with anterior cells encountered, on average, at a more rostral level of the spinal cord than posterior cells. A similar topographic arrangement was observed in the rostrocaudal distribution of Group I afferent fibres in the dorsal roots and motor axons from the two sets of motoneurones in the ventral roots. These findings are consistent with 'location specificity' (Scott & Mendell, 1976) being a factor which contributes to the observed pattern of homonymous Ia connexions. A role for 'species specificity' (Scott & Mendell, 1976) in determining the observed pattern of homonymous Ia connexions was indicated by species-dependent differences in e.p.s.p. amplitude in pairs of semimembranosus-anterior and -posterior motoneurones at similar rostrocaudal locations in the spinal cord. The pattern of heteronymous connexions to the semimembranosus motor nucleus also showed evidence for species specificity. However, no clear topographic pattern was evident in these connexions.

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.

Evidence is presented for the existence of synchrony between the spike trains of muscle afferents of the passive cat medial gastrocnemius muscle held at fixed length. Synchrony between the spike trains of a population of muscle afferents was quantified by means of a synchronization index (Is), derived from spike-triggered averages of the muscle-nerve neurogram and the rectified neurogram. A previously used test based solely upon the neurogram average (Watt, Stauffer, Taylor, Reinking & Stuart, 1976) is shown to be invalid. The differences between experimentally derived Is values and theoretical Is values derived for the condition of asynchrony were compared to estimated confidence limits for those differences. This comparison revealed that twenty-two of fifty-three muscle-afferent spike trains whose rectified averages satisfied certain conditions for interpreting the Is were synchronized with the discharge of other afferents. The form of the rectified averages of another eight afferents suggested that these afferents might also have been synchronized. Synchrony in the discharge of muscle afferents was found in three experiments in which the neurogram was recorded from a single nerve branch to medial gastrocnemius, as well as in the data of experiments in which the whole muscle nerve was used. The degree of synchrony was similar for Ia, spindle group II and Ib afferents. The magnitude of the synchrony found in these experiments was judged by comparison to the results of analog simulations and the increase in Is values resulting from the application of small, quick stretches to the medial gastrocnemius muscle. The degree of synchrony found on average was approximately equivalent to that of a single spike occurring once for every four discharges of the reference spike train. Simulations were performed to determine the distortion of monosynaptic excitatory post-synaptic potentials (e.p.s.p.s) obtained by spike-triggered averaging which would be produced by synchrony between the spike trains of Ia and spindle group II afferents of the magnitude found in this study. These simulations indicate that the apparent amplitude would be increased by approximately 4 microV on average. Both the 10-90% rise time and the half-width would increase, the effects being greater for smaller e.p.s.p.s. Consequently, the synchrony found in this study is of most concern in the study of small post-synaptic potentials, such as those due to spindle group II afferents.

In anesthetized cats, medial gastrocnemius motor units (MUs) were electrically stimulated via their ventral-root axons with independent random patterns. Muscle tension and homonymous alpha-motoneuron (alpha-MN) membrane potential fluctuations in response to these stimuli were recorded simultaneously. Cross-correlating these two signals in temporal relation to the stimuli showed the covariance of the two signals around their respective means. With moderate to strong MU-MN couplings indicated by clear and large average membrane potential changes (PSP trajectories), the correlation coefficients tended to be positive at times when the PSP hyperpolarized, and vice versa. These relations are probably caused by the non-linear behavior of MUs, muscle receptors and afferent pathways. Thus, the signal transfer from motor efferents back to homonymous alpha-MNs depended upon the level of background tension, upon which MU twitches were superimposed.

Evidence is presented that marked changes in the electromyographic (EMG) activity of single motor units often occur during a fatigue-test paradigm (12) widely used for the classification of mammalian motor units into fast-fatigable (FF), fast-intermediate-fatigable, fast-fatigue-resistant and slow categories (11), particularly in type FF units. Force output and EMG activity were measured in single motor units of the tibialis posterior muscle of anasthetized cats, while each unit was subjected to a fatigue test consisting of 4 min of motor-axon stimulation, using 1 Hz 330 ms trains of 0.1 ms shocks at 40 Hz. As a measure of the temporal characteristics of the EMG waveform, the reciprocal of the interval between first positive and subsequent negative peak was measured. For parameters of EMG magnitude, peak-to-peak amplitude and area were measured. The fatigue test was shown to produce, on average, significantly greater alterations in the values of the EMG parameters of FF units than of the other unit types. There were no significant EMG alterations among the other unit types. The results are discussed in relation to the interpretation of EMG depression as an indication of excitation failure and the relative fatigability and EMG depression of different motor unit types.