Excitatory and inhibitory postsynaptic potentials in alpha-motoneurons produced during fictive locomotion by stimulation of the mesencephalic locomotor region

We tested the hypothesis that stimulation of the mesencephalic locomotor region (MLR) activates polysynaptic pathways that project to lumbar spinal motoneurons and are involved in the initiation of locomotion. Fictive locomotion was produced by MLR stimulation, and intracellular records of evoked postsynaptic potentials (PSPs) in alpha-motoneurons were computer analyzed. Stimulation of sites in the MLR that were maximally effective for the initiation of locomotion produced excitatory and inhibitory postsynaptic potentials (EPSPs and IPSPs) in all the motoneurons examined. The amplitudes of the PSPs increased as locomotion commenced. The EPSPs were largest during the depolarized phase of the step cycle, and in 17 of our 22 cells the EPSP was replaced by an IPSP of slightly longer latency during the hyperpolarized phase. The mean latency of the EPSPs measured from the stimulus artifact produced by stimulation of the MLR was 5.1 ms (3.0-7.0 ms). In all cases, the IPSP occurred 0.6 ms or more after the onset of the EPSP in the same cell. Later PSPs were sometimes observed as well. The effects of constant current injection on the membrane potential oscillations associated with fictive locomotion (locomotor drive potentials) were examined. The results showed that the amplitudes of the locomotor drive potentials (LDPs) could be affected by depolarizing and hyperpolarizing current injection. The data is consistent with the LDP having a predominant inhibitory component, which is more readily altered by current injection than is the excitatory component. The effect of constant current injections on the MLR-evoked PSPs was also examined, and it was observed that both EPSPs and IPSPs could be affected by the injected currents. The EPSPs increased in amplitude with constant hyperpolarizing current injection, and this fact rules out the possibility that the EPSP is actually a reversed IPSP. The IPSP was decreased in amplitude by hyperpolarizing current injection. Combined stimulation of the MLR and the ipsilateral high-threshold muscle or cutaneous afferents produced facilitation of both short- and long-latency MLR-evoked PSPs, suggesting that the two pathways share common interneurons. The possibility that the long-latency PSPs are produced by rapid oscillation in the locomotor central pattern generator is discussed. We concluded that MLR stimulation that evokes fictive locomotion produces both excitation and inhibition of spinal motoneurons. Spinal interneuronal systems are implicated and may be those involved in the initiation and control of locomotion. The probable relay sites for the descending pathway from the MLR to motoneurons are discussed.     

Motoneuron input-resistance changes during fictive locomotion produced by stimulation of the mesencephalic locomotor region

Input-resistance changes during fictive locomotion were monitored in a variety of extensor and flexor hindlimb alpha-motoneurons in precollicular, postmammillary decerebrate cats induced to "walk" by electrical stimulation of the mesencephalic locomotor region (MLR). Using intracellular recording techniques and injected hyperpolarizing current pulses, the changes in the motoneuron input resistance recorded at the motoneuron soma were examined during nonlocomoting control periods as well as during the depolarized and hyperpolarized phases of the membrane potential oscillations (locomotor drive potentials, or LDPs) of fictive locomotion. In 28 of the 52 motoneurons examined, no change in the input resistance between the control and locomotor periods was observed. The remainder of the cells displayed a decrease (less than 20%) in input resistance when fictive stepping commenced. Over 80% of all the motoneurons depolarized (mean depolarization 4 mV), whereas only one LG motoneuron hyperpolarized (2 mV) with the onset of stimulation of the MLR. The remaining motoneurons did not display such changes. In 43 out of 52 motoneurons examined, no significant change in the input resistance could be observed between the depolarized and hyperpolarized phases of the step cycle. A decrease in the input resistance during the depolarized phase of the LDP was observed in four LG motoneurons, whereas five other motoneurons (2 LG, 1 TA, 1 PB, and 1 ST) displayed an increased input resistance during the depolarized phase compared with the hyperpolarized phase of locomotion. The data are consistent with the presence of an excitatory synaptic input alternating with an inhibitory input to the motoneuron during the fictive step cycle.(ABSTRACT TRUNCATED AT 250 WORDS)     

Vestibulospinal effects on hindlimb motoneurons of the frog

Summary Field and intracellular potentials were recorded in the lumbar spinal cord of the frog following stimulation of the anterior branch of the vestibular nerve and vestibular nucleus. The field potential recorded in the motoneuron pool after VIIIth nerve stimulation consisted of two presynaptic positive-negative potentials (latencies 1.7 and 2.6 msec) followed by a slow negative wave. The latency of the first presynaptic field potential was only 0.6 msec longer than the presynaptic field potential evoked by stimulation of the vestibular nucleus; it is suggested that electrotonic coupling in the vestibular nuclei is responsible for the fast vestibulospinal transmission.Whereas VIIIth nerve stimulation produced EPSPs in both flexor (peroneal) and extensor (tibial) motoneurons, IPSPs were found only in extensor motoneurons. The functional implication of these findings was discussed. Comparison of PSP latencies with the extracellular presynaptic field potentials generated by VIIIth nerve or nucleus stimulation indicated that EPSPs were produced by the excitatory action of vestibulospinal axons on motoneurons. The longer latencies of the vestibular induced IPSPs suggested that they were generated indirectly by inhibitory spinal interneurons. Preliminary experiments on the interaction of segmental and vestibular induced PSPs suggest that the latter are generated close to the soma of motoneurons.     

Phasic control of the transmission in the excitatory and inhibitory reflex pathways from cutaneous afferents to α-motoneurones during fictive locomotion in cats

In high spinal paralyzed cats the effect of cutaneous nerve stimulation on lumbar motoneurons was investigated during fictive locomotion. EPSPs evoked from the cutaneous afferents were generally larger during the active phase of the motoneurones, while IPSPs tended to increase during the reciprocal phase. In some cases EPSPs occurred during the active phase, while IPSPs dominated during the reciprocal phase. Apparently, the transmission in the excitatory and inhibitory segmental reflex pathways from cutaneous afferents to α-motoneurones depends on the phase of the step cycle, but there is no general phase dependent alternating switching between these two pathways.     

Corticospinal control of locomotor pathways generating extensor activities in the cat

Interneuronal convergence of corticospinal and segmental pathways involved with the generation of extensor activities during locomotion was investigated in decerebrate and partially spinalized cats. L-dihydroxyphenylalanine (L-DOPA) was slowly injected until long-latency, long-lasting discharges could be evoked by the stimulation of contralateral flexor reflex afferents (coFRA) and the group I autogenetic inhibition was reversed to polysynaptic excitation in extensor motoneurons. Under these conditions, we stimulated in alternation the contralateral pyramidal tract (PT), group I afferents from knee and ankle extensor muscles, and both stimuli together. We did the same for the stimulation of PT and of coFRA. Clear polysynaptic EPSPs could be evoked from all three sources in 32 extensor motoneurons. Convergence was inferred from spatial facilitation, which occurred when the amplitude of the EPSPs evoked by the combined stimuli was notably larger than the algebraic sum of the EPSPs evoked by individual stimulation. Spatial facilitation was found between PT and extensor group I inputs in 30/59 tests (51%) in 20 motoneurons and in all cases (6/6) between PT and coFRA in six motoneurons. When fictive locomotion was induced with further injection of L-DOPA, PT descending volleys from the same stimulating site could reset the stepping rhythm by initiating bursts of activity in all extensors. These results indicate that at least some of the corticospinal fibers project onto interneurons shared by the coFRA and the polysynaptic excitatory group I pathways to extensors. The implications of such convergence patterns on the organization of the extensor "half-center" for locomotion are discussed.     

Modulation of short latency cutaneous excitation in flexor and extensor motoneurons during fictive locomotion in the cat

Summary We examined modulation of transmission in short-latency, distal hindlimb cutaneous reflex pathways during fictive locomotion in 19 decerebrate cats. Fictive stepping was produced either by electrical stimulation of the mesencephalic locomotor region (MLR) or by administration of Nialamide and 1-DOPA to acutely spinalized animals. Postsynaptic potentials (PSPs) produced by electrical stimulation of low threshold afferents (< 2.5 times threshold) in the superficial peroneal (SP), sural, saphenous or medial plantar nerves were recorded intracellularly from various extensor (n = 28) and flexor (n = 24) motoneurons and averaged throughout the step cycle, together with voltage responses to intrasomatic constant current pulses (in order to monitor relative cell input resistance). Each motoneuron studied displayed rhythmic background oscillations in membrane potential and correlated variations in input resistance. The average input resistance of extensor motoneurons was lowest during mid-flexion, when the cells were relatively hyperpolarized and silent. Conversely, average input resistance of flexor motoneurons was highest during mid-flexion, when they were depolarized and active. The amplitude of the minimum-latency excitatory components of PSPs produced by cutaneous nerve stimulation were measured from computer averaged records representing six subdivisions of the fictive step cycle. Oligosynaptic EPSP components were consistently modulated only in the superficial peroneal responses in flexor motoneurons, which exhibited enhanced amplitude during the flexion phase. With the other skin nerves tested (sural, saphenous, and plantar), no consistent patterns of modulation were observed during fictive locomotion. We conclude that transmission through some, but not all, oligosynaptic excitatory cutaneous pathways is enhanced by premotoneuronal mechanisms during the flexion phase of fictive stepping in several cat hindlimb motor nuclei. The present results suggest that the patterns of interaction between the locomotor central pattern generator and excitatory cutaneous reflex pathways depend on the source of afferent input and on the identity of the target motoneuron population.     

The role of Renshaw cells in locomotion: antagonism of their excitation from motor axon collaterals with intravenous mecamylamine

Summary The contribution of Renshaw cell (RC) activity to the production of fictive locomotion in the mesencephalic preparation was examined using the nicotinic antagonist mecamylamine (MEC). After the i.v. administration of 3 doses of MEC (1.0 mg/kg) the following observations were made: 1) ventral root (VR) evoked discharge of RCs was decreased by up to 87.7%, 2) recurrent inhibitory postsynaptic potentials recorded in alpha motoneurons were greatly reduced or abolished, and 3) the rhythmic firing of RCs during the fictive step cycle was abolished in 83% of the cells examined. Locomotor drive potentials (LDPs) in motoneurons persisted during the fictive step cycle after MEC administration. Bursts of motoneuron firing during each fictive step cycle were characterized by increased frequency and number of spikes after MEC, although the burst duration was unaltered for similar step cycle lengths. A greater number and frequency of spikes per burst was also observed in Ia inhibitory interneurons (IaINs), which remained rhythmically active after MEC administration. It is concluded that Renshaw cells are not an integral part of the spinal central pattern generator for locomotion, nor do they control the timing of the motoneuron or IaIN bursts of firing during fictive locomotion. The data are consistent with a role for RCs in limiting the firing rates of motoneurons and IaINs during each burst.     

An intracellular study of perineal and hindlimb afferent inputs onto sphincter motoneurons in the decerebrate cat

Summary The external urethral sphincter (EUS) and external anal sphincter (EAS) are striated muscles that function to maintain urinary and fecal continence respectively. This study examines the short-latency synaptic input from a variety of cutaneous perineal and muscle/cutaneous hindlimb afferents to the motoneurons innervating these muscles. Intracellular recordings from anti dromically identified EUS and EAS motoneurons provided records of the postsynaptic potentials (PSPs) produced by electrical stimulation of peripheral afferents in decerebrate or chloralose anesthetized cats. Excitatory postsynaptic potentials (EPSPs) were produced in most EUS and EAS motoneurons by stimulation of ipsilateral and contralateral sensory pudendal (SPud) and superficial perineal (SPeri) cutaneous nerves. The shortest cen tral latencies in the study (1.5 ms) suggest that there are disynaptic excitatory, in addition to tri-and oligosynap tic, connections within these reflex pathways. EPSPs mixed with longer latency inhibitory potentials (E/I PSPs) were observed in both motoneuron populations but were found more frequently in EAS motoneurons. These E/I PSPs were evoked more often from contralat eral afferents than from ipsilateral afferents. Cutaneous nerves innervating the hindlimb had weaker if any synaptic effects on sphincter motoneurons. Stimulation of ipsilateral hindlimb muscle nerves rarely produced PSPs in EUS motoneurons and had weak synaptic actions on EAS motoneurons. In 2 of 22 animals (both decerebrate), large inhibitory potentials predominated over early small EPSPs suggesting that inhibitory pathways from these afferents to sphincter motoneurons can be released under certain circumstances. The relation between the segmental afferents to EUS and EAS motoneurons and the neural circuitry influencing them during micturition and defecation are discussed.     

Synaptic inputs from low threshold afferents of trunk muscles to motoneurons innervating the longissimus lumborum muscle in the spinal cat

(1) We studied the reflex actions of group I and II afferents to longissimus lumborum (Long) motoneurons in the L1–L5 spinal segments from the epaxial muscle, m. Long, and the hypaxial muscle, m. obliquus externus abdominus (OEA). (2) Postsynaptic potentials (PSPs) recorded from 140 Long motoneurons in 30 spinal cats were analyzed. Under the present experimental conditions, the stimulation of Long and OEA nerves at an intensity below 1.5 times threshold (T) activated only group I muscle afferents, while stimulations at 2–5T activated group II muscle afferents as well. (3) The incidence of PSPs was related to the proximity of the spinal segments of the nerves stimulated to the spinal segment of the motoneurons; the shorter the distance the larger the PSPs and higher incidence of PSPs. The Long motoneurons received group I afferent input mainly from the same and adjacent segments, and received group II afferent inputs from a wider range of segments. (4) A short (i.e., less than 1.0 ms) latency of excitatory PSPs (EPSPs) evoked by ipsilateral group I afferents of Long at the same or adjacent segment indicated a monosynaptic connection. In general, the central latencies became longer as the distance between spinal segments of stimulated nerves and motoneurons increased. Major PSP components were produced by polysynaptic neuronal pathways. The spatial facilitation between PSPs evoked by afferents of different nerves (i.e., ipsilateral Long (iLong) and contralateral Long (cLong) of the same segment; iLongs of different segments; and iLong and iOEA of the same segment) indicated that they shared common interneurons. (5) Although iLong and iOEA muscle afferents produced predominantly EPSPs, and contralateral muscle afferents elicited predominantly IPSPs in Long motoneurons at each spinal segment, the patterns of convergence from Long and OEA muscle afferents of different spinal segments and of different sides differed considerably among motoneurons. (6) These findings demonstrated various input patterns of individual motoneurons within the same motoneuron pool, which might reflect the complexity of neuronal control of the back muscles for various trunk movements, including lateral and dorsal bending, rotating, and fixation of the trunk. Electronic Publication     

Neuronal activity in the lateral vestibular nucleus of the cat

The synaptic input to Deiters neurones evoked by stimulation of peripheral somatic nerves was measured by intracellular recordings. EPSPs with broad receptive fields and latencies which indicate polysynaptic connexions were commonly evoked from the FRA. In other cells, low threshold cutaneous afferents were effective at rather short latencies suggesting oligosynaptic connexions from fast ascending fibres. One example was found of EPSPs due to low threshold muscle afferents. IPSPs due to climging fibre activation of Purkinje cells as observed in most of the neurones were evoked by cutaneous volleys above 1.5-2.0T and muscle volleys above 5T (above 3-3.5T in case of Q). Often, IPSPs were evoked by stimulation of nerves, to the segmental level of which the the vestibulospinal neurone under investigation projected. A small proportion of cells received short latency IPSPs involving direct fast mossy fibre tracts, which were evoked from low threshold cutaneous afferents. IPSPs due to polysynaptic mossy fibre activation of Purkinje cells were evoked from the FRA bilaterally and from ipsilateral cutaneous afferents at 1.5-2.0T ("prolonged inhibition"). Prolonged excitatory/inhibitory events mediated by mossy fibre pathways may be involved in quadruped locomotion or other processes making use of a broad motor integration.     

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.     

Monosynaptic inhibition of neck motoneurons by the medial vestibular nucleus

Summary Stimulation of the brain stem in cats anesthetized with pentobarbital evoked short-latency IPSPs in many neck motoneurons. From the segmental delay of these IPSPs, and from comparison of their latencies with those of monosynaptic EPSPs evoked in the same motoneuron population by stimulation of the brain stem, it is concluded that the IPSPs are monosynaptic and are produced by descending inhibitory fibers.As many as thirteen electrodes were inserted into the medulla and pons to compare threshold stimuli required to evoke monosynaptic IPSPs from different locations. The points with the lowest threshold were in the medial vestibular nucleus and the medial longitudinal fasciculus. The IPSPs are apparently produced by fibers that originate in the medial vestibular nucleus and reach the upper cervical segments via the MLF.Electrical stimulation of the ipsilateral labyrinth often produces disynaptic IPSPs in neck motoneurons, very probably by means of a relay in the medial nucleus. This inhibitory pathway between labyrinth and neck motoneurons, together with the previously described excitatory pathway relaying in Deiters' nucleus, provides some of the pathways utilized by the labyrinth in regulation of head position.     

Supraspinal facilitation of cutaneous polysynaptic EPSPs in cat medial gastrocnemius motoneurons

Summary We examined the characteristics of postsynaptic potentials (PSPs) produced in antidromically-identified medial gastrocnemius (MG) -motoneurons by electrical stimulation of low threshold (< 3×T) distal limb cutaneous afferents in the sural (SUR) nerve in adult cats anesthetized with -chloralose, together with the effects on SUR PSPs of supraspinal conditioning stimulation of the contralateral red nucleus (RN) and pyramidal tract (PT). In the majority of MG motoneurons, SUR afferents with electrical thresholds < 1.5×T produced early excitatory synaptic potentials (EPSPs) with minimum central latency of about 2.0 ms, suggesting activation of a trisynaptic segmental pathway with two interposed interneurons. Such early EPSPs were often detectable with stimuli < 1.2×T, as determined by recording the compound action potential in the sciatic nerve and from the first appearance of the N₁ wave of the cord dorsum potential. Inhibitory synaptic potentials (IPSPs) were regularly produced by SUR volleys of only slightly greater strength (often as low as 1.3×T) and these had minimum central latencies of about 3.0 ms (about 1.0 ms longer than the earliest EPSPs), suggesting a three interneuron central pathway.Repetitive stimulation of RN and PT regularly produced facilitation of both EPSP and IPSP components in the SUR response, suggesting that these supraspinal systems directly or indirectly excite some of the same interneurons that convey the SUR effects to MG motoneurons. When using very low strength SUR stimuli, PT conditioning produced relatively pure facilitation of the SUR EPSPs but with larger SUR volleys, PT clearly facilitated both EPSPs and IPSPs. RN conditioning produced more parallel facilitation of SUR EPSPs and IPSPs. Supraspinal control of the polysynaptic pathway producing SUR EPSPs is of particular interest because of earlier evidence that this pathway is differentially distributed to motoneurons of fast twitch versus slow twitch MG motor units.Supported by USPHS Postdoctoral Fellowship 1F32NS 06131Supported by Muscular Dystrophy Society of America Post-doctoral FellowshipSupported by USPHS Postdoctoral Fellowship 1F32NS 05677     

Ia inhibitory interneurons and Renshaw cells as contributors to the spinal mechanisms of fictive locomotion

The activity of selected single alpha-motoneurons, Renshaw cells (RCs), and Ia inhibitory interneurons (IaINs) during fictive locomotion was recorded via microelectrodes in decerebrate (precollicular-postmammillary) cats in which fictive locomotion was induced by stimulation of the mesencephalic locomotor region. The interrelationships in the timing and frequency of discharge among these three interconnected cell types were determined by comparing their averaged step cycle firing histograms, which were normalized in reference to motoneuron activity recorded in ventral root filaments. Previous findings that RCs are rhythmically active during locomotion and discharge in phase with the motoneurons from which they are excited were confirmed, and further details of the phase relationships between RC and alpha-motoneuron activity during fictive locomotion were obtained. Flexor and extensor RCs became active after the onset of flexor and extensor motoneuron activity, respectively. Maximal activity in extensor RCs occurred at the end of the extension phase coincidental with the onset of hyperpolarization and a decrease in activity in extensor motoneurons. Maximal flexor RC activity occurred during middle to late flexion and was temporally related to the onset of reduced flexor motoneuron activity. The IaINs recorded in the present experiments were rhythmically active during fictive locomotion, as previously reported. The quadriceps IaINs were mainly active during the extension phase of the step cycle, along with extensor RCs. Thus the known inhibition of quadriceps IaINs by RCs coupled to quadriceps and other extensor motoneurons is obviously not sufficient to interfere with the appropriate phasing of IaIN activity and reciprocal inhibition during fictive locomotion, as had been speculated. Most of the quadriceps IaINs analyzed exhibited a decrease in discharge frequency at the end of the extension phase of the step cycle, which was coincidental with increased rates of firing in extensor RCs. These data are consistent with the possibility that extensor RCs contribute to the reduction in quadriceps IaIN discharge at the end of the extension phase of the step cycle. The possibility that IaIN rhythmicity during fictive locomotion arises from periodic inhibition, possibly from Renshaw cells, was tested by stimulating the reciprocal inhibitory pathway throughout the fictive step cycle. The amplitude of Ia inhibitory postsynaptic potentials (IPSPs) varied significantly throughout the fictive step cycle in 14 of the 17 motoneurons tested, and, in 11 of these 14 motoneurons, the Ia IPSPs were maximal during the phase of the step cycle in which the motoneuron was most     

Identification of excitatory interneurons contributing to generation of locomotion in lamprey: structure, pharmacology, and function

1. In the in vitro preparation of the lamprey spinal cord, paired intracellular recordings of membrane potential were used to identify interneurons producing excitatory postsynaptic potentials (EPSPs) on myotomal motoneurons. 2. Seventy-nine interneurons (8.4% of all neuron-motoneuron pairs tested) elicited unitary EPSPs that followed one-for-one at short, constant latencies and were therefore considered monosynaptic according to conventional criteria. Evidence was obtained for selectivity and divergence of excitatory interneuron (EIN) outputs and for convergence of EIN input to motoneurons. 3. The neurotransmitter released by EINs may be an excitatory amino acid such as glutamate, because the EPSPs were depressed by antagonists of excitatory amino acids. 4. Intracellular dye injection revealed that EINs have small cell bodies (average 11 x 27 microns), transversely oriented dendrites, and thin (less than 3 microns) slowly conducting axons (0.7 m/s) that project caudally and ipsilaterally. One EIN exhibited a system of thin multi-branching axon collaterals with periodic swellings. Ultrastructurally, these swellings contained clear spherical vesicles, and they apposed postsynaptic membrane specializations. 5. During fictive locomotion, the membrane-potential oscillations of EINs were greater in amplitude than, but similar in shape and timing to, those of their postsynaptic motoneurons. EINs fired action potentials during fictive locomotion and contributed to the depolarization of motoneurons. 6. These interneurons are proposed to be a source of excitation to motoneurons and interneurons in the lamprey spinal cord, participating in motor activity including locomotion.     

Synaptic actions of cutaneous A delta and C fibers on primate hindlimb alpha-motoneurons

Postsynaptic potentials evoked in hindlimb alpha-motoneurons by stimulation of a cutaneous nerve (sural) with finely graded stimulus strengths were analyzed in the primate, monitoring the spinal cord potentials and afferent nerve volleys in the sural nerve. It was observed that activities in A alpha beta, A delta and C fibers of the cutaneous nerve elicited characteristic excitatory and/or inhibitory postsynaptic potentials (EPSPs and/or IPSPs) with different latencies and durations in extensor and flexor motoneurons. Volleys in A delta fibers of the cutaneous nerve produced EPSPs in 57% of flexor and 31% of extensor motoneurons tested, whereas IPSPs were produced by A delta volleys in 41% of flexor and 62% of extensor motoneurons. EPSPs with longer latencies and longer durations were evoked by cutaneous C fiber volleys in 55% of flexor and 34% of extensor motoneurons, whereas IPSPs due to C volleys were recorded in 9% of flexor and 14% of extensor motoneurons. A alpha beta and A delta volleys caused motoneurons to fire in several instances, and some motoneurons discharged repetitively during the depolarizations evoked by activities in C fibers of the nerve. Central latency for transmission in interneuronal chains in the spinal cord was estimated from the onset of the cord potential (N3 wave) to the onset of the postsynaptic potential evoked by A delta volleys. Ranges of central latencies of the EPSPs and IPSPs evoked by A delta volleys were 2.0-7.0 ms and 3.5-8.5 ms, respectively. It is postulated that there may be at least two interneurons interposed in the excitatory reflex pathway from A delta afferent fibers to motoneurons and the A delta inhibitory pathway may involve longer interneuronal chains. In a few motoneurons, however, sural volleys with strengths sufficient to activate A delta fibers produced EPSPs with a central latency of about 1 ms, suggesting activation of a disynaptic segmental pathway with one interposed interneuron. Stimulation of the sural nerve with strengths sufficient to activate cutaneous C fibers produced slow negative cord dorsum potentials with long latencies. It is proposed that primate motoneurons, which show characteristic postsynaptic potentials evoked by cutaneous A delta and C fiber volleys, may provide a suitable model for analyzing the role of high threshold cutaneous afferent fibers not only in the flexor withdrawal reflex but also in motor control functions.     

Synaptic organization of tectal-facial pathways in cat. II. Synaptic potentials following midbrain tegmentum stimulation.

1. The organization of the synaptic pathways underlying midbrain tegmentum influence over the facial musculature was studied with the use of an acute electrophysiological approach in the cat. Under pentobarbital sodium anesthesia, synaptic potentials were recorded intracellularly in antidromically identified facial motoneurons following electrical stimulation of the paralemniscal zone. The cells of origin and the pathways responsible for the potentials evoked from the paralemniscal zone were defined with the use of retrograde transport of horseradish peroxidase (HRP). The putative role of the paralemniscal zone with regard to the production of disynaptic, tectally evoked potentials in facial motoneurons was investigated both by inactivating this nucleus with injections of lidocaine and by making acute brain stem lesions to sever the paralemniscal-facial and other afferent pathways. 2. Following paralemniscal stimulation, monosynaptic, excitatory postsynaptic potentials (EPSPs) with latencies ranging from 0.6 to 0.9 ms, steep rising phases, and amplitudes in excess of 4.0 mV were recorded in motoneurons of the temporal and auriculoposterior subdivisions, which supply the pinna muscles. Smaller amplitude EPSPs (less than 1.0 mV) with monosynaptic latencies were observed in the zygomatic subdivision. Polysynaptic EPSPs with latencies ranging from 1.0 to 1.8 ms were also observed in all three of these subdivisions. However, only long-latency EPSPs, arriving at 2.0 ms or later, were present in ventral subdivision motoneurons. 3. Inhibitory postsynaptic potentials (IPSPs) were also frequently recorded in facial motoneurons after paralemniscal stimulation. Monosynaptic IPSPs with latencies ranging from 0.8 to 1.2 ms and amplitudes in excess of 4.0 mV were recorded in facial motoneurons of the temporozygomatic and auriculoposterior subdivisions, as were polysynaptic IPSPs with latencies ranging from 1.2 to 1.8 ms. IPSPs were sometimes observed in combination with a smaller, shorter latency EPSPs. Only long-latency IPSPs of greater than 2.0 ms were recorded in ventral subdivision motoneurons. In all cases, both the EPSPs and the IPSPs were graded in character and could be augmented by multiple stimuli. 4. The contralateral paralemniscal zone and the supraoculomotor area, bilaterally, represented the two most prominent afferent sources labeled after HRP injection of the facial nucleus. The superior colliculus and numerous reticular formation regions were also identified as facial nucleus afferents by the presence of retrogradely labeled cells. The retrogradely labeled cells in the paralemniscal zone exhibited heterogeneous soma size. HRP-labeled axons of the paralemniscal-facial pathway were observed to cross the midline by traveling ventral to the brachium conjunctivum in the caudal mesencephalon.(ABSTRACT TRUNCATED AT 400 WORDS)     

The activity of spinal commissural interneurons during fictive locomotion in the lamprey

Commissural interneurons in the lamprey coordinate activity of the hemisegmental oscillators to ensure proper left-right alternation during swimming. The activity of interneuronal axons at the ventral commissure was studied together with potential target motoneurons during fictive locomotion in the isolated lamprey spinal cord. To estimate the unperturbed activity of the interneurons, axonal recordings were chosen because soma recordings inevitably will affect the level of membrane depolarization and thereby spike initiation. Of 227 commissural axons recorded during locomotor activity, 14 produced inhibitory and 3 produced excitatory postsynaptic potentials (PSPs) in target motoneurons. The axons typically fired multiple spikes per locomotor cycle, with approximately 10 Hz sustained frequency. The average shortest spike interval in a burst corresponded to an instantaneous frequency of approximately 50 Hz for both the excitatory and inhibitory axons. The maximum number of spikes per locomotor cycle was inversely related to the locomotor frequency, in accordance with previous observations in the spinal hemicord preparation. In axons that fired multiple spikes per cycle, the mean interspike intervals were in the range in which the amplitude of the slow afterhyperpolarization (sAHP) is large, providing further support for the role of the sAHP in spike timing. One hundred ninety-five axons (86%) fired rhythmically during fictive locomotion, with preferred phase of firing distributed over either the segmental locomotor burst phase (40% of axons) or the transitional phase (between bursts; 60%). Thus in lamprey commissural interneurons, we found a broad distribution of firing rates and phases during fictive locomotion.     

An ascending spinal pathway transmitting a central rhythmic pattern to the magnocellular red nucleus in the cat

The activity of cells in the magnocellular red nucleus (RNm) was recorded extra and intracellularly in the curarized thalamic cat performing fictive locomotion. The locomoter episodes were detected from the rhythmic activity recorded in the motor nerves of the contralateral hindlimb. It was confirmed that, during fictive locomotion, a large proportion of the rubrospinal cells (56% in our sample) exhibit a rhythmic pattern of activity which is synchronized with the efferent spinal motor nerve activity. On the basis of the intracellular recordings it was established that phases of intense synaptic activity with mixed excitatory postsynaptic potentials (EPSPs) and inhibitory postsynaptic potentials (IPSPs) are involved in this rhythmicity. After eliminating the cerebellar input to the RNm, it was observed that the cells still received intense excitatory and inhibitory inputs, resulting in a continuous modulation of their membrane potential, due to the occurrence of EPSPs and IPSPs. During fictive locomotor like activity and after elimination of the cerebellar afferents to the RNm, it was observed that the spontaneous PSPs in RNm cells (in the case of 45% of the cells) were organized in repetitive subthreshold bursts occurring in phase relationships with the activity recorded in the motor nerves. Some extracellularly recorded cells (12%) showed a rhythmic firing pattern. It is generally recognized that, in the thalamic cat preparation, the locomotor pattern observed in efferent nerves originates from the central pattern generator (CPG) of the spinal cord. It therefore seems likely that the rhythmicity observed here in the RNm may originate from the spinal CPG and be transmitted through the spino rubral pathway ascending in the ventral part of the cord. It is concluded that the spino rubral pathway may transmit both somatosensory information and corollary discharges relating to the activity of the spinal CPG for locomotion.     

Postsynaptic potentials in the hypoglossal motoneurons set up by hypoglossal nerve stimulation.

In nembutalized cats intracellular potentials were recorded from hypoglossal motoneurons innervating either protruder or retractor muscles of the tonge (protruder and retractor motoneurons: P-Mns and R-Mns). Responses to stimulation of the hypoglossal nerve were explored and found to consist of an antidromic spike followed by an afterhyperpolarization (AHP) and a postsynaptic potential (PSP). When hypoglossal nerve stimulation was made with an intensity three times as large as the threshold for the hypoglossal motor fibers, the PSPs became evident under blockage of soma-dendritic invasion of the antidromic spike. In most of P-Mns or R-Mns, the PSPs were IPSPs, independent of the side of peripheral stimulation. The latencies were about 12 msec. Even when the cell membrane was hyperpolarized by injecting a hyperpolarizing current of up to 16 nA, the reversal point of the IPSP was difficult to find. In a small fraction of hypoglossal motoneurons the PSPs to hypoglossal nerve stimulation were EPSPs with latencies of 10 to 12 msec.