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.     

Evidence for restricted central convergence of cutaneous afferents on an excitatory reflex pathway to medial gastrocnemius motoneurons

1. We previously reported that excitatory postsynaptic potentials (EPSPs) produced by low-threshold electrical stimulation of the caudal cutaneous sural nerve (CCS) occur preferentially and with the shortest central latencies in the medial gastrocnemius (MG) portion of the triceps surae motor nuclei. The present study employs the spatial facilitation technique to assess interneuronal convergence on the short-latency excitatory pathway from CCS to MG by several other ipsilateral hindlimb afferents [the lateral cutaneous sural (LCS), caudal cutaneous femoral (CCF), saphenous (SAPH), superficial peroneal (SP), posterior tibial (TIB), and posterior articular (Joint) nerves]. 2. Spatial facilitation of CCF EPSPs in MG motoneurons was demonstrated with conditioning stimulation of the LCS, CCF, SAPH, SP, and TIB nerves, but was most readily and consistently observed with CCF conditioning. Facilitation of CCS and CCF EPSPs was obtained in individual MG motoneurons with a wide range of condition-test intervals. 3. CCF EPSPs in MG motoneurons produced by twice threshold (2T) afferent stimulation had a mean latency of 4.8 ms and often appeared as slowly rising, asynchronous potentials. On the other hand, 2T CCS EPSPs had a mean latency of 2.8 ms and appeared as sharper rising, less variable depolarizations. The optimum condition-test interval for facilitation of CCS and CCF EPSPs was found to be 5.2 ms on average, with CCS stimulation delayed from that of CCF. The longer latency of CCF EPSPs and the finding that the minimum condition-test interval was on the order of 3.9 ms suggests that convergence occurs late in the excitatory CCF pathway to MG motoneurons. 4. Convergence between excitatory pathways to MG from CCF and CCS afferents is discussed with regard to the original observations of Hagbarth on the location of cutaneous receptive fields and excitation of ankle extensors. In addition, evidence for the segregation of these specialized reflex pathways from those involved in general flexion reflexes is discussed.     

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.     

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.     

Effects on peroneal motoneurons of cutaneous afferents activated by mechanical or electrical stimulations

The postsynaptic potentials elicited in peroneal motoneurons by either mechanical stimulation of cutaneous areas innervated by the superficial peroneal nerve (SP) or repetitive electrical stimulation of SP were compared in anesthetized cats. After denervation of the foot sparing only the territory of SP terminal branches, reproducible mechanical stimulations were applied by pressure on the plantar surface of the toes via a plastic disk attached to a servo-length device, causing a mild compression of toes. This stimulus evoked small but consistent postsynaptic potentials in every peroneal motoneuron. Weak stimuli elicited only excitatory postsynaptic potentials (EPSPs), whereas increase in stimulation strength allowed distinction of three patterns of response. In about one half of the sample, mechanical stimulation or trains of 20/s electric pulses at strengths up to six times the threshold of the most excitable fibers in the nerve evoked only EPSPs. Responses to electrical stimulation appeared with 3-7 ms central latencies, suggesting oligosynaptic pathways. In another, smaller fraction of the sample, inhibitory postsynaptic potentials (IPSPs) appeared with an increase of stimulation strength, and the last fraction showed a mixed pattern of excitation and inhibition. In 24 of 32 motoneurons where electrical and mechanical effects could be compared, the responses were similar, and in 6 others, they changed from pure excitation on mechanical stimulation to mixed on electrical stimulation. With both kinds of stimulation, stronger stimulations were required to evoke inhibitory postsynaptic potentials (IPSPs), which appeared at longer central latencies than EPSPs, indicating longer interneuronal pathways. The similarity of responses to mechanical and electrical stimulation in a majority of peroneal motoneurons suggests that the effects of commonly used electrical stimulation are good predictors of the responses of peroneal motoneurons to natural skin stimulation. The different types of responses to cutaneous afferents from SP territory reflect a complex connectivity allowing modulations of cutaneous reflex responses in various postures and gaits.     

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.     

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.     

Low-threshold,short-latency cutaneous reflexes during fictive locomotion in the “semi-chronic” spinal cat

Summary Low-threshold, short-latency cutaneous reflexes evoked in ipsilateral hindlimb motor nerves were examined during fictive locomotion. Locomotion in 11 anaemically decerebrated spinal animals (1–3 weeks after transection at T13-L1) was induced by administration of clonidine, l-dopa and nialamide; by administration of the latter two drugs only; or by exteroceptive stimulation in the absence of any drugs. The caudal and lateral cutaneous sural, caudal cutaneous femoral, saphenous and superficial peroneal nerves were stimulated at low threshold (1.5–3 T). Pooled results from all combinations of cutaneous nerves stimulated and muscle nerves recorded show that the initial response was excitatory in 40 of 50 triceps surae and 17 of 20 semitendinosus (St) electroneurograms (ENGs). These excitatory responses occurred at latencies that ranged from 5 to 15 ms and tended to be maximal during the motor nerve's active period in the step cycle (i.e. they were modulated in a phase-dependent manner). Only three inhibitory responses (9–12 ms earliest latency) were encountered in total: in two St ENGs of one animal and in one lateral gastrocnemius-soleus ENG of a different animal. In two animals a second excitatory response (15–25 ms latency) was sometimes recorded in triceps surae and St nerves and, interestingly, could be modulated out of phase with the early response. Weak short-latency excitatory reflexes were also found in contralateral St ENGs when examined. Finally, among medial gastrocnemius, lateral gastrocnemius and soleus nerves, excitatory responses due to stimulation of any particular cutaneous nerve tended to be modulated similarly but were of consistently different amplitude among the three. This finding, together with the general observation that excitatory reflexes produced by stimulation of a particular cutaneous nerve were modulated similarly in extensors (or flexors) of different animals, suggests that spinal circuits generating locomotion may indeed exert a stereotypic control over interneurons in specific cutaneous reflex pathways to motoneurons. The results are primarily discussed in terms of the existing evidence for short-latency excitatory cutaneous reflexes in extensors in a variety of locomotive and non-locomotive preparations.     

Direct excitation of neck motoneurons by interstitiospinal fibers

1. Responses of neck motoneurons to stimulation of the interstitial nucleus of cajal (INC) were recorded intracellularly in cats under chloralose anesthesia. When stimuli were applied within or close to the INC, short latency, monosynaptic excitatory postsynaptic potentials (EPSPs) were evoked in many neck motoneurons. Such EPSPs were not evoked by stimulating mesencephalic regions outside the INC. 2. Stimulation of the ipsilateral INC produced monosynaptic EPSPs consistently in biventer cervicis-complexus (BCC) motoneurons, while such EPSPs were observed in about two thirds of the splenius (SP) motoneurons and half of the trapezius (TR) motoneurons tested. Stimulation of the contralateral INC produced weak monosynaptic EPSPs in about half the BCC motoneurons and in a few SP and TR motoneurons. All types of motoneurons also received longer latency, apparently polysynaptic, PSPs from both INCs. In BCC and TR motoneurons these were mainly EPSPs, in SP, mixed excitatory and inhibitory PSPs. 3. Monosynaptic EPSPs evoked by INC stimulation were not eliminated by acute and chronic parasagittal and transverse lesions placed to interrupt the bifurcating axons of all vestibulospinal and many reticulospinal neurons. No significant collision was observed between EPSPs evoked by INC and vestibular or reticular stimulation. The EPSPs evoked by stimulation of the INC therefore appear to have been produced by activation of interstitiospinal neurons rather than by an axon reflex mechanism. 4. The properties of a number of interstitiospinal neurons were observed while recording extracellularly from the mesencephalon to map the location of the INC. One third of the interstitiospinal neurons activated antidromically from the C4 segment could also be activated antidromically from L1. These lumbar-projecting neurons had conduction velocities ranging from 15--123 m/s. Several interstitiospinal neurons sending axons to the ventral horn of the neck segments were identified and two of these were found to be branching neurons that projected both to the neck and to lower levels of the spinal cord.     

A differential synaptic input to the motor nuclei of triceps surae from the caudal and lateral cutaneous sural nerves

1. Postsynaptic potentials (PSPs) were recorded in 115 triceps surae motoneurons of 10 chloralose-anesthetized adult cats (spinal cord intact), upon electrical stimulation of the caudal and lateral cutaneous sural nerve branches (CCS and LCS, respectively). 2. With twice threshold (2T) stimulation of CCS, excitatory PSPs (EPSPs) were the predominant effect in 95% of all medial gastrocnemius (MG) motoneurons tested (min. central latency 1.5 ms; mean 2.4 ms). In only a few MG cells was the EPSP followed by an inhibitory postsynaptic potential (IPSP) and in only one cell was an IPSP the sole effect. Increasing the stimulus intensity to 5T tended to enhance both the later EPSP and IPSP components, with less change in the amplitude or latency of the earliest EPSPs. 3. In lateral gastrocnemius (LG) and soleus (SOL) motoneurons, 2T CCS stimulation led to either inhibition or no potential change in the majority of cells tested: EPSPs were the predominant effect in only 15 and 30% of LG and SOL cells, respectively (min. central latency 2.5 ms; mean 3.0 ms) and rarely occurred without subsequent inhibition. Again, increasing the stimulus intensity to 5T had more of an effect on later rather than earlier PSP components. 4. A predominance of depolarization in MG motoneurons but not in SOL motoneurons is in agreement with previous findings that CCS excitation is more powerful in "fast type" triceps surae motoneurons. However, the strong predominance of hyperpolarizing effects of CCS stimulation in the present LG population is evidence that such an organization does not transcend triceps surae motor nuclei as a whole. 5. Postsynaptic effects of LCS stimulation at 2T were frequently weak or absent but increasing the stimulus intensity to 5T produced predominant inhibition in 71% of all triceps surae motoneurons studied (n = 107). Of the few cells which did receive excitation from this nerve, most were MG, a few were SOL, and none were LG. These EPSPs occurred more frequently at 5T than at lower stimulation strengths. 6. The results indicate that excitation produced by electrical stimulation of the ipsilateral CCS nerve occurs preferentially in the MG portion of triceps surae and with the shortest central latencies. Effects of LCS stimulation are largely inhibitory throughout the motor nuclei comprising triceps surae but even here, the presence of excitation occurs more frequently in MG. A comparison of these results with those in other reports is discussed.     

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.     

Cooperation of muscle and cutaneous afferents in the feedback of contraction to peroneal motoneurons

Peroneal motoneurons were recorded intracellularly in anesthetized cats during sustained submaximal contractions of peroneus brevis muscle (PB) elicited by repetitive electrical stimulation of motor axons in the distal portion of cut ventral root filaments. Mechanical stimulation of the territory innervated by the superficial peroneal nerve (SP) was applied during contraction to assess the influence of afferents from this territory on the contraction-induced excitation of motoneurons. In 21 peroneal motoneurons in which PB contraction evoked excitatory potentials, a stimulation engaging mechanoreceptors located in the skin around toes was found to either enhance (in 12 motoneurons) or reduce (in 9 motoneurons) the contraction-induced excitatory potentials. Among positive effects, six showed simple summation of the responses to each individual stimulus, suggesting a convergence of afferent pathways on motoneurons. In six other motoneurons, complex interactions were observed, as may result from convergence at a premotoneuronal level. Among negative effects, a single instance was observed of inhibitory facilitation, as may result from convergence of cutaneous and muscular, possibly Ib, afferents on inhibitory interneurons. Several pathways, mediating either facilitory or inhibitory influences, are available for cooperation of muscle and cutaneous input, allowing flexibility of motoneuron activation in different tasks.     

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.     

Synaptic linkage in the vestibulo-ocular and cerebello-vestibular pathways to the VIth nucleus in the rabbit

Summary Intra- and extra-cellular responses were recorded with glass microelectrodes from motoneurons in the VIth cranial nuclei of anesthesized rabbits. VIth nucleus motoneurons were identified by their antidromic activation from the VIth nerve. In these motoneurons stimulation of the ipsilateral VIIIth nerve produced IPSPs with disynaptic latencies (mean and S.D., 1.08 ± 0.1 msec) while stimulation of the contralateral VIIIth nerve produced EPSPs with disynaptic latencies (mean and S.D., 1.20 ± 0.18 msec). Correspondingly, direct stimulation of the ipsilateral medial vestibular nucleus (MV), produced IPSPs with monosynaptic latencies (mean and S.D., 0.61±0.15 msec) while direct stimulation of the contralateral MV produced EPSPs with monosynaptic latencies (mean and S.D., 0.61±0.09 msec). Further, with the recording electrode placed within the VIth nucleus to observe the extracellular potentials corresponding to the intracellularly recorded IPSPs and EPSPs, the medulla was systematically tracked with a monopolar stimulating electrode. It was demonstrated that the inhibitory relay cells could be effectively stimulated in the rostral half of the ipsilateral MV and the excitatory relay cells in the rostral half of the contralateral MV.Pharmacological investigation suggested that the inhibitory transmitter involved in the vestibular inhibition is gamma amino-butyric acid or a related substance.Electric stimulation of the flocculus produced a prominant depression in the inhibitory vestibulo-ocular reflex pathway to the VIth nucleus, while the excitatory pathway was free of any similar flocculus inhibition.     

Direct projections from vestibular nuclei to facial nucleus in cats

Postsynaptic potentials were recorded from motoneurons in the facial nucleus in response to stimulation of the vestibular and trigeminal nerves. The motoneurons were identified by antidromic activation from their peripheral axons. Disynaptic excitatory and inhibitory postsynaptic potentials (EPSPs and IPSPs) and mixed EPSP/IPSPs were recorded in response to vestibular nerve stimulation, ranging in latency from 0.9 to 2.1 ms, with most at 1.5 ms. Activity in secondary vestibular axons recorded within the facial nucleus occurred at a latency of 0.7-1.1 ms. The amplitudes of the vestibular postsynaptic potentials were small, generally less than a millivolt, but double shocks produced marked summation. The average time to peak of ipsilateral vestibular EPSPs, 1.1 ms, was faster than that of either ipsilateral IPSPs, 1.6 ms, or contralateral EPSPs, 1.4 ms. The double-spiked vestibular activity was detectable in double-peaked PSPs. Disynaptic EPSPs, ranging in latency from 2.0 to 3.0 ms, were recorded in response to trigeminal nerve stimulation. The average time to peak was 1.3 ms. The multiple-spiked activity of the trigeminal neurons was detectable in multipeaked EPSPs. Inhibitory ipsilateral effects (Vi IPSPs) were recorded twice as often as excitatory ipsilateral effects (Vi EPSPs), being found in 29% versus 15% of the motoneurons. Contralateral effects were found in 13% of the motoneurons studied, and almost all were excitatory. Analysis of synaptic potential shapes suggested that the excitatory and inhibitory vestibular synapses probably contact distal dendrites preferentially, with the excitatory connections being somewhat closer to the soma. The trigeminal inputs probably contact the facial motoneurons more extensively near the soma. Horseradish peroxidase was injected into the facial nucleus, and retrograde uptake by vestibular neurons was studied. The majority of filled vestibular neurons was ipsilateral to the injection site, especially in the medial vestibular nucleus, ventral y group, and supravestibular nucleus. On the contralateral side, filled vestibular cells were found almost exclusively in the medial nucleus. Filled cells were also noted in the trigeminal nucleus, predominantly ipsilaterally at all rostrocaudal levels. We have demonstrated monosynaptic projections to facial motoneurons from both vestibular and trigeminal nuclei. The trigeminal input is likely to be involved in facial reflexes, especially blinking and grimacing. The afferent vestibular population overlaps that going to the oculomotor and cervical motoneurons; these projections may be collaterals of single vestibular neurons.4+.     

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     

Synaptic inhibition of cat phrenic motoneurons by internal intercostal nerve stimulation.

Intracellular recordings from 65 phrenic motoneurons (PMNs) in the C5 segment and recordings of C5 phrenic nerve activity were made in 27 pentobarbitone-anesthetized, paralyzed, and artificially ventilated adult cats. Inhibition of phrenic nerve activity and PMN membrane potential hyperpolarization (48/55 PMNs tested) was seen after stimulation of the internal intercostal nerve (IIN) at a mean latency to onset of 10.3 +/- 2.7 ms. Reversal of IIN-evoked hyperpolarization (n = 14) by injection of negative current or diffusion of chloride ions occurred in six cases, and the hyperpolarization was reduced in seven others. Stimulation of the IIN thus activates chloride-dependent inhibitory synaptic inputs to most PMNs. The inhibitory phrenic nerve response to IIN stimulation was reduced by ipsilateral transection of the lateral white matter at the C3 level and was converted to an excitatory response by complete ipsilateral cord hemisection at the same level. After complete ipsilateral hemisection of the spinal cord at C3 level, stimulation of the IIN evoked both excitatory and inhibitory postsynaptic potentials (EPSPs and IPSPs) in PMNs (n = 10). It was concluded that IIN stimulation can evoke both excitatory and inhibitory responses in PMNs using purely spinal circuitry, but that excitatory responses are normally suppressed by a descending pathway in intact animals. Fifteen PMNs were tested for possible presynaptic convergence of inputs in these reflex pathways, using test and conditioning stimuli. Significant enhancement (>20%) of IPSPs were seen in seven of eight IIN-evoked responses using pericruciate sensorimotor cortex (SMC) conditioning stimuli, but only one of five IIN-evoked responses were enhanced by superior laryngeal nerve (SLN) conditioning stimuli. The IIN-evoked IPSP was enhanced in one of two motoneurons by stimulation of the contralateral phrenic nerve. It was concluded that presynaptic interneurons were shared by the IIN and SMC pathways, but uncommonly by other pathways. These results indicate that PMNs receive inhibitory synaptic inputs from ascending thoracocervical pathways and from spinal interneurons. These inhibitory reflex pathways activated by afferent inputs from the chest wall may play a significant role in the control of PMN discharge, in parallel with disfacilitation following reduced activity in bulbospinal neurons projecting to PMNs.     

Functional organization of vestibular and visual inputs to neck and forelimb motoneurons in the frog.

1. Intracellular responses in neck and forelimb motoneurons to electrical stimulation of the vestibular nerve, the optic tectum, and the optic nerve were studied in frog. 2. Stimulation of the anterior branch of the vestibular nerve typically produced EPSPs, bilaterally, in neck, shoulder (DOR), and forelimb extensor (TRI, RAD) motoneurons, and bilateral IPSPs in forelimb adductor (PED) and flexor (ULN, COR) motoneurons. 3. Latencies of PSPs recorded in neck, shoulder, and proximal extensor motoneurons (TRI) were mostly in the disynaptic range, whereas many of those recorded in distal extensor (RAD) and in adductor and flexor motoneurons involved three synapses. 4. Lesion of the vestibulospinal fibers greatly reduced the vestibular nerve-evoked field potentials in the spinal cord and the occurrence of PSPs in forelimb motoneurons. These results as well as the latency measurements suggest that the pathway linking vestibular nerve and forelimb motoneurons mainly consists of vestibulospinal fibers, though involvement of other structures for production of later PSPs could not be completely ruled out. Hemisection of the brain stem at its most caudal level showed that the pathway to the contralateral motoneurons crosses at the level of brain stem as well as in the spinal cord. 5. Stimulation of the optic tectum produced EPSPs, IPSPs, and a mixture of EPSPs and IPSPs in neck, shoulder, and forelimb motoneurons, bilaterally. Most frequently, a combination of an excitation and inhibition was observed. The pathway from the optic tectum to neck and limb motoneurons is at least dysnaptic in nature. 6. Stimulation of the optic nerve produced IPSPs and a mixture of EPSPs and IPSPs in neck and forelimb motoneurons. Impulses originating from the optic nerve descend as far as to lumbar motoneurons producing EPSP-IPSP sequences bilaterally. 7. Interaction studies suggested that the vestibular and optic pathways to neck and forelimb motoneurons are separate from each other so that the site of integration of vestibular and visual input occurs at the level of motoneurons. 8. Evidence for electronic coupling among forelimb motoneurons and electrical synaptic transmission in th pathway linking vestibular nerve and forelimb motoneurons is presented.     

Rescue of motoneurons from the axotomized state by regeneration into a sensory nerve in cats.

1. We studied the electrical properties of spinal motoneurons, the axons of which had regenerated into a cutaneous nerve. 2. In cats, all or part of the medial gastrocnemius (MG) muscle nerve was cut and directed distally into the caudal cutaneous sural (CCS) nerve, a sensory (primarily cutaneous) nerve. One or 2 yr later, electrical properties [conduction velocity (CV), rheobase (Irh), input resistance (RN), afterhyperpolarization (AHP), and excitatory postsynaptic potentials (EPSPs)] of MG motoneurons that had cross-regenerated into the CCS nerve were determined. These were compared with properties of normal and of axotomized MG motoneurons and with data from previous studies in which MG motoneurons had reinnervated their own or a foreign muscle. 3. Electrical stimulation of the MG-innervated CCS nerve produced no detected mechanical activity, indicating an absence of muscle innervation. Tactile stimulation of skin did not activate these motoneurons; i.e., they did not acquire properties of cutaneous afferents. 4. The CV and Irh of MG motoneurons axotomized 11 mo declined by 48 and 60%, respectively. 5. The CV of MG motoneurons that had regenerated through CCS was only slightly slower than normal, similar to that of MG motoneurons that reinnervated the "slow" muscle soleus (Foehring and Munson 1990). 6. The Irh and RN were also similar to those of MG motoneurons that had regenerated into the soleus muscle. 7. Electrical stimulation of the lateral gastrocnemius-soleus nerve generated EPSPs of normal or almost normal amplitude in MG motoneurons axotomized for 11 mo or cross-regenerated into CCS up to 2 yr.(ABSTRACT TRUNCATED AT 250 WORDS)     

Supraspinal control of a short-latency cutaneous pathway to hindlimb motoneurons

Summary The effects of two supraspinal systems on transmission through a short latency hindlimb cutaneous reflex pathway were studied in cats anesthetized with pentobarbital or -chloralose. Fleshman et al. (1984) described a mixed excitatoryinhibitory input from low threshold superficial peroneal (SP) afferents to flexor digitorum longus (FDL) motoneurons with central latencies so short as to suggest a disynaptic component in the initial excitatory phase of the PSP. In the present study, conditioning stimulation of either the red nucleus (RN) or the pyramidal tract (PT) caused a marked decrease in latency and increase in amplitude of both the excitatory and inhibitory components of the SP PSP in FDL motoneurons and several other motoneuron species. The minimal central latencies of the conditioned initial excitatory phase of the PSPs were on the order of 1.5 ms, consistent with the possibility of a disynaptic linkage. The facilitatory effects of RN and PT conditioning were observed in both anesthetic conditions, although preparation-specific differences in latency were observed. Lesion experiments suggested that the interneurons involved in this pathway are located caudal to the L5 segment, most likely in segments L6 and L7.