Projections of pyramidal tract cells to alpha-motoneurones innervating hind-limb muscles in the monkey.

1. We have investigated the spatial organization of monosynaptic corticospinal projections to hind-limb motoneurones, using near threshold stimulation of the surface of the precentral gyrus to activate pyramidal tract (PT) cells and intracellular recording from motoneurones to detect the resulting e.p.s.p.s. 2. Monosynaptic e.p.s.p.s. of cortical origin were seen in all motoneurone species investigated, those of distal as well as of proximal hind-limb muscles. The proportion of motoneurones in which the e.s.p.s. were evoked and the amplitudes of the latter indicated a more extensive cortical projection to motor nuclei for distal than for proximal muscles, as previously found for forelimb motoneurones. 3. Cortical areas from which monosynaptic e.p.s.p.s. were evoked in individual motoneurones were remarkably large, most often between 3 and 7 mm2. Several motoneurones appeared to have two or three separate areas within the hind-limb division of the motor cortex. 4. Areas of location of pyramidal tract cells projecting to various motoneurones innervating one muscle were usually not identical. They overlapped often only partially or did not overlap at all. 5. Areas of location of pyramidal tract cells projecting to motor nuclei for different muscles often showed an extensive overlap. When it occurred, various motoneurones of a given motor nucleus had common cortical projection areas with motoneurones of other motor nuclei, either to synergistic or to antagonistic muscles. Our results give further evidence for overlapping of areas of cortical projections to motoneurones and speak against a mosaic-like organization of pyramidal tract cells projecting to different motor nuclei. 6. The rise times of cortically evoked e.p.s.p.s. indicate that the corticospinal tract fibres terminate on motoneurones at approximately similar distances from the soma as group Ia afferents. The small amplitudes of the majority of e.p.s.p.s. evoked by near threshold cortical stimulation therefore suggest that unitary e.p.s.p.s of cortical origin are small and that the density of pyramidal tract cells projecting to individual motoneurones is usually low, even in the centrum of projection areas. 7. Effects of intracortical stimulation depended on the stimulus strength. With currents of 2-3 muA, e.p.s.p.s were usually evoked in one motoneurone species or in close synergists. With currents of 5-10 muA, largest e.p.s.p.s a number of other motoneurones. Latencies of descending volleys in the lumbar corticospinal tract indicated that intracortical stimuli activated pyramidal tract cells indirectly; the effects of these stimuli could thus not be used to indicate the location of pyramidal tract cells responsible for them.     

Integration in descending motor pathways controlling the forelimb in the cat

A further analysis has been made of inhibitory pathways to motoneurones via C3-C4 propriospinal neurones (PNs). Intracellular recording was made from triceps brachi motoneurones and effects from higher centres and forelimb afferents on corticospinal IPSPs were investigated after transection of the corticospinal tract at the C5/C6 border. The shortest latencies of the IPSPs evoked by stimulation of the pyramid were as brief as those of the pyramidal EPSPs (Illert et al. 1977). It is postulated that the minimal linkage of the pyramidal IPSPs is disynaptic via inhibitory C3-C4 PNs projecting directly to motoneurones. It was confirmed that pyramidal IPSPs usually are depressed by volleys in forelimb motor axon collaterals (Illert and Tanaka 1978). A quantitative comparison was made of the recurrent depression of pyramidal IPSPs and of IPSPs caused by activation of the Ia inhibitory interneurones. The result support the hypothesis of two parallel inhibitory cortico-motoneuronal pathways via C3-C4 PNs, one disynaptic via the inhibitory PNs and the other trisynaptic via excitatory PNs and Ia inhibitory interneurones. Pyramidal volleys also evoked late IPSPs which in some cases were not depressed from forelimb motor axon collaterals. It is postulated that the late IPSPs are partly due to activation of inhibitory C3-C4 PNs. Disynaptic pyramidal IPSPs were effectively facilitated by volleys in rubro-, tecto- and reticulospinal fibres - but not from vestibulospinal fibres - showing a convergence from the former descending tracts on common inhibitory C3-C4 PNs. Projection from forelimb afferents and corticospinal fibres on common inhibitory C3-C4 PNs was revealed by strong facilitation of disynaptic pyramidal IPSPs from cutaneous forelimb afferents. No corresponding effect was evoked from C2 neck afferents. Stimulation in the lateral reticular nucleus (LRN) evoked monosynaptic IPSPs in some motoneurones. The results of threshold mapping in and around the LRN suggest that the IPSPs are caused by antidromic stimulation of ascending collaterals of inhibitory neurones also projecting to motoneurones, possibly the inhibitory C3-C4 PNs.     

Premotor interneurones contributing to actions of feline pyramidal tract neurones on ipsilateral hindlimb motoneurones

The aim of the study was to analyse the potential contribution of excitatory and inhibitory premotor interneurones in reflex pathways from muscle afferents to actions of pyramidal tract (PT) neurones on ipsilateral hindlimb motoneurones. Disynaptic EPSPs and IPSPs evoked in motoneurones in deeply anaesthetized cats by group Ia, Ib and II muscle afferents were found to be facilitated by stimulation of the ipsilateral, as well as of contralateral, PT. The ipsilateral actions were evoked by either uncrossed or double-crossed pathways. The results show that interneurones mediating reflex actions of muscle afferents may be activated strongly enough by PT stimulation to contribute to movements initiated by ipsilateral PT neurones and that PT actions relayed by them might be enhanced by muscle stretches and/or contractions. However, in some motoneurones disynaptic IPSPs and EPSPs evoked from group Ib or II afferents were depressed by PT stimulation. In order to analyse the basis of this depression, the transmitter content in terminals of 11 intracellularly labelled interneurones excited by PT stimulation was defined immunohistochemically and their axonal projections were reconstructed. The interneurones included 9 glycinergic and 2 glutamatergic neurones. All but one of these neurones were mono- or disynaptically excited by group I and/or II afferents. Several projected to motor nuclei and formed contacts with motoneurones. However, all had terminal projections to areas outside the motor nuclei. Therefore both inhibitory and excitatory interneurones could modulate responses of other premotor interneurones in parallel with direct actions on motoneurones.     

Effects from the vestibulospinal tract on transmission from primary afferents to ventral spino-cerebellar tract neurones.

Convergence of vestibulospinal and segmental effects onto spinal interneurones which project to the ventral spino-cerebellar tract (VSCT) neurones has been studied by intracellular recording in VSCT cells. The disynaptic Ia IPSPs evoked in a group of VSCT neurones from the quadriceps nerve are monosynaptically facilitated by the vestibulospinal tract while there was no facilitation of Ia IPSP evoked from a flexor nerve. These results support the view that Ia inhibition to VSCT cells and motoneurones is mediated by common interneurones. The disynaptic inhibition evoked in other VSCT cells from the vestibulospinal tract is facilitated by volleys in the contralateral flexor reflex afferents (FRA) or bilaterally from the FRA. It is postulated that these actions are mediated by collaterals of the interneurones responsible for the analogous effects in motoneurones. Findings are reported suggesting that the monosynaptic vestibulospinal EPSP in VSCT cells in most cases is collateral to the excitatory input to the last order interneurones of reflex pathways from the FRA to motoneurones and only exceptionally to the corresponding input to Ia inhibitory interneurones. In many VSCT cells the vestibulospinal tract evoked disynaptic EPSPs which are facilitated from the FRA; the functional significance of this action is uncertain. The results are consistent with the hypothesis that VSCT neurones signal information on interneuronal transmission to motoneurones.     

Recurrent inhibition of interneurones monosynaptically activated from group Ia afferents

1. Interneurones monosynaptically excited from large muscle spindle (Ia) afferents and inhibited from motor axon collaterals were searched for in the lumbar spinal cord of the cat.2. Monosynaptic Ia excitation was found in sixty-seven of sixty-nine interneurones inhibited by antidromic volleys. These interneurones were excited from Ia afferents from one or a few muscles (mainly close synergists). Volleys in high threshold muscle and skin afferents (FRA) evoked polysynaptic excitation or inhibition. Weak inhibition from Ia afferents (from antagonists to those giving Ia excitation) was seen in a few cells. Monosynaptic excitation was evoked from the ventral quadrant of the spinal cord and polysynaptic excitation from the dorsal quadrant.3. Inhibition from motor axon collaterals was evoked with a latency (1.2-2.0 msec) suggesting a disynaptic linkage and had the same time course as in motoneurones. It prevented synaptic activation of 60% of interneurones and decreased the firing index and delayed generation of spikes in the remaining.4. The interneurones with convergence of monosynaptic Ia excitation and inhibition from motor axon collaterals were found in the ventral horn dorsomedial to motor nuclei. No inhibition by antidromic volleys could be detected in interneurones located in intermediate nucleus and activated monosynaptically from Ia, Ib, group I or cutaneous afferents.5. It was concluded that the ventral Ia interneurones inhibited by volleys in recurrent motor axon collaterals mediate the reciprocal Ia inhibition to motoneurones.     

Uncrossed actions of feline corticospinal tract neurones on lumbar interneurones evoked via ipsilaterally descending pathways

Effects of stimulation of ipsilateral pyramidal tract (PT) fibres were analysed in interneurones in midlumbar segments of the cat spinal cord in search of interneurones mediating disynaptic actions of uncrossed PT fibres on hindlimb motoneurones. The sample included 44 intermediate zone and ventral horn interneurones, most with monosynaptic input from group I and/or group II muscle afferents and likely to be premotor interneurones. Monosynaptic EPSPs evoked by stimulation of the ipsilateral PT were found in 12 of the 44 (27%) interneurones, while disynaptic or trisynaptic EPSPs were evoked in more than 75%. Both appeared at latencies that were either longer or within the same range as those of disynaptic EPSPs and IPSPs evoked by PT stimuli in motoneurones, making it unlikely that premotor interneurones in pathways from group I and/or II afferents relay the earliest actions of uncrossed PT fibres on motoneurones. These interneurones might nevertheless contribute to PT actions at longer latencies. Uncrossed PT actions on interneurones were to a great extent relayed via reticulospinal neurones with axons in the ipsilateral medial longitudinal fascicle (MLF), as indicated by occlusion and mutual facilitation of actions evoked by PT and MLF stimulation. However, PT actions were also relayed by other supraspinal or spinal neurones, as some remained after MLF lesions. Mutual facilitation and occlusion of actions evoked from the ipsilateral and contralateral PTs lead to the conclusion that the same midlumbar interneurones in pathways from group I or II muscle afferents may relay uncrossed and crossed PT actions.     

Rubrospinal effects on ventral spinocerebellar tract neurones.

Stimulation of the contralateral red nucleus evoked monosynaptic EPSPs in 14 of 82 ventral spinocerebellar tract neurones. In some of these cells the monosynaptic EPSP was followed by a disynaptic IPSP. The remaining cell population received di- or polysynaptic PSPs from the rubrospinal tract, either EPSPs or IPSPs or both. Convergence of the rubrospinal tract onto interneurones of the segmental pathways projecting to VSCT cells was demonstrated. Rubrospinal volleys facilitated disynaptic Ia IPSPs evoked in VSCT neurones from both flexors and extensors, as well as disynaptic Ib IPSPs. Facilitation of the Ia interneurones was disynaptic whereas facilitation of Ib interneurones was monosynaptic. Disynaptic rubrospinal EPSPs and IPSPs were facilitated by volleys in ipsi- as well as in contralateral cutaneous and high threshold muscle afferents. The complex pattern of projections from the rubrospinal tract onto VSCT neurones and the related reflex pathways gives further support to the hypothesis that these tract cells convey information on transmission through interneurones of the spinal segmental mechanisms.     

Integration in descending motor pathways controlling the forelimb in the cat

Summary With intracellular recording from forelimb motoneurones the spatial facilitation technique has been used to investigate interaction between descending pathways and forelimb afferents.As previously shown for the hindlimb, pyramidal volleys effectively facilitate interneuronal transmission in reflex pathways from different primary afferents. Evidence is presented suggesting disynaptic excitation from corticospinal fibres of interneurones in the reciprocal Ia inhibitory pathway. Interneurones of other reflex pathways from group I muscle afferents receive monosynaptic pyramidal excitation. During pyramidal facilitation volleys in cutaneous afferents may evoke PSPs in motoneurones after a central delay of 1.3 ms suggesting that the minimal linkage is disynaptic.Information regarding convergence on the neurones intercalated in the disynaptic cortico-motoneuronal pathway was obtained by investigating the effect from primary afferents and from other descending pathways on the disynaptic pyramidal EPSPs. Volleys in cutaneous and group I muscle afferents facilitate transmission in the disynaptic cortico-motoneuronal pathway with a time course showing oligosynaptic (probably monosynaptic) action on the intercalated neurone. Rubrospinal volleys likewise effectively facilitate disynaptic cortico-motoneuronal transmission with a time course showing monosynaptic action on the intercalated neurone. Spatial facilitation experiments involving three tests revealed that those intercalated neurones which receive convergent monosynaptic excitation from corticospinal and rubrospinal fibres are excited also from cutaneous forelimb afferents.Disynaptic cortico-motoneuronal transmission was also monosynaptically facilitated by stimuli in the dorsal mesencephalic tegmentum probably activating tectospinal fibres. Disynaptic, presumed tectospinal EPSPs were facilitated from cutaneous forelimb afferents.The convergence onto the neurones intercalated in the disynaptic excitatory cortico-motoneuronal pathway suggests that these neurones integrate the activity in different descending pathways and primary forelimb afferents.Supported by the Deutsche ForschungsgemeinschaftIBRO/UNESCO Fellow     

Rubrospinal Effects on Ventral Spinocerebellar Tract Neurones

Stimulation of the contralateral red nucleus evoked monosynaptic EPSPs in 14 of 82 ventral spinocerebellar tract neurones. In some of these cells the monosynaptic EPSP was followed by a disynaptic IPSP. The remaining cell population received di- or polysynaptic PSPs from the rubrospinal tract, either EPSPs or IPSPs or both. Convergence of the rubrospinal tract onto interneurones of the segmental pathways projecting to VSCT cells was demonstrated. Rubrospinal volleys facilitated disynaptic Ia IPSPs evoked in VSCT neurones from both flexors and extensors, as well as disynaptic Ib IPSPs. Facilitation of the Ia interneurones was disynaptic whereas facilitation of Ib interneurones was monosynaptic. Disynaptic rubrospinal EPSPs and IPSPs were facilitated by volleys in ipsi- as well as in contralateral cutaneous and high threshold muscle afferents. The complex pattern of projections from the rubrospinal tract onto VSCT neurones and the related reflex pathways gives further support to the hypothesis that these tract cells convey information on transmission through interneurones of the spinal segmental mechanisms.     

Mutual inhibition between olivary cell groups projecting to different cerebellar microzones in the cat

Summary Intracellular recording was made in the C3-C4 segments from cell bodies of a previously described system of propriospinal neurones (PNs), which receive convergent monosynaptic excitation from different higher motor centres and mediate disynaptic excitation and inhibition from them to forelimb motoneurones. Inhibitory effects in these PNs have now been investigated with electrical stimulation of higher motor centres and forelimb nerves. Short-latency IPSPs were evoked by volleys in the cortico-, rubro- and tectospinal tracts and from the reticular formation. Latency measurements showed that those IPSPs which required temporal summation were disynaptically mediated. After transection of the corticospinal tract in C2, only small and infrequent disynaptic IPSPs were evoked from the pyramid. It is postulated that disynaptic pyramidal IPSPs only to a small extent are evoked by monosynaptic excitation of reticulospinal inhibitory neurones known to project directly to the PNs, and that they are mainly mediated by inhibitory interneurones in the C3-C4 segments. Tests with spatial facilitation revealed monosynaptic excitatory convergence from tecto-, rubro- and probably also from reticulospinal fibres on inhibitory interneurones monosynaptically excited from corticospinal fibres (interneuronal system I). Disynaptic IPSPs were also evoked in the great majority of the PNs by volleys in forelimb muscle and skin nerves. A short train of volleys was usually required to evoke these IPSPs from group I muscle afferents. In the case of cutaneous nerves and mixed nerves single volleys were often effective, and the lack of temporal facilitation of IPSPs produced by a train of volleys showed strong linkage from these nerves. The results obtained after transection of the dorsal column at different levels show that the relay is almost entirely rostral to the forelimb segments. Test with spatial facilitation revealed that interneurones monosynaptically activated from forelimb afferents receive convergent excitation from corticospinal but not or only weakly so from tecto- or rubrospinal fibres. There was also convergence from group I muscle afferents and low threshold cutaneous afferents on common interneurones. It is postulated that the disynaptic IPSPs from forelimb afferents are mediated by inhibitory interneurones (interneuronal system II) other than those receiving convergent descending excitation. Volleys in corticospinal fibres, in addition to the disynaptic IPSPs, evoke late IPSPs in the PNs. Similar late IPSPs were evoked from the ipsilateral forelimb by stimulation of the FRA. Monosynaptic IPSPs were evoked in the majority of the PNs on weak stimulation of the lateral reticular nucleus (LRN) and from regions dorsal to it. Results from threshold mapping suggest that these IPSPs are due to antidromic stimulation of ascending inhibitory neurones which also project to the C3-C4 PNs, and that the ascending collaterals terminate in the LRN or/and the base of the cuneate nuclei. Activity in the ascending collaterals may give higher centres information regarding inhibitory control of the PNs. It is postulated that interneuronal system I subserves descending feed-forward inhibition and interneuronal system II feed-back inhibition from the forelimb of transmission through the C3-C4 PNs to motoneurones.This work was supported by the Swedish Medical Research Council (project no. 94)     

Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. I. Disynaptic Ia inhibition of Ia inhibitory interneurones.

Interneurones identified as mediating the disynaptic reciprocal Ia inhibition of motoneurones (referred to as "Ia inhibitory interneurones") were recorded in the lumbar spinal cord of the cat. It was revealed that the Ia inhibitory interneurones themselves receive disynaptic Ia inhibition. The muscles from which this inhibition is evoked are strictly antagonistic to those supplying their Ia excitation. Similar to the Ia inhibition in motoneurones the Ia inhibition in the Ia inhibitory interneurones is decreased when preceded by an antidromic stimulation of ventral roots. Furthermore, transmission of Ia inhibition to the Ia inhibitory interneurones is facilitated from ipsilateral and contralateral primary afferents as well as several supraspinal pathways analogous to earlier findings for the Ia inhibition of motoneurones. The pattern and control of the Ia inhibition of motoneurones and of Ia inhibitory interneurones display so striking similarities that it is suggested that identical interneurones are responsible. The conclusion thus emerges that "opposite" Ia inhibitory interneurones (i.e. interneurones monosynaptically connected to antagonistic muscles) are mutually inhibiting each other. The functional significance of this organization is discussed.     

Integration in descending motor pathways controlling the forelimb in the cat

Summary A previously described disynaptic pathway from cortex to forelimb motoneurones whose intercalated neurones were excited both from other descending pathways and from forelimb afferents (Illert et al., 1976a, b) has been further analysed, mainly with respect to the location of the relay cells and their axons.Disynaptic EPSPs evoked in forelimb motoneurones by stimulation of the pyramid remained after complete transection of the corticospinal tract in C5 rostral to the forelimb segments but were abolished after a more rostral transection of the tract in the C2 segment. Corresponding findings were made with disynaptic rubral EPSPs after transection of the rubrospinal tract in these segments. It is concluded that disynaptic cortico-motoneuronal and rubro-motoneuronal excitation is relayed by propriospinal neurones originating in the C3–C4 segments. Other lesion experiments revealed that the axons of these propriospinal neurones descend to forelimb motoneurones in the ventrolateral part of the lateral funicle.Spatial facilitation of transmission from the corticospinal and rubrospinal tracts after transection of them in C5 occurred with a time course showing monosynaptic convergence from these pathways on common propriospinal neurones.Facilitation of disynaptic pyramidal EPSPs from the dorsal tegmentum remained after transection of the corticospinal tract at C5 but was abolished after a transection at C2. It is postulated that corticospinal and presumed tectospinal fibres converge onto common neurones in the propriospinal relay but evidence is also given for a more rostral relay (probably bulbar) with a similar convergence.The oligo- (probably mono-)synaptic facilitation of the disynaptic pyramidal EPSP evoked by volleys in cutaneous and group I muscle afferents from the forelimb likewise remained after a C5 transection of the corticospinal tract but was abolished after an additional C5 lesion in the dorsal column. It is concluded that propriospinal relay cells receive excitatory action from forelimb afferents ascending in the dorsal column. Spatial facilitation experiments using three tests revealed that propriospinal neurones monosynaptically excited from both corticospinal and rubrospinal fibres also receive excitation from cutaneous forelimb afferents.It is postulated that the propriospinal relay provides an important route for fast activation of forelimb motoneurones from the brain. The convergent monosynaptic excitation from several important motor centres in the brain is considered in relation to the general problem of the functional relationship between higher motor centres. The convergent action from forelimb afferents is taken to suggest that a descending command for a forelimb movement can be modified from the forelimb while on its way to the motoneurones.Supported by the Deutsche Forschungsgemeinschaft     

Convergence on Interneurones Mediating the Reciprocal Ia Inhibition of Motoneurones I. Disynaptic Ia Inhibition of Ia Inhibitory Interneurones

Interneurones identified as mediating the disynaptic reciprocal Ia inhibition of motoneurones (referred to as “Ia inhibitory interneurones”) were recorded in the lumbar spinal cord of the cat. It was revealed that the Ia inhibitory interneurones themselves receive disynaptic Ia inhibition. The muscles from which this inhibition is evoked are strictly antagonistic to those supplying their Ia excitation. Similar to the Ia inhibition in motoneurones the Ia inhibition in the Ia inhibitory interneurones is decreased when preceded by an antidromic stimulation of ventral roots. Furthermore, transmission of Ia inhibition to the Ia inhibitory interneurones is facilitated from ipsilateral and contralateral primary afferents as well as several supraspinal pathways analogous to earlier findings for the Ia inhibition of motoneurones. The pattern and control of the Ia inhibition of motoneurones and of Ia inhibitory interneurones display so striking similarities that it is suggested that identical interneurones are responsible. The conclusion thus emerges that “opposite” Ia inhibitory interneurones (i.e. interneurones monosynaptically connected to antagonistic muscles) are mutually inhibiting each other. The functional significance of this organization is discussed.     

Both dorsal horn and lamina VIII interneurones contribute to crossed reflexes from feline group II muscle afferents

Previous studies have demonstrated that group II muscle afferents exert powerful actions on contralateral motoneurones and that these actions are mediated primarily via lamina VIII commissural interneurones. We examined whether dorsal horn interneurones also contribute to these actions, as they have been shown to contribute to the actions of group II afferents on ipsilateral motoneurones. We tested the susceptibility of IPSPs and EPSPs evoked from group II afferents in contralateral motoneurones to presynaptic inhibition as an indicator of the relative contribution of dorsal horn interneurones to these PSPs, since the monosynaptic activation of dorsal horn interneurones is more weakly and more briefly depressed by presynaptic inhibition than is the monosynaptic activation of lamina VIII and other intermediate zone and ventral horn interneurones. While the earliest components of IPSPs and EPSPs evoked by group II afferents were abolished by conditioning stimulation of group II afferents, consistent with them being evoked disynaptically by commissural interneurones, trisynaptic components of these PSPs were only partly reduced and are therefore attributed to dorsal horn interneurones. The same conditioning stimuli depressed the disynaptic excitation of lamina VIII commissural interneurones by group II afferents much less effectively than they depressed monosynaptic excitation, indicating that dorsal horn interneurones contribute to this disynaptic excitation. On the basis of these observations we conclude that that dorsal horn interneurones contribute to the late actions of group II muscle afferents on contralateral motoneurones through their disynaptic actions on commissural interneurones.     

Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. III. Effects from supraspinal pathways.

Supraspinal effects were investigated in interneurones identified as mediating the disynaptic reciprocal Ia inhibition of motoneurones (referred to as Ia inhibitory interneurones). It was revealed that volleys in the vestibulospinal tract may evoke mono- and disynaptic EPSPs in interneurones monosynaptically excited from extensor muscles, i.e. extensor coupled Ia inhibitory interneurones. Flexor coupled interneurones instead received disynaptic inhibition. Volleys in the rubrospinal tract evoked a dominating polysynaptic excitation, usually mixed with inhibition, in flexor as well as extensor coupled interneurones. Disynaptic rubrospinal EPSPs and IPSPs were also revealed. The pyramidal tract also gives rise to a dominating polysynaptic excitation, usually mixed with inhibition, in flexor as well as extensor coupled Ia inhibitory interneurones. Rubrospinal and pyramidal volleys were shown to facilitate transmission in various segmental reflex pathways to the Ia inhibitory interneurones. A detailed comparison reveals a striking parallelism of segmental and supraspinal effects on alpha-motoneurones and Ia inhibitory interneurones connected to the same muscles. This considerably strengthens the hypothesis of an "alpha-gamma-linkage in the reciprocal inhibition".     

Convergence on interneurones mediating the reciprocal Ia inhibition of motoneurones. II. Effects from segmental flexor reflex pathways.

Interneurones identified as mediating the disynaptic reciprocal Ia inhibition of motoneurones (referred to as "Ia inhibitory interneurones") were recorded in the lumbar spinal cord of the cat. Volleys in ipsilateral and contralateral high threshold muscle afferents, cutaneous and high threshold joint afferents evoked a mixture of polysynaptic excitation and inhibition. These effects were ascribed to pathways activated by flexor reflex afferents (FRA) and in addition a specific ipsilateral low threshold cutaneous pathway. Ia inhibitory interneurones excited monosynaptically from flexor nerves received stronger net excitation by volleys in ipsilateral FRA than did extensor coupled interneurones, while the opposite pattern was seen from the contralateral FRA. These patterns are similar to those found in flexor and extensor motoneurones respectivey. The FRA inhibition in Ia inhibitory interneurones was partly mediated by "opposite" Ia inhibitory interneurones, i.e. those which are mediating the Ia inhibition of Ia inhibitory interneurones. The extent to which the FRA inhibition is transmitted by Ia inhibitory interneurones was roughly estimated by its susceptibility to recurrent depression by antidromic ventral root stimulation. The main conclusion is that most segmental pathways seem to evoke their effects in parallel to motoneurones and Ia inhibitory interneurones which are monosynaptically linked to the same muscle. The functional importance of this conclusion is discussed in a following report.     

Convergence on Interneurones Mediating the Reciprocal Ia Inhibition of Motoneurones III. Effects from supraspinal pathways

Supraspinal effects were investigated in interneurones identified as mediating the disynaptic reciprocal Ia inhibition of motoneurones (referred to as “Ia inhibitory interneurones”). It was revealed that volleys in the vestibulospinal tract may evoke mono- and disynaptic EPSPs in interneurones monosynaptically excited from extensor muscles, i.e. extensor coupled Ia inhibitory interneurones. Flexor coupled interneurones instead received disynaptic inhibition. Volleys in the rubrospinal tract evoked a dominating polysynaptic excitation, usually mixed with inhibition, in flexor as well as extensor coupled interneurones. Disynaptic rubrospinal EPSPs and IPSPs were also revealed. The pyramidal tract also gives rise to a dominating polysynaptic excitation, usually mixed with inhibition, in flexor as well as extensor coupled Ia inhibitory interneurones. Rubrospinal and pyramidal volleys were shown to facilitate transmission in various segmental reflex pathways to the Ia inhibitory interneurones. A detailed comparison reveals a striking parallelism of segmental and supraspinal effects on α-motoneurones and Ia inhibitory interneurones connected to the same muscles. This considerably strengthens the hypothesis of an “α–γ-linkage in the reciprocal inhibition”.     

Evidence for corticospinal excitation of presumed propriospinal neurones in man.

1. The possibility that stimulation of the motor cortex facilitates transmission in the pathway mediating non-monosynaptic ('propriospinal') excitation from low-threshold afferents to upper limb motoneurones was investigated. 2. Convergence between peripheral afferent volleys (from the ulnar or musculo-cutaneous nerve) and corticospinal volleys (evoked by magnetic stimulation of the motor cortex) was investigated using the spatial facilitation technique. Thus the effects of these volleys on the flexor carpi radialis H reflex were compared when applied separately and together. When cortical stimulation was optimal for the muscle from which the conditioning volley originated the facilitation of the reflex on combined stimulation was significantly larger than the algebraic sum of the effects of separate stimuli. 3. The extra facilitation on combined stimulation had all the characteristics of 'propriospinal' excitation (low threshold, long central delay, brief duration and depression when the afferent input was increased), and it is suggested that this reflects corticospinal excitation of 'propriospinal' neurones. 4. When varying the time interval between cortical and test stimulations, it was shown that extra facilitation on combined stimulation began 1 ms later than the onset of the control reflex facilitation. Assuming that the latter onset reflects the arrival of the monosynaptic corticospinal volley at the motoneurone pool, this 1 ms delay suggests a disynaptic pathway for the cortical excitation of motoneurones through 'propriospinal' neurones. 5. As at the onset of voluntary movement, the pattern of the cortical excitation of 'propriospinal' neurones was quite specific: extra facilitation of the reflex on combined stimulation only occurred when the cortical volley was preferentially directed to motoneurones supplying the muscle from which the afferents used for the peripheral volley originated. 6. It is concluded that corticospinal axons activate human 'propriospinal' neurones and thereby produce disynaptic excitation of the motoneurone pool. Given temporal summation with the monosynaptic excitation, this 'propriospinally mediated' disynaptic excitation might make a significant contribution to the evoked EMG potential.     

Reflex pathways from group II muscle afferents

The convergence of group II muscle afferents on interneurones in reflex pathways has been elucidated by investigating interaction in transmission to motoneurones. Recording was also made from interneurones activated from group II afferents. Maximal group II EPSPs evoked in motoneurones from different muscles (extensors or flexors and extensors) did not summate linearly but with a deficit of 35-40%. The corresponding deficit in summation with Ia EPSPs was 7%. It is suggested that the difference in deficit is caused largely by occlusion due to shared interneuronal discharge zones and that it gives an approximate minimal measure of the convergence of group II afferents from different muscles on the interneurones. Tests with weak group II volleys from different muscles gave no or little evidence for spatial facilitation in the disynaptic excitatory pathway to flexor motoneurones, and there was no or little temporal facilitation of transmission in this pathway. It is suggested that group II excitation of the interneurones in this pathway depends on few afferents giving large unitary EPSPs. Convergence of cutaneous afferents and joint afferents on the interneurones was evidenced by spatial facilitation from these afferents of group II transmission to motoneurones. Convergence on interneurones in the trisynaptic inhibitory pathway from group II afferents to extensor motoneurones was also investigated with the spatial facilitation technique. There was convergence on common interneurones of group II afferents from different muscles (extensors or flexors and extensors) and from cutaneous afferents as well as joint afferents. Trisynaptic group II IPSPs, including those depending on spatial facilitation from different muscles were resistant to recurrent depression from motor axon collaterals and are therefore not mediated by the reciprocal Ia inhibitory pathway. Interneurones with monosynaptic group II EPSPs were recorded from in the dorsal horn and intermediate region. Graded stimulation revealed large unitary EPSPs from few group II afferents. The EPSP evoked by a single group II afferent may produce firing (extracellular recording). Convergence of monosynaptic group II EPSPs from different muscles was rather limited but could be from flexors and extensors. Extensive multisensory convergence onto some of these interneurones was indicated by di- or polysynaptic EPSPs from group II and III muscle afferents, from joint afferents and from cutaneous afferents.(ABSTRACT TRUNCATED AT 400 WORDS)     

Neuronal relays in double crossed pathways between feline motor cortex and ipsilateral hindlimb motoneurones

Coupling between pyramidal tract (PT) neurones and ipsilateral hindlimb motoneurones was investigated by recording from commissural interneurones interposed between them. Near maximal stimulation of either the left or right PT induced short latency EPSPs in more than 80% of 20 commissural interneurones that were monosynaptically excited by reticulospinal tract fibres in the medial longitudinal fascicle (MLF). The EPSPs were evoked at latencies that were only 1–2 ms longer than those of EPSPs evoked from the MLF, compatible with a disynaptic coupling between PT fibres and these commissural interneurones. EPSPs evoked by PT stimulation were frequently associated with IPSPs which either followed or preceded the EPSPs. The latencies of the IPSPs (on average about 1 ms longer than latencies of the earliest EPSPs) indicated that they were mediated via single additional inhibitory interneurones. Records from a sample of nine commissural interneurones from a different population (with monosynaptic input from group I and/or II muscle afferents, and disynaptically excited from the MLF) suggest that actions of PT fibres on such interneurones are weaker because only four of them were excited by PT stimuli and at longer latencies. By demonstrating disynaptic coupling between PT neurones and commissural interneurones via reticulospinal fibres, the results provide a direct demonstration of trisynaptic coupling in the most direct pathways between PT neurones and ipsilateral motoneurones, and thereby strengthen the proposal that the double crossed pathways between PT neurones and ipsilateral motoneurones might be used to replace crossed actions of damaged PT neurones.