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

Abstract

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. We recently demonstrated that some actions of pyramidal tract (PT) neurones on ipsilateral hindlimb motoneurones are evoked via pathways that cross the midline twice. The first crossing occurs in the brainstem where PT neurones contact reticulospinal (RS) neurones with axons that descend in the contralateral medial longitudinal fascicle (MLF), as indicated in Fig. 1A. The second crossing occurs at a spinal level; it involves axons of contralaterally located midlumbar commissural interneurones activated by RS neurones which contact motoneurones on the side of location of the PT neurones (Bannatyne et al. 2003;Jankowska et al. 2003Jankowska et al. , 2005aEdgley et al. 2004). We proposed that the minimal coupling in these pathways is trisynaptic, with the first synapse between the PT and RS neurones, the second between the RS neurones and midlumbar commissural interneurones, and the third between the commissural interneurones and motoneurones. However, this proposal was based on indirect measurements -particularly the time course of facilitation of the actions of RS neurones on motoneurones by PT stimulation which can only be assessed with a relatively low time resolution (Edgley et al. 2004). Indirect rather than direct estimates of PT actions on ipsilateral motoneurones were used because postsynaptic potentials were only exceptionally evoked in motoneurones followin...

Organization of Functional Synaptic Connections between Medullary Reticulospinal Neurons and Lumbar Descending Commissural Interneurons in the Neonatal Mouse

“…Regarding the ipsilateral dCINs, this suggests the presence of crossed dCINmediated pathways from medullary reticulospinal neurons to contralateral trunk and hindlimb MNs. Similar crossed CINmediated pathways from pontine reticulospinal neurons to hindlimb MNs have been described in the anesthetized adult cat (Jankowska et al, 2003(Jankowska et al, , 2005(Jankowska et al, , 2006. Regarding the contralateral dCINs, our findings are in accordance with the suggested presence in the adult cat of a dCIN-mediated double-crossed pathway between medullary reticulospinal neurons and ipsilateral hindlimb MNs (Jankowska et al, 2003;Matsuyama et al, 2004b).…”

Cortical control of erector spinae muscles during arm abduction in humans

“…The fibres are thought to contribute more to the control of axial trunk muscles than limb muscles [34]. Several studies have shown that TMS can elicit responses in ipsilateral muscles, preferentially in axial muscles [9,10,[35][36][37][38], but it remains uncertain as to whether these responses are transmitted by an ipsilateral corticospinal tract [39]. The difference in latency of the erector spinae MEPs observed in the present study indicates that two pathways may be involved.…”

Reticulospinal pathways in the ventrolateral funiculus with terminations in the cervical and lumbar enlargements of the adult rat spinal cord

“…Approximately 30% of the total number of FG-labeled neurons were found to be commissural, allowing us to speculate that approximately 30% of the axons in the ventrolateral white matter arise from commissural reticulospinal neurons. The existence of such pathways is supported by Jankowska et al (2006) who describe double-crossed pathways involving commissural reticulospinal neurons along with their ability to activate hindlimb motoneurons caudal to an ipsilateral thoracic spinal cord hemisection. Matsuyama et al (2004) also emphasized the point that monosynaptic reticulospinal inputs (originating from either side of the brainstem) can coordinate bilateral CPG-related activity via spinal commissural interneuronal circuits in the cat spinal cord.…”