Bulbospinal control of spinal cord pathways generating locomotor extensor activities in the cat.

Intracellular recording of lumbosacral motoneurones in the decerebrate and partially spinalized cat injected with nialamide and L-dihydroxyphenylalanine (l-DOPA) was used to investigate the interneuronal convergence of two bulbospinal pathways and of the segmental pathways involved with the generation of extensor activities during locomotion. Deiter's nucleus (DN) or the medial longitudinal fasciculus (MLF) was stimulated in alternation with, and in combination with, stimulation of group I afferents from extensor muscles or of contralateral flexor reflex afferents (coFRA). The evoked polysynaptic EPSPs were recorded in extensor motoneurones when long-latency, long-lasting discharges were evoked by the stimulation of coFRA and when the group I autogenetic inhibition in extensors was reversed to polysynaptic excitation. Spatial facilitation was inferred 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. Both DN (16 motoneurones) and MLF inputs (8 motoneurones) showed spatial facilitation when preceded by coFRA stimuli and both could reset the rhythm of fictive stepping by triggering a precocious extensor phase. MLF showed spatial facilitation with extensor group I inputs in 69 % of trials but DN failed to show spatial facilitation in any cells. These results indicate that DN and MLF project to the coFRA pathways of the extensor half-centre for locomotion and MLF, but not DN, converge on segmental interneurones of the extensor group I pathways. The implications of such convergence patterns on the functional organization of the extensor half-centre are discussed. In the frame of a study on the intrinsic organization of the neuronal networks comprising the rhythm generator, we investigated the role of two of the major bulbospinal signals involved in the initiation and control of locomotion: the vestibulospinal and the reticulospinal pathways. We focussed our investigation on the interaction between each of these two descending pathways with segmental pathways which are thought to be sharing interneurones with the rhythm generators in the spinal cord: the pathways transmitting load signals from ankle and knee extensor muscles through group I afferents fibres (referred to as ‘extensor group I’ in the text). The extensor group I pathways excite extensor motoneurones to promote the thrust during the stance phase of walking (Duysens & Pearson, 1980; cf. Pearson et al. 1998). During fictive locomotion, stimulation of extensor nerves at group I strength can reset the locomotor rhythm, e.g. by interrupting the burst activity in flexor nerves and simultaneously triggering activity in extensor nerves (Conway et al. 1987; Gossard & Hultborn, 1991; Gossard et al. 1994). Moreover, repetitive stimulation of extensor group I fibres was found to entrain the stepping rhythm (Conway et al. 1987; Pearson et al. 1992). Further studies have revealed that both group Ia and Ib afferents from ankle and knee extensor muscles contribute to these effects by evoking di- and polysynaptic excitation to homonymous motoneurones instead of the classical autogenetic disynaptic inhibition observed in anaesthetized cats (Gossard et al. 1994; Guertin et al. 1995; McCrea et al. 1995). These findings have led to the hypothesis that extensor group I pathways may share some interneurones with the extensor half-centre (cf. Gossard & Hultborn, 1991). Thus, determining which supraspinal inputs converge onto these pathways should help fulfilling the functional identification of such interneurones during locomotion (Hultborn et al. 1998) which in turn may lead to a better understanding of the intrinsic connectivity of the central pattern generator (CPG). Our hypothesis is that descending and segmental pathways capable of resetting the locomotor rhythm do so via convergence onto common spinal interneuronal pathways. Convergence between descending and segmental inputs was tested using the spatial facilitation technique (Lundberg, 1975; Baldissera et al. 1981; Gossard et al. 1996; Burke, 1999) in lumbosacral extensor motoneurones recorded intracellularly in partially spinalized cats injected with nialamide and L-dihydroxyphenylalanine (l-DOPA; see Russel & Zajac, 1979; Gossard et al. 1994). Our results showed that vestibulospinal pathways originating from the Deiter's nucleus (DN), some reticulospinal descending tracts in the medial longitudinal fasciculus (MLF) and extensor group I fibres all have the ability to reset the locomotor rhythm. However, there was a complete absence of spatial facilitation between inputs from DN and of extensor group I afferents indicating that their signals are transmitted through separate spinal pathways. On the other hand, spatial facilitation between MLF and extensor group I inputs was found in 69 % of the trials, indicating that both pathways share some spinal interneurones. Some preliminary results have been reported before (Leblond & Gossard, 1996; Leblond et al. 1997, 1998).