Lumbar commissural interneurons with reticulospinal inputs in the cat: Morphology and discharge patterns during fictive locomotion

Abstract

The purpose of this study was 1). to characterize the morphology of lumbar commissural neurons (CNs) with reticulospinal inputs and 2). to quantitate their activity during locomotor rhythm generation. Intraaxonal recordings at the L4-7 level of the spinal cord were obtained in 67 neurons in the decerebrate, paralyzed cat. Fourteen of them were subsequently nearly fully visualized following their intraaxonal injection with the tracer neurobiotin. All 14 were CNs with axons projecting across the midline of the spinal cord. Their somata were located mainly in lamina VIII and additionally in laminae VII-VI. Most of the lamina VIII CNs were excited monosynaptically from reticulospinal pathways. They were judged to be interneuronal CNs if they had no, or a short, rostral projection. These CNs commonly gave off multiple axon collaterals in and around their somata's segmental level. They projected mainly to laminae VIII-VII and some additionally to lamina IX. Some laminae VIII and the laminae VII-VI CNs were excited polysynaptically from reticulospinal pathways or were not excited. They were judged to be long propriospinal or ascending tract CNs because they had only an ascending axon. Most lamina VIII CNs discharged rhythmically during fictive locomotion evoked by stimulation of the mesencephalic locomotor region, exhibiting one peak per locomotor cycle. The peak was in phase with neurographic activity of either a left or a right hindlimb extensor nerve. These results suggested that lamina VIII CNs are reciprocally connected bilaterally at each segmental level. Such an arrangement suggests their participation in the generation and coordination of reciprocal and bilateral locomotor activity.

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

“…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). In addition, our findings suggest the presence of another dCIN-mediated doublecrossed pathway between medullary reticulospinal neurons and ipsilateral trunk MNs.…”

“…Uncrossed and crossed MRF inputs to dCINs could be transmitted by respectively ipsilateral or commissural reticulospinal axon collaterals (Matsuyama et al, 2004b), potentially giving rise to single-crossed and doublecrossed dCIN-mediated reticulospinal pathways to lumbar MNs.…”

“…In addition, our findings suggest the presence of another dCIN-mediated doublecrossed pathway between medullary reticulospinal neurons and ipsilateral trunk MNs. An important line of future inquiry will be the extent to which the crossed connections involve commissural reticulospinal axon collaterals (Matsuyama et al, 2004b) in addition to interposed dCINs. Tests of monosynapticity as well as anatomical studies will be required to evaluate this.…”

Strategies for delineating spinal locomotor rhythm-generating networks and the possible role of Hb9 interneurones in rhythmogenesis

“…However, neither the precise connectivity of locomotor-related spinal interneurones nor their intrinsic properties have been defined. That is, despite the demonstration that many ventral interneurones are rhythmically active during locomotor activity in the cat (Angel et al, 2005;Baev et al, 1979;Gossard et al, 1994;Huang et al, 2000;Jankowska et al, 1967a;Matsuyama et al, 2004;Shefchyk et al, 1990) and rodent (Butt and Kiehn, 2003;Butt et al, 2005;Kiehn et al, 1996;Tresch and Kiehn, 1999;Zhong et al, 2006) little is known about the connectivity of these neurones…”

Descending Signals From the Pontomedullary Reticular Formation Are Bilateral, Asymmetric, and Gated During Reaching Movements in the Cat

“…Many reticular neurons innervate both cervical and lumbar levels of the spinal cord (Peterson et al 1975) and some neurons have axons that cross the midline at the cervical or lumbar levels and innervate the gray matter of both sides (Matsuyama et al 1988(Matsuyama et al , 1999. In addition, reticulospinal axons also terminate on commissural interneurons so that an action on contralateral activity may also be mediated by this pathway (Jankowska et al 2003;Matsuyama et al 2004). As such, there is a firm anatomical substrate demonstrating that reticulospinal neurons can produce widespread effects throughout the neuraxis, including both ipsi-and contralateral to the cell body.…”