Inter-enlargement pathways in the ventrolateral funiculus of the adult rat spinal cord

Abstract

The ventrolateral funiculus (VLF) in the spinal cord contains important ascending and descending pathways related to locomotion and interlimb coordination. The primary purpose of this descriptive study was to investigate the distribution of inter-enlargement pathways in the adult rat spinal cord with an emphasis on the VLF.We made discrete unilateral injections of Fluoro-Gold (FG) into the right VLF at T9, and either unilateral or bilateral injections of Fluoro-Ruby (FR) into the intermediate gray matter at the C5-6, C7-8, or L2 segmental levels. Inter-enlargement neurons with ascending axons in the right VLF were found bilaterally in laminae VII and VIII throughout the rostral lumbar spinal cord (L1-L3) and predominately contralaterally in the caudal lumbosacral (L4-S1) spinal cord. Following left unilateral FR injections at C5-6 or C7-8 and right unilateral VLF injections of FG at T9, very few double-labeled neurons could be found anywhere in the lumbar spinal cord. Similar injections of FR at L2 revealed an almost symmetrical bilateral distribution of double-labeled neurons throughout the cervical spinal cord (C1-C8).These results describe ascending and descending pathways within the spinal cord that interconnect the two enlargements and involve both commissural and ipsilateral interneurons. The majority of inter-enlargement neurons had axons within the ventrolateral funiculus at T9. These observations support the hypothesis that the VLF contains long ascending and descending axons with propriospinal inter-enlargement, commissural and ipsilateral connections that are anatomically well-suited to mediate interlimb coordination. Keywordspropriospinal pathways; interlimb coordination; Fluoro-Gold; Fluoro-Ruby There is renewed interest of late in propriospinal pathways due in part to reports of the spontaneous formation of new functional intraspinal circuitry following spinal cord injury (Bareyre et al., 2004) and the potential these pathways have in combinatorial repair strategies involving cellular transplantation and neurotrophin delivery (Jordan and Schmidt, 2002;Conta and Stelzner, 2004;Fouad et al., 2005). While many regions of the spinal cord possess the neural circuitry necessary to produce rhythmic activity, in the mammalian quadruped, separate central pattern generator (CPG) networks are thought to exist for the hindlimbs and forelimbs (Cazalets et al., 1995(Cazalets et al., , 1996Magnuson and Trinder, 1997; Correspondence to: David S.K. Magnuson, PhD, Department of Neurological Surgery, University of Louisville School of Medicine, 210 E. Grey St., Ste. 1102, Louisville, KY 40202, dsmagn01@louisville.edu, Phone (502) 852-6551, Fax (502) Magnuson et al., 1999;Ballion et al., 2001;Juvin et al., 2005). In the rat, intraspinal Kainic Acid injections have profound effects on locomotor function when delivered to the intermediate gray matter at L2 (Magnuson et al., 1999) and locomotor deficits resulting from moderately-severe contusion injuries are greater when the contusion is centered on the m...

Long and Short Multifunicular Projections of Sacral Neurons Are Activated by Sensory Input to Produce Locomotor Activity in the Absence of Supraspinal Control

“…In fact, our findings resemble more recent work showing the involvement of multifunicular descending projections in the control of overground locomotion (Brustein and Rossignol, 1998;Vilensky et al, 1992;Schucht et al, 2002;Loy et al, 2002a,b), and those reported for the bulbospinal pathways in the adult rat (Reed et al, 2006(Reed et al, , 2009. However, it is important to emphasize that the role of the VLF may have been underestimated in the present work, because some of the crossed VLF axons entered the VLF after traveling through the sacral VF (Fig.…”

Neurons in the lateral part of the lumbar spinal cord show distinct novel axon trajectories and are excited by short propriospinal ascending inputs

“…Despite the above one cannot rule out the possibility that some of these cells could be propriospinal neurons, since axons running in the anterolateral funiculus were shown to form inter-enlargement pathways between the cervical and lumbar spinal cord (Reed et al, 2006). Furthermore, contralateral lumbosacral lamina I neurons have been retrogradely labelled after tracer injections into the cervical ventral horn and some of them look very similar to bilaterally projecting cells of our study (Fig.…”

“…For this reason we believe that the presence of such projecting axons is more likely to be indication of the projection nature of the cells. However we have included a new block and added a new citation (Reed et al, 2006) in the discussion that deals with the issue of propriospinal cells.…”

Location of Spinal Cord Pathways That Control Hindlimb Movement Amplitude and Interlimb Coordination During Voluntary Swimming in Turtles

“…These results suggest that the spinal cord itself contains sufficient circuitry for 1:1 interlimb coordination. Furthermore, propriospinal fibers connecting the forelimb and hindlimb enlargements have been demonstrated in the ventral and/or ventrolateral white matter in turtles (Kusuma and ten Donkelaar 1980), cats (Giovanelli Barilari and Kuypers 1969), and rats (Reed et al 2006), indicating likely locations of axons contributing to interlimb phase control. Other studies in cats (Bem et al 1995;Brustein and Rossignol 1998;Gorska et al 1993aGorska et al ,b, 1996Jiang and Drew 1996;Kato 1992;Zmyslowski et al 1993) and rats (Loy et al 2002a,b;Schucht et al 2002) assessed the effects of spinal lesions on forelimb-hindlimb coordination, suggesting that both the DLF and VLF contained axons contributing to interlimb coupling.…”