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The Distribution of Primary Nitric Oxide Synthase- and Parvalbumin- Immunoreactive Afferents in the Dorsal Funiculus of the Lumbosacral Spinal Cord in a Dog

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1. The aim of the present study was to examine the distribution of unmyelinated, small-diameter myelinated neuronal nitric oxide synthase immunoreactive (nNOS-IR) axons and large-diameter myelinated neuronal nitric oxide synthase and parvalbumin-immunoreactive (PV-IR) axons in the dorsal funiculus (DF) of sacral (S1–S3) and lumbar (L1–L7) segments of the dog.

2. nNOS and PV immunohistochemical methods were used to demonstrate the presence of nNOS-IR and PV-IR in the large-diameter myelinated, presumed to be proprioceptive, axons in the DF along the lumbosacral segments.

3. Fiber size and density of nNOS-IR and PV-IR axons were used to compartmentalize the DF into five compartments (CI–CV). The first compartment (CI) localized in the lateralmost part of the DF, containing both unmyelinated and small-diameter myelinated nNOS-IR axons, is homologous with the dorsolateral fasciculus, or Lissauer tract. The second compartment (CII) having similar fiber organization as CI is situated more medially in sacral segments. Rostrally, in lower lumbar segments, CII moves more medially, and at upper lumbar level, CII reaches the dorsomedial angle of the DF and fuses with axons of CIV. CIII is the largest in the DF and the only one containing large-diameter myelinated nNOS-IR and PV-IR axons. The largest nNOS-IR and PV-IR axons of CIII (8.0–9.2 μm in diameter), presumed to be stem Ia proprioceptive afferents, are located in the deep portion of the DF close to the dorsal and dorsomedial border of the dorsal horn. The CIV compartment varies in shape, appearing first as a small triangular area in S3 and S2 segments, homologous with the Philippe–Gombault triangle. Beginning at S1 level, CIV acquires a more elongated shape and is seen throughout the lumbar segments as a narrow band of fibers extending just below the dorsal median septum in approximately upper two-thirds of the DF. The CV is located in the basal part of the DF. In general, CV is poor in nNOS-IR fibers; among them solitary PV-IR fibers are seen.

4. The analysis of the control material and the degeneration of the large- and medium-caliber nNOS-IR fibers after unilateral L7 and S1 dorsal rhizotomy confirmed that large-caliber nNOS-IR and and PV-IR axons, presumed to be proprioceptive Ia axons, and their ascending and descending collaterals are present in large number in the DF of the lumbosacral intumescence. However, in the DF of the upper lumbar segments, the decrease in the number of nNOS-IR and PV-IR fibers is quite evident.

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Abbreviations

CI–CV:

fibre compartments in DF

DF:

dorsal funiculus

DRG:

dorsal root ganglion

DREZ-one:

dorsal root entry zone

eNOS:

endothelial nitric oxide synthase

LB:

lateral bundle of the dorsal root

LS:

lumbosacral segments

MB:

medial bundle of the dorsal root

mNOS:

macrophage nitric oxide synthase

NADPHd:

nicotinamide adenine dinucleotide phosphate diaphorase

nNOS-IR:

neuronal nitric oxide synthase immunoreactivity

PV-IR:

parvalbumin immunoreactivity

TPG:

the triangle of Philippe–Gombault.

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Acknowledgments

The authors thank Mr. D. Krokavec, Ms. M. Špontáková, Mrs. M. Syneková, and Mrs. A.M. Košová for their excellent technical assistance. The experimental work was supported by the VEGA Grants No. 2/3217/23 and 2/5134/25 from the SAS, APVT Grant No. 51-013002, and NIH grants NS 32794 and NS 40386 to M.M.

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Authors and Affiliations

  1. Institute of Neurobiology, Slovak Academy of Sciences, Šoltésovej 4, 040 01, Košice, Slovak Republic

    Jozef Maršala, Nadežda Lukáčová, Dalibor Kolesár & Ján Gálik

  2. Department of Neurosurgery, Medical Faculty of P. J. Šafárik University, 040 01, Košice, Slovak Republic

    Igor Šulla

  3. Anesthesiology Research Laboratory, University of California, San Diego, La Jolla, CA, 92093-0818, USA

    Martin Maršala

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  1. Jozef Maršala
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Maršala, J., Lukáčová, N., Kolesár, D. et al. The Distribution of Primary Nitric Oxide Synthase- and Parvalbumin- Immunoreactive Afferents in the Dorsal Funiculus of the Lumbosacral Spinal Cord in a Dog. Cell Mol Neurobiol 27, 475–504 (2007). https://doi.org/10.1007/s10571-007-9140-6

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