Effects of spinal cord injury on neurofilament immunoreactivity and capsaicin sensitivity in rat dorsal root ganglion neurons innervating the urinary bladder

doi:10.1016/S0306-4522(97)00376-X

Neuroscience

Volume 83, Issue 2, 1998, Pages 633-643

https://doi.org/10.1016/S0306-4522(97)00376-X Get rights and content

Abstract

The effect of chronic spinal cord transection on neurofilament immunoreactivity and capsaicin sensitivity of L6 and S1 dorsal root ganglion neurons innervating the urinary bladder was examined using an antibody (RT97) against 200 000 mol. wt subunit of neurofilament protein and a cobalt uptake assay, respectively. Bladder afferent neurons labelled by axonal transport of a fluorescent dye (Fast Blue) injected into the bladder wall were identified in sections of intact dorsal root ganglia and among dissociated neurons in short-term culture. Approximately two thirds of bladder afferent neurons from spinal intact rats were neurofilament-poor (i.e. C-fibre neurons). These neurons were on average 37% smaller in cross-sectional area than neurofilament-rich neurons (Aδ-fibre neurons). In spinal intact rats, 78% of neurofilament-poor dissociated bladder afferent neurons were sensitive to capsaicin, while only 6.2% of neurofilament-rich neurons were capsaicin-sensitive. Dissociated bladder afferent neurons from spinal transected animals had larger diameters (34.2±1.1 μm) than those from spinal intact animals (29.2±1.2 μm). In tissue sections from dorsal root ganglia, the mean cross-sectional area of bladder afferent neuron profiles in spinal transected animals was also larger by approximately 35% than in spinal intact animals. Immunoreactivity to neurofilament protein which occurred in 32% of bladder afferent neurons in spinal intact animals was detected in a larger percentage (56% to 62%) of neurons from spinal transected animals. Conversely, the population of capsaicin-sensitive dissociated neurons was reduced from 55% in spinal intact rats to 38% in spinal transected rats.

These results indicate that spinal cord injury induces functional and morphological plasticity in C-fibre visceral afferent neurons innervating the urinary bladder.

Section snippets

Spinal cord transection

Experiments were performed on spinal intact and chronic spinal transected adult female Sprague–Dawley rats (180–230 g, Hilltop Lab Animals, Inc.). Care and handling of animals were in accordance with institutional guidelines and approved by the University of Pittsburgh IACUC. The spinal cord was completely transected at the level between T8 and T9 under halothane anaesthesia.[26]The space between the retracted ends of the spinal cord was packed with Gelfoam and the incision was sutured. The

Unidentified dissociated neurons

The dissociated neurons were primarily spherical and rarely had detectable neurites after short term culture (24–36 h). The unlabelled neurons obtained from either spinal intact or spinal transected rats exhibited similar capsaicin sensitivity (CoS precipitate) and neurofilament immunoreactivity (staining with RT97 antibody). In spinal intact (Fig. 1) and spinal transected rats (Fig. 2), respectively, 52.2% (258 of 464 cells) and 54.6% of the cells (260 of 476 cells) exhibited moderate to

Discussion

The present results indicate that in chronic paraplegic rats which are known to have enlarged hyperactive urinary bladders,26, 27, 28afferent neurons innervating the bladder exhibit morphological, immunocytochemical and pharmacological changes. Bladder afferent neurons from paraplegic rats identified by the presence of a fluorescent axonal tracer in L6–S1 DRG sections or dissociated cell cultures were: (i) larger in size, (ii) more likely to exhibit neurofilament immunoreactivity and (iii) less

Conclusions

Spinal cord injury can induce various changes in afferent neurons innervating the urinary bladder in the rat. It is likely that these changes are dependent upon interactions between the hypertrophied target organ and the afferent neurons, possibly mediated by trophic factors released by the bladder smooth muscle.

Acknowledgements

This work was supported in part by NIH grant DK 49430, U.S.A. and Grant-in-Aid (No. 07671720) for Scientific Research from Ministry of Education, Science and Culture, Japan.

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Effects of spinal cord injury on neurofilament immunoreactivity and capsaicin sensitivity in rat dorsal root ganglion neurons innervating the urinary bladder

Abstract

Section snippets

Spinal cord transection

Unidentified dissociated neurons

Discussion

Conclusions

Acknowledgements

Brain Res.

Pain

Brain Res.

J. auton. nerv. Syst.

Trends Neurosci.

Neurosci. Lett.

Prog. Brain Res.

J. auton. nerv. Syst.

Brain Res.

J. auton. nerv. Syst.

Brain Res. Bull.

Neuroscience

Pain

Brain Res.

Neurosci. Lett.

Neuron

Segmental localization of sensory cells that innervate the bladder

J. comp. Neurol.

Nerve growth factor (NGF) differentially regulates the chemosensitivity of adult rat cultured sensory neurons

J. Neurosci.

Early molecular response to rabbit bladder outlet obstruction

Neurourol. Urodyn.

Effects of capsaicin on micturition and associated reflexes in rats

Am. J. Physiol.

Mechanisms underlying the recovery of urinary bladder function following spinal cord injury

J. auton. nerv. Syst.

Mechanisms underlying the recovery of lower urinary tract function following spinal cord injury

Paraplegia