Extent of Nociceptive Dermatomes in Adult Rats Is Not Primarily Maintained by Axonal Competition

doi:10.1006/exnr.1997.6734

Experimental Neurology

Volume 150, Issue 1, March 1998, Pages 115-121

https://doi.org/10.1006/exnr.1997.6734 Get rights and content

Abstract

Nociceptive innervation territories of individual peripheral and spinal nerves in the skin of the rat hind paw were investigated. In addition, the hypothesis that competitive interactions among the axons from adjacent dorsal root ganglia (DRG) play an important role in maintenance of dermatomal extent in adult animals was tested. The area of innervation territories of individual spinal and peripheral nerves was determined by nociceptive pinch test of the skin after extirpation of adjacent DRGs or transection of adjacent peripheral nerves, respectively. Positions of nociceptive dermatomes and innervation territories of peripheral nerves were similar to the territories innervated by the C-fibers described earlier by dye extravasation technique. In contrast, our results convincingly demonstrated substantial overlap of nociceptive (probably Aδ) fibers from adjacent dermatomes in which the autonomous innervation areas were only about one-half of the maximal areas. Nociceptive territories of peripheral nerves overlapped, too. Accordingly, we could find no autonomous innervation area of the sural nerve. Two weeks after extirpation of adjacent DRGs, the area of each of the isolated dermatomes L3, L4, and L5 increased only by about 10%, and it did not change detectably during the next 6 months. The results of our study (a) support the view that innervation fields supplied by the nociceptive (probably Aδ) fibers are greater and display more overlap than those supplied by the C-fibers of the same nerve and (b) suggest that axonal competition for innervation territory is not decisive for maintenance of dermatomal borders in the adult rat.

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It is possible that our experimental model did not allow the greater growing potential of the collaterally sprouting sensory axons in females than in males to result in more extensive reinnervation of the skin in the innervation field of the peroneal nerve in the dorsal foot. It has been shown that the nociceptive territories of peripheral nerves in the hind foot of the rat are overlapping and that the sural nerve has no autonomous innervation territory.24 After transection of the peroneal nerve at the beginning of our experiment, the cutaneous axon terminals of the uninjured sural nerve began to collaterally sprout into the adjacent denervated skin of the peroneal nerve territory in the dorsal foot.2,21,23,24,26
Sex-related differences in the recovery of cutaneous nociception after end-to-side nerve repair were examined in rats. Recovery of nociception in the dorsal foot was determined by skin pinch test 19 weeks after the proximal end of the distal stump of the transected peroneal nerve was sutured to the side of the adjacent intact sural nerve (end-to-side nerve coaptation). Axon sprouts in the recipient peroneal nerve were counted by light and electron microscopy. Recovery of nociception due to axon sprouting through the end-to-side coaptation was found in 87% of females and in 60% of males. The area of nociception was not significantly different (P = 0.59) between females and males (13 ± 8% and 11 ± 9%, respectively). The number of myelinated axons in the recipient peroneal nerve (but not of unmyelinated axons) was significantly larger (P = 0.028) in females (median = 512, 25th and 75th percentiles: 467 and 594) than in males (median = 322, 25th and 75th percentiles: 239 and 468). The majority of these axons in females and males were thin fibres, and recipient nerves in both groups were responsive to nerve pinch test. In conclusion, collateral sprouting of thin myelinated nociceptive axons into the end-to-side coapted nerve is more abundant in female than in male rats. However, recovery of cutaneous mechano-nociception due to sprouting of these axons was not different between the two sexes. Possible reasons are discussed.

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Regular ArticleExtent of Nociceptive Dermatomes in Adult Rats Is Not Primarily Maintained by Axonal Competition

Abstract

Exp. Neurol.

Brain Res.

Exp. Neurol.

Neurosci. Lett.

Neurosci. Lett.

Dorsal root ganglia development in chicks following partial ablation of the neural crest

Neurosci. Abstr.

Effects of reduction of nerve centers on the development of residual ganglia and on nerve patterns in the wing of the chick embryo

J. Exp. Zool.

Hyperplasia in the spinal sensory system of the frog. II. Central and peripheral connectivity patterns

J. Comp. Neurol.

Two modes of cutaneous reinnervation following peripheral nerve injury

J. Comp. Neurol.

Endogenous NGF and nerve impulses regulate the collateral sprouting of sensory axons in the skin of the adult rat

J. Neurosci.

The lumbar, sacral and coccygeal tactile dermatomes of the dog

J. Comp. Neurol.

The dermatomes in man

Brain

The formation of appropriate central and peripheral connexions by foreign sensory neurones of the bullfrog

J. Physiol.

The pathology of herpes zoster and its bearing on sensory localization

Brain

Organization of tactile dermatomes, C1 through L4, in cat

J. Neurophysiol.

Absence of functional collateral sprouting of mechanoreceptor axons into denervated areas of mammalian skin

Exp. Neurol.

Regular Article
Extent of Nociceptive Dermatomes in Adult Rats Is Not Primarily Maintained by Axonal Competition