Explosive Autotomy Induced by Simultaneous Dorsal Column Lesion and Limb Denervation: A Possible Model for Acute Deafferentation Pain

Abstract

We report on a new "explosive" form of self-mutilation behavior (autotomy) characterized by rapid onset (1-2 days), short duration (1-2 days), and unpredictable progression. The possible neural mechanism(s) underlying this novel behavior were examined in rats by combining at varying time intervals one leg denervation with a lesion to the dorsal columns (DC lesion) or to a dorsolateral funiculus (DLF lesion). DC lesion, followed immediately by leg denervation, resulted in explosive autotomy in 62% of the rats and regular autotomy in 25% of the rats. Regular autotomy was characterized by slow onset (2-3 weeks), prolonged duration (2-3 weeks), and stereotyped progression from distal to proximal parts of the leg. DC lesion, followed 1 week later by leg denervation, resulted in regular autotomy in 71% of the rats which was not different from autotomy resulting from denervation alone. DC lesion preceded 1 week earlier by leg denervation resulted in slightly accelerated regular autotomy in 77% of the rats. Simultaneous DC lesion and leg denervation immediately preceded by application of a local anesthetic (4% procaine) for 30 or 60 min to the exposed lumbar spinal cord resulted in regular autotomy in all rats. All rats in a sham group, in which the procaine was replaced by normal saline, exhibited explosive autotomy. DLF lesion, followed immediately by leg denervation, resulted in accelerated regular autotomy. Our results support the hypothesis that explosive autotomy, following simultaneous DC lesion and leg denervation, could be due to the simultaneous injury to the peripheral and central ends of the primary afferent neurons that are involved in either nociceptive transmission or modulation, combined with injury to other afferent fibers involved in nociceptive transmission. It is felt that explosive autotomy could serve as an animal model for acute deafferentation pain exhibited by patients following acute neural trauma.