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The Journal of Neuroscience, February 15, 2000, 20(4):1538-1549

Synaptic Reorganization in the Substantia Gelatinosa After Peripheral Nerve Neuroma Formation: Aberrant Innervation of Lamina II Neurons by A Afferents

Ikuhide Kohama, Kuniko Ishikawa, and Jeffery D. Kocsis

Department of Neurology and PVA/EPVA Neuroscience Research Center, Yale University School of Medicine, New Haven, Connecticut 06510, and Rehabilitation Research Center, Veterans Affairs Medical Center, West Haven, Connecticut 06516

Intracellular recording and extracellular field potential (FP) recordings were obtained from spinal cord dorsal horn neurons (laminae I-IV) in a rat transverse slice preparation with attached dorsal roots. To study changes in synaptic inputs after neuroma formation, the sciatic nerve was sectioned and ligated 3 weeks before in vitro electrophysiological analysis. Horseradish peroxidase labeling of dorsal root axons indicated that A fibers sprouted into laminae I-II from deeper laminae after sciatic nerve section. FP recordings from dorsal horns of normal spinal cord slices revealed long-latency synaptic responses in lamina II and short-latency responses in lamina III. The latencies of synaptic FPs recorded in lamina II of the dorsal horn after sciatic nerve section were reduced. The majority of monosynaptic EPSPs recorded with intracellular microelectrodes from lamina II neurons in control slices were elicited by high-threshold nerve stimulation, whereas the majority of monosynaptic EPSPs recorded in lamina III were elicited by low-threshold nerve stimulation. After sciatic nerve section, 31 of 57 (54%) EPSPs recorded in lamina II were elicited by low-threshold stimulation. The majority of low-threshold EPSPs in lamina II neurons after axotomy displayed properties similar to low-threshold EPSPs in lamina III of control slices. These results indicate that reoccupation of lamina II synapses by sprouting A fibers normally terminating in lamina III occurs after sciatic nerve neuroma formation. Furthermore, these observations indicate that the lamina II neurons receive inappropriate sensory information from low-threshold mechanoreceptor after sciatic nerve neuroma formation.

Key words: axotomy; neuroma; synaptic reorganization; dorsal horn; substantia gelatinosa; A afferents; pain

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Copyright © 2000 Society for Neuroscience  0270-6474/00/2041538-12$05.00/0

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