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Optically Recorded Response of the Superficial Dorsal Horn: Dissociation From Neuronal Activity, Sensitivity to Formalin-Evoked Skin Nociceptor Activation

¹Department of Cell and Molecular Physiology and ²Department of Biomedical Engineering School of Medicine, University of North Carolina, Chapel Hill, North Carolina

Submitted 22 September 2004; accepted in final form 24 February 2005

In rat spinal cord, slice repetitive electrical stimulation of the dorsal root at an intensity that activates C-fibers evokes a slow-to-develop and prolonged (30–50 s) change in light transmittance (OIS_DR) in the superficial part of the ipsilateral dorsal horn (DH_s). Inhibition of astrocyte metabolism [by bath-applied 400 µM fluoroacetate and 200 µM glutamine (FAc + Gln)] or interference with glial and neuronal K⁺ transport [by 100 µM 4-aminopyridine (4-AP)] leads to dissociation of the OIS_DR and the postsynaptic DH_s response to a single-pulse, constant-current dorsal root stimulus (P-PSP_DR). The OIS_DR decreases under FAc+Gln, whereas the P-PSP_DR remains unaltered; under 4-AP, the P-PSP_DR increases, but the OIS_DR decreases. In contrast, both the OIS_DR and P-PSP_DR increase when K⁺o is elevated to 8 mM. These observations from slices from normal subjects are interpreted to indicate that the OIS_DR mainly reflects cell volume and light scattering changes associated with DH_s astrocyte uptake of K⁺ and glutamate (GLU). In slices from subjects that received an intracutaneous injection of formalin 3–5 days earlier, both the OIS_DR and the response of the DH_s ipsilateral to the injection site to 100-ms local application (via puffer pipette) of 15 mM K⁺ or 100 µM GLU were profoundly reduced, and the normally exquisite sensitivity of the DH_s to elevated K⁺o is decreased. Considered collectively, the observations raise the possibility that impaired regulation of DH_s K⁺o and GLU_o may contribute to initiation and maintenance of the CNS pain circuit and sensorimotor abnormalities that develop following intracutaneous formalin injection.

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