Cross-inhibition of mechanoreceptive inputs in dorsal root ganglia of peripheral inflammatory cats

Abstract

Primary afferent neurons in mammalian dorsal root ganglia (DRGs) normally function as independent sensory communication elements. However, it has recently been shown that most DRG neurons are transiently activated when axons of neighboring neurons of the same ganglion are stimulated repetitively and the cross-depolarization contributes to this mutual cross-excitation. Here, we reported the cross-inhibition of mechanoreceptive information in DRG under peripheral inflammatory condition. Intracellular recordings were made in vivo from A-type afferent neurons in cat L 6–7 DRGs. Among spontaneously firing neurons both from control (Con) and carrageenan (Carg) injected cats, some A-type afferent neurons showed to have two distinct receptive fields on the hindpaw. Mechanical stimulation of one receptive field increased the ongoing activities, while stimulation of the other receptive field led to a decrease of spontaneous firings of the same neuron. These two distinct receptive fields are termed excitatory receptive field (ERF) and inhibitory receptive field (IRF), respectively. Peripheral inflammation significantly increased the prevalence of Aβ and Aδ neurons with two distinct receptive fields (Aβ: Con, 1.34%, n=149; Carg, 6.59%, n=182; P<0.05; Aδ: Con, 0%, n=138, Carg, 3.9%, n=102, P<0.05). Most interestedly, ERF stimulation-induced enhancement of cell firings can be suppressed by IRF stimulation. Similarly, IRF stimulation-induced decrease of cell discharges can be reversed by ERF stimulation. This interaction was not affected by cutting the dorsal roots at the place close to the recorded DRG. Preapplication of naloxone and yohimbine did not block the interaction. Taken together with previous reports, this intraganglionic cross-talking appears to be mediated by collision of retrograde spread of action potentials, or/and at least in part, by an activity-dependent diffusible excitatory substance released from neuronal somata and/or adjacent axons, and detected by neighboring cell somata.