Footshock stress differentially affects responses of two subpopulations of spinal dorsal horn neurons to urinary bladder distension in rats

This investigation examined the effect of footshock on responses of 283 spinal dorsal horn neurons (DHNs) to urinary bladder distension (UBD). Female rats were treated with seven daily sessions of footshock (chronic footshock, CFS), six accommodation sessions followed by one exposure to footshock (acute footshock, AFS) or handled similarly without receiving any footshock (no footshock, NFS). After the final footshock or NFS session, rats were anesthetized, a laminectomy performed and extracellular single-unit recordings of L6–S1 DHNs obtained in intact or spinalized preparations. Neurons were classified as Type I—inhibited by heterotopic noxious conditioning stimuli (HNCS) or as Type II—not inhibited by HNCS—and characterized for spontaneous activity and for neuronal discharges evoked by graded UBD. A differential effect of footshock-induced stress was noted on neuronal subgroups. In intact preparations, Type I neurons were less responsive to UBD after either chronic or acute stress, while Type II neurons demonstrated significantly augmented responses to UBD. This enhanced neuronal responsiveness to UBD was present in spinalized preparations following exposure to CFS but not AFS. Type I neurons were still less responsive to stress in spinalized preparations following CFS and AFS. This study provides further evidence that (1) at least two populations of spinal neurons exist which encode for visceral stimuli and are likely to have distinct roles in visceral nociception, and that (2) the chronic stress-induced enhancement of DHN responses to UBD involves changes at the spinal level while the acute stress effects are dependent on a supraspinal substrate.

Research Highlights
► The effect of footshock stress on spinal neuronal responses to bladder distension was assessed.
► Type I neurons were less responsive to bladder distension after footshock stress.
► Type II neurons demonstrated enhanced excitability to bladder distension.
► Spinalization abolished the enhanced responsiveness to UBD only after an acute footshock stressor.
► Chronic and acute stress involves spinal and supraspinal substrates, respectively.