Neonatal hind paw injury alters processing of visceral and somatic nociceptive stimuli in the adult rat

Abstract

Tissue damage during the first few weeks after birth can have profound effects on sensory processing in the adult. We have recently reported that a short-lasting inflammation of the neonatal rat hind paw produces baseline hypoalgesia and exacerbated hyperalgesia after reinflammation of that hind paw in the adult. Because the contralateral hind paw and forepaws also displayed hypoalgesia, we speculated that effects of the initial injury were not somatotopically restricted and would alter visceral sensory processing as well. In the present study we tested this hypothesis by examining the effects of neonatal hind paw injury at P3 or P14 on visceral and somatic sensitivity in the adult rat. In P3 rats, the visceromotor response evoked by colorectal distention in the absence of colonic inflammation was attenuated in carrageenan-treated neonatal rats compared to naive rats. Colonic inflammation in the adult reversed this hypoalgesia and evoked a level of visceral hyperalgesia similar to naive rats. There were no consequences of the P14 injury observed in the adult. In a second experiment, colonic inflammation in naive rats induced viscerosomatic inhibition to thermal stimulation of the forepaw and hind paw. This inhibition was reversed, and the paw withdrawal latency was slightly decreased in neonatal (P3) carrageenan-treated rats. Rats treated on P14 appeared similar to naive rats. These data support the hypothesis that neonatal hind paw injury during a critical period permanently alters sensory processing of multiple sensory modalities in the adult. Animals develop with greater inhibitory processing of somatic and visceral stimuli throughout the neuraxis. However, inflammation in the adult in previously uninjured tissue reverses the hypoalgesia and evokes development of normal hyperexcitability associated with tissue injury.

Perspective: Trauma experienced by premature infants can lead to alterations in sensory processing throughout life. This study shows that short-term somatic tissue injury to neonatal rats during a well-defined critical period alters several aspects of viscerosensory processing in the adult, demonstrating that injury to one tissue affects sensory processing throughout the body.