Medullary dorsal horn neuronal activity in rats with persistent temporomandibular joint and perioral inflammation

Studies at spinal levels indicate that peripheral tissue or nerve injury in duces a state of hyperexcitability of spinal dorsal horn neurons that parti cipates in the development of persistent pain and hyperalgesia. It has not been demonstrated that persistent injury in the orofacial region leads to a similar state of central hyperexcitability in the trigeminal system. The p urpose of the present study was to conduct a parametric analysis of the res ponse properties of nociceptive and nonnociceptive neurons in trigeminal nu cleus caudalis (medullary dorsal hem, MDH) in a rat model of persistent oro facial inflammation. Neurons were recorded extracellularly and classified a s low-threshold mechanoreceptive (LTM, n = 49), wide dynamic range (WDR, n = 82), and nociceptive-specific (NS, n = II) neurons according to their res ponse properties to mechanical stimuli applied to their cutaneous receptive fields (RFs). The inflammation was induced 24 h before the recordings by i njecting complete Freund's adjuvant (CFA) into the temporomandibular joint (TMJ) capsule or the perioral (PO) skin. The mean areas of the high-thresho ld RFs of WDR neurons in TMJ (8.66 +/- 0.61 cm(2), n = 25) and PO (5.61 +/- 2.07 cm(2), n = 25) inflamed rats were significantly larger than those in naive rats (1.10 +/- 0.16 cm(2), n = 32). The mean RF size in TMJ-inflamed rats also was significantly larger than that in PO-inflamed rats (P < 0.01) . Furthermore the mean area of the RFs of NS neurons (3.74 +/- 1.44 cm(2), n = 5) was significantly larger in TMJ inflamed rats as compared with naive rats (0.4 +/- 0.09 cm(2), n = 3) (P < 0.05). The background activity in th e TMJ- and PO-inflamed rats was generally greater in WDR and NS neurons, bu t less in LTM neurons, when compared with naive rats. The responses of WDR neurons to noxious mechanical stimuli were increased significantly in TMJ-i nflamed rats (P < 0.05) as compared with naive rats. WDR neuronal responses to mechanical stimulation also were increased in PO-inflamed rats but to a lesser extent than in TMJ-inflamed rats. The injection of CFA into the TMJ or PO skin resulted in reduced responses of LTM neurons to mechanical stim uli. The responses of MDH nociceptive neurons to 48-55 degrees C heating we re greater in inflamed rats as compared with naive rats. A subpopulation of WDR neurons recorded from TMJ (n = 4 of 10) or PO (n = 3 of 13)-injected r ats responded to cooling in addition to heating of the RFs but did not grad e their responses with changes in stimulus intensity. These results indicat e that persistent orofacial inflammation produced hyperexcitability of MDH nociceptive neurons. TMJ inflammation resulted in more robust changes in MD H nociceptive neurons as compared with PO inflammation, consistent with pre vious studies of increased inflammation, increased MDH Fos-protein expressi on, and increased MDH preprodynorphin mRNA expression in this deep tissue o rofacial model of pain and hyperalgesia. The inflammation-induced MDH hyper excitability may contribute to mechanisms of persistent pain associated wit h orofacial deep tissue painful conditions.