1. The extracellular activity of 196 single neurons in subnucleus caudalis (medullary dorsal horn) of the trigeminal (V) spinal tract nucleus was examined in chloralose-anesthesized, paralyzed cats. Electrical, mechanical, and algesic chemical stimuli were applied to the exposed temporomandibular joint (TMJ) in order to activate TMJ afferents. Seventy-eight neurons were studied that responded to electrical stimulation of the TMJ at a mean latency of 9.9 +/- 4.8 (SD) ms. 2. All neurons with TMJ input received additional afferent input, predominantly from facial skin or intraoral sites. Caudalis neurons were classified on the basis of their cutaneous mechanoreceptive field properties as low-threshold mechanoreceptive (LTM), wide dynamic range (WDR), or nociceptive specific (NS); a few neurons unresponsive to cutaneous stimuli were responsive to manipulation of deep subcutaneous structures. A sample of caudalis neurons was tested for responsiveness to electrical TMJ stimulation after the mechanoreceptive field properties of the neurons were determined. In this sample, 24% of the LTM neurons, 29% of the WDR neurons, 36% of the NS neurons, and 57% of the neurons with input from deep structures were responsive to TMJ stimulation. The WDR and NS neurons with TMJ inputs had mechanoreceptive field properties and laminar locations in caudalis that were comparable to those previously described for cutaneous nociceptive neurons in caudalis; also in accordance with recent studies, 74% of the neurons tested showed convergence of tooth pulp and/or hypoglossal (XII) nerve afferent inputs. 3. In contrast to the LTM neurons, the WDR and NS neurons were especially responsive to intense mechanical and algesic chemical stimulation of the TMJ as well as to electrical stimulation of TMJ afferents. For example, 71% of the WDR and NS neurons excited by electrical stimulation of the TMJ afferents and tested for their responsiveness to injections of algesic chemicals (7% NaCl, KCl, bradykinin, histamine) into the TMJ responded to at least one of these chemicals. The temporal characteristics of these responses were quantified. 4. The TMJ afferent inputs to the WDR and NS neurons were considered to be predominantly of a nociceptive character because of (1) the long latency and high threshold of most TMJ-evoked responses, which are consistent with previous demonstrations that small-diameter afferents predominantly supply the TMJ and, (2) the preferential responsiveness to noxious mechanical and chemical stimulation of TMJ afferents of neurons which were functionally identified as cutaneous nociceptive neurons.(ABSTRACT TRUNCATED AT 400 WORDS)