1. Single-unit recordings were made, under moderate gaseous anesthesia (33% O2-66% N2O + 0.5/0.6% halothane), in the ventrobasal (VB) thalamic complex of rats (n = 42) with a mononeuropathy created 2-3 wk beforehand, by four loose ligatures around the common sciatic nerve. Before the recording session, three behavioral nociceptive tests to both mechanical and thermal stimuli revealed that these rats exhibited clear hyperalgesia (excessive reactions to noxious stimuli) and allodynia (nociceptive reactions to stimuli usually perceived as nonnoxious). 2. Neurons, characterized by their responses to manual mechanical stimuli, were classified into two groups: group 1 neurons exclusively driven by light tactile stimuli applied to the receptive field (RF), strictly contralateral to the recording site; and group 2 neurons, driven by sustained pinch applied to a large RF, often bilateral. 3. From the total population of neurons (n = 386), only those responding to stimuli applied to one posterior paw were studied; the proportion (35-40%) of these cells was comparable in each of the two VB: n = 93/262 and 44/124 in the VB contralateral (VBc) and ipsilateral (VBi) to the damaged nerve, respectively. The proportions of each functional group of neurons (group 1 or 2) were also similar on each side. 4. For all group 1 neurons the RFs size was comparable to that observed in normal rats. In the VBi the responses of these neurons presented the classical response pattern observed for VB neurons involved in touch transmission, as did the VBc group 1 neurons with RFs in the saphenous (Sa) territory. In sharp contrast, activities of VBc group 1 neurons with RFs in the sciatic (Sc) nerve territory exhibited several abnormalities: higher background activity, fading of the response with repetitive stimulation, and afterdischarges outlasting the applied stimulus. 5. As in normal rats, 52% of VB group 2 neurons exhibited bilateral symmetrical RFs. Their responses to mechanical stimuli were often greater for stimuli applied to the affected paw, and some of them could be activated by moderate pressure to this paw. Heat responses also illustrated the profound increased sensitivity of the lesioned side, and the activation threshold to thermal stimulation of these group 2 neurons was lowered by 4-6 degrees C compared to normal values. In addition, these neurons responded to immersion of the lesioned paw in a 10 degrees C water bath, a stimulus that was ineffective when applied to the opposite paw.(ABSTRACT TRUNCATED AT 250 WORDS)