The present study analyzes the activity of 120 neurons recorded in the two ventro-postero-medial (VPM) nuclei of the thalamus in a rat model of trigeminal neuropathic pain. Twenty-eight rats were tested 2 weeks after a chronic constriction injury (CCI) of the infraorbital nerve (IoN). These animals exhibited violent pain-related reactions to extremely weak mechanical stimuli applied to the lesioned and, to a lesser extent, unlesioned IoN territories. The activities of neurons recorded in the VPMc (n = 80) and VPMi (n = 40), contralateral and ipsilateral to the injured nerve, respectively, were compared with those of 62 neurons recorded in the VPM of ten normal rats (VPMn). The neuronal background activity was higher in the VPM of CCI-IoN rats than in normal rats (about 4 vs 1 spike/s). The proportion of neurons which were driven by mechanical stimulations applied contralaterally to their recording site, was comparable in the three VPM (63-70%), but the effective stimulus modality differed significantly between the normal and the lesioned rats. In particular, the number of neurons driven by vibrissa or guard hair movements dramatically decreased in the VPM of CCI-IoN rats, mainly in the VPMc (67% of neurons with a receptive field (RF) in the VPMn vs 12% in the VPMc). Inversely, a consistent number of neurons in both the VPMc and VPMi were driven by other stimulus modalities applied to the IoN territory (moderate pressure for VPMc neurons, pinch or pinprick for both VPMc and VPMi neurons). The responses so induced were especially intense and included afterdischarges. In contrast to the VPMn neurons, the RFs of both the VPMc and VPMi neurons included two vibrissae at least, and were occasionally discontinuous and multimodal, including both vibrissae and cutaneous areas for VPMc units. The bilateral changes in VPM responsiveness and in behavior suggest the involvement of central processing of sensory information, which are set off by the CCI-IoN. The putative mechanisms and functional implication of the changes in the VPM neuronal activities are discussed.