Single neurons were recorded from the ventral posteromedial thalamic nucleus (VPM) of urethan-anesthetized rats. Six of these animals were intact, 28 sustained kainic acid (KA) lesions of trigeminal nucleus principalis (PrV), and 9 received similar lesions of trigeminal subnucleus interpolaris (SpVi). Four animals sustained PrV lesions that were followed, at an interval of 1-3 mo, by KA injections into SpVi. Special attention was paid to the receptive-field characteristics of neurons that were sensitive to deflection of the mystacial vibrissae. In normal animals, we recorded a total of 167 VPM neurons, 85% (n = 142) of which were vibrissa sensitive. The remaining VPM cells were excited by either guard hair deflection (8.4%), indentation of the skin (0.6%), or deflection of either vibrissae or guard hairs (1.8%). Seven cells (4.2%) were unresponsive. The topography of the trigeminal representation in VPM was similar to that reported previously by Waite (59). Vibrissa-sensitive neurons in intact rats generally gave rapidly adapting responses (84.5%), and only 16.2% were directionally selective. The vast majority (80.3%) of the vibrissa-sensitive cells were activated by deflection of only one whisker (1.2 +/- 0.5, mean +/- SD); none were excited by deflection of more than four vibrissae. Injections of KA into SpVi of otherwise intact rats (n = 9) had no appreciable effect on the receptive-field characteristics of vibrissa-sensitive VPM neurons. Injections of KA into PrV markedly altered the receptive-field properties of VPM cells. Recordings were made from 45 VPM neurons over a period extending from 0 to 10 h after KA injections into PrV in five rats. Of these cells, 4.4% were excited by vibrissa deflection and the remainder were unresponsive. Additional recordings from SpVi and the superior colliculus of these same animals indicated that the neurotoxin probably did not damage interpolaris neurons or their axons. Recordings were made from 394 VPM cells in 22 rats that survived 1-6 days after KA lesions of PrV. These experiments demonstrated an increase in the number of thalamic cells that were responsive to peripheral stimulation over this period. By 6 days after the lesion (4 animals), 52.8% of the 73 VPM neurons we recorded were excited by somatosensory stimuli. Of these, 89.5% were activated by deflection of one or more mystacial vibrissae. The average number of whiskers that excited a given VPM cell in these rats was 6.3 +/- 2.0 (SD). Recordings were made from VPM in five rats that survived 30-90 days after KA injections in PrV.(ABSTRACT TRUNCATED AT 400 WORDS)