The response characteristics of lamina I neurones recorded extracellularly in the lumbosacral enlargement of chloralose-anaesthetized cats were examined with peripheral nerve electrical stimulation, adequate mechanical and thermal stimulation of hind-limb skin, and algesic mechanical and chemical stimulation of musculotendinous structures, particularly the gastrocnemius-soleus (g.s.) muscle. Antidromic activation from an electrode array that spanned the contralateral thalamus was used to identify lamina I spinothalamic tract (lam.I-s.t.t.) neurones. Recordings were made from a total of 218 lumbosacral lam.I-s.t.t. neurones. Their mean central conduction latency was 90.1 ms (range 20-300 ms), corresponding to a mean conduction velocity of 3.7 m/s (range 1.1-16.7). Neurones responsive only to peripheral A delta fibre stimulation had significantly shorter central conduction latencies (mean = 62.8 ms) than those with both A delta and C fibre input (mean = 81.9 ms) and those with only C fibre input (mean = 134.6 ms). Of these 218 neurones, 103 (47%) projected only to medial thalamus, 41 (19%) only to lateral thalamus, and 56 (26%) to both; 18 (8%) were classified as mid-thalamic projecting cells. About 10% of all cells had ongoing activity when first isolated. Ninety-three lam.I-s.t.t. neurones responded to stimulation of the sciatic nerve. The response characteristics of forty-seven of these were examined with the complete set of stimuli used. Twenty-four non-s.t.t. lamina I neurones were also characterized for comparison. Twenty-eight of the lam.I-s.t.t. neurones tested with the complete set of stimuli responded specifically to either cutaneous noxious (n = 19), cutaneous innocuous cold (n = 6) or algesic musculo-tendinous (n = 3) stimulation. Thirteen neurones responded to cutaneous noxious stimulation, and, in addition, to cold stimulation (n = 6), to deep stimulation (n = 4), or to both (n = 3). Six cells did not respond to any of the natural stimuli employed. All of the cold-specific and many of the multireceptive cold-sensitive neurones had ongoing discharge. The average central conduction latencies of cold-sensitive neurones (65.5 ms) and unresponsive neurones (48.7 ms) were shorter than that of nociceptive neurones (91.2 ms). Two response categories had distinct thalamic projection patterns. The majority of cold-specific neurones projected only to medial thalamus. Almost all multireceptive cold-sensitive neurones projected to both medial and lateral thalamus.(ABSTRACT TRUNCATED AT 400 WORDS)