The cutaneous receptive fields, long ascending projections, and responses to colorectal distension (20-100 mmHg) and tail movement of 252 neurons in spinal segments L6-S1 were characterized in pentobarbital- or halothane-N2O anesthetized, physiologically intact male rats. Seventeen additional neurons were studied in spinalized rats. Neurons studied were located within 0.5 mm of the midline at depths 0.2-1.4 mm from the spinal cord dorsum and included the area immediately dorsal and lateral to the central canal. Colorectal distension and/or antidromic invasion from the contralateral ventral quadrant of the cervical spinal cord were used as search stimuli. One hundred seventeen neurons responded to noxious colorectal distension; many had long ascending projections and convergent somatic input from deep joint receptors, ipsilateral perianal/scrotal cutaneous receptive fields, or both. Stimulus-response functions (SRFs) of 45 neurons to graded colorectal distension were linear, allowing extrapolation of threshold distending pressures to neuronal response. Neurons responsive to colorectal distension were subdivided into four classes based on their initial response colorectal distension (75-80 mmHg, 20 s). Short-latency abrupt (SL-A) neurons were excited at short latency by colorectal distension; activity abruptly returned to base line following termination of distension. Most SL-A neurons had long ascending projections, convergent somatic receptive fields, and 4/6 tested were excited by bradykinin administered intraarterially. The threshold distending pressure, estimated from the SRFs of 19 SL-A neurons, extrapolated to 2.7 mmHg. Short-latency sustained (SL-S) neurons were also excited at short latency by colorectal distension, but responses were sustained for 4-120 s following termination of distension. Most SL-S neurons had long ascending projections, convergent somatic receptive fields, and 18/20 tested were excited by intraarterial bradykinin. The threshold distending pressure, estimated from the SRFs of 20 SL-A neurons, extrapolated to 17.0 mmHg. Long-latency (LL) neurons were excited by colorectal distension at long latency following the onset of distension. No LL neurons had demonstrable long ascending projections, and few had convergent excitatory somatic fields. Three of five LL neurons were excited by intraarterial bradykinin. The threshold distending pressure, estimated from the SRFs of six LL neurons, extrapolated to 9.8 mmHg. Inhibited (INHIB) neurons were spontaneously active and were inhibited by colorectal distension.(ABSTRACT TRUNCATED AT 400 WORDS)