We analyzed the activity of 51 trigeminothalamic neurons in the medullary dorsal horn (trigeminal nucleus caudalis) of monkeys during the performance of behavioral tasks requiring the monkeys to discriminate innocuous and noxious thermal stimuli applied to the face and to detect the onset of visual stimuli. Static properties of trigeminothalamic neurons in behaving monkeys were similar to those in anesthetized monkeys. Responses to passively presented mechanical and thermal stimuli, receptive-field properties, and conduction velocities did not differ in the awake and anesthetized states. For most wide dynamic range and nociceptive-specific trigeminothalamic neurons, there was a negative correlation between the magnitude of thermally evoked activity and behavioral latencies to discriminate 47 and 49 degrees C stimuli. Thus, both groups of neurons provide information that could be used by the monkey to discriminate noxious thermal stimuli. The magnitude of thermal responses of trigeminothalamic neurons was modulated by the behavioral significance of the stimulus. Behaviorally relevant thermal stimuli presented during the thermal discrimination task produced a greater neuronal response than equivalent irrelevant thermal stimuli presented between behavioral trials or presented while the monkey performed the visual detection task. Neurons whose activity is modulated by behavioral state are likely to be involved in discrimination of thermal stimuli, since the activity of these neurons correlates with the behavioral response to the stimuli and information from the modulated neurons is sent to the thalamus. Some trigeminothalamic neurons that exhibited somatosensory responses also responded to behaviorally relevant stimuli and events associated with trial initiation and receipt of reward in the behavioral tasks. Similar events outside a behavioral task evoked no neuronal responses. These task-related responses were similar to those described previously for medullary dorsal horn neurons not identified as to projection sites (14).(ABSTRACT TRUNCATED AT 400 WORDS)