Medullary dorsal horn neurons with trigeminal sensory properties have been previously shown to have additional responses associated with cues relevant to the successful execution of a behavioral task. These "task-related" responses were evoked by environmental cues but were independent of the specific stimulus parameters. We have examined further the characteristics of task-related responses in medullary dorsal horn neurons of three monkeys. Single-unit activity was recorded while the monkeys were performing behavioral tasks that required them to discriminate thermal or visual stimuli for a liquid reward. Forty-five percent (34/75) of the medullary dorsal horn neurons studied exhibited task-related activity that was significantly correlated with the stereotypical behavioral events that occurred during the tasks. Similar events occurring outside of the task produced no response. In addition to the task-related activity of these medullary dorsal horn neurons, responses to mechanical and/or thermal stimuli presented within the neuron's receptive field were demonstrated in 28 of 34 cases. These sensory responses also were evoked by the same stimuli presented outside of the behavioral task. Fifteen of the neurons with task-related responses could be activated antidromically from thalamic stimulating electrodes. Task-related responses were categorized according to their relationship to the three phases of the behavioral trial: trial initiation, trial continuation, and trial termination. Although an individual task-related response was associated with a single behavioral event, most medullary dorsal horn neurons (30/34) exhibited a reproducible pattern of task-related responses that occurred during more than one phase of the trial. Trial-initiation task-related responses were subdivided depending on their correlation with specific events that occurred within that phase of the trial. One-third of the 18 excitatory trial-initiation responses were associated with the visual stimulus that cued the monkey to begin the trial; the remaining two-thirds were associated with the monkey's press of the button that actually initiated the trial. Trial-continuation task-related responses (observed while the monkey waited for a thermal stimulus that triggered a rewarded motor response) were shown to be independent of the actual temperature of the thermal stimulus. In addition these trial-continuation task-related responses were also noted during trials without a thermal stimulus, in which the trigger cue was the onset of a light (in a visual task).(ABSTRACT TRUNCATED AT 400 WORDS)