Wide dynamic range but not nociceptive-specific neurons encode multidimensional features of prolonged repetitive heat pain

Abstract

1. To better characterize temporal and spatial mechanisms involved in the coding of prolonged nociceptive stimuli in the spinal cord, the responses of dorsal horn wide dynamic range (WDR) and nociceptive-specific (NS) neurons to prolonged, repetitive noxious heat stimuli (45–49 degrees C) were examined in unanesthetized, spinal cord transected rats. To relate these neuronal responses to conscious dimensions of pain, human subjects were presented with identical types of prolonged, repetitive stimuli, so that psychophysical ratings of pain intensity and pain unpleasantness could be compared with the magnitudes and temporal features of the responses of NS and WDR neurons. 2. WDR neurons exhibited high rates of impulse discharge throughout 45 min of repetitive nociceptive stimulation, with only partial reduction (31% decrease from peak rates) occurring after 2 min of stimulation. In sharp contrast, NS neurons stimulated under the same conditions displayed substantial reduction of firing (73% decrease from peak rates) after a brief, initial period of activity that occurred within 2 min after onset of stimulation. Psychophysical ratings of pain intensity and pain unpleasantness, like the responses of WDR neurons, did not decrease substantially from initial levels during 7 min of painful stimulation. Furthermore, these ratings remained at high levels during time periods where the impulse frequencies of NS neurons were only at 27% of maximal levels. 3. Graded nociceptive stimuli were employed to characterize the ability of WDR neurons to encode nociceptive intensity over long durations of repetitive stimulation and to delineate further the relationship between WDR and psychophysical responses. Both WDR discharge frequencies and psychophysical ratings of pain intensity and unpleasantness increased in a monotonic manner to graded increases in stimulus temperatures. 4. These results indicate that pain does not decrease substantially during the course of prolonged, repetitive nociceptive stimulation. The fact that the responses of NS neurons decline significantly, whereas both WDR and psychophysical responses do not, suggests that WDR neurons alone are sufficient to evoke both sensory intensity and affective responses to prolonged pain. Furthermore, because subjects could localize and qualitatively describe pain at times when responses of NS neurons were minimal, WDR neurons alone can encode some spatial and qualitative aspects of pain.