Thalamic VPM nucleus in the behaving monkey. I. Multimodal and discriminative properties of thermosensitive neurons.
1. The role of the thalamic ventroposterior medial (VPM) nucleus in the discriminative aspects of nociception and thermoreception was evaluated in alert, trained rhesus monkeys. Single-unit responses were recorded from VPM while the monkeys performed a battery of tasks involving noxious heat, innocuous cool, and air-puff stimuli presented to the face. The discriminative ability of the monkey was compared directly with the responses of single neurons, to determine whether the neuronal response could subserve the monkey's discriminative behavior. 2. Most thermally sensitive neurons exhibited multimodal properties. Only 18% responded exclusively to heat (HT-Heat neurons), whereas 27% responded to innocuous mechanical, as well as noxious mechanical and heat stimuli (WDR-Heat). Twenty-three percent responded to innocuous mechanical stimuli and innocuous skin cooling (Mechano-Cool), and 32% responded to mechanical, innocuous cool, and noxious heat stimuli (WDR-Heat-Cool). 3. Almost all mechanical receptive fields were confined to one division of the trigeminal nerve. This was true for all of the above categories of VPM neurons, even those showing highly convergent properties (WDR-Heat-Cool). 4. Heat-activated neurons produced graded responses to noxious skin heating in the 46 to 49 degrees C range. Stimulus-response functions of neurons that responded to both heat and cool did not differ from those of neurons that responded exclusively to skin heating. 5. When the monkeys were detecting small changes in the intensity of a noxious heat stimulus (e.g., from 47 to 47.1-47.8 degrees C), heat-activated neurons responded to the smallest temperature changes that could be detected by the monkeys. Further, there was a high correlation between the monkey's success in detecting the stimulus changes and the magnitude of the neuronal responses to those changes. 6. Although the responsiveness of VPM cool-activated neurons was not compared with the monkeys' threshold for detecting cooling changes, larger stimulus changes (2 degrees C) that the monkey reliably detected produced significant neuronal responses. Further studies are needed to determine whether VPM neurons respond to the smallest detectable changes in skin cooling. 7. Several thermally sensitive VPM neurons were tested under two attentional conditions: 1) while the monkey was required to attend to a visual stimulus, and 2) while it was required to attend to the thermal stimulus to obtain reward. None showed a significant difference in heat- or cool-evoked activity in the two attentional states.(ABSTRACT TRUNCATED AT 400 WORDS)
Bushnell
M C
MC
Centre de recherche en sciences neurologiques, Université de Montreal, Quebec, Canada.
Duncan
G H
GH
Tremblay
N
N
D000344:Afferent Pathways / Q000502:physiology; D000818:Animals; D001070:Appetitive Behavior / Q000502:physiology; D001288:Attention / Q000502:physiology*; D001931:Brain Mapping; D004193:Discrimination Learning / Q000502:physiology*; D005073:Evoked Potentials, Somatosensory / Q000502:physiology; D005145:Face / Q000294:innervation; D008253:Macaca mulatta; D008297:Male; D008465:Mechanoreceptors / Q000502:physiology; D009474:Neurons / Q000502:physiology; D009619:Nociceptors / Q000502:physiology*; D013787:Thalamic Nuclei / Q000502:physiology*; D013823:Thermoreceptors / Q000502:physiology*; D013697:Thermosensing / Q000502:physiology*; D014110:Touch / Q000502:physiology