SOMATOSENSORY, MULTISENSORY, AND TASK-RELATED NEURONS IN CORTICAL AREA 7B (PF) OF UNANESTHETIZED MONKEYS

1. The goal of this study was to quantitatively characterize the respo nse properties of somatosensory and multisensory neurons in cortical a rea 7b (or PF) of monkeys that were behaviorally trained to perform an appetitive tolerance-escape task. Particular emphasis was given to ch aracterizing nociceptive thermal responses and correlating such respon ses to thermal pain tolerance as measured by escape frequency. 2. A to tal of 244 neurons that responded to somatosensory stimulation alone o r to both somatosensory and visual stimulation (multisensory) were iso lated and studied in the trigeminal region of cortical area 7b. Thirty neurons responded only to visual stimulation. Thermoreceptive neurons formed similar to 13% (31 of 244) of the neurons that had somatosenso ry response properties. Thermal nociceptive neurons made up similar to 9% (21 of 244) of the neurons that had somatosensory response propert ies or similar to 68% (21 of 31) of the neurons that had thermorecepti ve response properties. Thermal nociceptive neurons responded either e xclusively to noxious thermal stimuli (high-threshold thermoreceptive, HTT) or differentially to nonnoxious and noxious thermal stimuli (wid e-range thermoreceptive, WRT). Multimodal HTT neurons had nonnocicepti ve (low-threshold mechanoreceptive, LTM) and/or nociceptive (nocicepti ve-specific, wide-dynamic-range) mechanical receptive fields, whereas multimodal WRT neurons had only nonnociceptive (LTM) mechanical recept ive fields. Thermal nonnociceptive neurons (low-threshold thermorecept ive, LTT) made up similar to 3% (8 of 244) of the neurons that had som atosensory properties or similar to 26% (8 of 31) of the neurons that were thermoreceptive. The background discharge of two thermoreceptive neurons (6%, 2 of 31) was inhibited by innocuous thermal stimulation. 3. Thermal nociceptive neurons (HTT and WRT) were functionally differe ntiated by statistical analyses into subpopulations that did encode (H TT-EN, WRT-EN) and did not encode (HTT-NE, WRT-NE) the magnitude of no xious thermal stimulus intensities. The mean slopes and median regress ion coefficients for the stimulus-response (S-R) functions of HTT-EN a nd WRT-EN neurons, respectively, were significantly greater than those for the S-R functions of HTT-NE and WRT-NE neurons. In contrast to HT T-NE and WRT-NE neurons, HTT-EN and WRT-EN neurons reliably encoded th e magnitude of noxious thermal intensity by grading their mean dischar ge frequency. 4. The S-R functions of HTT-EN and WRT-EN neurons, unlik e those of HTT-NE and WRT-NE neurons, closely approximated stimulus in tensity-escape frequency functions. The S-R function of an individual HTT-EN or WRT-EN neuron, in contrast to the S-R function of an HTT-NE or WRT-NE neuron, was found to be significantly correlated to the beha vioral S-R function from each respective monkey. 5. Some HTT and WRT n eurons (7 of 21) were multisensory and responded to stimulation of spa tially aligned visual and cutaneous receptive fields. Threatening or n ovel visuosensory stimuli that approached the face along a trajectory aligned with the most sensitive portion of the cutaneous receptive fie ld evoked the highest mean discharge frequency. Visuosensory responses were often sustained by holding the visual targets close to the cutan eous receptive field. The maximum peak discharge frequencies in respon se to noxious thermal and visual stimulation were approximately equal. 6. A total of 36 task-related neurons were either inhibited or excite d during performance of the appetitive tolerance-escape task without t hermal stimulation applied to the face. Inhibition of activity in some task-related neurons (11 of 17 tested) was reversed by innocuous or n oxious heating of the face. 7. Histological reconstruction of recordin g sites in the area 7b revealed no somatotopic representation of the t rigeminal nerve subdivisions, no visuotopic representation of visual s pace, and no functional segregation of cell types (i.e., HTT, WRT, LTT ). 8. The sources of afferent nociceptive input to the first and secon d somatosensory cortices and area 7b as well as the response propertie s of nociceptive neurons in these cortical areas are discussed with re spect to current concepts of serial and parallel processing of somatos ensory information in the primate cortex. Converging lines of evidence from both clinical and experimental studies support a role for area 7 b in nociception and pain perception and in spatially directed attenti on. 9. A synthesis of evidence from many fields of study indicates tha t area 7b is an important site for multisensory convergence and integr ation of somatosensory and visual inputs. The functional and behaviora l significance of multisensory integration in area 7b is discussed wit h a special emphasis on nociceptive information processing.