NEURONS IN THE RAT SPINAL TRIGEMINAL COMPLEX DRIVEN BY CORNEAL NOCICEPTORS - RECEPTIVE-FIELD PROPERTIES AND EFFECTS OF NOXIOUS-STIMULATION OF THE CORNEA

1. A survey of the receptive-field properties of neurons in the spinal trigeminal complex driven by stimulation of corneal afferents has bee n carried out. The afferent inputs to these neurons from the cornea an d from the adjacent skin were studied as well as changes in the excita bility of the cells and in the size of their receptive fields after th ermal noxious stimulation of the cornea.2. Single-unit electrophysiolo gical recordings were made in pentobarbitone anesthetized rats from 54 neurons all of which were activated by mechanical stimulation of the ipsilateral cornea. Seventeen of these neurons were activated only by corneal stimulation and the other 37 had an additional cutaneous recep tive field in the periorbital skin. Of the 37 neurons with a cutaneous receptive field, 29 were activated exclusively by noxious stimulation of the skin (Class 3) and the remaining 8 were driven by both innocuo us and noxious cutaneous stimuli (Class 2). 3. All of the neurons were located in the ventro-lateral area of a region of the spinal trigemin al complex between +0.5 mm and -1.0 m m from the obex. This area corre sponds to the most caudal part of subnucleus interpolaris, the transit ion zone between interpolaris and caudalis and the rostral half of sub nucleus caudalis. Most neurons were located in the superficial layers of this part of the spinal trigeminal complex. No differences were obs erved between the locations of the recording sites of neurons with an exclusive corneal input and those with a corneal and a cutaneous recep tive field. 4. The mean size of the cutaneous receptive field of Class 2 neurons was 45.6 +/- 8 (SE) mm2, whereas Class 3 neurons had signif icantly (P < 0.001) smaller cutaneous fields (mean 15.2 mm2 +/- 2). Th e cutaneous von Frey thresholds of Class 2 neurons were significantly (P < 0.001) lower (8.64 mN +/- 1.8) than those of Class 3 cells (34.34 mN +/- 3.5). Corneal receptive fields included the entire cornea with von Frey thresholds ranging from 0.1 to 2 mN, which indicates that th e corneal input was mediated by mechanosensitive nociceptors. No diffe rences were observed between the corneal thresholds of Class 2 and Cla ss 3 cells or between those of cells with and without additional cutan eous receptive fields. 5. The responses to corneal heating of seven of the neurons in the sample were studied. Of these, six neurons were dr iven only by corneal afferents and one had an additional Class 3 cutan eous receptive field. All seven neurons were excited by the heating st imuli with response thresholds ranging from 41 to 45-degrees-C. All ne urons encoded the intensity of the stimuli with progressively higher f iring rates. 6. After the application of the noxious heating stimuli a ll seven neurons showed additional cutaneous fields that included port ions of the periorbital skin or an enlarged cutaneous field. The mean area of the new and enlarged skin fields was 19.3 mm2 +/- 4. 1. All th e new and enlarged fields were of the Class 3 type, that is, the neuro ns could only be activated by noxious stimulation of the skin and did not respond to innocuous inputs. The new and enlarged fields remained for at least 30 min. Neurons that showed the highest levels of heat-ev oked activity also showed the largest cutaneous fields after the stimu lation. 7. These results show that neurons in the spinal trigeminal co mplex with a corneal input are located in the ventro-lateral region of caudal interpolaris and rostral caudalis and that the vast majority o f them (46/54, 85%) are nociceptor-specific (driven either by corneal nociceptors only or by corneal and cutaneous nociceptors). The recepti ve fields of these neurons can increase in size following corneal noxi ous stimulation, which suggests some plasticity in the corneal nocicep tive pathway. However, these plastic changes do not seem to alter the basic nociceptive-specific properties of the cells.