The Journal of Neurophysiology Vol. 82 No. 5 November 1999, pp. 2092-2107
Copyright ©1999 by the American Physiological Society

Responses of Medullary Dorsal Horn Neurons to Corneal Stimulation by CO₂ Pulses in the Rat

Departments of  ¹Neuroscience and  ²Surgery, Brown University/Rhode Island Hospital, Providence, Rhode Island 02903; and  ³Faculty of Dentistry, University of Toronto, Toronto, Ontario M5G 1G6, Canada

Hirata, Harumitsu, James W. Hu, and David A. Bereiter. Responses of Medullary Dorsal Horn Neurons to Corneal Stimulation by CO₂ Pulses in the Rat. J. Neurophysiol. 82: 2092-2107, 1999. Corneal-responsive neurons were recorded extracellularly in two regions of the spinal trigeminal nucleus, subnucleus interpolaris/caudalis (Vi/Vc) and subnucleus caudalis/upper cervical cord (Vc/C1) transition regions, from methohexital-anesthetized male rats. Thirty-nine Vi/Vc and 26 Vc/C1 neurons that responded to mechanical and electrical stimulation of the cornea were examined for convergent cutaneous receptive fields, responses to natural stimulation of the corneal surface by CO₂ pulses (0, 30, 60, 80, and 95%), effects of morphine, and projections to the contralateral thalamus. Forty-six percent of mechanically sensitive Vi/Vc neurons and 58% of Vc/C1 neurons were excited by CO₂ stimulation. The evoked activity of most cells occurred at 60% CO₂ after a delay of 7-22 s. At the Vi/Vc transition three response patterns were seen. Type I cells (n = 11) displayed an increase in activity with increasing CO₂ concentration. Type II cells (n = 7) displayed a biphasic response, an initial inhibition followed by excitation in which the magnitude of the excitatory phase was dependent on CO₂ concentration. A third category of Vi/Vc cells (type III, n = 3) responded to CO₂ pulses only after morphine administration (>1.0 mg/kg). At the Vc/C1 transition, all CO₂-responsive cells (n = 15) displayed an increase in firing rates with greater CO₂ concentration, similar to the pattern of type I Vi/Vc cells. Comparisons of the effects of CO₂ pulses on Vi/Vc type I units, Vi/Vc type II units, and Vc/C1 corneal units revealed no significant differences in threshold intensity, stimulus encoding, or latency to sustained firing. Morphine (0.5-3.5 mg/kg iv) enhanced the CO₂-evoked activity of 50% of Vi/Vc neurons tested, whereas all Vc/C1 cells were inhibited in a dose-dependent, naloxone-reversible manner. Stimulation of the contralateral posterior thalamic nucleus antidromically activated 37% of Vc/C1 corneal units; however, no effective sites were found within the ventral posteromedial thalamic nucleus or nucleus submedius. None of the Vi/Vc corneal units tested were antidromically activated from sites within these thalamic regions. Corneal-responsive neurons in the Vi/Vc and Vc/C1 regions likely serve different functions in ocular nociception, a conclusion reflected more by the difference in sensitivity to analgesic drugs and efferent projection targets than by the CO₂ stimulus intensity encoding functions. Collectively, the properties of Vc/C1 corneal neurons were consistent with a role in the sensory-discriminative aspects of ocular pain due to chemical irritation. The unique and heterogeneous properties of Vi/Vc corneal neurons suggested involvement in more specialized ocular functions such as reflex control of tear formation or eye blinks or recruitment of antinociceptive control pathways.