The Journal of Neurophysiology Vol. 77 No. 6 June 1997, pp. 3252-3266
Copyright ©1997 The American Physiological Society

Quantitative Analysis of Orofacial Thermoreceptive Neurons in the Superficial Medullary Dorsal Horn of the Rat

W. D. Hutchison, J. Tsoukatos, and J. O. Dostrovsky

Department of Physiology, Medical Sciences, University of Toronto, Toronto, Ontario M5S 1A8, Canada

Hutchison, W. D., J. Tsoukatos, and J. O. Dostrovsky. Quantitative analysis of orofacial thermoreceptive neurons in the superficial medullary dorsal horn of the rat. J. Neurophysiol. 77: 3252-3266, 1997. Surprisingly little is known concerning the central processing of innocuous thermal somatosensory information. The aim of the present study was to obtain quantitative data on the characteristics of neurons in the rat superficial medullary dorsal horn (sMDH) that responded to innocuous thermal stimulation of the rat's face and tongue. Single-unit extracellular recordings were obtained in chloralose-urethane anesthetized rats. A total of 153 thermoreceptive neurons was studied. Of these, 146 were excited by cooling and inhibited by warming and were classified as COLD cells. The remaining seven cells were excited by innocuous warming of the skin or tongue. Of 123 COLD cells tested, 33% were excited by touch and 22% by pinch stimuli delivered to the thermoreceptive field. Of the 50 COLD cells tested, 46% were excited also by noxious heating (50°C for 5 s). Most (82/121) of the receptive fields were located on the upper lip, 25 on the tongue, and most of the remaining on the lower lip. Receptive fields were generally small (1-5 mm²). In some experiments, electrical stimulation in the thalamus was performed, and nine COLD cells could be activated antidromically. The responses of 38 COLD cells to incremental 5°C cooling steps were examined quantitatively. Thermal stimuli were applied to facial or lingual receptive fields of sMDH neurons with a computer-controlled Peltier thermode starting from 33°C, decreasing to 8 or 3°C, and returning to 33°C. Most COLD cells (26/38) had both static and dynamic responses; 7 had mainly dynamic and 5 mainly static responses to step decreases in temperature. Rat sMDH COLD cells could be classified into three groups depending on their stimulus-response functions. The first group (Type 1, n = 19) had a bell-shaped static stimulus response function. The second group (Type 2) had a high maintained or increasing static firing rate as the temperature decreased <18°C (n = 10). Type 3 COLD cells had mainly dynamic properties (n = 7). Many of the cells in all groups were excited by noxious mechanical stimulation. Type 2 cells differed from the other two groups in that most did not respond to noxious thermal stimuli (hot) and many responded to innocuous tactile stimuli. Neurons from each of the three groups of COLD cells could be activated antidromically from contralateral thalamus. These data suggest that there is little central processing of thermal information at the first central synapse for Type 1 neurons, however, the responses of the other two types may be due to central processing and convergence. The demonstration of rat sMDH COLD cells with distinctive stimulus-response functions to thermal shifts suggests separate functional roles of these neurons in the ascending thermal sensory pathway.

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