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

W. D. Hutchison, J. Tsoukatos, J. O. Dostrovsky
1997 Journal of Neurophysiology  
Quantitagion in many species (mouse, rat, guinea pig, rabbit, bat, tive analysis of orofacial thermoreceptive neurons in the superficial cat, monkey, and human) (Boman 1958; Davies et al. 1985; medullary dorsal horn of the rat. J. Neurophysiol. 77: 3252-3266, Dubner et al. 1975; Duclaux et al. 1980; Heinz et al. 1990; 1997 . Surprisingly little is known concerning the central processing Hellon 1983; Hensel and Kenshalo 1969; Molinari and Kensof innocuous thermal somatosensory information. The
more » ... information. The aim of the halo 1977; Perl 1990; Poulos and Lende 1970a,b; Sumino present study was to obtain quantitative data on the characteristics and Dubner 1981). Most of these studies reported the exisof neurons in the rat superficial medullary dorsal horn (sMDH) tence of cooling specific (COLD) primary afferents and that responded to innocuous thermal stimulation of the rat's face failed to find afferents responding to innocuous warming of and tongue. Single-unit extracellular recordings were obtained in the orofacial region, probably because WARM fibers are chloralose-urethane anesthetized rats. A total of 153 thermoreceptive neurons was studied. Of these, 146 were excited by cooling less numerous and more difficult to record from because and inhibited by warming and were classified as COLD cells. The they are unmyelinated. COLD primary afferent fibers are remaining seven cells were excited by innocuous warming of the excited by cooling stimuli and decrease their firing rate in skin or tongue. Of 123 COLD cells tested, 33% were excited by response to warming of the receptive field. They have protouch and 22% by pinch stimuli delivered to the thermoreceptive nounced dynamic responses to cooling steps and adapt to a field. Of the 50 COLD cells tested, 46% were excited also by static firing rate that is dependent on skin temperature and noxious heating (¢50ЊC for 5 s). Most (82/121) of the receptive that is maximal at Ç18-25ЊC. Most reports indicate that fields were located on the upper lip, 25 on the tongue, and most static firing of COLD primary afferents drops markedly or of the remaining on the lower lip. Receptive fields were generally ceases at temperatures õ18ЊC, although a few reports have small (1-5 mm 2 ). In some experiments, electrical stimulation in revealed the existence of some afferents that maintain or the thalamus was performed, and nine COLD cells could be activated antidromically. The responses of 38 COLD cells to incremen-even increase their firing at lower temperatures (Hensel and tal 5ЊC cooling steps were examined quantitatively. Thermal stim-Kenshalo 1969; LaMotte and Thalhammer 1982). COLD uli were applied to facial or lingual receptive fields of sMDH fibers have small punctate receptive fields, and slowly conneurons with a computer-controlled Peltier thermode starting from ducting axons, which are primarily in the Ad range although 33ЊC, decreasing to 8 or 3ЊC, and returning to 33ЊC. Most COLD some COLD C fibers have been reported in the limb (Lacells (26/38) had both static and dynamic responses; 7 had mainly Motte and Thalhammer 1982). Most studies have reported dynamic and 5 mainly static responses to step decreases in temperathat thermoreceptors are not excited by innocuous mechaniture. Rat sMDH COLD cells could be classified into three groups cal stimuli , although two depending on their stimulus-response functions. The first group studies in the rat reported mechanically sensitive Ad COLD (Type 1, n Å 19) had a bell-shaped static stimulus response funcfibers (Davies 1984; Pierau et al. 1975). It is also well tion. The second group (Type 2) had a high maintained or increasing static firing rate as the temperature decreased õ18ЊC (n Å 10). known that some low-threshold mechanoreceptors respond Type 3 COLD cells had mainly dynamic properties (n Å 7). Many phasically to rapid and large drops in skin temperature (Burof the cells in all groups were excited by noxious mechanical ton et al. 1972; Hensel and Zotterman 1951; Iggo and Muir stimulation. Type 2 cells differed from the other two groups in that 1969). It appears that at least some COLD afferents may most did not respond to noxious thermal stimuli (hot) and many respond to noxious mechanical stimuli, but this has not been responded to innocuous tactile stimuli. Neurons from each of the studied systematically or quantitatively (Darian-Smith 1984; three groups of COLD cells could be activated antidromically from Hellon 1983). However, many of the COLD afferents are contralateral thalamus. These data suggest that there is little central activated by noxious heat stimulation, and this discharge is processing of thermal information at the first central synapse for frequently termed a "paradoxical" response (Darian-Smith Type 1 neurons, however, the responses of the other two types may Dubner et al. 1975; Long 1977) . These studies largely be due to central processing and convergence. The demonstration confirm the predictions of the psychophysicists of the last of rat sMDH COLD cells with distinctive stimulus-response functions to thermal shifts suggests separate functional roles of these century such as von Frey and Blix, who observed discrete neurons in the ascending thermal sensory pathway. COLD and WARM spots on the skin surface and proposed that they give rise to the specific sensations of cold or warmth, respectively, when stimulated (see Hensel 1973a).
doi:10.1152/jn.1997.77.6.3252 pmid:9212272 fatcat:nmra6ks2tjcb7ec7qgplac6h5m