Spinothalamic lamina I neurones selectively responsive to cutaneous warming in cats

Abstract

1. In order to further characterize the role of lamina I as the source of central ascending neural pathways for thermoreception and thermoregulation, experiments were performed on anaesthetized cats to determine the quantitative response characteristics of warming-specific lumbosacral spinothalamic lamina I neurones. 2. We identified 10 neurones out of 474 that were selectively excited by cutaneous warming (Warm cells). Their thresholds were all in the range 35-37 degrees C at a baseline of 34.5 degrees C, and their discharge linearly encoded the temperature of graded, innocuous warming stimuli with a sensitivity of 2.1 Hz x degrees C(-1). 3. The stimulus-response function of the Warm cells plateaued at temperatures that were in the noxious heat range. 4. The Warm cells were distinguished from other classes of spinothalamic lamina I neurones by their peripheral inputs, central conduction velocities and level of ongoing activity. 5. The discharge of Warm cells compares well with the known human psychophysics of warm sensibility, and these neurones are likely to be crucial to discriminative thermoreception. Additionally, a role in thermoregulation, a defining feature of mammalian homeostasis, is suggested.

Figure 1. Identification of STT lamina I Warm neurones

A, one-for-one following of a train of 6 antidromic pulses (•, 60 μA, 2 ms, 250 Hz) delivered from the electrode in the contralateral basal part of the ventromedial nucleus (vVMb). Conduction distance, 330 mm. B, collision of the first impulse in a train of 3 antidromic action potentials (150 Hz) due to an orthodromic impulse (*) occurring within the critical interval. The arrow indicates the point at which the first antidromic impulse would have occurred. C, a pair of responses from the same unit during electrical stimulation of the receptive field showing time-locked (monosynaptic) responses at C-fibre latency. The stimuli were applied at the beginning of each trace. Conduction distance, 360 mm. D, location of the recording site in lamina I of the spinal cord. E, contralateral thalamus showing effective sites for antidromic activation. CL, central lateral n.; H, habenula; LG, lateral geniculate n.; LP, lateral posterior n.; MD, medial dorsal n.; PV, paraventricular n.; R, reticular n.; Sm, submedial n.; VPL, ventral posterior lateral n.; VPM, ventral posterior medial n.; ZI, zona incerta.

Figure 3. Innocuous temperature encoding by Warm neurones

A, individual stimulus-response curves for all 8 Warm neurones that were quantitatively characterized. B, population means (± 1 s.d.). The continuous line is the linear regression (r = 0.60), and the dashed lines are the 95 % confidence limits. Firing rates are given in impulses (imp) per second.

Figure 2. Quantitative response characteristics of Warm neurones

Original histogram records (1 s bins) from all 8 Warm neurones that were tested quantitatively. The lower pair of records are specimen temperature traces obtained from a thermocouple fixed to the surface of the thermode.

Figure 4. Warm neurones do not encode noxious heat stimuli

A, pair of records from the same Warm neurone illustrating its response to an innocuous (38.7 °C) and a noxious (53.0 °C) heat stimulus. The traces are, from the top downward, firing rate of the unit in 1 s bins, temperature and the single-unit recording. B, individual stimulus-response curves for all 8 Warm neurones to innocuous and noxious heat stimuli. C, population stimulus-response curve (means ± 1 s.d.).