Encoding of corneal input in two distinct regions of the spinal trigeminal nucleus in the rat: Cutaneous receptive field properties, responses to thermal and chemical stimulation, modulation by diffuse noxious inhibitory controls, and projections to the parabrachial area

To determine whether corneal input is processed similarly at rostral and caudal levels of the spinal trigeminal nucleus, the response properties of second-order neurons at the transition between trigeminal subnucleus interpolaris and subnucleus caudalis (Vi/Vc) and at the transition between subnucleus caudalis and the cervical spinal cord (Vc/Ci) were compared. Extracellular single units were recorded in 68 Sprague-Dawley rats under chloralose or urethan/chloralose anesthesia. Neurons that responded to electrical stimulation of the cornea at the Vi/Vc transition region (n = 61) and at laminae I/II of the Vc/Ci transition region (n = 33) were classified regarding 1) corneal mechanical threshold; 2) cutaneous mechanoreceptive field, if present; 3) electrical input characteristics (A and/or C fiber); 4) response to thermal stimulation; 5) response to the small-fiber excitant, mustard oil (MO), applied to the cornea; 6) diffuse noxious inhibitory controls (DNIC); and 7) projection status to the contralateral parabrachial area (PBA). On the basis of cutaneous receptive field properties, neurons were classified as low-threshold mechanoreceptive (LTM), wide dynamic range (WDR), nociceptive specific (NS), or deep nociceptive (D). All neurons recorded at the Vc/Ci transition region were either WDR (n = 19) or NS (n = 14). In contrast, 54% of the Vi/Vc neurons had no cutaneous receptive field. Of those Vi/Vc neurons that had a cutaneous receptive field, 57% were LTM, 25% were WDR, and 18% were D. All Vc/C₁ neurons responded to noxious thermal and MO stimulation. Only 22 of 47 and 13 of 19 Vi/Vc corneal units responded to thermal or MO stimulation, respectively. At the Vc/C₁ transition region, 12 of 17 neurons demonstrated DNIC, whereas at the Vi/Vc transition region, DNIC was present in only 4 of 26 neurons. Of 15 Vc/C₁ corneal units, 12 could be antidromically activated from the contralateral PBA (average latency 6.29 ms, range 1.8-26 ms). None of 22 Vi/Vc corneal units tested could be antidromically activated from the PBA. These findings suggest that neurons in laminae I/II at the Vc/C₁ transition and at the Vi/Vc transition process corneal input differently. Neurons in laminae I/II at the Vc/C₁ transition process corneal afferent input consistent with that from other orofacial regions. Corneal-responsive neurons at the Vi/Vc transition region maybe important in motor reflexes or in recruitment of descending antinociceptive controls.