Stimulation of craniofacial muscle afferents induces prolonged facilitatory effects in trigeminal nociceptive brain-stem neurones

Abstract

Stimulation of small-diameter afferents supplying deep tissues has been shown to increase the excitability of spinal cord neurones responding to cutaneous afferent inputs. This facilitation has been implicated as integral central mechanisms of deep pain that may contribute to the tenderness and spread and/or referral of pain following injury of deep tissues. In view of the recent documentation of deep craniofacial afferent inputs, as well as cutaneous afferent inputs to the trigeminal (V) spinal tract nucleus, we wished to determine the effects of deep inputs excited by the small-fibre irritant mustard oil on trigeminal nociceptive neurones. The extracellular activity of single brain-stem neurones was recorded in subnuclei caudalis and oralis of the V spinal tract nucleus of anaesthetized rats. The neurones were classified as low-threshold mechanosensitive (LTM), wide dynamic range (WDR) and nociceptive specific (NS) on the basis of their cutaneous mechanoreceptive field properties and their responses evoked by electrical stimulation of their cutaneous afferent inputs. Injection of 5% mustard oil (2–5, μl) into the deep masseter muscle produced a facilitatory effect in 12 of 27 nociceptive neurones tested in caudalis and in 5 of 12 nociceptive neurones in oralis. This effect was reflected in an expansion of the cutaneous mechanoreceptive field, an increase in spontaneous activity or an increase in responsivity to electrical stimulation of cutaneous afferent inputs to the neurones. The facilitation was reversible and typically became apparent within 3–5 min of the injection, reached its peak at 5–10 min, and lasted for 20–30 min. These findings document for the first time the sensitivity of the cutaneous receptive field properties of V brain-stem nociceptive neurones to facilitatory influences from deep craniofacial afferents, and point to possible mechanisms that may contribute to the tenderness, spread and referral of pain that may result from trauma to deep craniofacial tissues.