Noxious Lingual Stimulation Influences the Excitability of the Face Primary Motor Cerebral Cortex (Face MI) in the Rat

Abstract

Adachi K, Murray GM, Lee J-C, Sessle BJ. Noxious lingual stimulation influences the excitability of the face primary motor cerebral cortex (face MI) in the rat. J Neurophysiol 100: 1234 -1244. First published July 2, 2008 doi:10.1152/jn.90609.2008. The mechanisms whereby orofacial pain affects motor function are poorly understood. The aims were to determine whether 1) lingual algesic chemical stimulation affected face primary motor cerebral cortex (face MI) excitability defined by intracortical microstimulation (ICMS); and 2) any such effects were limited to the motor efferent MI zones driving muscles in the vicinity of the noxious stimulus. Ketamine-anesthetized Sprague-Dawley male rats were implanted with electromyographic (EMG) electrodes into anterior digastric, masseter, and genioglossus muscles. In 38 rats, three microelectrodes were located in left face MI at ICMS-defined sites for evoking digastric and/or genioglossus responses. ICMS thresholds for evoking EMG activity from each site were determined every 15 min for 1 h, then the right anterior tongue was infused (20 l, 120 l/h) with glutamate (1.0 M, n ϭ 18) or isotonic saline (n ϭ 7). Subsequently, ICMS thresholds were determined every 15 min for 4 h. In intact control rats (n ϭ 13), ICMS thresholds were recorded over 5 h. Only left and right genioglossus ICMS thresholds were significantly increased (Յ350%) in the glutamate infusion group compared with intact and isotonic saline groups (P Ͻ 0.05). These dramatic effects of glutamate on ICMS-evoked genioglossus activity contrast with its weak effects only on right genioglossus activity evoked from the internal capsule or hypoglossal nucleus. This is the first documentation that intraoral noxious stimulation results in prolonged neuroplastic changes manifested as a decrease in face MI excitability. These changes appear to occur predominantly in those parts of face MI that provide motor output to the orofacial region receiving the noxious stimulation.

Effects of incisor extraction on jaw and tongue motor representations within face sensorimotor cortex of adult rats

“…However, this is unlikely, in that the sham-extraction group, which also underwent intraoral surgery, did not show any changes within face-M1 or face-S1, and its ICMS features did not differ from those of the naive group. Furthermore, whereas tooth extraction in the present study induced an increased RAD representation, intraoral nociceptive inputs to the brain evoked by injection of the algesic glutamate into the tongue in rats (Adachi et al, 2008) and application of capsaicin to the tongue in healthy humans (Boudreau et al, 2007) resulted in decreased face-M1 excitability suggestive of decreased motor representations (Monfils et al, 2005;Ridding and Rothwell, 1997).…”

Muscle Pain Differentially Modulates Short Interval Intracortical Inhibition and Intracortical Facilitation in Primary Motor Cortex

“…14 However, a decrease in excitability following muscle pain applied to the lingual region in rats is specific to areas that provide motor output to the region receiving pain. 1 There are several possible explanations for the relative lack of focality observed in human hand muscles. First, hypertonic saline infusion delivered to intrinsic hand muscles produces diffuse symptoms throughout the hand and occasionally the forearm.…”

“…19 Muscle pain arising from excitation of group III and IV afferents is likely to affect motor output at multiple levels of the motor system. 23 Although an effect of muscle pain on motor cortex is likely, evidence is limited, 1,27,31,34,42,43 and the mechanisms underlying such an effect are largely unknown.…”

“…For example, during muscle pain, motor unit discharge rates are slower, 13,24 maximal voluntary contraction force is reduced, 17 fMRI signal intensity is increased in motor cortex, 34 and intracortical miscrostimulation thresholds are increased in animal models. 1 Changes at the muscle have been excluded as the peripheral M-wave (muscle compound action potential), contractile properties, and conduction velocity of action potentials along the muscle fiber membrane are unchanged. 13,17,41,42 Some studies using transcranial magnetic stimulation (TMS) demonstrate suppression of motor-evoked potentials (which could be due to either cortical or spinal depression) in the early phase of pain followed by a later decrease in H-reflex amplitudes (this is the electrical analogue of the stretch reflex and its depression is likely to be due to depression of motoneurons).…”

Neuroplasticity of face sensorimotor cortex and implications for control of orofacial movements

“…Cortical changes may be involved in such behavioural changes since significantly increased ICMS thresholds for the tongue (genioglossus) motor representation occur in face MI for several hours after acute noxious stimulation of the rat tongue [105]. This effect is primarily reflected intracortical changes and specifically targets motor outputs to the region (tongue) in the vicinity of the noxious stimulus site.…”