Activation properties of trigeminal motoneurons in participants with and without bruxism

Abstract

In animals, sodium- and calcium-mediated persistent inward currents (PICs), which produce long-lasting periods of depolarization under conditions of low synaptic drive, can be activated in trigeminal motoneurons following the application of the monoamine serotonin. Here we examined if PICs are activated in human trigeminal motoneurons during voluntary contractions and under physiological levels of monoaminergic drive (e.g., serotonin and norepinephrine) using a paired motor unit analysis technique. We also examined if PICs activated during voluntary contractions are larger in participants who demonstrate involuntary chewing during sleep (bruxism), which is accompanied by periods of high monoaminergic drive. In control participants, during a slowly increasing and then decreasing isometric contraction, the firing rate of an earlier-recruited masseter motor unit, which served as a measure of synaptic input to a later-recruited test unit, was consistently lower during derecruitment of the test unit compared with at recruitment (ΔF = 4.6 ± 1.5 imp/s). The ΔF, therefore, is a measure of the reduction in synaptic input needed to counteract the depolarization from the PIC to provide an indirect estimate of PIC amplitude. The range of ΔF values measured in the bruxer participants during similar voluntary contractions was the same as in controls, suggesting that abnormally high levels of monoaminergic drive are not continually present in the absence of involuntary motor activity. We also observed a consistent "onion skin effect" during the moderately sized contractions (<20% of maximal), whereby the firing rate of higher threshold motor units discharged at slower rates (by 4-7 imp/s) compared with motor units with relatively lower thresholds. The presence of lower firing rates in the more fatigue-prone, higher threshold trigeminal motoneurons, in addition to the activation of PICs, likely facilitates the activation of the masseter muscle during motor activities such as eating, nonnutritive chewing, clenching, and yawning.

Keywords: motoneurons; pain; plateaus; sleep bruxism.

Fig. 1.

The amplitude of persistent inward currents [PICs (ΔF)] in nonbruxer (NBrux) participants. A: instantaneous firing rate of lower threshold control (bottom) and higher threshold test (middle) motor unit during isometric contraction (bite force: top). Thick black line represents 5th order polynomial (smoothed rate) fit through the firing rates. Dotted vertical lines mark time of recruitment and derecruitment of the test unit. Solid horizontal lines indicate smoothed firing rate of control unit when test unit was recruited and derecruited, with the difference between the 2 rates (ΔF) marked by the arrow. Insets: overlain traces of control and test motor units. B: smoothed mean firing rate of control unit from A plotted against smoothed mean firing rate of test unit during contraction (black circles) and relaxation (open circles) phase of contraction. *Beginning of test unit firing. C: control unit firing rate at time of recruitment of test unit plotted against control unit rate when test unit was derecruited for 45 contractions from the 9 NBrux participants (5 contractions per participant, different symbol for each participant). Solid line marks slope of 1 (parity line). Mean of data is shown by the large gray circle and error bars represent SD. D: mean ΔFs (±SD) measured in biceps brachii, soleus, and tibialis anterior muscles (black bars) compared with mean ΔF for masseter muscle (white bar).

Fig. 2.

Mean firing rate and recruitment threshold. A: firing rate profiles of three sequentially recruited motor units during an isometric, triangular contraction in a NBrux participant (control: black circles; test-1: white circles; test-2: gray circles). B: same as in A for a control and test-1 unit pair in another NBrux participant. C: group mean firing rates of early-recruited control units (18.5 ± 3.9i mp/s) and later recruited test-1 (14.9 ± 3.0 imp/s) and test-2 (11.8 ± 3.7 imp/s) units from NBrux participants. Numbers of units analyzed are indicated in each bar graph, and error bars represent means ± SE. A one-way ANOVA with post hoc Bonferroni t-tests were used. D: recruitment thresholds, expressed as a percent maximum voluntary contraction (%MVC) for control (5.0 ± 3.4%), test-1 (8.3 ± 4.5%), and test-2 (11.3 ± 5.4%) units. A one-way ANOVA on ranks with post hoc Dunn's test was used. *P < 0.05, **P < 0.001.

Fig. 3.

Differences in recruitment thresholds and mean firing rates. A: calculation of recruitment threshold difference between control (bottom) and test-1 (middle) motor units during a voluntary contraction (force expressed as %MVC, top). Dashed vertical lines mark start of firing of control and test-1 units and corresponding recruitment forces for the control (RT:C) and test-1 (RT:T1) units. Arrow marks the difference in recruitment force (ΔRT) between the 2 units. B: difference in mean rate between a control and test-1, control and test-2, or test-1 and test-2 motor unit pair plotted against the corresponding difference between their recruitment thresholds (n = 60 unit pairs). A linear regression is fit through the data points (r = 0.43, P = 0.0007).

Fig. 4.

ΔF in Brux participants. A: instantaneous firing rate of a lower threshold control (bottom) and higher threshold test (middle) motor units during isometric contraction in Brux-2 (A) and Brux-4 (B) participants. Same format as Fig. 1. Note different scales in A and B. C: group mean ΔF from NBrux (black bar: 4.6 ± 1.6 imp/s) and Brux (white bar: 4.5 ± 1.2 imp/s) participants (Student's t-test, P = 0.83). D: ΔF plotted against peak force (%MVC) reached during each contraction for the 9 NBrux (black circles, solid line, n = 45 contractions) and 13 Brux participants (open circles, dashed line, n = 65 contractions).