Chewing and Cognitive Improvement: The Side Matters

Abstract

Chewing improves cognitive performance, which is impaired in subjects showing an asymmetry in electromyographic (EMG) masseter activity during clenching. In these subjects, the simultaneous presence of an asymmetry in pupil size (anisocoria) at rest indicates an imbalance in Ascending Reticular Activating System (ARAS) influencing arousal and pupil size. The aim of the present study was to verify whether a trigeminal EMG asymmetry may bias the stimulating effect of chewing on cognition. Cognitive performance and pupil size at rest were recorded before and after 1 min of unilateral chewing in 20 subjects with anisocoria, showing an EMG asymmetry during clenching. Unilateral chewing stimulated performance mainly when it occurred on the side of lower EMG activity (and smaller pupil size). Following chewing on the hypotonic side, changes in cognitive performance were negatively and positively correlated with those in anisocoria and pupil size, respectively. We propose that, following chewing on the hypotonic side, the arousing effects of trigeminal stimulation on performance are enhanced by a rebalancing of ARAS structures. At variance, following chewing on the hypertonic side, the arousing effect of trigeminal stimulation could be partially or completely prevented by the simultaneous increase in ARAS imbalance.

Keywords: anisocoria; cognitive performance; locus coeruleus; pupil size; trigeminal asymmetry; unilateral chewing.

FIGURE 1

Flowchart of the experiments. (A) Preliminary session, time 0 days. (B) Stimulation session, time 18–24 days. (C) Experimental session, time 80–86 days. Rounded corners rectangles indicate the pupil size/performance measurements and the experimental procedures operated in each session. T1 and T2 correspond to 0 and 30 min soon after the period of unilateral chewing, respectively.

FIGURE 2

Pupil size in right and left dominant subjects.

FIGURE 3

Changes in performance, pupil size and anisocoria elicited by unilateral chewing within the whole population. Changes in PI (A), SR (B), pupil size on the hypertonic (C) and hypotonic (D) side, as well as in anisocoria (E) are expressed as differences between T1/T2 and T0 values. Continuous and dotted lines refer to changes elicited by chewing on the hypotonic and hypertonic side, respectively. Asterisks refer to significant differences with respect to T0. *p < 0.05, **p < 0.01, and ***p < 0.005. Error bars represent SE of the mean.

FIGURE 4

Changes in performance, pupil size, and anisocoria elicited by unilateral chewing among right and left dominant subjects. Changes in PI (A), SR (B), pupil size on the hypertonic (C) and hypotonic (D) side, as well as in anisocoria (E) are expressed as differences between T1/T2 and T0 values. Upper and lower rows represent right and left dominant subjects, respectively. Continuous and dotted lines refer to changes elicited by chewing on the hypotonic and hypertonic side, respectively. Asterisks refer to significant differences with respect to T0. *p < 0.05, **p < 0.01, and ***p < 0.005. Error bars represent SE of the mean.

FIGURE 5

Relation between changes in PI and pupil size. Scatterplots of the changes in PI and in pupil size values observed on the hypertonic (A,C) and the hypotonic (B,D) sides, following unilateral chewing on the hypotonic (A,B) and the hypertonic (C,D) side. The regression lines refer to all the plotted points. In each graph, the black dots and the open dots represent the right and the left dominant subjects, respectively.

FIGURE 6

Relation between changes in SR and pupil size. Scatterplots of the changes in SR and in pupil size values observed on the hypertonic (A,C) and the hypotonic (B,D) sides, following unilateral chewing on the hypotonic (A,B) and the hypertonic (C,D) side. The regression lines refer to all the plotted points. In each graph, the black dots and the open dots represent the right and the left dominant subjects, respectively.

FIGURE 7

Relation between changes in performance-related parameters (PI, SR) and anisocoria. Changes in PI have been displayed in panels (A,B). Changes in SR can be found in panels (C,D). Data relative to unilateral chewing on the hypotonic and hypertonic side are shown in panels (A,C) and (B,D), respectively. The regression lines refer to all the plotted points. In each graph, the black dots and the open dots represent the right and the left dominant subjects, respectively.