Elsevier

Brain Research

Volume 1350, 2 September 2010, Pages 151-158
Brain Research

Research Report
Carbohydrate in the mouth immediately facilitates motor output

https://doi.org/10.1016/j.brainres.2010.04.004Get rights and content

Abstract

The presence of carbohydrate in the mouth can immediately improve physical performance. How this occurs is not well understood. Here we used transcranial magnetic stimulation of primary motor cortex (M1) to investigate the effects of non-sweet carbohydrate on corticomotor excitability and voluntary force production. In Experiment 1, 16 participants performed a fatiguing isometric elbow flexion exercise for 30 min, and Motor evoked potentials (MEPs) were recorded from the biceps brachii during maximal voluntary force (MVF) produced every 2 min. After 11 min participants drank a carbohydrate solution (CHO) or an energy-free placebo solution (PLA), in a double-blind, cross-over protocol. MEP amplitude increased by 30%, and MVF increased by 2%, immediately after carbohydrate ingestion. There was no relationship between the facilitation of MEP amplitude and plasma glucose or magnitude of fatigue. In a control experiment, 17 participants alternately mouth-rinsed CHO and PLA, in a randomized, double-blind protocol. MEPs were recorded from right first dorsal interosseous at rest or during isometric contraction. MEP amplitude increased by 9% with CHO, when the muscle was voluntarily activated. In both experiments, there were no effects on silent period duration, indicating that MEP facilitation was not due to reduced inhibition within M1. This is the first demonstration that carbohydrate in the mouth immediately increases the excitability of the corticomotor pathway, prior to its ingestion. Afference from oral receptors is integrated with descending motor output, perhaps via nuclei in the brainstem. This novel form of sensorimotor integration facilitates corticomotor output to both fatigued and fresh muscle.

Introduction

Sensory receptors in the mouth and pharynx are activated by the presence and ingestion of food. These sensory inputs affect voluntary motor behaviour, in addition to subserving perception and initiating early digestive reflexes (Zafra et al., 2006). Remarkably, the mere presence of carbohydrate in the mouth has been shown to improve performance during prolonged physical activity (Carter et al., 2004, Chambers et al., 2009, Rollo et al., 2008). There is also compelling evidence that carbohydrate in the mouth increases neural activity in a number of regions of the brain (Chambers et al., 2009, Smeet et al., 2007). To date, the functional significance of this signalling pathway has not been explored, and the mechanisms involved are not understood. The aim of this study was to investigate whether descending corticomotor output to fatigued muscle is altered by the presence of carbohydrate in the mouth.

Fatigue during prolonged physical activity can be thought of as a conservation strategy, to prevent severe energy depletion and extreme perturbations in metabolic homoeostasis (Hargreaves, 2008, Noakes et al., 2005). It is well known that the voluntary cessation of prolonged exercise coincides with muscle glycogen depletion and hypoglycemia (Coggan and Coyle, 1991). Fatigue involves a progressive reduction in neural drive to the exercising musculature that is at least partly supraspinal in origin, due to reduced output from the primary motor cortex (Taylor et al., 2006). This conservation strategy becomes apparent during times of energy crisis (Nybo, 2003), and appears to be related to energy availability. Afferent information regarding energy available in the blood, muscle and liver, may be integrated with afferent information regarding the imminent availability of energy in the process of being ingested. If fuel-sensing receptors in the mouth activate neural pathways, ingesting carbohydrate may have immediate neural consequences, prior to its incorporation into body tissue.

This is the first study to investigate whether the presence of carbohydrate in the mouth modifies corticomotor excitability and voluntary force production. In Experiment 1 we used an established model of fatiguing arm exercise (Fig. 1) to test the hypothesis that carbohydrate ingestion would facilitate corticomotor excitability immediately, prior to any peripheral substrate and endocrine responses. A second experiment was then performed to examine whether mouth-rinsing a carbohydrate solution (without ingesting), was sufficient to facilitate corticomotor excitability during muscle activation, but in the absence of fatigue.

Section snippets

Experiment 1

Sixteen participants completed the fatigue protocol twice, 1 week apart, with a carbohydrate drink administered in one session (CHO) and a placebo drink in the other (PLA). As expected, there were no effects of drink on measures made immediately before solution ingestion (Table 1). There was no difference in the mean maximal force produced by each arm (left: mean 360.7 ± 94.6 N; right: 354.0 ± 79.7 N; two-tailed paired t-test, t15 = 0.59, p > 0.5). The frequency distribution of participants' glucose

Discussion

This is the first study to show that ingestion of carbohydrate can immediately improve human performance by increasing corticomotor excitability and maximum voluntary force production. This immediate ergogenic effect precedes substrate or endocrine signalling from the viscera. The mechanism is most likely neural, and represents a novel form of sensorimotor integration.

Sweet taste receptors were activated by equivalent concentrations of an artificial sweetener in the CHO and PLA solutions. The

Experiment 1

Nineteen healthy young males participated. Three were withdrawn from the analysis due to their inability to consistently produce MVF. The mean age of the remaining 16 participants was 25 years (range 21–36 years). All were right-handed with a mean laterality quotient of + 84.3 (range + 50.0  + 100.0) (Oldfield, 1971). All participants gave written informed consent, the study was conducted in accordance with the Declaration of Helsinki, and was approved by the institutional ethics committee.

Acknowledgments

We thank the following for providing assistance with data collection and analysis: C. Dillen, A. Dooley, D. Greybe, M. Hacket, S. Janus, C. Kelly, S. Mitchley, I. Shalmiyeva, C. Turner and F. Noten, C. Bradford, P. Lacey for technical support.

This study was funded by the University of Auckland.

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    These authors contributed equally to this work.

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