Extracellular electrical recordings have been, and continue to be, extremely helpful in understanding the rhythmic pacemaker activities in the gut. In a recent Perspectives article (Problems with extracellular recording of electrical activity in gastrointestinal muscle. Nat. Rev. Gastroenterol. Hepatol. 13, 731–741; 2016)1, attempts have been made to question this technique, which is unfortunate owing to the potential discreditation of seminal previous and current studies. The main issue reported by Sanders et al.1 is that movements can cause artefacts in the electrical recordings, but anyone who works with extracellular electrodes is aware of this issue and how potential pitfalls can easily be avoided2.
Alvarez3 was the first to record electrical activity of the gut in 1922 and he already understood the issue of movement contamination: “the most remarkable thing about these action currents is that they are produced constantly in stomachs and intestines which, so far as the eye can detect, are absolutely motionless”. Furthermore, Alvarez noted that the electrical activity was similar whether contractions occurred or not. Extracellular recording is a very powerful technique as it can be performed in vivo or ex vivo in whole organs; hence, in complete or near complete physiological conditions. They can also be recorded even when powerful contractions occur, a feat no other technique to measure electrical activity can accomplish; hence, an advantage of the technique, not a problem.
In Figure 3 from their article, Sanders et al.1 show an example in which electrical activity disappears when contraction stops. However, those familiar with this technique know that this situation can happen with a poor electrode position. Lammers and co-workers have contributed enormously to our understanding of the network properties of the interstitial cells of Cajal by recording, amongst others, slow-wave propagation in the small intestine of a cat simultaneously with 240 extracellular electrodes4. As the purpose was to understand fundamental properties of pacemaker activity, the experiments were done in the absence of contractile activity. Only this technique could have proven that slow-wave activity easily traverses from the proximal end of the intestine all the way to the distal intestine4. Only this technique could have demonstrated the paucity of pacemaking activity at the pyloric sphincter in rats and mice, which is needed to insulate the different activities and functions of gastric and duodenal pacemaking5.
Extracellular electrodes are sensitive enough to distinguish slow waves from smooth muscle action potentials, and detailed knowledge has emerged from this technique regarding the behaviour of patches of action potentials superimposed on the slow waves6 (Fig. 1). Another example is our understanding of the waxing and waning electrical slow-wave activity that accompanies the classic segmentation motor pattern of the small intestine7. As this activity is accompanied by vigorous contractile activity, a flexible extracellular electrode is the perfect way to record accompanying electrical activity. After we performed this technique in rats, we confirmed the waxing and waning pattern with intracellular electrodes in mice and showed that the patterns of intracellular and extracellular activity were the same7.
Detailed slow-wave conduction abnormalities were recorded recently in patients with gastroparesis — an amazing accomplishment that will be of critical importance in elucidating one aspect of the pathophysiology of this disease8. The future of science lies in the elucidation of mechanisms by a variety of methods and extracellular recording needs to be embraced as a powerful technique, and sometimes the only one suitable technique.
References
Sanders, K. M., Ward, S. M. & Hennig, G. W. Problems with extracellular recording of electrical activity in gastrointestinal muscle. Nat. Rev. Gastroenterol. Hepatol. 13, 731–741 (2016).
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Lammers, W. J. & Stephen, B. Origin and propagation of individual slow waves along the intact feline small intestine. Exp. Physiol. 93, 334–346 (2008).
Wang, X. Y., Lammers, W. J., Bercik, P. & Huizinga, J. D. Lack of pyloric interstitial cells of Cajal explains distinct peristaltic motor patterns in stomach and small intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 289, G539–G549 (2005).
Lammers, W. J., Slack, J. R., Stephen, B. & Pozzan, O. The spatial behaviour of spike patches in the feline gastroduodenal junction in vitro. Neurogastroenterol. Motil. 12, 467–473 (2000).
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Acknowledgements
I gratefully acknowledge that Professor Wim Lammers provided the original version of Figure 1, provided minor adjustments and gave permission to use the figure.
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Huizinga, J. The powerful advantages of extracellular electrical recording. Nat Rev Gastroenterol Hepatol 14, 372 (2017). https://doi.org/10.1038/nrgastro.2017.16
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DOI: https://doi.org/10.1038/nrgastro.2017.16
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