J Neurogastroenterol Motil 2015; 21(4): 623-624  https://doi.org/10.5056/jnm15069
Measuring Gastrointestinal Electrical Activity With Extracellular Electrodes
Gregory O’Grady1,2, Timothy R Angeli2, Peng Du2, and Leo K Cheng2,3
1Department of Surgery, University of Auckland, Auckland, New Zealand, 2Auckland Bioengineering Institute, University of Auckland, Auckland, New Zealand, 3Department of Surgery, Vanderbilt University, Nashville, Tennessee, USA
Published online: October 31, 2015.
© The Korean Society of Neurogastroenterology and Motility. All rights reserved.

cc This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

TO THE EDITOR: We read with interest the paper by Worth et al,1 concerning the regulation of gastric electrical and mechanical activity by cholinesterases. We congratulate the authors on this interesting study.

However, we were surprised to read the following statements: “Recording electrical activity by extracellular array electrodes was thought in the past to be a more effective method for detecting breakdown in electrical continuity.... However, recordings via this technique are due largely to movement artifacts rather than to valid electrophysiological recordings of membrane currents (slow waves).”

The authors support this statement with a single reference, ignoring all competing evidence supporting the validity of extracellular recordings, as addressed in recent publications, editorials and letters.2?6 It is important to present a balanced factual assessment on the validity of extracellular recordings, so that readers and reviewers remain correctly informed about the technique.

In the study cited by Worth et al,1 slow waves could not be recorded in vitro using extracellular electrodes. However, failing to record slow waves in one study does not mean they cannot be recorded generally. The claims in this study have been discredited for well-documented reasons,2?5 including extensive use of incorrect filters.6 In addition, extracellular recordings are more challenging in vitro, as coherent propagating wavefronts are required, and frequency gradients can be disturbed in isolated preparations.3

We invite the authors to consider the following data, from our recent in vivo study validating extracellular recordings (Figure),4 showing representative gastric slow wave recordings from multiple extracellular modalities, consistent with a century of extracellular studies.7

We invite the authors to consider: (1) how movement artifacts could generate 2 such different configurations across 2 extracellular methods (Figure A and D), which happen to ideally match slow wave membrane potential biophysics?4 And (2) how movement artifacts could explain such data given that tissue motion in our study was completely suppressed using nifidepine, as demonstrated in high-definition video mapping?4

Clearly, extracellular recordings accurately reflect slow wave membrane potential fields when correctly applied, and they therefore remain a “gold standard” tool in gastrointestinal physiology.8 In truth, extracellular array recordings would have been an ideal method for Worth et al1 to use, as they generate rich spatio-temporal data on slow wave propagation,9,10 which would have nicely complimented their excellent motility maps.

Fig. 1. The morphology of suction extracellular slow wave potentials (A) approximates intracellular slow wave recordings, while their second derivative (C) appropriately approximates the morphology of potentials recorded by conventional contact extracellular electrodes (D). Adapted from Angeli et al.

  1. Worth, AA, Forrest, AS, Peri, LE, Ward, SM, Hennig, GW, and Sanders, KM (2015). Regulation of gastric electrical and mechanical activity by cholinesterases in mice. J Neurogastroenterol Motil. 21, 200-216.
    Pubmed KoreaMed CrossRef
  2. O’Grady, G (2012). Gastrointestinal extracellular electrical recordings: fact or artifact?. Neurogastroenterol Motil. 24, 1-6.
  3. O’Grady, G, Pullan, AJ, and Cheng, LK (2012). The analysis of human gastric pacemaker activity. J Physiol. 590, 1299-1300.
  4. Angeli, TR, Du, P, and Paskaranandavadivel, N (2013). The bioelectrical basis and validity of gastrointestinal extracellular slow wave recordings. J Physiol. 591, 4567-4579.
    Pubmed KoreaMed CrossRef
  5. O’Grady, G, Angeli, T, Du, P, and Cheng, LK (2015). Concerning the validity of gastrointestinal extracellular recordings. Physiol Rev. 95, 691-692.
  6. Paskaranandavadivel, N, O’Grady, G, Du, P, and Cheng, LK (2013). Comparison of filtering methods for extracellular gastric slow wave recordings. Neurogastroenterol Motil. 25, 79-83.
    KoreaMed CrossRef
  7. Szurszewski, JH (1998). A 100-year perspective on gastrointestinal motility. Am J Physiol. 274, G447-G453.
  8. Sarna, SK (2013). The gold standard for interpretation of slow wave frequency in in vitro and in vivo recordings by extracellular electrodes. J Physiol. 591, 4373-4374.
    Pubmed KoreaMed CrossRef
  9. Lammers, WJ, Stephen, B, and Karam, SM (2012). Functional reentry and circus movement arrhythmias in the small intestine of normal and diabetic rats. Am J Physiol Gastrointest Liver Physiol. 302, G684-G689.
  10. O’Grady, G, Angeli, T, and Du, P (2012). Abnormal initiation and conduction of slow wave activity in gastroparesis, defined by high-resolution electrical mapping. Gastroenterology. 143, Array-Array.

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