Gastrointestinal extracellular electrical recordings: fact or artifact?

Abstract

Extracellular electrical recordings underpin an important literature of basic and clinical motility science. In this edition of Neurogastroenterology & Motility, Sanders and colleagues report that contraction artifacts could be recorded from in-vitro murine gastric tissues using extracellular electrodes, and that true extracellular bioelectrical activity could not be detected when the contractions were suppressed. The authors interpret their findings to mean that previous extracellular studies have generally assayed contraction artifacts, rather than bioelectrical activity, and suggest that movement suppression is an obligatory control for extracellular experiments. If their interpretation is correct, these claims would be significant, requiring a reinterpretation of many studies, and posing major challenges for future in-vivo and especially clinical work. However, a demonstration that motion artifacts can be recorded from murine in-vitro tissue does not necessarily mean that other extracellular studies also represented artifacts. This viewpoint evaluates the new work of Sanders and colleagues in light of the competing literature, and finds a considerable volume of evidence to support the veracity of GI extracellular electrical recordings. It is reasoned from biophysical principles, technical considerations, and experimental studies, that motion artifacts cannot explain GI extracellular electrical recordings in general, and that bioelectrical fact and artifact can be readily and reliably distinguished in most contexts. Calls for obligatory motion suppression for extracellular studies are therefore not supported. However, the artifacts recorded by Sanders and colleagues nevertheless serve as a reminder that educated caution is needed when recording, filtering and interpreting extracellular data.

Iterative Covariance-Based Removal of Time-Synchronous Artifacts: Application to Gastrointestinal Electrical Recordings

“…Time-synchronous artifacts were intrinsic in the data set, i.e., not introduced artificially. We emphasize that such artifacts arise from extrinsic, non-GI biologic noise sources, not from intrinsic GI contractile activity [21]. …”

Measuring Gastrointestinal Electrical Activity With Extracellular Electrodes

“…[2][3][4][5][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][3][4][5] including extensive use of in-correct 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.…”

Concerning the Validity of Gastrointestinal Extracellular Recordings

“…These criticisms have now been thoroughly discredited (1,7,9,10,12). The claims were based on a single murine study (2), performed in vitro, a context in which extracellular recordings are challenging and may be unreliable due to the effects of tissue isolation (7,9,12,13).…”

“…The claims were based on a single murine study (2), performed in vitro, a context in which extracellular recordings are challenging and may be unreliable due to the effects of tissue isolation (7,9,12,13). Indeed, no potentials were ever recorded in this study that could be regarded as representative of slow waves (7). This was likely because extracellular methods were incorrectly applied (7), including the use of filters that excluded the dominant frequency range in which slow waves occur (10).…”