Movement based artifacts may contaminate extracellular electrical recordings from GI muscles

Abstract

Background Electrical slow waves drive peristaltic contractions in the stomach and facilitate gastric emptying. In gastroparesis and other disorders associated with altered gastric emptying, motility defects have been related to altered slow wave frequency and disordered propagation. Experimental and clinical measurements of slow waves are made with extracellular or abdominal surface recording. Methods We tested the consequences of muscle contractions and movement on biopotentials recorded from murine gastric muscles with array electrodes and pairs of silver electrodes. Key Results Propagating biopotentials were readily recorded from gastric sheets composed of the entire murine stomach. The biopotentials were completely blocked by nifedipine (2 μmol L−1) that blocked contractile movements and peristaltic contractions. Wortmannin, an inhibitor of myosin light chain kinase, also blocked contractions and biopotentials. Stimulation of muscles with carbachol increased the frequency of biopotentials in control conditions but failed to elicit biopotentials with nifedipine or wortmannin present. Intracellular recording with microelectrodes showed that authentic gastric slow waves occur at a faster frequency typically than biopotentials recorded with extracellular electrodes, and electrical slow waves recorded with intracellular electrodes were unaffected by suppression of movement. Electrical transients, equal in amplitude to biopotentials recorded with extracellular electrodes, were induced by movements produced by small transient stretches (<1 mm) of paralyzed or formalin fixed gastric sheets. Conclusions & Inferences These data demonstrate significant movement artifacts in extracellular recordings of biopotentials from murine gastric muscles and suggest that movement suppression should be an obligatory control when monitoring electrical activity and characterizing propagation and coordination of electrical events with extracellular recording techniques.

Regulation of Gastric Electrical and Mechanical Activity by Cholinesterases in Mice

“…[38][39][40] However, recordings via this technique are due largely to movement artifacts rather than to valid electrophysiological recordings of membrane currents (slow waves). 41 For this reason we employed motility imaging so we could record the progress of gastric peristaltic contractions unambiguously. These studies clearly demonstrated development of functional uncoupling and disruption of gastric peristalsis in response to cholinesterase inhibitors.…”

The gold standard for interpretation of slow wave frequency in in vitro and in vivo recordings by extracellular electrodes

“…Since then the recording of slow waves by extracellular and intracellular electrodes has served as an important tool to understand gut motility function in health and disease. Two recent publications raised questions about the fidelity of extracellular electrodes in recording slow waves (Bayguinov et al 2011;Rhee et al 2011). The authors used extracellular and intracellular electrodes to record from isolated muscle strips or gastric sheets.…”

Measuring Gastrointestinal Electrical Activity With Extracellular Electrodes: Author's Reply

“…In describing our rationale for the technology chosen, we made reference to the unsuitability of extracellular electrical recording as a means to measure changes in slow waves, because movement artifacts dominate these measurements. 2 In a previous study we found that when movements are blocked, under conditions in which slow waves are unaffected, the signals recorded with extracellular metal electrodes and many have attributed to electrophysiological events (slow waves), are inhibited. 2 Thus the signals monitored by extracellular electrodes are largely artifacts of movement and do not represent authentic slow wave activity.…”

“…2 In a previous study we found that when movements are blocked, under conditions in which slow waves are unaffected, the signals recorded with extracellular metal electrodes and many have attributed to electrophysiological events (slow waves), are inhibited. 2 Thus the signals monitored by extracellular electrodes are largely artifacts of movement and do not represent authentic slow wave activity. In light of these observations, which have been reproduced in mouse, dog, monkey and human gastric muscles when movement is suppressed, it is important for studies utilizing extracellular electrical recording to be accompanied by rigorous tests insuring that the electrical signals claimed to be slow waves persist after movement is stabilized.…”

“…4 We have suggested that the best approach to make clear association between extracellular recording and authentic slow waves is rigorous stabilization of movements in vitro, as described in the addendum of our previous paper. 2 If one is determined to monitor contraction by just looking at the tissue, then relatively high power objectives would be needed to allow observations of the tiny movements that cause significant signals (ie, several 10 seconds of Vs) to be picked up by extracellular electrodes. We fully realize the time, effort and resources that O'Grady et al 3 have invested in extracellular recording and modeling the data derived from these measurements, and we sincerely hope new ideas might be developed to alleviate movement artifacts or amplify the field potentials caused by slow waves to a level where they can be captured by extracellular recording.…”