Electrogastrography for psychophysiological research: Practical considerations, analysis pipeline, and normative data in a large sample

Abstract

Electrogastrography (EGG) is the noninvasive electrophysiological technique used to record gastric electrical activity by means of cutaneous electrodes placed on the abdomen. EGG has been so far mostly used in clinical studies in gastroenterology, but it represents an attractive method to study brain-viscera interactions in psychophysiology. Compared to the literature on electrocardiography for instance, where practical recommendations and normative data are abundant, the literature on EGG in humans remains scarce. The aim of this article is threefold. First, we review the existing literature on the physiological basis of the EGG, pathways of brain-stomach interactions, and experimental findings in the cognitive neuroscience and psychophysiology literature. We then describe practical issues faced when recording the EGG in young healthy participants, from data acquisition to data analysis, and propose a semi-automated analysis pipeline together with associated MATLAB code. The analysis pipeline aims at identifying a regular rhythm that can be safely attributed to the stomach, through multiple steps. Finally, we apply these recording and analysis procedures in a large sample (N = 117) of healthy young adult male and female participants in a moderate (<5 hr) to prolonged (>10 hr) fasting state to establish the normative distribution of several EGG parameters. Our results are overall congruent with the clinical gastroenterology literature, but suggest using an electrode coverage extending to lower abdominal locations than current clinical guidelines. Our results indicate a marginal difference in EGG peak frequency between male and female participants, and that the gastric rhythm becomes more irregular after prolonged fasting.

Keywords: electrogastrography; gastric rhythm; normative data; power and phase analysis; processing pipeline.

Figure 1

(a) Recording setup. Cutaneous electrodes are placed on the left abdomen of the participant in a grid‐like arrangement and connected to DC amplifiers. Ref. and Gnd correspond to Reference and Ground, respectively. (b) Example of raw data in one participant, where the gastric rhythm is visible as cycles of ~20 s length. Respiratory cycles are much faster (typically 3 to 5 s length). Heartbeats appear as transients every ~0.8 s (inset). EGG amplitude in this participant is close the median value observed in 100 participants. (c) Power spectrum at each of the seven recording electrodes. Peak frequency is indicated by a star on the channel with the largest power (black line). The white area corresponds to the normal frequency range of the EGG, also known as normogastria (2 to 4 cpm or 0.033 to 0.066 Hz). Inset: Electrode layout with the location of the electrode displaying the largest spectral power marked with a blue star. (d) Spectral density over a wider frequency range at the selected channel, revealing the spectral signatures of the respiratory (~0.3 Hz) and cardiac rhythms (~1.5 Hz)

Figure 2

The stomach and the generation of the gastric slow rhythm. (a) Anatomical regions of the stomach, with the main divisions into fundus, corpus, and antrum. The gastric rhythm originates from the pacemaker region (orange) near the greater curvature of the mid/upper corpus. From here, it entrains other pacemaker cells, resulting in traveling rings of electrical wavefronts in the direction of the antrum (O’Grady et al., 2010). (b) The Interstitial Cells of Cajal (ICC, blue) are the generators of the gastric rhythm. They lay in the stomach wall, between and within the circular and longitudinal muscle layers. An additional thin oblique muscle layer located in the innermost part of the stomach, adjacent to the circular layer, is not represented here. The electrical activity of the pacemaker is passed through the entire ICC network and is also passively conducted into coupled muscle cells. ICCs make synapse‐like contact with vagal sensory neurons (Powley et al., 2008), presented in green, in a structure known as intramuscular arrays, that can detect mechanical changes in smooth muscles. Adapted from Koch & Stern, 2004

Figure 3

Projections of vagal and spinal afferents from the gastrointestinal tract to the brain. Afferents target brainstem nuclei (purple) including nucleus tractus solitarius (NTS) and parabrachial nucleus (PBN). The NTS and PBN in turn project to various subcortical structures, including the neuromodulatory structures (blue), as well as subcortical (red) and cortical (yellow) regions. Another spinal afferent pathway bypasses the brainstem and directly targets the thalamus. Abbreviations: Amy, amygdala; Cer, cerebellum; CM, cingulate motor regions; Hc, hippocampus; Hyp, hypothalamus; Ins, insula; LC, locus coeruleus; NTS, nucleus of the solitary tract; PBN, parabrachial nucleus; RN, raphe nucleus; SI, primary somatosensory; SII, secondary somatosensory; SN, substantia nigra; St, striatum; Th, thalamus; vmPFC, ventromedial prefrontal cortex. Modified from Azzalini et al., 2019

Figure 4

Localization of electrodes with respect to anatomical landmarks (umbillicus, xiphoid process, mid‐clavicular line, and coastal margin). (a) Setup for a unipolar montage. The circle area and color code at each electrode location indicate how often this electrode was found to display the largest gastric rhythm, in a sample of 100 healthy participants with a good spectral signature of the gastric rhythm. (b) Setup for a bipolar montage, better suited for fMRI recordings. See text for detailed explanations. REF: Reference. GND: Ground

Figure 5

Two examples of EGG signal and corresponding amplitude and phase that reveal a highly regular rhythm (top) or a mostly regular rhythm (bottom). (a) Top row: Raw signal (grey) with superimposed filtered EGG (blue), obtained by filtering the raw signal ±0.015 Hz around the peak frequency of the recording. The Hilbert transform generates two time series: the amplitude envelope (middle row) and instantaneous phase of the gastric rhythm in radians (bottom row). (b) Distribution of cycle durations. Red dotted lines indicate mean cycle duration ± three SDs. In this example, the distribution of cycle duration is quite narrow, without any outlier. (c) Example of a different recording with mostly regular phase time series. The gastric rhythm is not always visible to the naked eye in the raw signal (top row) and its amplitude is sometimes very low (middle row). A cycle shaded in red and marked by a red arrow shows a nonmonotonous change in phase (bottom row) and concomitant low amplitude. (d) Histogram of cycle duration. The cycle with nonmonotonous change in phase in (c) appears as an outlier (red arrow). The cycle is considered as an artifact (nonmonotonicity and cycle duration) and therefore discarded from further analysis

Figure 6

Examples of power spectra of data included in further analysis (a) or discarded (b‐f). Each line corresponds to a recording channel, and the spectral region highlighted in white corresponds to normogastria. (a) Power spectrum with a well‐defined spectral peak in the normogastric range, occurring in several channels at the same frequency. The star indicates peak frequency and the black line corresponds to the channel with the largest power at peak frequency. The red line represents the ideal filter, and the green line the best fit for the ideal filter. (b) Power spectrum with peaks at different frequencies in different channels. (c) Power spectrum with spectral peaks at two different frequencies. (d) Power spectrum with a broad peak, well defined in only one channel. (e) Several channels display a spectral peak but at different frequencies. (f) A well‐defined spectral peak is present, but only in one channel

Figure 7

Distribution of EGG features across a sample of 100 young healthy participants. (a) Distribution of SDs of cycle duration. A cutoff at six SDs (red shaded area) isolates four outlier participants with more irregular cycles. (b) Percentage of cycles in normogastria (2–4 cpm). A cut‐off at 70% (red shaded area), as proposed by the clinical literature (Riezzo et al., 2013) isolates the same four outlier participants. (c) EGG peak frequency in the 96 remaining participants, with a mean of 0.048 Hz and SD of 0.004 Hz. Peak frequency is higher in female (M = 0.0486 Hz, SD = 0.0044) than male (M = 0.0467 Hz, SD = 0.0039) participants (rank sum test z = −2.25, Bonferroni‐corrected p = .15). Horizontal bars represent the SD. (d) Robust correlation between BMI and average amplitude. BMI shows no significant relationship with mean amplitude (Bonferroni‐corrected p = 1). (e) Robust correlation between elapsed time since the last meal and variability of cycle duration, expressed in SD around the mean for each participant. Longer fasting is associated with higher cycle irregularity (robust regression, Bonferroni‐corrected p = .02, r ² = .09), an effect mostly driven by prolonged fasting (>10 hr). (f) Robust correlation between average amplitude and SD of cycle duration. There is a significant negative relationship, with higher amplitude being associated with lower variability of cycle duration (robust regression, p = .002, r ² = .10)

Figure 8

Decision tree with processing steps and corresponding criteria for a good quality recording/cycle. Grey numbers document the outcome of this procedure in a data set of 117 participants. (a) Decision tree for whether or not the recording can be retained for further analysis, depending on the presence of the spectral signature of the gastric rhythm and rhythm regularity. (b) Additional decision tree to detect artifacted cycles, based on the cycle duration and monotonicity of phase evolution

Figure 9

Percentage of EGG cycles classified as artifacted because of nonmonotonicity, as a function of EGG amplitude. Only 20% of the nonmonotonous cycles also have a very low amplitude