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. 2021 May 17;11(1):10394.
doi: 10.1038/s41598-021-89465-0.

Both high fat and high carbohydrate diets impair vagus nerve signaling of satiety

Hailley Loper  1   2 , Monique Leinen  1   2 , Logan Bassoff  1   2 , Jack Sample  3   4 , Mario Romero-Ortega  5 , Kenneth J Gustafson  3   6 , Dawn M Taylor  3   6   7 , Matthew A Schiefer  8   9   10
Affiliations

Both high fat and high carbohydrate diets impair vagus nerve signaling of satiety

Hailley Loper et al. Sci Rep. .

Abstract

Obesity remains prevalent in the US. One potential treatment is vagus nerve stimulation (VNS), which activates the sensory afferents innervating the stomach that convey stomach volume and establish satiety. However, current VNS approaches and stimulus optimization could benefit from additional understanding of the underlying neural response to stomach distension. In this study, obesity-prone Sprague Dawley rats consumed a standard, high-carbohydrate, or high-fat diet for several months, leading to diet-induced obesity in the latter two groups. Under anesthesia, the neural activity in the vagus nerve was recorded with a penetrating microelectrode array while the stomach was distended with an implanted balloon. Vagal tone during distension was compared to baseline tone prior to distension. Responses were strongly correlated with stomach distension, but the sensitivity to distension was significantly lower in animals that had been fed the nonstandard diets. The results indicate that both high fat and high carbohydrate diets impair vagus activity.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
(a) Schematic of the experimental setup. Blue lines contain water. The blue oval represents the implanted balloon. Red lines are data lines. The red circle in the cervical area is the target implant site of the MEA. The red circle on the hind paw was the target site of the infrared vitals-monitoring clip. (b) View of the cervical vagus nerve implanted with the Blackrock MEA. (c) Microprobes MEA. (d) Blackrock MEA. Note, that while the Blackrock array appears as a standard 8 × 8, 64-channel MEA, the electrodes in the array were wired to three different 16-channel headstages. Thus, the 8 × 8 array was divided into three 16-channel subarrays that were in a diagonal (bottom left to upper right) orientation and 16 additional channels within the 8 × 8 array (shaded white) were nonfunctional. For (b) to (d), the black bar is 1 mm.
Figure 2
Figure 2
Various metrics for the animals, categorized by diet. Diet types are standard (S), low fat high carbohydrate (LF-HC) and high fat low carbohydrate (HF-LC). Significant differences (p ≤ 0.05) are denoted with “*”.
Figure 3
Figure 3
The change observed in the mean area under the curve (AUC) within vagal nerve recordings as a function of stomach volume across trials and MEA channels. Diet types are standard (S), low fat high carbohydrate (LF-HC), and high fat low carbohydrate (HF-LC). Circles indicate means across animals, time samples, and MEA channels for each injected volume binned in 0.5 mL increments. Linear regression R2 values: 0.70, 0.80, and 0.73 for the standard, LF-HC, and HF-LC diets, respectively. The insets show 30 s of raw ENG at three different volumes from one MEA channel of one trial in an animal fed the standard diet.
Figure 4
Figure 4
Example of defining dynamic epochs in one trial. (a) The pressure and injected volume in the intragastric balloon over the course of a trial. The distension step size was 0.2 mL. (b) The ENG recorded throughout the trial. (c) The percent change in AUC relative to pre-distension (baseline). Here, the bar height is the percent change in AUC averaged over every 5 s within the epoch (Pre: N = 30, Sm: N = 11, Med: N = 467, Lrg: N = 465). Data from animal on the standard diet.
Figure 5
Figure 5
The change observed in the area under the curve (AUC) within vagal nerve recordings across animals, time samples, and MEA channels during large stomach distensions. Diet types are standard (S), low fat high carbohydrate (LF-HC), and high fat low carbohydrate (HF-LC). Significant differences (p ≤ 0.05) are denoted with “*”.
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