Vagotomy increases alcohol intake in female rats in diet dependent manner: Implications for increased alcohol use disorder after roux-en-y gastric bypass surgery

Orellana, Elise R.; Nyland, Jennifer E.; Horvath, Nelli; Hajnal, A.

doi:10.1016/j.physbeh.2021.113309

Cited by 7 publications

(7 citation statements)

References 45 publications

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“…The findings here indicate that disruption to the gastric branch of the vagus nerve increases EtOH intake and preference in the every‐other‐day two‐bottle choice model as well as increase EtOH‐conditioned place preference in male Sprague–Dawley rats. These findings extend our previous research indicating that gastric branch vagal disruptions, either directly or as part of the RYGB procedure, increases EtOH intake and preference in a continuous access two bottle choice model in both male and female Sprague–Dawley rats (Orellana et al., 2021; Thanos et al., 2012). Even though we used 4% EtOH in these intake studies, the overall g/kg levels achieved in these studies are similar to previous work in Sprague–Dawley rats in a similar two‐bottle choice model with 20% EtOH (Corongiu et al., 2022).…”

Section: Discussionsupporting

confidence: 90%

“…After full recovery from the surgeries (1–2 weeks), rats were given a two‐bottle choice test in which water (filtered tap water) and 4% EtOH (95%, Pharmco Products Inc., CT, diluted v/v in filtered tap water prepared weekly) were presented at the front of the home cage in inverted graded cylinders. The 4% EtOH concentration was chosen based on our previous studies (Orellana et al., 2021). Whereas water was available ad libitum every day, EtOH access was limited to Mondays, Wednesdays, and Fridays, presented in the morning (09:00) and removed 24 h later.…”

Section: Methodsmentioning

confidence: 99%

“…The vagus nerve has numerous branches that may have differing regulation of central‐peripheral functions, but based on the extensive vagus nerve damage induced by RYGB and the de novo risk for AUD following RYGB surgery in clinical populations, we hypothesized that the gastric branch of the vagus nerve may have important regulatory functions in relation to EtOH intake and preference. Our previous work highlights the role of the gastric vagus nerve on EtOH intake in the continuous two‐bottle choice assay in rats (Orellana et al., 2021) but whether disruptions to the vagus nerve influence EtOH intake and preference in other standard models has not been previously evaluated.…”

Section: Introductionmentioning

confidence: 99%

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Vagus nerve damage increases alcohol intake and preference in a nonpreferring rat line: Relationship to vagal regulation of the hypothalamic–pituitary–adrenal axis

Keller,

Snyder,

Coker

et al. 2024

Alcohol, Clinical and Experimental Research

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BackgroundClinical and preclinical research indicates that gastric weight loss surgeries, such as Roux‐en‐Y gastric bypass surgery, can induce alcohol use disorder (AUD). While numerous mechanisms have been proposed for these effects, one relatively unexplored potential mechanism is physical damage to the gastric branch of the vagus nerve, which can occur during bypass surgery. Therefore, we hypothesized that direct damage to the gastric branch of the vagus nerve, without altering other aspects of gastric anatomy, could result in increased alcohol intake.MethodsTo test this hypothesis, we compared alcohol intake and preference in multiple models in male Sprague–Dawley rats that received selective gastric branch vagotomy (VX) with rats who underwent sham surgery. Because the vagus nerve regulates hypothalamic‐pituitary‐adrenal (HPA) axis function, and alterations to HPA function are critical to the escalation of non‐dependent alcohol intake, we also tested the hypothesis that gastric VX increases HPA function.ResultsWe found that VX increases alcohol intake and preference in the every‐other‐day, two‐bottle choice test and increases preference for 1 g/kg alcohol in the conditioned place preference test. The effects were selective for alcohol, as sucrose intake and preference were not altered by VX. We also found that VX increases corticotropin releasing factor (CRF) mRNA in the paraventricular nucleus of the hypothalamus (PVN), increases putative PVN CRF neuronal action potential firing, and increases corticosterone levels.ConclusionsOverall, these findings suggest that the vagus nerve may play a critical role in regulating HPA axis function via modulation of PVN CRF mRNA expression and putative PVN CRF neuronal activity. Furthermore, disruptions to vagal regulation of HPA axis function may increase alcohol intake and preference.

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Section: Discussionsupporting

confidence: 90%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Vagus nerve damage increases alcohol intake and preference in a nonpreferring rat line: Relationship to vagal regulation of the hypothalamic–pituitary–adrenal axis

Keller,

Snyder,

Coker

et al. 2024

Alcohol, Clinical and Experimental Research

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“…Other studies further suggest that VX induces anhedonia-like behavior in multiple behavioral tasks (Klarer et al, 2019). However, previous studies utilizing the same limited VX surgery model used here showed increased alcohol intake (Orellana et al, 2021). Overall, future studies will be needed to address these disparities to determine the independent roles of both afferent and efferent vagal fibers in stress-related behaviors and PVN responsively.…”

Section: Discussionmentioning

confidence: 65%

The vagus nerve is critical for regulation of hypothalamic-pituitary-adrenal axis responses to acute stress

et al. 2021

Preprint

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The hypothalamic pituitary adrenal (HPA) axis is a critical regulator of physiologic and psychological responses to acute and chronic stressors. HPA axis function is control by numerous feedback inhibitory mechanisms, disruptions of which can lead to various psychiatric conditions, such as depression, posttraumatic stress disorder, and schizophrenia. Vagus nerve stimulation has been shown to be efficacious in these various mental health issues potentially via modulation of HPA axis function, but the mechanisms by which the vagus nerve may regulate HPA function has not been fully elucidated. In the present studies, we sought to test the hypothesis that the vagus nerve is a critical regulator of HPA function. Neuroendocrine function and neurocircuit changes in corticotropin releasing factor (CRF) neurons in the paraventricular nucleus of the hypothalamus (PVN) was examined following acute stress after subdiaphragmatic left vagotomy (VX) in adult male Sprague-Dawley rats. We found that VX mimics HPA activation seen in sham surgery animals exposed to acute restraint stress, particularly increased plasma corticosterone levels, elevated PVN CRF mRNA, and increased action potential firing of putative CRF neurons in PVN brain slices. Furthermore, VX animals exposed to acute restraint stress showed increased elevations of plasma corticosterone and PVN CRF mRNA which may be due to lack of compensatory PVN GABAergic signaling in response to acute stress. Both Sham/Stress and VX/no stress conditions increases action potential firing in putative PVN CRF neurons, but this effect was not seen in the VX/stress condition, suggesting that not all forms of stress compensation are lost following VX. Overall, these findings suggest that the vagus nerve may play a critical role in regulating HPA axis function via modulation of local PVN neurocircuit activity.

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“…While the exact underlying mechanism remains unknown, pre-clinical studies of RYGB points to neuronal plasticity occurring in the DVC following removal of gastric vagal afferents ( Browning et al, 2013 ; Browning and Hajnal, 2014 ; Ballsmider et al, 2015 ; Minaya et al, 2019 ). One recent preclinical study focused on damage to the gastric branches of the vagus nerve that is unavoidable in the RYGB procedure and found gastric vagal de-afferentation is sufficient to increase alcohol intake in both obese and lean rats ( Orellana et al, 2021b ), suggesting vagal afferent dysfunction and resulting alterations in DVC activity may play a critical role in AUD development.…”

Section: Clinical Relevance Of Dorsal Vagal Complex Neurotransmitter ...mentioning

confidence: 99%

Involvement of the Dorsal Vagal Complex in Alcohol-Related Behaviors

Keller

Hajnal

Browning

et al. 2022

Front. Behav. Neurosci.

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The neurobiological mechanisms that regulate the development and maintenance of alcohol use disorder (AUD) are complex and involve a wide variety of within and between systems neuroadaptations. While classic reward, preoccupation, and withdrawal neurocircuits have been heavily studied in terms of AUD, viable treatment targets from this established literature have not proven clinically effective as of yet. Therefore, examination of additional neurocircuitries not classically studied in the context of AUD may provide novel therapeutic targets. Recent studies demonstrate that various neuropeptides systems are important modulators of alcohol reward, seeking, and intake behaviors. This includes neurocircuitry within the dorsal vagal complex (DVC), which is involved in the control of the autonomic nervous system, control of intake of natural rewards like food, and acts as a relay of interoceptive sensory information via interactions of numerous gut-brain peptides and neurotransmitter systems with DVC projections to central and peripheral targets. DVC neuron subtypes produce a variety of neuropeptides and transmitters and project to target brain regions critical for reward such as the mesolimbic dopamine system as well as other limbic areas important for the negative reinforcing and aversive properties of alcohol withdrawal such as the extended amygdala. This suggests the DVC may play a role in the modulation of various aspects of AUD. This review summarizes the current literature on neurotransmitters and neuropeptides systems in the DVC (e.g., norepinephrine, glucagon-like peptide 1, neurotensin, cholecystokinin, thyrotropin-releasing hormone), and their potential relevance to alcohol-related behaviors in humans and rodent models for AUD research. A better understanding of the role of the DVC in modulating alcohol related behaviors may lead to the elucidation of novel therapeutic targets for drug development in AUD.

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Vagotomy increases alcohol intake in female rats in diet dependent manner: Implications for increased alcohol use disorder after roux-en-y gastric bypass surgery

Cited by 7 publications

References 45 publications

Vagus nerve damage increases alcohol intake and preference in a nonpreferring rat line: Relationship to vagal regulation of the hypothalamic–pituitary–adrenal axis

Vagus nerve damage increases alcohol intake and preference in a nonpreferring rat line: Relationship to vagal regulation of the hypothalamic–pituitary–adrenal axis

The vagus nerve is critical for regulation of hypothalamic-pituitary-adrenal axis responses to acute stress

Involvement of the Dorsal Vagal Complex in Alcohol-Related Behaviors

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