Gut vagal sensory signaling regulates hippocampus function through multi-order pathways

Suarez, Andrea N.; Hsu, Ted M.; Liu, Clarissa M.; Noble, Emily E.; Cortella, Alyssa M.; Nakamoto, Emily M; Hahn, Joel D.; Lartigue, Guillaume de; Kanoski, Scott E.

doi:10.1038/s41467-018-04639-1

Cited by 157 publications

(168 citation statements)

References 70 publications

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“…Clinically, vagus nerve stimulation (VNS) has been applied to inhibit central nervous system diseases, such as refractory epilepsy (Ben‐Menachem et al., ; Takaya, Terry, & Naritoku, ) and treatment‐resistant depression (Nemeroff et al., ; Wani, Trevino, Marnell, & Husain, ). Consistently, studies using rodents have demonstrated that artificial modulation of vagus nerve activity can alter brain electrical activity (Alexander et al., ; Cao et al., ; Larsen et al., ; Usami et al., ), stop seizures (Woodbury & Woodbury, ), evoke emotional responses, facilitate learning and decision‐making (Alvarez‐Dieppa, Griffin, Cavalier, & McIntyre, ; Cao et al., ; Pena et al., ; Suarez et al., ), even reduce food intake and body weight (Johannessen et al., ), and cardiac hemodynamic effects through activation of the efferent parasympathetic pathway (Yamakawa et al., ).…”

Section: Introductionmentioning

confidence: 84%

Vagus nerve spiking activity associated with locomotion and cortical arousal states in a freely moving rat

Shikano

Nishimura

Okonogi

et al. 2018

Eur J of Neuroscience

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The vagus nerve serves as a central pathway for communication between the central and peripheral organs. Despite traditional knowledge of vagus nerve functions, detailed neurophysiological dynamics of the vagus nerve in naïve behavior remain to be understood. In this study, we developed a new method to record spiking patterns from the cervical vagus nerve while simultaneously monitoring central and peripheral organ bioelectrical signals in a freely moving rat. When the rats transiently elevated locomotor activity, the frequency of vagus nerve spikes was correspondingly increased, and this activity was retained for several seconds after the increase in running speed terminated. Spike patterns of the vagus nerve were not robustly associated with which arms the animals entered on an elevated plus maze. During sniffing behavior, vagus nerve spikes were nearly absent. During stopping, the vagus nerve spike patterns differed considerably depending on external contexts and peripheral activity states associated with cortical arousal levels. Stimulation of the vagus nerve altered rat's running speed and cortical arousal states depending on running speed at the instant of stimulation. These observations are a new step for uncovering the physiological dynamics of the vagus nerve modulating the visceral organs such as cardiovascular, respiratory, and gastrointestinal systems.

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Section: Introductionmentioning

confidence: 84%

Vagus nerve spiking activity associated with locomotion and cortical arousal states in a freely moving rat

Shikano

Nishimura

Okonogi

et al. 2018

Eur J of Neuroscience

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“…Sections were collected in 5 series and stored in antifreeze solution at −20°C until further processing. General fluorescence IHC labeling procedures were performed, as reported Suarez et al, 2018). The following antibodies and dilutions were used: rabbit anti-RFP (1:2000, Rockland Inc., Limerick, PA, USA).…”

Section: Immunohistochemistrymentioning

confidence: 99%

Nucleus accumbens melanin-concentrating hormone signaling promotes feeding in a sex-specific manner

Terrill

Subramanian

Lan

et al. 2020

Preprint

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AbstractMelanin-concentrating hormone (MCH) is an orexigenic neuropeptide produced in the lateral hypothalamus and zona incerta that increases food intake. The neuronal pathways and behavioral mechanisms mediating the orexigenic effects of MCH are poorly understood, as is the extent to which MCH-mediated feeding outcomes are sex-dependent. Here we investigate the hypothesis that MCH-producing neurons act in the nucleus accumbens shell (ACBsh) to promote feeding behavior and motivation for palatable food in a sex-dependent manner. We utilized ACBsh MCH receptor (MCH1R)-directed pharmacology as well as a dual virus chemogenetic approach to selectively activate MCH neurons that project to the ACBsh. Results reveal that both ACBsh MCH1R activation and activating ACBsh-projecting MCH neurons increase consumption of standard chow and palatable sucrose in male rats without affecting motivated operant responding for sucrose, general activity levels, or anxiety-like behavior. In contrast, food intake was not affected in female rats by either ACBsh MCH1R activation or ACBsh-projecting MCH neuron activation. To determine a mechanism for this sexual dimorphism, we investigated whether the orexigenic effect of ACBsh MCH1R activation is reduced by endogenous estradiol signaling. In ovariectomized female rats on a cyclic regimen of either estradiol (EB) or oil vehicle, ACBsh MCH1R activation increased feeding only in oil-treated rats, suggesting that EB attenuates the ability of ACBsh MCH signaling to promote food intake. Collective results show that that MCH ACBsh signaling promotes feeding in an estrogen- and sex-dependent manner, thus identifying novel neurobiological mechanisms through which MCH and female sex hormones interact to influence food intake.

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“…The vagal nerve is one of the major connections of the gut-brain-axis. Interestingly, vagal gut-brain sensory (afferent) signaling was required for hippocampal-dependent learning processes as demonstrated by partially vagotomized rats in a modified Barnes maze [82]. Vagal afferent information is first received in the brain within the medial nucleus of the solitary tract which projects towards many brainstem and forebrain sites [83,84].…”

Section: Impact Of Microbial Amyloids On Host Health and Neurodegenermentioning

confidence: 99%

Amyloidogenic Peptides in Human Neuro-Degenerative Diseases and in Microorganisms: A Sorrow Shared Is a Sorrow Halved?

Endres

2020

Molecules

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The term “amyloid” refers to proteinaceous deposits of peptides that might be generated from larger precursor proteins e.g., by proteolysis. Common to these peptides is a stable cross-β dominated secondary structure which allows self-assembly, leading to insoluble oligomers and lastly to fibrils. These highly ordered protein aggregates have been, for a long time, mainly associated with human neurodegenerative diseases such as Alzheimer’s disease (Amyloid-β peptides). However, they also exert physiological functions such as in release of deposited hormones in human beings. In the light of the rediscovery of our microbial commensals as important companions in health and disease, the fact that microbes also possess amyloidogenic peptides is intriguing. Transmission of amyloids by iatrogenic means or by consumption of contaminated meat from diseased animals is a well-known fact. What if also our microbial commensals might drive human amyloidosis or suffer from our aggregated amyloids? Moreover, as the microbial amyloids are evolutionarily older, we might learn from these organisms how to cope with the sword of Damocles forged of endogenous, potentially toxic peptides. This review summarizes knowledge about the interplay between human amyloids involved in neurodegenerative diseases and microbial amyloids.

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Gut vagal sensory signaling regulates hippocampus function through multi-order pathways

Cited by 157 publications

References 70 publications

Vagus nerve spiking activity associated with locomotion and cortical arousal states in a freely moving rat

Vagus nerve spiking activity associated with locomotion and cortical arousal states in a freely moving rat

Nucleus accumbens melanin-concentrating hormone signaling promotes feeding in a sex-specific manner

Amyloidogenic Peptides in Human Neuro-Degenerative Diseases and in Microorganisms: A Sorrow Shared Is a Sorrow Halved?

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