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Article ; Online: Gastrointestinal dysmotility in rodent models of Parkinson's disease.

Pellegrini, Carolina / Travagli, R Alberto

American journal of physiology. Gastrointestinal and liver physiology

2024 Volume 326, Issue 4, Page(s) G345–G359

Abstract: Multiple studies describe prodromal, nonmotor dysfunctions that affect the quality of life of patients who subsequently develop Parkinson's disease (PD). These prodromal dysfunctions comprise a wide array of autonomic issues, including severe ... ...

Abstract	Multiple studies describe prodromal, nonmotor dysfunctions that affect the quality of life of patients who subsequently develop Parkinson's disease (PD). These prodromal dysfunctions comprise a wide array of autonomic issues, including severe gastrointestinal (GI) motility disorders such as dysphagia, delayed gastric emptying, and chronic constipation. Indeed, strong evidence from studies in humans and animal models suggests that the GI tract and its neural, mainly vagal, connection to the central nervous system (CNS) could have a major role in the etiology of PD. In fact, misfolded α-synuclein aggregates that form Lewy bodies and neurites, i.e., the histological hallmarks of PD, are detected in the enteric nervous system (ENS) before clinical diagnosis of PD. The aim of the present review is to provide novel insights into the pathogenesis of GI dysmotility in PD, focusing our attention on functional, neurochemical, and molecular alterations in animal models.
MeSH term(s)	Animals ; Humans ; Parkinson Disease ; Rodentia ; Quality of Life ; Gastrointestinal Diseases/etiology ; Enteric Nervous System
Language	English
Publishing date	2024-01-23
Publishing country	United States
Document type	Journal Article ; Review
ZDB-ID	603840-2
ISSN	1522-1547 ; 0193-1857
ISSN (online)	1522-1547
ISSN	0193-1857
DOI	10.1152/ajpgi.00225.2023
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Article ; Online: Experimental models of gut-first Parkinson's disease: A systematic review.

Videlock, Elizabeth J / Xing, Tiaosi / Yehya, Ashwaq Hamid Salem / Travagli, R Alberto

Neurogastroenterology and motility

2023 Volume 35, Issue 8, Page(s) e14604

Abstract: Background: There is strong support from studies in humans and in animal models that Parkinson's disease (PD) may begin in the gut. This brings about a unique opportunity for researchers in the field of neurogastroenterology to contribute to advancing ... ...

Abstract	Background: There is strong support from studies in humans and in animal models that Parkinson's disease (PD) may begin in the gut. This brings about a unique opportunity for researchers in the field of neurogastroenterology to contribute to advancing the field and making contributions that could lead to the ability to diagnose and treat PD in the premotor stages. Lack of familiarity with some of the aspects of the experimental approaches used in these studies may present a barrier for neurogastroenterology researchers to enter the field. Much remains to be understood about intestinal-specific components of gut-first PD pathogenesis and the field would benefit from contributions of enteric and central nervous system neuroscientists. Purpose: To address these issues, we have conducted a systematic review of the two most frequently used experimental models of gut-first PD: transneuronal propagation of α-synuclein preformed fibrils and oral exposure to environmental toxins. We have reviewed the details of these studies and present methodological considerations for the use of these models. Our aim is that this review will serve as a framework and useful reference for neuroscientists, gastroenterologists, and neurologists interested in applying their expertise to advancing our understanding of gut-first PD.
MeSH term(s)	Animals ; Humans ; Parkinson Disease/diagnosis ; alpha-Synuclein ; Central Nervous System ; Brain/metabolism ; Models, Theoretical
Chemical Substances	alpha-Synuclein
Language	English
Publishing date	2023-05-01
Publishing country	England
Document type	Systematic Review ; Journal Article ; Review ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, Non-U.S. Gov't
ZDB-ID	1186328-6
ISSN	1365-2982 ; 1350-1925
ISSN (online)	1365-2982
ISSN	1350-1925
DOI	10.1111/nmo.14604
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Article ; Online: Hypothalamic-vagal oxytocinergic neurocircuitry modulates gastric emptying and motility following stress.

Jiang, Yanyan / Travagli, R Alberto

The Journal of physiology

2020 Volume 598, Issue 21, Page(s) 4941–4955

Abstract: Key points: Stress triggers and exacerbates the symptoms of functional gastrointestinal disorders, such as delayed gastric emptying and impaired gastric motility. Understanding the mechanisms by which the neural circuits, impaired by stress, are ... ...

Abstract	Key points: Stress triggers and exacerbates the symptoms of functional gastrointestinal disorders, such as delayed gastric emptying and impaired gastric motility. Understanding the mechanisms by which the neural circuits, impaired by stress, are restored may help to identify potential targets for more effective therapeutic interventions. Oxytocin administration or release ameliorates the stress-induced delayed gastric emptying and motility. However, is it unclear whether the effects are mediated via the hypothalamic-pituitary-adrenocortical axis or the oxytocinergic projections from the paraventricular nucleus of the hypothalamus to brainstem neurones of the dorsal vagal complex. We used Cre-inducible designer receptors exclusively activated by designer drugs to demonstrate the fundamental role of the oxytocinergic hypothalamic-vagal projections in the gastric adaptation to stress. Abstract: Stress triggers and exacerbates the symptoms of functional gastrointestinal (GI) disorders, such as delayed gastric emptying and impaired gastric motility. The prototypical anti-stress hormone, oxytocin (OXT), plays a major role in the modulation of gastric emptying and motility following stress. It is not clear, however, whether the amelioration of dysregulated GI functions by OXT is mediated via an effect on the hypothalamic-pituitary-adrenocortical axis or the oxytocinergic projections from the paraventricular nucleus of the hypothalamus (PVN) to neurones of the dorsal vagal complex (DVC). In the present study we tested the hypothesis that the activity of hypothalamic-vagal oxytocinergic neurocircuits plays a major role in the gastric adaptation to stress. Cre-inducible designer receptors exclusively activated by designer drugs (DREADDs) were injected into the DVC of rats and retrogradely transported to allow selective expression in OXT neurones in the PVN. Following acute stress and either chronic heterotypic (CHe) or chronic homotypic (CHo) stress, gastric emptying was assessed via the [
MeSH term(s)	Animals ; Gastric Emptying ; Gastrointestinal Motility ; Hypothalamus ; Oxytocin ; Paraventricular Hypothalamic Nucleus ; Rats ; Vagus Nerve
Chemical Substances	Oxytocin (50-56-6)
Language	English
Publishing date	2020-09-07
Publishing country	England
Document type	Journal Article
ZDB-ID	3115-x
ISSN	1469-7793 ; 0022-3751
ISSN (online)	1469-7793
ISSN	0022-3751
DOI	10.1113/JP280023
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Article ; Online: Brainstem astrocytes control homeostatic regulation of caloric intake.

Clyburn, Courtney / Carson, Kaitlin E / Smith, Caleb R / Travagli, R Alberto / Browning, Kirsteen N

The Journal of physiology

2023 Volume 601, Issue 4, Page(s) 801–829

Abstract: Prolonged high-fat diet (HFD) exposure is associated with hyperphagia, excess caloric intake and weight gain. After initial exposure to a HFD, a brief (24-48 h) period of hyperphagia is followed by the regulation of caloric intake and restoration of ... ...

Abstract	Prolonged high-fat diet (HFD) exposure is associated with hyperphagia, excess caloric intake and weight gain. After initial exposure to a HFD, a brief (24-48 h) period of hyperphagia is followed by the regulation of caloric intake and restoration of energy balance within an acute (3-5 day) period. Previous studies have demonstrated this occurs via a vagally mediated signalling cascade that increases glutamatergic transmission via activation of NMDA receptors located on gastric-projecting neurons of the dorsal motor nucleus of the vagus (DMV). The present study used electrophysiological recordings from thin brainstem slice preparations, in vivo recordings of gastric motility and tone, measurement of gastric emptying rates, and food intake studies to investigate the hypothesis that activation of brainstem astrocytes in response to acute HFD exposure is responsible for the increased glutamatergic drive to DMV neurons and the restoration of caloric balance. Pharmacological and chemogenetic inhibition of brainstem astrocytes reduced glutamatergic signalling and DMV excitability, dysregulated gastric tone and motility, attenuated the homeostatic delay in gastric emptying, and prevented the decrease in food intake that is observed during the period of energy regulation following initial exposure to HFD. Understanding the mechanisms involved in caloric regulation may provide critical insights into energy balance as well as into the hyperphagia that develops as these mechanisms are overcome. KEY POINTS: Initial exposure to a high fat diet is associated with a brief period of hyperphagia before caloric intake and energy balance is restored. This period of homeostatic regulation is associated with a vagally mediated signalling cascade that increases glutamatergic transmission to dorsal motor nucleus of the vagus (DMV) neurons via activation of synaptic NMDA receptors. The present study demonstrates that pharmacological and chemogenetic inhibition of brainstem astrocytes reduced glutamatergic signalling and DMV neuronal excitability, dysregulated gastric motility and tone and emptying, and prevented the regulation of food intake following high-fat diet exposure. Astrocyte regulation of glutamatergic transmission to DMV neurons appears to involve release of the gliotransmitters glutamate and ATP. Understanding the mechanisms involved in caloric regulation may provide critical insights into energy balance as well as into the hyperphagia that develops as these mechanisms are overcome.
MeSH term(s)	Animals ; Rats ; Astrocytes/physiology ; Brain Stem/cytology ; Energy Intake ; Hyperphagia ; Rats, Sprague-Dawley ; Receptors, N-Methyl-D-Aspartate ; Vagus Nerve/physiology ; Diet, High-Fat
Chemical Substances	Receptors, N-Methyl-D-Aspartate
Language	English
Publishing date	2023-01-25
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	3115-x
ISSN	1469-7793 ; 0022-3751
ISSN (online)	1469-7793
ISSN	0022-3751
DOI	10.1113/JP283566
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Article ; Online: The substantia nigra modulates proximal colon tone and motility in a vagally-dependent manner in the rat.

Xing, Tiaosi / Nanni, Giorgia / Burkholder, Cameron R / Browning, Kirsteen N / Travagli, R Alberto

The Journal of physiology

2023 Volume 601, Issue 21, Page(s) 4751–4766

Abstract: A monosynaptic pathway connects the substantia nigra pars compacta (SNpc) to neurons of the dorsal motor nucleus of the vagus (DMV). This monosynaptic pathway modulates the vagal control of gastric motility. It is not known, however, whether this nigro- ... ...

Abstract	A monosynaptic pathway connects the substantia nigra pars compacta (SNpc) to neurons of the dorsal motor nucleus of the vagus (DMV). This monosynaptic pathway modulates the vagal control of gastric motility. It is not known, however, whether this nigro-vagal pathway also modulates the tone and motility of the proximal colon. In rats, microinjection of retrograde tracers in the proximal colon and of anterograde tracers in SNpc showed that bilaterally labelled colonic-projecting neurons in the DMV received inputs from SNpc neurons. Microinjections of the ionotropic glutamate receptor agonist, NMDA, in the SNpc increased proximal colonic motility and tone, as measured via a strain gauge aligned with the colonic circular smooth muscle; the motility increase was inhibited by acute subdiaphragmatic vagotomy. Upon transfection of SNpc with pAAV-hSyn-hM3D(Gq)-mCherry, chemogenetic activation of nigro-vagal nerve terminals by brainstem application of clozapine-N-oxide increased the firing rate of DMV neurons and proximal colon motility; both responses were abolished by brainstem pretreatment with the dopaminergic D1-like antagonist SCH23390. Chemogenetic inhibition of nigro-vagal nerve terminals following SNpc transfection with pAAV-hSyn-hM4D(Gi)-mCherry decreased the firing rate of DMV neurons and inhibited proximal colon motility. These data suggest that a nigro-vagal pathway modulates activity of the proximal colon motility tonically via a discrete dopaminergic synapse in a manner dependent on vagal efferent nerve activity. Impairment of this nigro-vagal pathway may contribute to the severely reduced colonic transit and prominent constipation observed in both patients and animal models of parkinsonism. KEY POINTS: Substantia nigra pars compacta (SNpc) neurons are connected to the dorsal motor nucleus of the vagus (DMV) neurons via a presumed direct pathway. Brainstem neurons in the lateral DMV innervate the proximal colon. Colonic-projecting DMV neurons receive inputs from neurons of the SNpc. The nigro-vagal pathway modulates tone and motility of the proximal colon via D1-like receptors in the DMV. The present study provides the mechanistic basis for explaining how SNpc alterations may lead to a high rate of constipation in patients with Parkinson's Disease.
MeSH term(s)	Humans ; Rats ; Animals ; Stomach/physiology ; Rats, Sprague-Dawley ; Substantia Nigra/metabolism ; Vagus Nerve/physiology ; Gastrointestinal Motility/physiology ; Colon ; Constipation/metabolism
Language	English
Publishing date	2023-09-29
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	3115-x
ISSN	1469-7793 ; 0022-3751
ISSN (online)	1469-7793
ISSN	0022-3751
DOI	10.1113/JP284238
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Article ; Online: Perinatal high-fat diet exposure alters oxytocin and corticotropin releasing factor inputs onto vagal neurocircuits controlling gastric motility.

Carson, Kaitlin E / Alvarez, Jared / Mackley, Jasmine Q / Travagli, R Alberto / Browning, Kirsteen N

The Journal of physiology

2023 Volume 601, Issue 14, Page(s) 2853–2875

Abstract: Perinatal high-fat diet (pHFD) exposure alters the development of vagal neurocircuits that control gastrointestinal (GI) motility and reduce stress resiliency in offspring. Descending oxytocin (OXT; prototypical anti-stress peptide) and corticotropin ... ...

Abstract	Perinatal high-fat diet (pHFD) exposure alters the development of vagal neurocircuits that control gastrointestinal (GI) motility and reduce stress resiliency in offspring. Descending oxytocin (OXT; prototypical anti-stress peptide) and corticotropin releasing factor (CRF; prototypical stress peptide) inputs from the paraventricular nucleus (PVN) of the hypothalamus to the dorsal motor nucleus of the vagus (DMV) modulate the GI stress response. How these descending inputs, and their associated changes to GI motility and stress responses, are altered following pHFD exposure are, however, unknown. The present study used retrograde neuronal tracing experiments, cerebrospinal fluid extraction, in vivo recordings of gastric tone, motility and gastric emptying rates, and in vitro electrophysiological recordings from brainstem slice preparations to investigate the hypothesis that pHFD alters descending PVN-DMV inputs and dysregulates vagal brain-gut responses to stress. Compared to controls, rats exposed to pHFD had slower gastric emptying rates and did not respond to acute stress with the expected delay in gastric emptying. Neuronal tracing experiments demonstrated that pHFD reduced the number of PVN
MeSH term(s)	Pregnancy ; Female ; Rats ; Animals ; Corticotropin-Releasing Hormone ; Oxytocin ; Rats, Sprague-Dawley ; Diet, High-Fat/adverse effects ; Stomach/physiology ; Gastrointestinal Motility ; Vagus Nerve/physiology
Chemical Substances	Corticotropin-Releasing Hormone (9015-71-8) ; Oxytocin (50-56-6)
Language	English
Publishing date	2023-05-17
Publishing country	England
Document type	Journal Article
ZDB-ID	3115-x
ISSN	1469-7793 ; 0022-3751
ISSN (online)	1469-7793
ISSN	0022-3751
DOI	10.1113/JP284726
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Article ; Online: Stress-induced neuroplasticity in the gastric response to brainstem oxytocin in male rats.

Jiang, Yanyan / Zimmerman, Julia E / Browning, Kirsteen N / Travagli, R Alberto

American journal of physiology. Gastrointestinal and liver physiology

2022 Volume 322, Issue 5, Page(s) G513–G522

Abstract: Previous studies have shown that pharmacological manipulations with stress-related hormones such as corticotropin-releasing factor and thyrotropin-releasing hormone induce neuroplasticity in brainstem vagal neurocircuits, which modulate gastric tone and ... ...

Abstract	Previous studies have shown that pharmacological manipulations with stress-related hormones such as corticotropin-releasing factor and thyrotropin-releasing hormone induce neuroplasticity in brainstem vagal neurocircuits, which modulate gastric tone and motility. The prototypical antistress hormone oxytocin (OXT) has been shown to modulate gastric tone and motility via vagal pathways, and descending hypothalamic oxytocinergic inputs play a major role in the vagally dependent gastric-related adaptations to stress. The aim of this study was to investigate the possible cellular mechanisms through which OXT modulates central vagal brainstem and peripheral enteric neurocircuits of male Sprague-Dawley rats in response to chronic repetitive stress. After chronic (5 consecutive days) of homotypic or heterotypic stress load, the response to exogenous brainstem administration of OXT was examined using whole cell patch-clamp recordings from gastric-projecting vagal motoneurons and in vivo recordings of gastric tone and motility. GABAergic currents onto vagal motoneurons were decreased by OXT in stressed, but not in naïve rats. In naïve rats, microinjections of OXT in vagal brainstem nuclei-induced gastroinhibition via peripheral release of nitric oxide (NO). In stressed rats, however, the OXT-induced gastroinhibition was determined by the release of both NO and vasoactive intestinal peptide (VIP). Taken together, our data indicate that stress induces neuroplasticity in the response to OXT in the neurocircuits, which modulate gastric tone and motility. In particular, stress uncovers the OXT-mediated modulation of brainstem GABAergic currents and alters the peripheral gastric response to vagal stimulation.
MeSH term(s)	Animals ; Brain Stem/physiology ; Male ; Neuronal Plasticity ; Oxytocin/pharmacology ; Rats ; Rats, Sprague-Dawley ; Stomach/physiology ; Vagus Nerve/physiology
Chemical Substances	Oxytocin (50-56-6)
Language	English
Publishing date	2022-02-16
Publishing country	United States
Document type	Journal Article
ZDB-ID	603840-2
ISSN	1522-1547 ; 0193-1857
ISSN (online)	1522-1547
ISSN	0193-1857
DOI	10.1152/ajpgi.00347.2021
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Article ; Online: Neurophysiology of the brain stem in Parkinson's disease.

Bove, Cecilia / Travagli, R Alberto

Journal of neurophysiology

2019 Volume 121, Issue 5, Page(s) 1856–1864

Abstract: Parkinson's disease (PD) is predominantly idiopathic in origin, and a large body of evidence indicates that gastrointestinal (GI) dysfunctions are a significant comorbid clinical feature; these dysfunctions include dysphagia, nausea, delayed gastric ... ...

Abstract	Parkinson's disease (PD) is predominantly idiopathic in origin, and a large body of evidence indicates that gastrointestinal (GI) dysfunctions are a significant comorbid clinical feature; these dysfunctions include dysphagia, nausea, delayed gastric emptying, and severe constipation, all of which occur commonly before the onset of the well-known motor symptoms of PD. Based on a distinct distribution pattern of Lewy bodies (LB) in the enteric nervous system (ENS) and in the preganglionic neurons of the dorsal motor nucleus of the vagus (DMV), and together with the early onset of GI symptoms, it was suggested that idiopathic PD begins in the ENS and spreads to the central nervous system (CNS), reaching the DMV and the substantia nigra pars compacta (SNpc). These two areas are connected by a recently discovered monosynaptic nigro-vagal pathway, which is dysfunctional in rodent models of PD. An alternative hypothesis downplays the role of LB transport through the vagus nerve and proposes that PD pathology is governed by regional or cell-restricted factors as the leading cause of nigral neuronal degeneration. The purpose of this brief review is to summarize the neuronal electrophysiological findings in the SNpc and DMV in PD.
MeSH term(s)	Animals ; Dopamine/metabolism ; Humans ; Parkinson Disease/metabolism ; Parkinson Disease/physiopathology ; Substantia Nigra/metabolism ; Substantia Nigra/physiopathology ; Synaptic Transmission
Chemical Substances	Dopamine (VTD58H1Z2X)
Language	English
Publishing date	2019-03-27
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	80161-6
ISSN	1522-1598 ; 0022-3077
ISSN (online)	1522-1598
ISSN	0022-3077
DOI	10.1152/jn.00056.2019
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Article ; Online: Central control of gastrointestinal motility.

Browning, Kirsteen N / Travagli, R Alberto

Current opinion in endocrinology, diabetes, and obesity

2018 Volume 26, Issue 1, Page(s) 11–16

Abstract: Purpose of review: This review summarizes the organization and structure of vagal neurocircuits controlling the upper gastrointestinal tract, and more recent studies investigating their role in the regulation of gastric motility under physiological, as ... ...

Abstract	Purpose of review: This review summarizes the organization and structure of vagal neurocircuits controlling the upper gastrointestinal tract, and more recent studies investigating their role in the regulation of gastric motility under physiological, as well as pathophysiological, conditions. Recent findings: Vagal neurocircuits regulating gastric functions are highly plastic, and open to modulation by a variety of inputs, both peripheral and central. Recent research in the fields of obesity, development, stress, and neurological disorders highlight the importance of central inputs onto these brainstem neurocircuits in the regulation of gastric motility. Summary: Recognition of the pivotal role that the central nervous system exerts in the regulation, integration, and modulation of gastric motility should serve to encourage research into central mechanisms regulating peripheral motility disorders.
MeSH term(s)	Animals ; Gastrointestinal Motility/physiology ; Gastrointestinal Tract/innervation ; Gastrointestinal Tract/physiology ; Humans ; Nerve Net/physiology ; Vagus Nerve/physiology
Language	English
Publishing date	2018-11-12
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	2272017-0
ISSN	1752-2978 ; 1752-296X
ISSN (online)	1752-2978
ISSN	1752-296X
DOI	10.1097/MED.0000000000000449
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Article ; Online: Novel transmitters in brain stem vagal neurocircuitry: new players on the pitch.

Bülbül, Mehmet / Travagli, R Alberto

American journal of physiology. Gastrointestinal and liver physiology

2018 Volume 315, Issue 1, Page(s) G20–G26

Abstract: The last few decades have seen a major increase in the number of neurotransmitters and neuropeptides recognized as playing a role in brain stem neurocircuits, including those involved in homeostatic functions such as stress responsiveness, ... ...

Abstract	The last few decades have seen a major increase in the number of neurotransmitters and neuropeptides recognized as playing a role in brain stem neurocircuits, including those involved in homeostatic functions such as stress responsiveness, gastrointestinal motility, feeding, and/or arousal/wakefulness. This minireview will focus on the known physiological role of three of these novel neuropeptides, i.e., apelin, nesfatin-1, and neuropeptide-S, with a special emphasis on their hypothetical roles in vagal signaling related to gastrointestinal motor functions.
MeSH term(s)	Brain Stem/metabolism ; Calcium-Binding Proteins/metabolism ; DNA-Binding Proteins/metabolism ; Gastrointestinal Motility/physiology ; Humans ; Nerve Tissue Proteins/metabolism ; Neuropeptides/metabolism ; Vagus Nerve/physiology
Chemical Substances	Calcium-Binding Proteins ; DNA-Binding Proteins ; Nerve Tissue Proteins ; Neuropeptides ; neuropeptide S, human ; nucleobindin
Language	English
Publishing date	2018-03-29
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	603840-2
ISSN	1522-1547 ; 0193-1857
ISSN (online)	1522-1547
ISSN	0193-1857
DOI	10.1152/ajpgi.00059.2018
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