Fos-containing neurons in medulla and pons after unilateral stimulation of the afferent abdominal vagus in conscious rabbits

doi:10.1016/0306-4522(94)90289-5

Neuroscience

Volume 59, Issue 4, April 1994, Pages 851-858

https://doi.org/10.1016/0306-4522(94)90289-5 Get rights and content

Abstract

Vagal afferents originating in abdominal viscera initiate numerous centrally-mediated responses, including behavioural, cardiovascular and hormonal changes associated with satiety, and nausea and vomiting. The present work was undertaken to map the pontomedullary distribution of neurons expressing Fos immunoreactivity following unilateral electrical stimulation of abdominal vagal afferents in conscious unanaesthetized rabbits. After 2 h of stimulation of the anterior trunk of the abdominal vagus nerve (20 Hz, 0.5mA, 0.5 ms duration, 4.5 min on, 0.5 min off), Fos-positive neurons were found in the area postrema, the nucleus tractus solitarius, the spinal nucleus of the trigeminal nerve, the caudal and the rostral ventrolateral medulla, the locus coeruleus, the subcoeruleus and the lateral parabrachial nucleus. In all these regions, more than 70% of Fos-containing neurons occurred on the ipsilateral side. In control animals only occasional Fos-immunoreactive neurons were observed, usually very faintly labelled. Simultaneous staining for both Fos and tyrosine hydroxylase revealed Fos immunoreactivity in catecholamine neurons, including A1, A2, C1, A5, subcoeruleus and locus coeruleus (A6) groups.

Our findings complement functional studies in the rabbit, identifying A1 neurons as part of the central pathway by which afferent abdominal vagal stimulation increases plasma vasopressin, and C1 neurons as part of the central pathway, whereby afferent abdominal vagal stimulation increases arterial pressure.

References (39)

BlessingW.W. et al.
Hypothalamic projections of medullary catecholamine neurons in the rabbit: a combined catecholamine fluorescence and HRP transport study
Brain Res. Bull.
(1982)
CraggB.G. et al.
Some reflexes mediated by the afferent fibers of the abdominal vagus in the rabbit and cat
Expl Neurol.
(1960)
GierobaZ.J. et al.
Abdominal vagal afferents excite A1 area neurons antidromically activated from the region of the supraoptic nucleus in the rabbit
Brain Res.
(1993)
GoodchildA.K. et al.
Evidence that adrenaline neurons in the rostral ventrolateral medulla have a vasopressor function
Neurosci. Lett.
(1984)
HawthornJ. et al.
Differential release of vasopressin and oxytocin in response to abdominal vagal afferent stimulation or apomorphine in the ferret
Brain Res.
(1988)
LiY.-W. et al.
Expression of c-fos protein in the medulla of conscious rabbits in response to baroreceptor activation
Neurosci. Lett.
(1992)
MooreS.D. et al.
Effects of blood pressure on A2 noradrenergic neurons
Brain Res.
(1985)
RicardoJ.A. et al.
Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain structures in the rat
Brain Res.
(1978)
RoweJ.W. et al.
Influence of the emetic reflex on vasopressin release in man
Kidney Int.
(1979)
SawchenkoP.E. et al.
The organization of noradrenergic pathways from the brainstem to the paraventricular and supraoptic nuclei in the rat
Brain Res. Rev.
(1982)

SumalK.K. et al.

Synaptic interaction of vagal afferents and catecholaminergic neurons in the rat nucleus tractus solitarius

Brain Res.

(1983)

AltschulerS.M. et al.

Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts

J. comp. Neurol.

(1989)

AndrewsP.L.R. et al.

Vagally mediated gastric motor and emetic reflexes evoked by stimulation of the antral mucosa in anaesthetized ferrets

J. Physiol., Lond.

(1988)

BlessingW.W. et al.

Inhibiting the rabbit caudal ventrolateral medulla prevents baroreceptorinitiated secretion of vasopressin

J. Physiol., Lond.

(1985)

CunninghamE.T. et al.

Anatomical specificity of noradrenergic inputs to the paraventricular and supraoptic nuclei of the rat hypothalamus

J. comp. Neurol.

(1988)

DampneyR.A.L.

Functional organization of central pathways regulating the cardiovascular system

Physiol. Rev.

(1994)

DingZ.-Q. et al.

Transneuronal labelling of neurons in rabbit brain after injection of Herpes simplex virus type 1 into the renal nerve

J. auton. nervous. Syst.

(1993)

GierobaZ.J. et al.

Vasopressin secretion after stimulation of the abdominal vagus in rabbit: role of A1 noradrenaline neurons

Am. J. Physiol.

(1994)

GierobaZ.J. et al.

Medullary pathways for adrenocorticotropic hormone and vasopressin secretion in rabbits

Am. J. Physiol.

(1992)

Cited by (65)

Bidirectional gut-brain communication: A role for orexin-A
2020, Neurochemistry International
It is increasingly evident that bidirectional gut-brain signaling provides a communication pathway that uses neural, hormonal, and immunological routes to regulate homeostatic mechanisms such as hunger/satiety as well as emotions and inflammation. Hence, disruption of the gut-brain axis can cause numerous pathophysiologies, including obesity and intestinal inflammatory diseases. One chemical mediator in the gut-brain axis is orexin-A, given that hypothalamic orexin-A affects gastrointestinal motility and secretion, and peripheral orexin in the intestinal mucosa can modulate brain functions, making possible an orexinergic gut-brain network. It has been proposed that orexin-A acts on this axis to regulate nutritional processes, such as short-term intake, gastric acid secretion, and motor activity associated with the cephalic phase of feeding. Orexin-A has also been related to stress systems and stress responses via the hypothalamic-pituitary-adrenal axis. Recent studies on the relationship of orexin with immune system-brain communications in an animal model of colitis suggested an immunomodulatory role for orexin-A in signaling and responding to infection by reducing the production of pro-inflammatory cytokines (e.g., tumor necrosis factor α, interleukin-6, and monocyte chemoattractant protein-1). These studies suggested that orexin administration might be of potential therapeutic value in irritable bowel syndrome or chronic intestinal inflammatory diseases, in which gastrointestinal symptoms frequently coexist with behavioral disorders, including loss of appetite, anxiety, depression, and sleeping disorders. Interventions in the orexinergic system have been proposed as a therapeutic approach to these diseases and for the treatment of chemotherapeutic drug-related hyperalgesia and fatigue in cancer patients.
Relevance of the nucleus of the solitary tract, gelatinous part, in learned preferences induced by intragastric nutrient administration
2017, Appetite
Food preferences have been investigated in Wistar rats utilizing a learned concurrent flavor preference behavioral procedure. Previous studies have demonstrated that the perivagal administration of neurotoxin capsaicin disrupts the learning of preferences induced by intragastric administration of rewarding nutrients (pre-digested milk). The vagus nerve projects almost exclusively towards the nucleus of the solitary tract (NST), a brain medullary gateway for visceral signals. The objective of this study was to investigate the participation of the lateral portion of the dorsomedial region, the gelatinous subnucleus (SolG), in the learning of a concurrent preference task. Results show that unlike neurologically intact animals, which learn this task correctly, animals lesioned in the gelatinous part of NST manifest a disruption of discrimination learning. Thus, intakes of the flavored stimulus paired with predigested liquid diet and of the flavored stimulus paired with physiological saline were virtually identical. However, SolG- and sham-lesioned groups consumed similar total amounts of both flavors. These findings suggest that SolG, as a relay of the vagus nerve, along with its anatomical projection, the external lateral parabrachial subnucleus (LPBe), may constitute an anatomical axis that is important in the induction of concurrent flavor/side preferences. It also appears to be relevant in other behavioral processes that require rapid processing of information from the upper gastrointestinal tract.
Disruption of re-intake after partial withdrawal of gastric food contents in rats lesioned in the gelatinous part of the nucleus of the solitary tract
2017, Appetite
Sensory information from the upper gastrointestinal tract is critical in food intake regulation. Signals from different levels of the digestive system are processed to the brain, among other systems, via the vagus nerve, which mainly projects towards the nucleus of the solitary tract (NST). The objective of this study was to analyze the participation of the gelatinous part (SolG) of the NST in short-term food intake. One-third of the stomach food content was withdrawn at 5 min after the end of a meal, and food was then available ad libitum for different time periods. SolG-lesioned and control animals ingested a similar amount of the initial liquid meal, but the former consumed significantly smaller amounts and failed to compensate for the food deficit, whereas the controls re-ingested virtually the same amount as extracted. These data suggest that the SolG, as in the case of related anatomical structures such as the vagus nerve or external lateral parabrachial subnucleus, may be relevant in particular circumstances that require the rapid processing of vagal-related food intake adjustment associated to the upper gastrointestinal tract.
Satiation and re-intake after partial withdrawal of gastric food contents: A dissociation effect in external lateral parabrachial lesioned rats
2016, Brain Research Bulletin
Citation Excerpt :
Both the neuronal activation and/or intake effects can also be abolished or attenuated by truncal vagotomy or by perivagal capsaicin treatment of the vagus nerve (Horn et al., 2001; Ladenheim and Ritter, 1991; Li and Rowland, 1995; Ritter et al., 1994; Smith et al., 1981; Yang et al., 2004). It has also been shown that LPB cell activity (including the external subnucleus), is sensitive to electrical stimulation of the vagus nerve (Gieroba and Blessing, 1994; Saleh and Cechetto, 1996) and NSTic (Suemori et al., 1994). Studies with c-fos techniques or single-unit recordings have also demonstrated activation of the LPB/LPBe after gastric distension (Baird et al., 2001), free feeding (Yamamoto et al., 1994), and infusion of nutrients into the stomach (Emond et al., 2001; Kobashi et al., 1993; Yamamoto and Sawa, 2000a, 2000b) or duodenum (Wang et al., 1992).
Sensory information from the gastrointestinal system can be transmitted to the brain through the vagus nerve, the intermediate-caudal region of the nucleus of the solitary tract (NST), and various subnuclei of the parabrachial complex, notably the external lateral subnucleus (LPBe). The objective of the present study was to examine the relevance of this subnucleus in satiation and food reintake after gastrointestinal food removal. LPBe-lesioned animals were subjected to a re-intake task following the partial withdrawal of gastric food contents shortly after satiation. Lesioned and control animals ingested a similar amount of the initial liquid meal. However, after withdrawal of one-third of the food consumed, LPBe-lesioned rats were not able to compensate for the deficit created, and their re-intake of food was significantly lower than the amount withdrawn after the satiating meal. In contrast, the food re-intake of control animals was similar to the amount withdrawn. Hence, the LPBe does not appear to be critical in the satiation process under the present experimental conditions. However, the LPBe may be part of a system that is essential in rapid visceral adjustments related to short-term food intake, as also shown in other gastrointestinal regulatory behaviors that require immediate processing of visceral sensory information.
The antidepressant mechanism of action of vagus nerve stimulation: Evidence from preclinical studies
2015, Neuroscience and Biobehavioral Reviews
Vagus nerve stimulation (VNS) is a proposed neuromodulatory treatment for medically refractory major depression. Although VNS is already used in clinical practice, the underlying mechanism of action remains unknown. The present review provides an overview of the preclinical VNS studies in view of two major hypotheses in depression research: the monoaminergic and the neural plasticity hypothesis of depression.
Nucleus of the solitary tract chemical stimulation induces extracellular norepinephrine release in the lateral and basolateral amygdala
2013, Brain Stimulation
Citation Excerpt :
Accordingly, the data presented here should be compared carefully with previous results obtained in awake freely moving animals, since the anesthetized preparation allows only to evaluate and dissect the more specific and reduced, stimulation effect of one structure like NTS, that is involved in complex interactions during awake animal behavior. Furthermore, the NE input in the amygdala could be explained not only by direct actions of the NTS projections to the BLA, but also by actions via polysynaptic pathway involving the LC [14,23–25], since NTS projections to the LC have been described [11,12]. However, the present results showed that NTS stimulation did not induce a significant NE increase in piriform cortex and other closer structures that also receive LC projections, suggesting that NTS stimulation produces the NE release in the amygdala mainly by direct NTS catecholamine connections to the amygdala.
The NTS catecholaminergic neurons, activated by a variety of afferent stimuli, are ideally situated to coordinate afferent signaling to multiple brain regions. In particular, there is evidence that systemic epinephrine injections induce a significant increase of norepinephrine (NE) in the amygdala during enhanced memory, which can be disrupted by NTS chemical blockade or interruption of vagal afferents. The present experiment was conducted to obtain information about the levels of NE release induced by activation of the whole NTS, which projects to the lateral and basolateral amygdala. Therefore, we compared NE levels before and after general stimulation of the NTS and the amygdala in anesthetized rats, without any behavioral or vagal stimulation, to find out the degree of noradrenergic activation modulated by the NTS through all its projections to the lateral and basolateral amygdala, as well as the degree of noradrenergic activation which may occur locally in the amygdala through rapid and general activation of this structure.

View all citing articles on Scopus

View full text

Fos-containing neurons in medulla and pons after unilateral stimulation of the afferent abdominal vagus in conscious rabbits

Abstract

Brain Res. Bull.

Expl Neurol.

Brain Res.

Neurosci. Lett.

Brain Res.

Neurosci. Lett.

Brain Res.

Brain Res.

Kidney Int.

Brain Res. Rev.

Brain Res.

Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts

J. comp. Neurol.

Vagally mediated gastric motor and emetic reflexes evoked by stimulation of the antral mucosa in anaesthetized ferrets

J. Physiol., Lond.

Inhibiting the rabbit caudal ventrolateral medulla prevents baroreceptorinitiated secretion of vasopressin

J. Physiol., Lond.

Anatomical specificity of noradrenergic inputs to the paraventricular and supraoptic nuclei of the rat hypothalamus

J. comp. Neurol.

Functional organization of central pathways regulating the cardiovascular system

Physiol. Rev.

Transneuronal labelling of neurons in rabbit brain after injection of Herpes simplex virus type 1 into the renal nerve

J. auton. nervous. Syst.

Vasopressin secretion after stimulation of the abdominal vagus in rabbit: role of A1 noradrenaline neurons

Am. J. Physiol.

Medullary pathways for adrenocorticotropic hormone and vasopressin secretion in rabbits

Am. J. Physiol.