Catecholamines inhibit neuronal activity in the glossopharyngeal–vagal motor complex of the Japanese eel: significance for controlling swallowing water

Ito, Sunao; Mukuda, Takao; Ando, Masahiro

doi:10.1002/jez.a.282

Cited by 11 publications

(10 citation statements)

References 19 publications

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“…Furthermore, it has been shown that the GVC neurons project directly to the striated muscles of the opercular membrane, pharynx, upper esophageal sphincter and esophageal body, all of which are implicated in swallowing (Mukuda and Ando, 2003b). It was also shown that the AP neurons project ventrally to the GVC (Ito et al, 2006). Although further experiments are required to identify precise neuronal networks that are involved in ANP-induced inhibition of drinking, it is possible that the AP acts as a center for integrating the information of dipsogenic and antidipsogenic hormones from the periphery and that it regulates the coordinated behaviour of swallowing through the vagus nerves in eels.…”

Section: Table·1 Brain Loci Stained By Trypan Blue and Npr-a Immunohmentioning

confidence: 99%

Area postrema, a brain circumventricular organ, is the site of antidipsogenic action of circulating atrial natriuretic peptide in eels

Tsukada

Nobata

Hyodo

et al. 2007

Journal of Experimental Biology

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SUMMARY Accumulating evidence indicates that circulating atrial natriuretic peptide(ANP) potently reduces excess drinking to ameliorate hypernatremia in seawater(SW) eels. However, the cerebral mechanism underlying the antidipsogenic effect is largely unknown. To localize the ANP target site in the brain, we examined the distribution of ANP receptors (NPR-A) in eel brain immunohistochemically using an antiserum specific for eel NPR-A. The immunoreactive NPR-A was localized in the capillaries of various brain regions. In addition, immunoreactive neurons were observed mostly in the medulla oblongata, including the reticular formation, glossopharyngeal-vagal motor complex, commissural nucleus of Cajal, and area postrema (AP). Trypan Blue, which binds serum albumin and does not cross the blood–brain barrier, was injected peripherally and stained the neurons in the AP but not other NPR-A immunopositive neurons. These histological data indicate that circulating ANP acts on the AP, which was further confirmed by physiological experiments. To this end, the AP in SW eels was topically destroyed by electric cauterization or were by chemical lesion of its neurons by kainic acid, and ANP (100 pmol kg–1) was then injected into the circulation. Both heat-coagulative and chemical lesions to the AP greatly reduced an antidipsogenic effect of ANP, but the ANP effect was retained in sham-operated eels and in those with lesions outside the AP. These results strongly suggest that the AP, a circumventricular organ without a blood–brain barrier, serves as a functional window of access for the circulating ANP to inhibit drinking in eels.

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Section: Table·1 Brain Loci Stained By Trypan Blue and Npr-a Immunohmentioning

confidence: 99%

Area postrema, a brain circumventricular organ, is the site of antidipsogenic action of circulating atrial natriuretic peptide in eels

Tsukada

Nobata

Hyodo

et al. 2007

Journal of Experimental Biology

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“…The commissural nucleus of Cajal (NCC), homologous to the nucleus tractus solitarius of mammals, is innervated by viscerosensory neurons in the catfish, goldfish, and mullet (4,7,22), just as the nucleus tractus solitarius is innervated by the sensory neurons from baroreceptors and visceral organs in mammals. In eels, the NCC neurons project to the glossopharyngeal-vagal motor complex neurons that project to the upper esophageal sphincter muscle to control drinking (17,30). Therefore, it is possible that the reflexgenic afferent input from peripheral baroreceptors activated the NCC neurons directly and inhibited drinking without mediation of the AP.…”

Section: Discussionmentioning

confidence: 99%

The area postrema in hindbrain is a central player for regulation of drinking behavior in Japanese eels

Nobata

Takei

2011

American Journal of Physiology-Regulatory, Integrative and Comp

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Nobata S, Takei Y. The area postrema in hindbrain is a central player for regulation of drinking behavior in Japanese eels. Am J Physiol Regul Integr Comp Physiol 300: R1569 -R1577, 2011. First published March 30, 2011 doi:10.1152/ajpregu.00056.2011It is recognized that fish will drink the surrounding water by reflex swallowing without a thirst sensation. We evaluated the role of the area postrema (AP), a sensory circumventricular organ (CVO) in the medulla oblongata, in the regulation of drinking behavior of seawater (SW) eels. The antidipsogenic effects of ghrelin and atrial natriuretic peptide and hypervolemia and hyperosmolemia (1 M sucrose or 10% NaCl) as well as the dipsogenic effects of angiotensin II and hypovolemia (hemorrhage) were profoundly diminished after AP lesion (APx) in eels compared with sham controls. However, the antidipsogenic effect of urotensin II was not influenced by APx, possibly due to the direct baroreflex inhibition on the swallowing center in eels. When ingested water was drained via an esophageal fistula, water intake increased 30-fold in sham controls but only fivefold in APx eels, suggesting a role for the AP in continuous regulation of drinking by SW eels. After transfer from freshwater to SW, APx eels responded normally with an immediate burst of drinking, but after 4 wk these animals showed a much greater increase in plasma osmolality than controls, suggesting that the AP is involved in acclimation to SW by fine tuning of the drinking rate. Taken together, the AP in the hindbrain of eels plays an integral role in SW acclimation, acting as a conduit of information from plasma for the regulation of drinking, probably without a thirst sensation. This differs from mammals in which sensory CVOs in the forebrain play pivotal roles in thirst regulation. dehydration; ghrelin; angiotensin; circumventricular organ; thirst IN VERTEBRATES, COMPOSITION and volume of the extracellular and intracellular fluids is regulated by behavioral and physiological mechanisms that have been obtained over the course of evolution. Osmoregulators maintain osmolality of the extracellular fluid near a set point value regardless of environmental conditions, which is achieved by balancing the gain and loss of water and ions (3). Among the vertebrate osmoregulators, it is the fishes whose extracellular fluid osmolality is most influenced by the environment, since, either in freshwater (FW) or seawater (SW), they are in direct contact with the environmental medium via respiratory epithelia. In regard to water regulation in FW fishes, excretion is more important than ingestion as FW fishes face constant osmotic gain of water. In contrast, fishes in SW have to drink water constantly to compensate for the osmotic loss of water across body surfaces (5,11,34). In fact, eels that are prevented from drinking die of severe cellular and extracellular dehydration 5 days after SW transfer (38). Previous findings indicate that regulation of drinking is crucial for survival of teleost fishes in SW and that euryhaline fish...

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“…This area is dominated by motoneurons that innervate the UES (Mukuda and Ando 2003a). These neurons typically fire spontaneously and show large amplitude spikes (>75 µV) (Ito et al 2006).…”

Section: Methodsmentioning

confidence: 99%

“…These motoneurons are cholinergic (Mukuda and Ando 2003a) and constrict the pharyngeal muscle and UES through acetylcholine (Kozaka and Ando 2003). Ito et al (2006) in the eel reported that motor neurons in GVC fire spontaneously at high frequency using the isolated brain specimens and the firing activity was inhibited by catecholamines.…”

Section: Introductionmentioning

confidence: 99%

Central regulation of the pharyngeal and upper esophageal reflexes during swallowing in the Japanese eel

Mukuda

Ando

2009

J Comp Physiol A

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We investigated the regulation of the pharyngeal and upper esophageal reflexes during swallowing in eel. By retrograde tracing from the muscles, the motoneurons of the upper esophageal sphincter (UES) were located caudally within the mid-region of the glossopharyngeal-vagal motor complex (mGVC). In contrast, the motoneurons innervating the pharyngeal wall were localized medially within mGVC. Sensory pharyngeal fibers in the vagal nerve terminated in the caudal region of the viscerosensory column (cVSC). Using the isolated brain, we recorded 51 spontaneously active neurons within mGVC. These neurons could be divided into rhythmically (n = 8) and continuously (n = 43) firing units. The rhythmically firing neurons seemed to be restricted medially, whereas the continuously firing neurons were found caudally within mGVC. The rhythmically firing neurons were activated by the stimulation of the cVSC. In contrast, the stimulation of the cVSC inhibited firing of most, but not all the continuously firing neurons. The inhibitory effect was blocked by prazosin in 17 out of 38 neurons. Yohimbine also blocked the cVSC-induced inhibition in five of prazosin-sensitive neurons. We suggest that the neurons in cVSC inhibit the continuously firing motoneurons to relax the UES and stimulate the rhythmically firing neurons to constrict the pharynx simultaneously.

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Catecholamines inhibit neuronal activity in the glossopharyngeal–vagal motor complex of the Japanese eel: significance for controlling swallowing water

Cited by 11 publications

References 19 publications

Area postrema, a brain circumventricular organ, is the site of antidipsogenic action of circulating atrial natriuretic peptide in eels

Area postrema, a brain circumventricular organ, is the site of antidipsogenic action of circulating atrial natriuretic peptide in eels

The area postrema in hindbrain is a central player for regulation of drinking behavior in Japanese eels

Central regulation of the pharyngeal and upper esophageal reflexes during swallowing in the Japanese eel

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