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Brain glucose and insulin: effects on food intake and brain biogenic amines of rainbow trout

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Abstract

The effects of central (intracerebroventricular, 9 μg fish−1) and peripheral (intraperitoneal, 4 mg kg−1) administration of bovine insulin, as well as the effect of hyperglycemia (oral administration of 1 g glucose fish−1) and brain glucodeprivation (intracerebroventricular administration of 2-deoxy-D-glucose) on food intake and levels of brain (telencephalon, preoptic area, and hypothalamus) biogenic amines (serotonin, dopamine, noradrenaline and their metabolites 5-hydroxyindoleacetic acid, and dihydroxyphenylacetic acid) were assessed on rainbow trout (Oncorhynchus mykiss). Treatment with insulin inhibited food intake after 26 or 52 h of administration, central or peripheral, respectively. This effect was still apparent after 74 h of central treatment. When assessing changes in the levels of biogenic amines after 26 h of central insulin administration, there was a significant increase in the levels of 5-hydroxyindoleacetic acid, and in the ratio of dihydroxyphenylacetic acid/dopamine of insulin-treated fish, in telencephalon and hypothalamus, respectively. These results suggest that peripherally administered insulin is involved in a feedback regulatory loop with food intake and body weight. Moreover, at least part of the effects of insulin could be mediated by hypothalamic dopaminergic activity. The strong hyperglycemia induced by oral administration of glucose did not induce significant changes either on food intake (control versus treated), or in brain levels of biogenic amines. The intracerebroventricular administration of 2-deoxy-D-glucose induced an increase in food intake without altering plasma glucose levels, suggesting that fish brain possesses a control system for detecting hypoglycemia in plasma and therefore keep brain glucose levels high enough for brain function.

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Abbreviations

2-DG:

2 Deoxy-D-glucose

5-HIAA:

5-Hydroxyindoleacetic acid

5-HT:

5-Hydroxytryptamine or serotonin

DA:

Dopamine

DOPAC:

Dihydroxyphenylacetic acid

EDTA:

Ethylenediaminetetraacetic acid

FI:

Food intake

HPLC:

High pressure liquid chromatography

icv:

Intracerebroventricular

i.p.:

Intraperitoneal

MS 222:

3-Aminobenzoic acid ethyl esther methanesulfonate salt

NA:

Noradrenaline

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Acknowledgements

This study was supported by Xunta de Galicia research Grant (PGIDT99PXI20001B and PGIDIT03PXIB20001PR) to M.A. The experiments described comply with the principles of animal care from the Spanish government and the European Union (L358/1, 18/12/1986).

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Correspondence to M. Aldegunde.

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Soengas, J.L., Aldegunde, M. Brain glucose and insulin: effects on food intake and brain biogenic amines of rainbow trout. J Comp Physiol A 190, 641–649 (2004). https://doi.org/10.1007/s00359-004-0524-5

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  • DOI: https://doi.org/10.1007/s00359-004-0524-5

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