Vagal gustatory reflex circuits for intraoral food sorting behavior in the goldfish: Cellular organization and neurotransmitters

Authors

  • Takanori Ikenaga,

    1. Rocky Mountain Taste & Smell Center, Department of Cell and Developmental Biology, University of Colorado Denver School of Medicine, Aurora, Colorado 80045
    Current affiliation:
    1. Laboratory of Biological Information I, Graduate School of Life Science, University of Hyogo, Ako-gun, Hyogo 678-1297, Japan
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  • Tatsuya Ogura,

    1. Rocky Mountain Taste & Smell Center, Department of Cell and Developmental Biology, University of Colorado Denver School of Medicine, Aurora, Colorado 80045
    2. Department of Biological Sciences, University of Maryland Baltimore County, Baltimore, Maryland 21250
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  • Thomas E. Finger

    Corresponding author
    1. Rocky Mountain Taste & Smell Center, Department of Cell and Developmental Biology, University of Colorado Denver School of Medicine, Aurora, Colorado 80045
    • Department of Cell and Developmental Biology, University of Colorado at Denver and Health Sciences Center, Mailstop 8108, P.O. Box 6511, Aurora, CO 80045
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Abstract

The sense of taste is crucial in an animal's determination as to what is edible and what is not. This gustatory function is especially important in goldfish, who utilize a sophisticated oropharyngeal sorting mechanism to separate food from substrate material. The computational aspects of this detection are carried out by the medullary vagal lobe, which is a large, laminated structure combining elements of both the gustatory nucleus of the solitary tract and the nucleus ambiguus. The sensory layers of the vagal lobe are coupled to the motor layers via a simple reflex arc. Details of this reflex circuit were investigated with histology and calcium imaging. Biocytin injections into the motor layer labeled vagal reflex interneurons that have radially directed dendrites ramifying within the layers of primary afferent terminals. Axons of reflex interneurons extend radially inward to terminate onto both vagal motoneurons and small, GABAergic interneurons in the motor layer. Functional imaging shows increases in intracellular Ca++ of vagal motoneurons following electrical stimulation in the sensory layer. These responses were suppressed under Ca++-free conditions and by interruption of the axons bridging between the sensory and motor layers. Pharmacological experiments showed that glutamate acting via (±)-α-amino-3-hydroxy- 5-ethylisoxazole-4-propioinc acid (AMPA)/kainate and N-methyl-D-aspartic acid (NMDA) receptors mediate neurotransmission between reflex interneurons and vagal motoneurons. Thus, the vagal gustatory portion of the viscerosensory complex is linked to branchiomotor neurons of the pharynx via a glutamatergic interneuronal system. J. Comp. Neurol. 516:213–225, 2009. © 2009 Wiley-Liss, Inc.

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