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Review, Cognition and Behavior

The Role of the Gustatory System in the Coordination of Feeding

Vladimiros Thoma, Kimiko Kobayashi and Hiromu Tanimoto
eNeuro 10 November 2017, 4 (6) ENEURO.0324-17.2017; https://doi.org/10.1523/ENEURO.0324-17.2017
Vladimiros Thoma
1Department of Biology, Miyagi University of Education, Sendai, Miyagi 980-0845, Japan
2Graduate School of Life Sciences, Tohoku University, Sendai, Miyagi 980-8577, Japan
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Kimiko Kobayashi
2Graduate School of Life Sciences, Tohoku University, Sendai, Miyagi 980-8577, Japan
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Hiromu Tanimoto
2Graduate School of Life Sciences, Tohoku University, Sendai, Miyagi 980-8577, Japan
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    Figure 1.

    The feeding sequence of Drosophila. A, Initially, a hungry fly will search for food. This appetitive exploration relies on visual and chemical cues. As soon as the fly steps on food, it suppresses its movement (B), lowers its posture (C), and extends its proboscis (D). The extension of the proboscis comprises of four steps that use different muscles (i-iii). A schematic of the surface of the proboscis, showing the spreading of the labella from below, is shown in the last step (inset). Consequently, (E) the fly ingests food until satiated and then (F) retracts its proboscis and (G) moves away.

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    Figure 2.

    Neuronal circuits coordinating feeding in Drosophila. A, Schematic of an adult fruit fly, indicating the central nervous system, comprising of the brain and thoracic ganglia (white). The position of the gustatory organs (wings, tarsi, labella, and pharyngeal organs) are highlighted. B, GRNs in the wings (green) are critical for long-range foraging. C, Circuits controlling the PER on leg stimulation. Out of two groups of leg GRNs, brain-projecting GRNs (magenta) are more critical for PER, likely through more direct interactions with a brain command neuron. Locally-projecting GRNs (green) exert a smaller role, likely through SGNs (black). D, Circuits controlling PER on labelar stimulation. Labelar GRNs (green) connect to SGNs in the brain (black) that integrate taste and hunger. E, Circuits controlling food ingestion. Pharyngeal GRNs regulate feeding by prolonging (magenta cell) or decreasing (green cells) ingestion time. The sucking command neuron (black) directly receives information from pharyngeal GRNs, integrates it with hunger and likely activates the central pattern generator that controls pumping. F, Circuits controlling locomotion suppression when feeding. Locally-projecting leg GRNs (green) suppress movement on food encounter. Proboscis extension also suppresses locomotion, although the underlying circuits are unknown. Question marks (?) indicate speculative or unknown pathways. For simplicity, only one or a few GRNs or SGNs per category are shown.

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    Figure 3.

    The role of gustatory information in the feeding coordination of catfish and sea anemones. A, Catfish have external and internal taste buds. The former control prey-capture behaviors, while the latter control ingestive behaviors such as chewing and swallowing. B, The sea anemone Anthopleura captures food (gray circle) with its tentacles, brings it to its mouth, and swallows it. Asparagine and glutathione, likely released from sting-injured prey, control tentacle movements and swallowing, respectively.

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    Figure 4.

    Neuronal circuits underlying suppression of escape responses during feeding in leeches and crayfish. A, In leeches, stimulation of taste sensory neurons in the lip inhibits nociceptive neurons through serotonergic interneurons. B, In crayfish, taste and postingestive information suppresses the escape command neurons.

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eneuro: 4 (6)
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Vol. 4, Issue 6
November/December 2017
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The Role of the Gustatory System in the Coordination of Feeding
Vladimiros Thoma, Kimiko Kobayashi, Hiromu Tanimoto
eNeuro 10 November 2017, 4 (6) ENEURO.0324-17.2017; DOI: 10.1523/ENEURO.0324-17.2017

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The Role of the Gustatory System in the Coordination of Feeding
Vladimiros Thoma, Kimiko Kobayashi, Hiromu Tanimoto
eNeuro 10 November 2017, 4 (6) ENEURO.0324-17.2017; DOI: 10.1523/ENEURO.0324-17.2017
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  • Article
    • Visual Abstract
    • Abstract
    • Significance Statement
    • Introduction
    • Execution of Behavioral Sequences during Feeding
    • Feeding Sequences of Other Animals
    • Suppression of Competing Behaviors during Feeding
    • Conclusions
    • Acknowledgments
    • Footnotes
    • References
    • Synthesis
    • Author Response
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Keywords

  • coordination
  • evolution
  • feeding behavior
  • Gustatory Sensory Neuron
  • neuroethology
  • taste

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