The belly rules the nose: feeding state-dependent modulation of peripheral chemosensory responses
Highlights
► Feeding state and food alter chemosensory behaviors. ► Chemosensory neuron response properties are altered by feeding/fasting. ► Feeding state information is transmitted via conserved neuromodulatory pathways.
Introduction
An animal's feeding state and food availability can profoundly affect its olfactory and gustatory responses. Thus, while hunger sensitizes our chemosensory abilities to maximize our ability to find food, even the most delectable confections may not tempt us when sated (well, maybe sometimes). Although learning, culture and psychological factors complicate feeding behaviors in humans, in general, feeding state and the presence of food alter dietary choice, food searching and appetitive behaviors across species, driven partly by changes in chemosensory preferences (e.g. [1, 2, 3]). Thus, the modulation of chemosensory responses as a function of nutritional state is a common feature of nervous systems regardless of their complexity.
In principle, information regarding our feeding state can interface with sensory processing pathways at any level, from peripheral to central brain regions. Indeed, chemical stimulus-evoked activity is altered in an internal energy state-dependent manner in both higher order processing centers as well as at the first synapse between sensory and interneurons in different species (e.g. [4, 5, 6]). While food-dependent modulation of central neurons can coordinately alter responses to a suite of sensory stimuli, it is now becoming increasingly clear that food and feeding state gate responses in chemosensory cells themselves, thereby modulating specific chemosensory behaviors. Here, I review recent findings in C. elegans and Drosophila regarding modulation of peripheral chemosensory neuron properties by feeding/fasting state and food perception. I refer the reader to recent reviews and articles discussing similar mechanisms in the mammalian olfactory and gustatory systems (e.g. [1, 7, 8, 9, 10, 11]).
Section snippets
Modulation of chemosensory responses by starvation or satiety
Hungry and satiated animals exhibit markedly distinct responses to attractive or noxious chemicals. Metabolites, neuropeptides, monogenic amines and hormones including dopamine, insulin, serotonin and neuropeptide Y produced by the brain as well as peripheral tissues such as the gut act in a complex manner to inform the body of its nutritional status and energy requirements [12, 13]. Despite the significant differences in nervous system architecture between vertebrates and invertebrates, many
Acute modulation of chemosensory responses by food
In addition to being gated by prior feeding experience, sensory responses can also be acutely regulated by the presence or absence of food. In this context, I define acute regulation as alteration of sensory responses to a stimulus based upon simultaneous presentation of the stimulus and food. Information about food and a chemical stimulus can be integrated in parallel channels, and this information in turn can modulate behavior either by feedback regulation of sensory neuron activity, or
Plasticity in chemosensory responses upon prior pairing of food and chemicals
Pairing of food with odors increases the appetitive value of the odors, whereas conversely, pairing of an odor with starvation or another aversive stimulus decreases subsequent responses to the odor in both C. elegans and Drosophila [54, 55]. This behavioral plasticity has been shown to occur in higher integrative centers of the brain [54, 55]. However, at least in one recent report in C. elegans, this plasticity has clearly been shown to arise from changes in chemosensory neuron response
Conclusions
A clear theme running through the above discussion is the remarkable complexity of mechanisms by which internal nutritional state information is transmitted to the chemosensory system to change behavior. However, this is probably only the proverbial tip of the iceberg. What is the reason for this complexity? For one, nutritional state-dependent chemosensory gating is not a binary ON–OFF switch. Instead, responses are likely to be precisely calibrated according to not just whether the animal has
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
I am grateful to David Doroquez for providing the illustrations. I thank Cori Bargmann, Denise Ferkey, Leslie Griffith, Bill Schafer and Kristin Scott for discussion, and Cori Bargmann, Leslie Griffith and Kristin Scott for comments on the manuscript. This work is funded by the NSF (IOS 0842452) and the NIH (GM081639).
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