The belly rules the nose: feeding state-dependent modulation of peripheral chemosensory responses

doi:10.1016/j.conb.2012.08.001

Current Opinion in Neurobiology

Volume 23, Issue 1, February 2013, Pages 68-75

https://doi.org/10.1016/j.conb.2012.08.001 Get rights and content

Feeding history and the presence of food dramatically alter chemosensory behaviors. Recent results indicate that internal nutritional state can gate peripheral gustatory and olfactory sensory responses to affect behavior. Focusing primarily on recent work in C. elegans and Drosophila, I describe the neuromodulatory mechanisms that translate feeding state information into changes in chemosensory neuron response properties and behavioral output.

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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Insects are equipped with neurological, physiological, and behavioral tools to locate potential food sources and assess their nutritional quality based on volatile and chemotactile cues. We summarize current knowledge on insect taste perception and the different modalities of reception and perception. We suggest that the neurophysiological mechanisms of reception and perception are closely linked to the species-specific ecology of different insects. Understanding these links consequently requires a multidisciplinary approach. We also highlight existing knowledge gaps, especially in terms of the exact ligands of receptors, and provide evidence for a perceptional hierarchy suggesting that insects have adapted their reception and perception to preferentially perceive nutrient stimuli that are important for their fitness.
Dehydrated Drosophila melanogaster track a water plume in tethered flight
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Perception of sensory stimuli can be modulated by changes in internal state to drive contextually appropriate behavior. For example, dehydration is a threat to terrestrial animals, especially to Drosophila melanogaster due to their large surface area to volume ratio, particularly under the energy demands of flight. While hydrated D. melanogaster avoid water cues, while walking, dehydration leads to water-seeking behavior. We show that in tethered flight, hydrated flies ignore a water stimulus, whereas dehydrated flies track a water plume. Antennal occlusions eliminate odor and water plume tracking, whereas inactivation of moist sensing neurons in the antennae disrupts water tracking only upon starvation and dehydration. Elimination of the olfactory coreceptor eradicates odor tracking while leaving water-seeking behavior intact in dehydrated flies. Our results suggest that while similar hygrosensory receptors may be used for walking and in-flight hygrotaxis, the temporal dynamics of modulating the perception of water vary with behavioral state.
The emergence and influence of internal states
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Citation Excerpt :
However, changes in gene expression have been notably detected across feeding states. For example, feeding state-dependent changes in neuromodulator (Entchev et al., 2015) and chemoreceptor (Sengupta, 2013) expression in C. elegans have been linked to satiety-related behavioral changes. Similarly, food deprivation alters the expression of hundreds of genes in AGRP neurons of the hypothalamus (Henry et al., 2015).
Animal behavior is shaped by a variety of “internal states”—partially hidden variables that profoundly shape perception, cognition, and action. The neural basis of internal states, such as fear, arousal, hunger, motivation, aggression, and many others, is a prominent focus of research efforts across animal phyla. Internal states can be inferred from changes in behavior, physiology, and neural dynamics and are characterized by properties such as pleiotropy, persistence, scalability, generalizability, and valence. To date, it remains unclear how internal states and their properties are generated by nervous systems. Here, we review recent progress, which has been driven by advances in behavioral quantification, cellular manipulations, and neural population recordings. We synthesize research implicating defined subsets of state-inducing cell types, widespread changes in neural activity, and neuromodulation in the formation and updating of internal states. In addition to highlighting the significance of these findings, our review advocates for new approaches to clarify the underpinnings of internal brain states across the animal kingdom.
C. elegans Males Integrate Food Signals and Biological Sex to Modulate State-Dependent Chemosensation and Behavioral Prioritization
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Citation Excerpt :
One mechanism by which internal state influences behavior is through modulation of sensory perception. For example, nutritional state can modulate sensory function to focus a hungry animal’s attention on food-associated stimuli while attenuating the perception of cues that inhibit feeding [1, 2]. Biological sex and reproductive status can also influence sensory function: biological sex modulates sensory responses of C. elegans to pheromones and food [3], and female reproductive state influences the detection and processing of pheromonal and olfactory signals in both Drosophila and mice [4, 5].
Dynamic integration of internal and external cues is essential for flexible, adaptive behavior. In C. elegans, biological sex and feeding state regulate expression of the food-associated chemoreceptor odr-10, contributing to plasticity in food detection and the decision between feeding and exploration. In adult hermaphrodites, odr-10 expression is high, but in well-fed adult males, odr-10 expression is low, promoting exploratory mate-searching behavior. Food-deprivation transiently activates male odr-10 expression, heightening food sensitivity and reducing food leaving. Here, we identify a neuroendocrine feedback loop that sex-specifically regulates odr-10 in response to food deprivation. In well-fed males, insulin-like (insulin/IGF-1 signaling [IIS]) and transforming growth factor β (TGF-β) signaling repress odr-10 expression. Upon food deprivation, odr-10 is directly activated by DAF-16/FoxO, the canonical C. elegans IIS effector. The TGF-β ligand DAF-7 likely acts upstream of IIS and links feeding to odr-10 only in males, due in part to the male-specific expression of daf-7 in ASJ. Surprisingly, these responses to food deprivation are not triggered by internal metabolic cues but rather by the loss of sensory signals associated with food. When males are starved in the presence of inedible food, they become nutritionally stressed, but odr-10 expression remains low and exploratory behavior is suppressed less than in starved control males. Food signals are detected by a small number of sensory neurons whose activity non-autonomously regulates daf-7 expression, IIS, and odr-10. Thus, adult C. elegans males employ a neuroendocrine feedback loop that integrates food detection and genetic sex to dynamically modulate chemoreceptor expression and influence the feeding-versus-exploration decision.
Neuropeptide signaling regulates pheromone-mediated gene expression of a chemoreceptor gene in c. Elegans
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Animals need to be able to alter their developmental and behavioral programs in response to changing environmental conditions. This developmental and behavioral plasticity is mainly mediated by changes in gene expression. The knowledge of the mechanisms by which environmental signals are transduced and integrated to modulate changes in sensory gene expression is limited. Exposure to ascaroside pheromone has been reported to alter the expression of a subset of putative G protein-coupled chemosensory receptor genes in the ASI chemosensory neurons of C. elegans (Kim et al., 2009; Nolan et al., 2002; Peckol et al., 1999). Here we show that ascaroside pheromone reversibly represses expression of the str-3 chemoreceptor gene in the ASI neurons. Repression of str-3 expression can be initiated only at the L1 stage, but expression is restored upon removal of ascarosides at any developmental stage. Pheromone receptors including SRBC-64/66 and SRG-36/37 are required for str-3 repression. Moreover, pheromone-mediated str-3 repression is mediated by FLP-18 neuropeptide signaling via the NPR-1 neuropeptide receptor. These results suggest that environmental signals regulate chemosensory gene expression together with internal neuropeptide signals which, in turn, modulate behavior.
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View full text

The belly rules the nose: feeding state-dependent modulation of peripheral chemosensory responses

Highlights

Introduction

Section snippets

Modulation of chemosensory responses by starvation or satiety

Acute modulation of chemosensory responses by food

Plasticity in chemosensory responses upon prior pairing of food and chemicals

Conclusions

References and recommended reading

Acknowledgements

Behav Brain Res

Physiol Behav

Prog Neurobiol

Front Neuroendocrinol

Peptides

Cell

Curr Biol

Curr Biol

Neuron

J Neurosci

Pharmacol Biochem Behav

Cell

Neuron

J Exp Biol

Cell

Nat Neurosci

Philos Trans R Soc Lond B

EMBO J

J Neurosci

Environmental signals modulate olfactory acuity, discrimination, and memory in Caenorhabditis elegans

Learn Mem

Regulation of feeding behavior in adult Drosophila melanogaster varies with feeding regime and nutritional state

J Exp Biol

Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex

J Neurophysiol

Candidate gustatory interneurons modulating feeding behavior in the Drosophila brain

PLoS Biol

Terminal nerve-derived neuropeptide Y modulates physiological responses in the olfactory epithelium of hungry axolotls (Ambystoma mexicanum)

J Neurosci

Expression of insulin system in the olfactory epithelium: first approaches to its role and regulation

J Neuroendocrinol

Modulation of spontaneous and odorant-evoked activity of rat olfactory sensory neurons by two anorectic peptides, insulin and leptin

J Neurophysiol

Gustatory signaling in the periphery: detection, transmission, and modulation of taste information

Biol Pharm Bull

Roles of hormones in taste signaling

Results Probl Cell Differ

Feeding signals and brain circuitry

Eur J Neurosci