Sensitivity of olfactory sensory neurons to food cues is tuned to nutritional states by Neuropeptide Y signaling

• Published in: Journal of neurochemistry 2021-12, Vol.159 (6), p.1028-1044
• Main Authors: Kaniganti, Tarun, Deogade, Ajinkya, Maduskar, Aditi, Mukherjee, Arghya, Guru, Akash, Subhedar, Nishikant, Ghose, Aurnab
• Format: Article
• Language: English
• Subjects: Amino acids; Animals; Animals, Genetically Modified; Channel gating; Chemoreception; Cues; Danio rerio; Eating - physiology; Feeding behavior; Female; Food; Humans; Hunger; Information processing; Male; Modulation; Neuroethology; Neuromodulation; Neurons; Neuropeptide Y; Neuropeptide Y - analysis; Neuropeptide Y - biosynthesis; Neuropeptides; nutritional state; Nutritional Status - physiology; Odorants; Olfaction; Olfactory epithelium; Olfactory Mucosa - chemistry; Olfactory Mucosa - metabolism; Olfactory perception; Olfactory receptor neurons; Olfactory Receptor Neurons - chemistry; Olfactory Receptor Neurons - metabolism; olfactory sensitivity; olfactory sensory neurons; Olfactory system; Olfactory thresholds; Phospholipase C; Physiology; Satiety; Sensitivity; Sensory neurons; Sensory perception; Signaling; Smell; Terminal nerve; Zebrafish
• ISSN: 0022-3042; 1471-4159
• DOI: 10.1111/jnc.15488

Modulation of sensory perception by homeostatic feedback from physiological states is central to innate purposive behaviors. Olfaction is an important predictive modality for feeding‐related behaviors and its modulation has been associated with hunger‐satiety states. However, the mechanisms mapping internal states to chemosensory processing in order to modify behavior are poorly understood. In the zebrafish olfactory epithelium, a subset of olfactory sensory neurons (OSNs) and the terminal nerve projections express neuropeptide Y (NPY). Using a combination of neuronal activity and behavioral evaluation, we find that NPY signaling in the peripheral olfactory system of zebrafish is correlated with its nutritional state and is both necessary and sufficient for the olfactory perception of food‐related odorants. NPY activity dynamically modulates the microvillar OSN activation thresholds and acts cooperatively with amino acid signaling resulting in a switch‐like increase in OSN sensitivity in starved animals. We suggest that cooperative activation of phospholipase C by convergent signaling from NPY and amino acid receptors is central to this heightened sensitivity. This study provides ethologically relevant, physiological evidence for NPY signaling in the modulation of OSN sensitivity to food‐associated amino acid cues. We demonstrate sensory gating directly at the level of OSNs and identify a novel mechanistic framework for tuning olfactory sensitivity to prevailing energy states. Cover Image for this issue: https://doi.org/10.1111/jnc.15091 Neuropeptide Y, an orexigenic neuropeptide, is expressed in the OSNs and the TN neurons of the OB of zebrafish. Under conditions of starvation, the levels of this peptide increase in the OE, OB and TN. We show that this increase in NPY signalling leads to an increase in the sensitivity of OSNs to food‐associated odorants. Relative to fed animals, exposure of starved animals to food‐related odorants leads to greater OSN activation, which is manifested as an increased attraction to the food cues. (OE: olfactory epithelium; OB: Olfactory bulb; TN; Terminal Nerve; OSN: Olfactory sensory neurons). Cover Image for this issue: https://doi.org/10.1111/jnc.15091