Bidirectional Anticipation of Future Osmotic Challenges by Vasopressin Neurons

• Published in: Neuron (Cambridge, Mass.) Mass.), 2017-01, Vol.93 (1), p.57-65
• Main Authors: Mandelblat-Cerf, Yael, Kim, Angela, Burgess, Christian R., Subramanian, Siva, Tannous, Bakhos A., Lowell, Bradford B., Andermann, Mark L.
• Format: Article
• Language: English
• Subjects: Animals; Arginine Vasopressin - metabolism; Cues; Drinking Behavior - physiology; Electrophysiology; Experiments; Feeding Behavior - physiology; Fiber Photometry; Food and water cues; Food restriction; Homeostasis; Mice; Neuroendocrine neuron; Neurons; Neurons - metabolism; Neurons - physiology; Osmolar Concentration; Osmotic Pressure; Plasma osmolality; Posterior pituitary; Preingestive; Presystemic; Supraoptic nucleus; Supraoptic Nucleus - cytology; Vasopressin; Vasopressins - metabolism
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2016.11.021

Ingestion of water and food are major hypo- and hyperosmotic challenges. To protect the body from osmotic stress, posterior pituitary-projecting, vasopressin-secreting neurons (VPpp neurons) counter osmotic perturbations by altering their release of vasopressin, which controls renal water excretion. Vasopressin levels begin to fall within minutes of water consumption, even prior to changes in blood osmolality. To ascertain the precise temporal dynamics by which water or food ingestion affect VPpp neuron activity, we directly recorded the spiking and calcium activity of genetically defined VPpp neurons. In states of elevated osmolality, water availability rapidly decreased VPpp neuron activity within seconds, beginning prior to water ingestion, upon presentation of water-predicting cues. In contrast, food availability following food restriction rapidly increased VPpp neuron activity within seconds, but only following feeding onset. These rapid and distinct changes in activity during drinking and feeding suggest diverse neural mechanisms underlying anticipatory regulation of VPpp neurons. •Recordings from vasopressin neuroendocrine motor neurons (VPpp) in behaving mice•Feeding, but not cues predicting food, increase VPpp neuron activity within seconds•Drinking and cues predicting water reduce VPpp neuron activity within seconds•Drinking-related reductions in activity reach steady state prior to systemic feedback Using electrophysiological and optical methods, Mandelblat-Cerf and colleagues demonstrate that ingestion of water or food leads to rapid, presystemic decreases or increases in activity of vasopressin neurons, respectively. Surprisingly, learned sensory cues predicting water, but not food, also modulated activity.