Neurons for hunger and thirst transmit a negative-valence teaching signal

Nature

Volumn 521, Issue 7551, 2015, Pages 180-185

  Betley, J Nicholas ^a   Xu, Shengjin ^a   Cao, Zhen Fang Huang ^a   Gong, Rong ^a   Magnus, Christopher J ^a   Yu, Yang ^a   Sternson, Scott M ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BEHAVIORAL RESPONSE; CELL ORGANELLE; ENVIRONMENTAL CUE; HOMEOSTASIS; NEUROLOGY; PHYSIOLOGY; RODENT; SIGNAL;

ARTICLE; BEHAVIOR; BRAIN DEPTH STIMULATION; CELLS BY BODY ANATOMY; CONDITIONED TASTE AVERSION TEST; FLAVOR; FLUID INTAKE; FOOD INTAKE; HOMEOSTASIS; HORMONAL REGULATION; HUMAN; HUNGER; NERVE CELL; NERVE CONDUCTION; NONHUMAN; PHOTOACTIVATION; PHOTOSTIMULATION; PLACE PREFERENCE; PRIORITY JOURNAL; STARVATION; THIRST; ANIMAL; ANIMAL MODEL; ASSOCIATION; DEHYDRATION; DRINKING; EATING; FOOD; FOOD PREFERENCE; HYPOTHALAMUS; MALE; METABOLISM; MOUSE; PHYSIOLOGY;

MUS;

AGOUTI RELATED PROTEIN;

AGOUTI-RELATED PROTEIN; ANIMALS; CUES; DEHYDRATION; DRINKING; EATING; FOOD; FOOD PREFERENCES; HOMEOSTASIS; HUNGER; HYPOTHALAMUS; MALE; MICE; MODELS, ANIMAL; NEURONS; STARVATION; THIRST;

EID: 84929359280     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14416     Document Type: Article

References (47)

1. van den Top, M., Lee, K., Whyment, A. D., Blanks, A. M. & Spanswick, D. Orexigen-sensitive NPY/AgRP pacemaker neurons in the hypothalamic arcuate nucleus. Nature Neurosci. 7, 493-494 (2004).
2. Krashes, M. J. et al. Rapid, reversible activation of AgRP neurons drives feeding behavior in mice. J. Clin. Invest. 121, 1424-1428 (2011).
3. Luquet, S., Perez, F. A., Hnasko, T. S. & Palmiter, R. D. NPY/AgRP neurons are essential for feeding in adult mice but can be ablated in neonates. Science 310, 683-685 (2005).
4. Aponte, Y., Atasoy, D. & Sternson, S. M. AGRP neurons are sufficient to orchestrate feeding behavior rapidly and without training. Nature Neurosci. 14, 351-355 (2011).
5. Atasoy, D., Betley, J. N., Su, H. H. & Sternson, S. M. Deconstruction of a neural circuit for hunger. Nature 488, 172-177 (2012).
6. Sternson, S. M. Hypothalamic survival circuits: blueprints for purposive behaviors. Neuron 77, 810-824 (2013).
7. Yiin, Y. M., Ackroff, K. & Sclafani, A. Flavor preferences conditioned by intragastric nutrient infusions in food restricted and free-feeding rats. Physiol. Behav. 84, 217-231 (2005).
8. Dickinson, A. & Balleine, B. in Stevens' Handbook of Experimental Psychology Vol. 3 (ed. R. Gallistel) Ch. 12 497-533 (John Wiley & Sons, 2002).
9. Rescorla, R. A. & Solomon, R. L. Two-process learning theory: relationships between Pavlovian conditioning and instrumental learning. Psychol. Rev. 74, 151-182 (1967).
10. Mackintosh, N. J. Conditioning and Associative Learning (Oxford Univ. Press, 1983).
11. Berridge, K. C. Motivation concepts in behavioral neuroscience. Physiol. Behav. 81, 179-209 (2004).
12. Cabanac, M. Physiological role of pleasure. Science 173, 1103-1107 (1971).
13. Robinson, M. J. & Berridge, K. C. Instant transformation of learned repulsion into motivational "wanting". Curr. Biol. 23, 282-289 (2013).
14. Hull, C. L. Principles of Behavior (D. Appleton-Century Co., 1943).
15. Navratilova, E. et al. Pain relief produces negative reinforcement through activation of mesolimbic reward-valuation circuitry. Proc. Natl Acad. Sci. USA 109, 20709-20713 (2012).
16. Sidman, M. Avoidance conditioningwith brief shock and no exteroceptive warning signal. Science 118, 157-158 (1953).
17. Margules, D. L. & Olds, J. Identical "feeding" and "rewarding" systemsin the lateral hypothalamus of rats. Science 135, 374-375 (1962).
18. Jennings, J. H., Rizzi, G., Stamatakis, A. M., Ung, R. L. & Stuber, G. D. The inhibitory circuit architecture of the lateral hypothalamus orchestrates feeding. Science 341, 1517-1521 (2013).
19. Stunkard, A. J. & Rush, J. Dieting and depression reexamined. A critical review of reports of untoward responses during weight reduction for obesity. Ann. Intern. Med. 81, 526-533 (1974).
20. Keys, A., Brozek, J., Henshel, A., Mickelsen, O. & Taylor, H. L. The Biology of Human Starvation Vol. II (Univ. of Minnesota Press, 1950).
21. Wadden, T. A., Stunkard, A. J. & Smoller, J. W. Dieting and depression: a methodological study. J. Consult. Clin. Psychol. 54, 869-871 (1986).
22. Takahashi, K. A. & Cone, R. D. Fasting induces a large, leptin-dependent increase in the intrinsic action potential frequency of orexigenic arcuate nucleus neuropeptide Y/Agouti-related protein neurons. Endocrinology 146, 1043-1047 (2005).
23. Betley, J. N., Cao, Z. F., Ritola, K. D. & Sternson, S. M. Parallel, redundant circuit organization for homeostatic control of feeding behavior. Cell 155, 1337-1350 (2013).
24. Magnus, C. J. et al. Chemical and genetic engineering of selective ion channel-ligand interactions. Science 333, 1292-1296 (2011).
25. Cravens, R. W. & Renner, K. E. Conditioned hunger. J. Exp. Psychol. 81, 312-316 (1969).
26. Ghosh, K. K. et al. Miniaturized integration of a fluorescence microscope. Nature Methods 8, 871-878 (2011).
27. Chen, T. W. et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295-300 (2013).
28. Johnson, R. F., Beltz, T. G., Thunhorst, R. L. & Johnson, A. K. Investigations on the physiological controls of water and saline intake in C57BL/6 mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285, R394-R403 (2003).
29. Oka, Y., Ye, M. & Zuker, C. S. Thirst driving and suppressing signals encoded by distinct neural populations in the brain. Nature 520, 394-352 (2015).
30. Chen, Y., Lin, Y. C., Kuo, T. W. & Knight, Z. A. Sensory detection of food rapidly modulates arcuate feeding circuits. Cell 160, 829-841 (2015).
31. Olds, J. in Brain Stimulation and Motivation: Research and Commentary (ed. E.S. Valenstein) 81-99 (Scott, Foresman and Company, 1973).
32. Jennings, J. H. et al. Visualizing hypothalamic network dynamics for appetitive and consummatory behaviors. Cell 160, 516-527 (2015).
33. Saper, C. B., Chou, T. C. & Elmquist, J. K. The needto feed: homeostatic andhedonic control of eating. Neuron 36, 199-211 (2002).
34. Domingos, A. I. et al. Leptin regulates the reward value of nutrient. Nature Neurosci. 14, 1562-1568 (2011).
35. Egecioglu, E. et al. Ghrelin increases intake of rewarding food in rodents. Addict. Biol. 15, 304-311 (2010).
36. Wang, Q. et al. Arcuate AgRP neurons mediate orexigenic and glucoregulatory actions of ghrelin. Mol. Metabol. 3, 64-72 (2014).
37. Yang, Y., Atasoy, D., Su, H. H. & Sternson, S. M. Hunger states switch a flip-flop memory circuit via a synaptic AMPK-dependent positive feedback loop. Cell 146, 992-1003 (2011).
38. Krashes, M. J. et al. An excitatory paraventricular nucleus to AgRP neuron circuit that drives hunger. Nature 507, 238-242 (2014).
39. Rolls, B. J. et al. Thirst following water deprivation in humans. Am. J. Physiol. 239, R476-R482 (1980).
40. Atasoy, D., Aponte, Y., Su, H. H. & Sternson, S. M. A. FLEX switch targets channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J. Neurosci. 28, 7025-7030 (2008).
41. Tsai, H. C. et al. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324, 1080-1084 (2009).
42. Branson, K., Robie, A. A., Bender, J., Perona, P. & Dickinson, M. H. High-throughput ethomics in large groups of Drosophila. Nature Methods 6, 451-457 (2009).
43. Stamatakis, A. M. & Stuber, G. D. Activation of lateral habenula inputs to the ventral midbrain promotes behavioral avoidance. Nature Neurosci. 15, 1105-1107 (2012).
44. Hagan, M. M. et al. Long-term orexigenic effects of AgRP-(83-132) involve mechanisms other than melanocortin receptor blockade. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279, R47-R52 (2000).
45. Krashes, M. J., Shah, B. P., Koda, S. & Lowell, B. B. Rapid versus delayed stimulation of feeding by the endogenously released AgRP neuron mediators GABA, NPY, and AgRP. Cell Metab. 18, 588-595 (2013).
46. Avants, B. B., Epstein, C. L., Grossman, M. & Gee, J. C. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med. Image Anal. 12, 26-41 (2008).
47. Mukamel, E. A., Nimmerjahn, A. & Schnitzer, M. J. Automated analysis of cellular signals from large-scale calcium imaging data. Neuron 63, 747-760 (2009).