Agouti-related peptide neural circuits mediate adaptive behaviors in the starved state

Nature Neuroscience

Volumn 19, Issue 5, 2016, Pages 734-741

  Padilla, Stephanie L ^a   Qiu, Jian ^b   Soden, Marta E ^c   Sanz, Elisenda ^d   Nestor, Casey C ^b   Barker, Forrest D ^a   Quintana, Albert ^d   Zweifel, Larry S ^c   Rønnekleiv, Oline K ^b,e   Kelly, Martin J ^b,e   Palmiter, Richard D ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d INSTITUT DE NEUROCIÈNCIES   (Spain)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGOUTI RELATED PEPTIDE; NERVE PROTEIN; UNCLASSIFIED DRUG; AGOUTI RELATED PROTEIN; AGOUTI-RELATED PEPTIDE, (YC(CRFFNAFC)Y); PEPTIDE FRAGMENT;

ADAPTIVE BEHAVIOR; AGGRESSION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL NUCLEUS; MEDIAL AMYGDALA; MOUSE; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STARVATION; STRIA TERMINALIS; SYNAPSE; TERRITORIALITY; AMYGDALA; ANIMAL; FEAR; GENE TARGETING; HYPOTHALAMUS; MALE; METABOLISM; NERVE CELL; NERVE TRACT; PATHOPHYSIOLOGY; PHYSIOLOGY; SEPTUM NUCLEUS;

AGGRESSION; AGOUTI-RELATED PROTEIN; AMYGDALA; ANIMALS; FEAR; GENE KNOCK-IN TECHNIQUES; HYPOTHALAMUS; MALE; MICE; NEURAL PATHWAYS; NEURONS; PEPTIDE FRAGMENTS; SEPTAL NUCLEI; STARVATION;

EID: 84961727540     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4274     Document Type: Article

References (54)

1. Sih, A. Optimal behavior: can foragers balance two conflicting demands? Science 210, 1041-1043 (1980).
2. Krebs, J.R. Optimal foraging, predation risk and territory defense. Ardea 68, 83-90 (1980).
3. Brown, J.L. The evolution of diversity in avian territorial systems. Wilson Bull. 76, 160-169, http://www.jstor.org/stable/4159278 (1964).
4. Anderson, P.K. Foraging range in mice and voles-The role of risk. Can. J. Zool. 64, 2645-2653 (1986).
5. Magnhagen, C. Predation risk and foraging in juvenile pink (Oncorhynchus gorbuscha) and chum salmon (O. keta). Can. J. Fish. Aquat. Sci. 45, 592-596 (1988).
6. Kohler, S.L. & Mcpeek, M.A. Predation risk and the foraging behavior of competing stream insects. Ecology 70, 1811-1825 (1989).
7. Whitham, J. & Mathis, A. Effects of hunger and predation risk on foraging behavior of graybelly salamanders, Eurycea multiplicata. J. Chem. Ecol. 26, 1659-1665 (2000).
8. Hahn, T.M., Breininger, J.F., Baskin, D.G. & Schwartz, M.W. Coexpression of Agrp and NPY in fasting-Activated hypothalamic neurons. Nat. Neurosci. 1, 271-272 (1998).
9. 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).
10. 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).
11. Krashes, M.J. et al. Rapid, reversible activation of AgRP neurons drives feeding behavior in mice. J. Clin. Invest. 121, 1424-1428 (2011).
12. Aponte, Y., Atasoy, D. & Sternson, S.M. AGRP neurons are sufficient to orchestrate feeding behavior rapidly and without training. Nat. Neurosci. 14, 351-355 (2011).
13. Horvath, T.L., Bechmann, I., Naftolin, F., Kalra, S.P. & Leranth, C. Heterogeneity in the neuropeptide Y-containing neurons of the rat arcuate nucleus: GABAergic and non-GABAergic subpopulations. Brain Res. 756, 283-286 (1997).
14. Broberger, C., Johansen, J., Johansson, C., Schalling, M. & Hökfelt, T. The neuropeptide Y/agouti gene-related protein (AGRP) brain circuitry in normal, anorectic, and monosodium glutamate-Treated mice. Proc. Natl. Acad. Sci. USA 95, 15043-15048 (1998).
15. Cowley, M.A. et al. Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 411, 480-484 (2001).
16. Padilla, S.L., Carmody, J.S. & Zeltser, L.M. Pomc-expressing progenitors give rise to antagonistic neuronal populations in hypothalamic feeding circuits. Nat. Med. 16, 403-405 (2010).
17. 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).
18. Liu, H. et al. Transgenic mice expressing green fluorescent protein under the control of the melanocortin-4 receptor promoter. J. Neurosci. 23, 7143-7154 (2003).
19. Kishi, T. et al. Expression of melanocortin 4 receptor mRNA in the central nervous system of the rat. J. Comp. Neurol. 457, 213-235 (2003).
20. Stowers, L., Cameron, P. & Keller, J.A. Ominous odors: olfactory control of instinctive fear and aggression in mice. Curr. Opin. Neurobiol. 23, 339-345 (2013).
21. Pereno, G.L., Balaszczuk, V. & Beltramino, C.A. Detection of conspecific pheromones elicits fos expression in GABA and calcium-binding cells of the rat vomeronasal system-medial extended amygdala. J. Physiol. Biochem. 67, 71-85 (2011).
22. Lin, D. et al. Functional identification of an aggression locus in the mouse hypothalamus. Nature 470, 221-226 (2011).
23. Hong, W., Kim, D.W. & Anderson, D.J. Antagonistic control of social versus repetitive self-grooming behaviors by separable amygdala neuronal subsets. Cell 158, 1348-1361 (2014).
24. Armbruster, B.N., Li, X., Pausch, M.H., Herlitze, S. & Roth, B.L. Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc. Natl. Acad. Sci. USA 104, 5163-5168 (2007).
25. Dietrich, M.O., Zimmer, M.R., Bober, J. & Horvath, T.L. Hypothalamic Agrp neurons drive stereotypic behaviors beyond feeding. Cell 160, 1222-1232 (2015).
26. Laundré, J.W. Ecology. How large predators manage the cost of hunting. Science 346, 33-34 (2014).
27. Wang, L. & Anderson, D.J. Identification of an aggression-promoting pheromone and its receptor neurons in Drosophila. Nature 463, 227-231 (2010).
28. Boyden, E.S., Zhang, F., Bamberg, E., Nagel, G. & Deisseroth, K. Millisecond-Timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8, 1263-1268 (2005).
29. Atasoy, D., Betley, J.N., Su, H.H. & Sternson, S.M. Deconstruction of a neural circuit for hunger. Nature 488, 172-177 (2012).
30. Liu, J., Garza, J.C., Li, W. & Lu, X.Y. Melanocortin-4 receptor in the medial amygdala regulates emotional stress-induced anxiety-like behaviour, anorexia and corticosterone secretion. Int. J. Neuropsychopharmacol. 16, 105-120 (2013).
31. King, B.M., Cook, J.T., Rossiter, K.N. & Rollins, B.L. Obesity-inducing amygdala lesions: examination of anterograde degeneration and retrograde transport. Am. J. Physiol. Regul. Integr. Comp. Physiol. 284, R965-R982 (2003).
32. Xu, P. et al. Estrogen receptor-α in medial amygdala neurons regulates body weight. J. Clin. Invest. 125, 2861-2876 (2015).
33. Lin, S., Boey, D. & Herzog, H. NPY and Y receptors: lessons from transgenic and knockout models. Neuropeptides 38, 189-200 (2004).
34. Sanz, E. et al. Cell-Type-specific isolation of ribosome-Associated mRNA from complex tissues. Proc. Natl. Acad. Sci. USA 106, 13939-13944 (2009).
35. Heimer-McGinn, V., Murphy, A.C., Kim, J.C., Dymecki, S.M. & Young, P.W. Decreased dendritic spine density as a consequence of tetanus toxin light chain expression in single neurons in vivo. Neurosci. Lett. 555, 36-41 (2013).
36. Han, S., Soleiman, M.T., Soden, M.E., Zweifel, L.S. & Palmiter, R.D. Elucidating an affective pain circuit that creates a threat memory. Cell 162, 363-374 (2015).
37. Lo, L. & Anderson, D.J. A Cre-dependent, anterograde transsynaptic viral tracer for mapping output pathways of genetically marked neurons. Neuron 72, 938-950 (2011).
38. Swanson, L.W. Cerebral hemisphere regulation of motivated behavior. Brain Res. 886, 113-164 (2000).
39. Canteras, N.S., Simerly, R.B. & Swanson, L.W. Organization of projections from the medial nucleus of the amygdala: A PHAL study in the rat. J. Comp. Neurol. 360, 213-245 (1995).
40. Niimi, K. et al. Heterogeneous electrophysiological and morphological properties of neurons in the mouse medial amygdala in vitro. Brain Res. 1480, 41-52 (2012).
41. Bian, X. Physiological and morphological characterization of GABAergic neurons in the medial amygdala. Brain Res. 1509, 8-19 (2013).
42. Keshavarzi, S., Sullivan, R.K., Ianno, D.J. & Sah, P. Functional properties and projections of neurons in the medial amygdala. J. Neurosci. 34, 8699-8715 (2014).
43. Cruikshank, S.J., Urabe, H., Nurmikko, A.V. & Connors, B.W. Pathway-specific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons. Neuron 65, 230-245 (2010).
44. Sun, Q.Q., Akk, G., Huguenard, J.R. & Prince, D.A. Differential regulation of GABA release and neuronal excitability mediated by neuropeptide Y1 and Y2 receptors in rat thalamic neurons. J. Physiol. (Lond.) 531, 81-94 (2001).
45. Sun, Q.Q., Huguenard, J.R. & Prince, D.A. Neuropeptide Y receptors differentially modulate G-protein-Activated inwardly rectifying K+ channels and high-voltage-Activated Ca2+ channels in rat thalamic neurons. J. Physiol. (Lond.) 531, 67-79 (2001).
46. Bosch, M.A., Tonsfeldt, K.J. & Ronnekleiv, O.K. mRNA expression of ion channels in GnRH neurons: subtype-specific regulation by 17β-estradiol. Mol. Cell. Endocrinol. 367, 85-97 (2013).
47. Behbehani, M.M. Functional characteristics of the midbrain periaqueductal gray. Prog. Neurobiol. 46, 575-605 (1995).
48. Kennedy, A. et al. Internal states and behavioral decision-making: Toward an integration of emotion and cognition. Cold Spring Harb. Symp. Quant. Biol. 79, 199-210 (2014).
49. 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).
50. Betley, J.N. et al. Neurons for hunger and thirst transmit a negative-valence teaching signal. Nature 521, 180-185 (2015).
51. Sanz, E. et al. Fertility-regulating Kiss1 neurons arise from hypothalamic POMC-expressing progenitors. J. Neurosci. 35, 5549-5556 (2015).
52. Gore, B.B., Soden, M.E. & Zweifel, L.S. Manipulating gene expression in projection-specific neuronal populations using combinatorial viral approaches. Curr. Protoc. Neurosci. 65, 4.35 (2013).
53. Qiu, J. et al. Rapid signaling of estrogen in hypothalamic neurons involves a novel G-protein-coupled estrogen receptor that activates protein kinase C. J. Neurosci. 23, 9529-9540 (2003).
54. Sparta, D.R. et al. Construction of implantable optical fibers for long-Term optogenetic manipulation of neural circuits. Nat. Protoc. 7, 12-23 (2012).