Appetitive changes during salt deprivation are paralleled by widespread neuronal adaptations in nucleus accumbens, lateral hypothalamus, and central amygdala

Journal of Neurophysiology

Volumn 108, Issue 4, 2012, Pages 1089-1105

  Tadon, Shashank ^a   Simon, Sidney A ^a   Nicolelis, Miguel A L ^a,b  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b Edmond and Lily Safra International Institute of Neuroscience   (Brazil)

Author keywords

Feeding; Hedonic value; Motivational value; Salt appetite; Water deprivation

Indexed keywords

SODIUM CHLORIDE; SUCROSE;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; APPETITE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN NERVE CELL; CENTRAL NUCLEUS (AMYGDALA); LATERAL HYPOTHALAMUS; MOTIVATION; NERVE CELL STIMULATION; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; RAT; SODIUM RESTRICTION; WATER DEPRIVATION;

ADAPTATION, PHYSIOLOGICAL; AMYGDALA; ANIMALS; APPETITIVE BEHAVIOR; HYPOTHALAMIC AREA, LATERAL; NEURONS; NUCLEUS ACCUMBENS; RATS; RATS, LONG-EVANS; SODIUM CHLORIDE, DIETARY;

EID: 84865101957     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00236.2012     Document Type: Article

References (82)

1. Azuma S, Yamamoto T, Kawamura Y. Studies on gustatory responses of amygdaloid neurons in rats. Exp Brain Res 56: 12-22, 1984.
2. Benavides DR, Quinn JJ, Zhong P, Hawasli AH, DiLeone RJ, Kansy JW, Olausson P, Yan Z, Taylor JR, Bibb JA. Cdk5 modulates cocaine reward, motivation, and striatal neuron excitability. J Neurosci 27: 12967-12976, 2007.
3. Bernard JF, Alden M, Besson JM. The organization of the efferent projections from the pontine parabrachial area to the amygdaloid complex: a Phaseolus vulgaris leucoagglutinin (PHA-L) study in the rat. J Comp Neurol 329: 201-229, 1993.
4. Berridge KC, Flynn FW, Schulkin J, Grill HJ. Sodium depletion enhances salt palatability in rats. Behav Neurosci 98: 652-660, 1984.
5. Carelli RM, Ijames SG, Crumling AJ. Evidence that separate neural circuits in the nucleus accumbens encode cocaine versus "natural" (water and food) reward. J Neurosci 20: 4255-4266, 2000.
6. Carlezon WA Jr, Thomas MJ. Biological substrates of reward and aversion: a nucleus accumbens activity hypothesis. Neuropharmacology 56, Suppl 1: 122-132, 2009.
7. Clark JJ, Bernstein IL. Reciprocal cross-sensitization between amphetamine and salt appetite. Pharmacol Biochem Behav 78: 691-698, 2004.
8. Clark JJ, Bernstein IL. Sensitization of salt appetite is associated with increased "wanting" but not "liking" of a salt reward in the sodium-deplete rat. Behav Neurosci 120: 206-210, 2006.
9. Contreras RJ. Changes in gustatory nerve discharges with sodium deficiency: a single unit analysis. Brain Res 121: 373-378, 1977.
10. Davis JD, Smith GP. Analysis of the microstructure of the rhythmic tongue movements of rats ingesting maltose and sucrose solutions. Behav Neurosci 106: 217-228, 1992.
11. De Luca LA Jr, Vendramini RC, Pereira DT, Colombari DA, David RB, de Paula PM, Menani JV. Water deprivation and the double-depletion hypothesis: common neural mechanisms underlie thirst and salt appetite. Braz J Med Biol Res 40: 707-712, 2007.
12. Dong Y, Green T, Saal D, Marie H, Neve R, Nestler EJ, Malenka RC. CREB modulates excitability of nucleus accumbens neurons. Nat Neurosci 9: 475-477, 2006.
13. Frazier CR, Mrejeru A. Predicted effects of a pause in D1 and D2 medium spiny neurons during feeding. J Neurosci 30: 9964-9966, 2010.
14. Galaverna O, De Luca LA Jr, Schulkin J, Yao SZ, Epstein AN. Deficits in NaCl ingestion after damage to the central nucleus of the amygdala in the rat. Brain Res Bull 28: 89-98, 1992.
15. Geerling JC, Loewy AD. Aldosterone-sensitive neurons in the nucleus of the solitary tract: bidirectional connections with the central nucleus of the amygdala. J Comp Neurol 497: 646-657, 2006a.
16. Geerling JC, Loewy AD. Aldosterone-sensitive neurons in the nucleus of the solitary: efferent projections. J Comp Neurol 498: 223-250, 2006b.
17. Geerling JC, Loewy AD. Central regulation of sodium appetite. Exp Physiol 93: 177-209, 2008.
18. Gerfen CR. Synaptic organization of the striatum. J Electron Microsc Tech 10: 265-281, 1988.
19. Grippo AJ, Moffitt JA, Beltz TG, Johnson AK. Reduced hedonic behavior and altered cardiovascular function induced by mild sodium depletion in rats. Behav Neurosci 120: 1133-1143, 2006.
20. Groenewegen HJ, Berendse HW, Haber SN. Organization of the output of the ventral striatopallidal system in the rat: ventral pallidal efferents. Neuroscience 57: 113-142, 1993.
21. Grossman SE, Fontanini A, Wieskopf JS, Katz DB. Learning-related plasticity of temporal coding in simultaneously recorded amygdala-cortical ensembles. J Neurosci 28: 2864-2873, 2008.
22. Gutierrez R, Carmena JM, Nicolelis MA, Simon SA. Orbitofrontal ensemble activity monitors licking and distinguishes among natural rewards. J Neurophysiol 95: 119-133, 2006.
23. Gutierrez R, Simon SA, Nicolelis MA. Licking-induced synchrony in the taste-reward circuit improves cue discrimination during learning. J Neurosci 30: 287-303, 2010.
24. Hahn JD, Swanson LW. Distinct patterns of neuronal inputs and outputs of the juxtaparaventricular and suprafornical regions of the lateral hypothalamic area in the male rat. Brain Res Rev 64: 14-103, 2010.
25. Hartfield AW, Moore NA, Clifton PG. Effects of clozapine, olanzapine and haloperidol on the microstructure of ingestive behaviour in the rat. Psychopharmacology (Berl) 167: 115-122, 2003.
26. Heimer L, Zahm DS, Churchill L, Kalivas PW, Wohltmann C. Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 41: 89-125, 1991.
27. Jacobs KM, Mark GP, Scott TR. Taste responses in the nucleus tractus solitarius of sodium-deprived rats. J Physiol 406: 393-410, 1988.
28. Johnson AK. The sensory psychobiology of thirst and salt appetite. Med Sci Sports Exerc 39: 1388-1400, 2007.
29. Johnson AK, Thunhorst RL. The neuroendocrinology of thirst and salt appetite: visceral sensory signals and mechanisms of central integration. Front Neuroendocrinol 18: 292-353, 1997.
30. Katafuchi T, Oomura Y, Yoshimatsu H. Single neuron activity in the rat lateral hypothalamus during 2-deoxy-D-glucose induced and natural feeding behavior. Brain Res 359: 1-9, 1985.
31. Kelley AE. Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning. Neurosci Biobehav Rev 27: 765-776, 2004.
32. Kelley AE, Baldo BA, Pratt WE, Will MJ. Corticostriatal-hypothalamic circuitry and food motivation: integration of energy, action and reward. Physiol Behav 86: 773-795, 2005.
33. Kourrich S, Thomas MJ. Similar neurons, opposite adaptations: psychostimulant experience differentially alters firing properties in accumbens core versus shell. J Neurosci 29: 12275-12283, 2009.
34. Kralik JD, Dimitrov DF, Krupa DJ, Katz DB, Cohen D, Nicolelis MA. Techniques for long-term multisite neuronal ensemble recordings in behaving animals. Methods 25: 121-150, 2001.
35. Krause M, German PW, Taha SA, Fields HL. A pause in nucleus accumbens neuron firing is required to initiate and maintain feeding. J Neurosci 30: 4746-4756, 2010.
36. Lansink CS, Goltstein PM, Lankelma JV, Pennartz CM. Fast-spiking interneurons of the rat ventral striatum: temporal coordination of activity with principal cells and responsiveness to reward. Eur J Neurosci 32: 494-508, 2010.
37. Lastra G, Dhuper S, Johnson MS, Sowers JR. Salt, aldosterone, and insulin resistance: impact on the cardiovascular system. Nat Rev Cardiol 7: 577-584, 2010.
38. Lei Q, Yan J, Huang T, Shi J, Yang X, Lv B, Li Q. Role of the lateral hypothalamus in modulating responses of parabrachial gustatory neurons in the rat. Brain Res Bull 77: 165-171, 2008.
39. Liedtke WB, McKinley MJ, Walker LL, Zhang H, Pfenning AR, Drago J, Hochendoner SJ, Hilton DL, Lawrence AJ, Denton DA. Relation of addiction genes to hypothalamic gene changes subserving genesis and gratification of a classic instinct, sodium appetite. Proc Natl Acad Sci USA 108: 12509-12514, 2011.
40. Loriaux AL, Roitman JD, Roitman MF. Nucleus accumbens shell, but not core, tracks motivational value of salt. J Neurophysiol 106: 1537-1544, 2011.
41. Lundy RF Jr, Blair M, Horvath N, Norgren R. Furosemide, sodium appetite, and ingestive behavior. Physiol Behav 78: 449-458, 2003.
42. Lundy RF Jr, Norgren R. Activity in the hypothalamus, amygdala, and cortex generates bilateral and convergent modulation of pontine gustatory neurons. J Neurophysiol 91: 1143-1157, 2004.
43. Lundy RF Jr, Norgren R. Pontine gustatory activity is altered by electrical stimulation in the central nucleus of the amygdala. J Neurophysiol 85: 770-783, 2001.
44. Martinez WL, Martinez AR. Monte Carlo methods for inferential statistics. In: Computational Statistics Handbook with MATLAB. Boca Raton, FL: Chapman & Hall/CRC, 2002, p. 191-228.
45. McCaughey SA, Scott TR. Rapid induction of sodium appetite modifies taste-evoked activity in the rat nucleus of the solitary tract. Am J Physiol Regul Integr Comp Physiol 279: R1121-R1131, 2000.
46. Morris MJ, Na ES, Grippo AJ, Johnson AK. The effects of deoxycorticosterone-induced sodium appetite on hedonic behaviors in the rat. Behav Neurosci 120: 571-579, 2006.
47. Morris MJ, Na ES, Johnson AK. Salt craving: the psychobiology of pathogenic sodium intake. Physiol Behav 94: 709-721, 2008.
48. Na ES, Morris MJ, Johnson AK. Behavioral cross-sensitization between morphine-induced locomotion and sodium depletion-induced salt appetite. Pharmacol Biochem Behav 93: 368-374, 2009.
49. Na ES, Morris MJ, Johnson RF, Beltz TG, Johnson AK. The neural substrates of enhanced salt appetite after repeated sodium depletions. Brain Res 1171: 104-110, 2007.
50. Nakamura K, Norgren R. Sodium-deficient diet reduces gustatory activity in the nucleus of the solitary tract of behaving rats. Am J Physiol Regul Integr Comp Physiol 269: R647-R661, 1995.
51. Nakamura K, Norgren R. Taste responses of neurons in the nucleus of the solitary tract of awake rats: an extended stimulus array. J Neurophysiol 70: 879-891, 1993.
52. Nishijo H, Norgren R. Parabrachial neural coding of taste stimuli in awake rats. J Neurophysiol 78: 2254-2268, 1997.
53. Nishijo H, Ono T, Uwano T, Kondoh T, Torii K. Hypothalamic and amygdalar neuronal responses to various tastant solutions during ingestive behavior in rats. J Nutr 130: 954S-959S, 2000.
54. Nishijo H, Uwano T, Tamura R, Ono T. Gustatory and multimodal neuronal responses in the amygdala during licking and discrimination of sensory stimuli in awake rats. J Neurophysiol 79: 21-36, 1998.
55. Norgren R. Gustatory responses in the hypothalamus. Brain Res 21: 63-77, 1970.
56. Ottersen OP. Afferent connections to the amygdaloid complex of the rat and cat: II. Afferents from the hypothalamus and the basal telencephalon. J Comp Neurol 194: 267-289, 1980.
57. Ravel S, Legallet E, Apicella P. Responses of tonically active neurons in the monkey striatum discriminate between motivationally opposing stimuli. J Neurosci 23: 8489-8497, 2003.
58. Roitman MF, Bernstein IL. Amiloride-sensitive sodium signals and salt appetite: multiple gustatory pathways. Am J Physiol Regul Integr Comp Physiol 276: R1732-R1738, 1999.
59. Roitman MF, Na E, Anderson G, Jones TA, Bernstein IL. Induction of a salt appetite alters dendritic morphology in nucleus accumbens and sensitizes rats to amphetamine. J Neurosci 22: RC225, 2002.
60. Roitman MF, Wheeler RA, Carelli RM. Nucleus accumbens neurons are innately tuned for rewarding and aversive taste stimuli, encode their predictors, and are linked to motor output. Neuron 45: 587-597, 2005.
61. Saper CB, Chou TC, Elmquist JK. The need to feed: homeostatic and hedonic control of eating. Neuron 36: 199-211, 2002.
62. Schulkin J, Leibman D, Ehrman RN, Norton NW, Ternes JW. Salt hunger in the rhesus monkey. Behav Neurosci 98: 753-756, 1984.
63. Schwartzbaum JS, Morse JR. Taste responsivity of amygdaloid units in behaving rabbit: a methodological report. Brain Res Bull 3: 131-141, 1978.
64. Shekhtman E, Geerling JC, Loewy AD. Aldosterone-sensitive neurons of the nucleus of the solitary tract: multisynaptic pathway to the nucleus accumbens. J Comp Neurol 501: 274-289, 2007.
65. Shimura T, Komori M, Yamamoto T. Acute sodium deficiency reduces gustatory responsiveness to NaCl in the parabrachial nucleus of rats. Neurosci Lett 236: 33-36, 1997.
66. Stapleton JR, Lavine ML, Wolpert RL, Nicolelis MA, Simon SA. Rapid taste responses in the gustatory cortex during licking. J Neurosci 26: 4126-4138, 2006.
67. Swanson LW. Cerebral hemisphere regulation of motivated behavior. Brain Res 886: 113-164, 2000.
68. Taha SA, Fields HL. Encoding of palatability and appetitive behaviors by distinct neuronal populations in the nucleus accumbens. J Neurosci 25: 1193-1202, 2005.
69. Tamura R, Norgren R. Repeated sodium depletion affects gustatory neural responses in the nucleus of the solitary tract of rats. Am J Physiol Regul Integr Comp Physiol 273: R1381-R1391, 1997.
70. Tindell AJ, Smith KS, Pecina S, Berridge KC, Aldridge JW. Ventral pallidum firing codes hedonic reward: when a bad taste turns good. J Neurophysiol 96: 2399-2409, 2006.
71. Touzani K, Taghzouti K, Velley L. Cellular organization of lateral hypothalamic efferents to the central amygdaloid nucleus of the rat. Neuroreport 7: 517-520, 1996.
72. Uwano T, Nishijo H, Ono T, Tamura R. Neuronal responsiveness to various sensory stimuli, and associative learning in the rat amygdala. Neuroscience 68: 339-361, 1995.
73. Voorhies AC, Bernstein IL. Induction and expression of salt appetite: effects on Fos expression in nucleus accumbens. Behav Brain Res 172: 90-96, 2006.
74. Wiest MC, Bentley N, Nicolelis MA. Heterogeneous integration of bilateral whisker signals by neurons in primary somatosensory cortex of awake rats. J Neurophysiol 93: 2966-2973, 2005.
75. Wolf G, Quartermain D. Sodium chloride intake of adrenalectomized rats with lateral hypothalamic lesions. Am J Physiol 212: 113-118, 1967.
76. Yamamoto T, Matsuo R, Kiyomitsu Y, Kitamura R. Response properties of lateral hypothalamic neurons during ingestive behavior with special reference to licking of various taste solutions. Brain Res 481: 286-297, 1989.
77. Yarom O, Cohen D. Putative cholinergic interneurons in the ventral and dorsal regions of the striatum have distinct roles in a two choice alternative association task. Front Syst Neurosci 5: 36, 2011.
78. Yasui Y, Tsumori T, Oka T, Yokota S. Amygdaloid axon terminals are in contact with trigeminal premotor neurons in the parvicellular reticular formation of the rat medulla oblongata. Brain Res 1016: 129-134, 2004.
79. Young AM, Joseph MH, Gray JA. Increased dopamine release in vivo in nucleus accumbens and caudate nucleus of the rat during drinking: a microdialysis study. Neuroscience 48: 871-876, 1992.
80. Zahm DS. Functional-anatomical implications of the nucleus accumbens core and shell subterritories. Ann NY Acad Sci 877: 113-128, 1999.
81. Zahm DS, Heimer L. Two transpallidal pathways originating in the rat nucleus accumbens. J Comp Neurol 302: 437-446, 1990.
82. Zhang DM, Epstein AN, Schulkin J. Medial region of the amygdala: involvement in adrenal-steroid-induced salt appetite. Brain Res 600: 20-26, 1993.