The biopsychology of salt hunger and sodium deficiency

Pflugers Archiv European Journal of Physiology

Volumn 467, Issue 3, 2015, Pages 445-456

  Hurley, Seth W ^a   Johnson, Alan Kim ^a,b,c  

^a University of Iowa   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c UNIVERSITY OF IOWA   (United States)

Author keywords

Homeostasis; Hypertension; Mood; Motivation and reward; Salt appetite

Indexed keywords

SODIUM CHLORIDE; SALT INTAKE;

ANHEDONIA; COGNITION; FATIGUE; HUMAN; NEUROBIOLOGY; NONHUMAN; PRIORITY JOURNAL; PSYCHOLOGY; REVIEW; REWARD; SALT INTAKE; SENSITIZATION; SODIUM APPETITE; SODIUM DEFICIENCY; SODIUM DEPLETION; WITHDRAWAL SYNDROME; ANIMAL; APPETITE; ELECTROLYTE BALANCE; HUNGER; HYPONATREMIA; METABOLISM; TASTE;

ANIMALS; APPETITE; HUMANS; HUNGER; HYPONATREMIA; SODIUM CHLORIDE, DIETARY; TASTE; TASTE PERCEPTION; WATER-ELECTROLYTE BALANCE;

EID: 84925490646     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1676-y     Document Type: Review

References (134)

1. Barelare B, Richter CP (1937) Increased sodium chloride appetite in pregnant rats. Am J Physiol 121(1):185
2. Bates GP and Miller VS (2008) Sweat rate and sodium loss during work in the heat. J Occup Med Toxicol 3(4)
3. Beauchamp GK et al (1990) Experimental sodium depletion and salt taste in normal human volunteers. Am J Clin Nutr 51(5):881–889
4. Berridge KC, Robinson TE, Aldridge JW (2009) Dissecting components of reward: ‘liking’, ‘wanting’, and learning. Curr Opin Pharmacol 9(1):65–73
5. Berridge KC, Schulkin J (1989) Palatability shift of a salt-associated incentive during sodium depletion. Q J Exp Psychol 41(2):121–138
6. Berridge KC et al (1984) Sodium depletion enhances salt palatability in rats. Behav Neurosci 98(4):652–660
7. Bibbins-Domingo K et al (2010) Projected effect of dietary salt reductions on future cardiovascular disease. N Engl J Med 362(7):590–599
8. Bindra D (1959) Motivation: a systematic reinterpretation. The Ronald Press Company, New York
9. Bolles RC (1975) Theory of motivation, Second Edition. Harper & Row, New York
10. Bou-Holaigah I et al (1995) The relationship between neurally mediated hypotension and the chronic fatigue syndrome. JAMA 274(12):961–967
11. Brockbank E (1929) Miners’ cramp. Br Med J 1(3549):65
12. Brown AM (1980) Receptors under pressure. An update on baroreceptors. Circ Res 46(1):1–10
13. Brown JE, Toma RB (1986) Taste changes during pregnancy. Am J Clin Nutr 43(3):414
14. Brown IJ et al (2009) Salt intakes around the world: implications for public health. Int J Epidemiol 38(3):791–813
15. Bryant RW et al (1980) Arousal of a specific and persistent sodium appetite in the rat with continuous intracerebroventricular infusion of angiotensin II. J Physiol 301(1):365
16. Campbell WB, Brooks SN, Pettinger WA (1974) Angiotensin II- and angiotensin III-induced aldosterone release vivo in the rat. Science 184(4140):994–996
17. Carlezon WA, Chartoff EH (2007) Intracranial self-stimulation (ICSS) in rodents to study the neurobiology of motivation. Nat Protoc 2(11):2987–2995
18. Center for Disease Control (2014) Chronic fatigue syndrome. [cited 2014; Available from: http://www.cdc.gov/cfs/]
19. Clark JJ, Bernstein IL (2006) Sensitization of salt appetite is associated with increased “wanting” but not “liking” of a salt reward in the sodium-deplete rat. Behav Neurosci 120(1):206
20. Conover KL, Woodside B, Shizgal P (1994) Effects of sodium depletion on competition and summation between rewarding effects of salt and lateral hypothalamic stimulation in the rat. Behav Neurosci 108(3):549
21. Contreras RJ (1977) Changes in gustatory nerve discharges with sodium deficiency: a single unit analysis. Brain Res 121(2):373–378
22. Contreras RJ, Frank M (1979) Sodium deprivation alters neural responses to gustatory stimuli. J Gen Physiol 73(5):569–594
23. Contreras RJ, Stetson PW (1981) Changes in salt intake lesions of the area postrema and the nucleus of the solitary tract in rats. Brain Res 211(2):355–366
24. Cotman CW, Monaghan DT, Ganong AH (1988) Excitatory amino acid neurotransmission: NMDA receptors and Hebb-type synaptic plasticity. Annu Rev Neurosci 11:61–80
25. Crystal SR, Bernstein IL (1995) Morning sickness: impact on offspring salt preference. Appetite 25(3):231–240
26. Dahl LK (1961) Possible role of chronic excess salt consumption in the pathogenesis of essential hypertension. Am J Cardiol 8(4):571–575
27. Dahl LK (1972) Salt and hypertension. Am J Clin Nutr 25(2):231–244
28. Dahl LK, Love RA (1957) Etiological role of sodium chloride intake in essential hypertension in humans. J Am Med Assoc 164(4):397
29. De Gobbi JIF et al (2008) Right atrial stretch alters fore- and hind-brain expression of c-fos and inhibits the rapid onset of salt appetite. J Physiol 586(15):3719–3729
30. De Luca LA et al (2010) Water deprivation-induced sodium appetite. Physiol Behav 100(5):535–544
31. Denton DA (1957) The study of sheep with permanent unilateral parotid fistulae. Q J Exp Physiol Cognate Med Sci 42(1):72–95
32. Denton DA (1982) The hunger for salt: an anthropological, physiological, and medical analysis. Springer, New York
33. Denton DA et al (1984) Stress, ACTH, salt intake and high blood pressure. Clin Exp Hypertens 6(1–2):403–415
34. Epstein AN (1982) Mineralocorticoids and cerebral angiotensin may act together to produce sodium appetite. Peptides 3(3):493–494
35. Epstein AN (1991) Neurohormonal control of salt intake in the rat. Brain Res Bull 27(3–4):315–320
36. Epstein AN (1991) Thirst and salt intake: a personal review and some suggestions. In D. Ramsay & D. Booth (Eds.), Thirst (pp. 481-501): Springer London
37. Falk JL (1965) Water intake and NaCl appetite in sodium depletion. Psychol Rep 16:315–325
38. Falk JL (1966) Serial sodium depletion and NaCl solution intake. Physiol Behav 1(1):75–77
39. Faure A et al (2008) Mesolimbic dopamine in desire and dread: enabling motivation to be generated by localized glutamate disruptions in nucleus accumbens. J Neurosci 28(28):7184–7192
40. Ferguson AV, Washburn DL (1998) Angiotensin II: a peptidergic neurotransmitter in central autonomic pathways. Prog Neurobiol 54(2):169–192
41. Fessler DMT (2003) An evolutionary explanation of the plasticity of salt preferences: prophylaxis against sudden dehydration. Med Hypotheses 61(3):412–415
42. Fitts DA, Masson DB (1990) Preoptic angiotensin and salt appetite. Behav Neurosci 104(4):643–650
43. Fitzsimons JT (1979) The physiology of thirst and sodium appetite. Monographs of the Physiological Society no 35. Cambridge University Press, Cambridge
44. Fluharty SJ, Epstein AN (1983) Sodium appetite elicited by intracerebroventricular infusion of angiotensin II in the rat: II. Synergistic interaction with systemic mineralocorticoids. Behav Neurosci 97(5):746
45. Frankmann SP et al (1986) A single experience with hyperoncotic colloid dialysis persistently alters water and sodium intake. In: The physiology of thirst and sodium appetite. NATO ASI series. Plenum, New York
46. Fregly MJ, Rowland NE (1985) Role of renin-angiotensin-aldosterone system in NaCl appetite of rats. Am J Physiol Regul Integr Comp Physiol 248(1):R1–R11
47. Ganten D, Hutchinson JS, Schelling P (1975) The intrinsic brain iso-renin--angiotensin system in the rat: its possible role in central mechanisms of blood pressure regulation. Clin Sci Mol Med Suppl 2:265s–268s
48. Glanzman DL (2010) Common mechanisms of synaptic plasticity in vertebrates and invertebrates. Curr Biol 20(1):R31–R36
49. Gomez-Sanchez CE et al (1997) Aldosterone biosynthesis in the rat brain. Endocrinology 138(8):3369
50. Gomez-Sanchez EP et al (2005) Is aldosterone synthesized within the rat brain? Am J Physiol Endocrinol Metab 288(2):E342–E346
51. Grill HJ, Norgren R (1978) The taste reactivity test. I. Mimetic responses to gustatory stimuli in neurologically normal rats. Brain Res 143(2):263–279
52. Grippo AJ et al (2006) Reduced hedonic behavior and altered cardiovascular function induced by mild sodium depletion in rats. Behav Neurosci 120(5):1133
53. Heale V, Harley C (1990) MK-801 and AP5 impair acquisition, but not retention, of the Morris milk maze. Pharmacol Biochem Behav 36(1):145–149
54. Hebb DO (1949) The organization of behavior. Wiley, New York
55. Henry JP (1988) Stress, salt and hypertension. Soc Sci Med 26(3):293–302
56. Hong S et al (2011) Negative reward signals from the lateral habenula to dopamine neurons are mediated by rostromedial tegmental nucleus in primates. J Neurosci Off J Soc Neurosci 31(32):11457–11471
57. Hurley SW, Johnson AK (2013) Dissociation of thirst and sodium appetite in the furo/cap model of extracellular dehydration and a role for N-methyl-D-aspartate receptors in the sensitization of sodium appetite. Behav Neurosci 127(6):890–898
58. Hurley SW, Johnson AK (2014) The role of the lateral hypothalamus and orexin in ingestive behavior: a model for the translation of past experience and sensed deficits into motivated behaviors. Front Syst Neurosci 8:216
59. Hurley SW, Thunhorst RL, Johnson AK (2013) Sodium appetite sensitization. In: De Luca LA, Johnson AK, Menani JV (eds) Neurobiology of body fluid homeostasis: transduction and integration (series IV: frontiers in neuroscience). Taylor and Francis, Boca Raton, pp 279–301
60. Hurley SW et al (2014) Sensitization of sodium appetite: evidence for sustained molecular changes in the lamina terminalis. Am J Physiol Regul Integr Comp Physiol 307(12):R1405–R1412
61. Jacobs KM, Mark GP, Scott TR (1988) Taste responses in the nucleus tractus solitarius of sodium-deprived rats. J Physiol 406(1):393
62. Jalowiec JE (1974) Sodium appetite elicited by furosemide: effects of differential dietary maintenance. Behav Biol 10(3):313–327
63. Jhou TC et al (2009) The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses. Neuron 61(5):786–800
64. Johnson AK (2007) The sensory psychobiology of thirst and salt appetite. Med Sci Sports Exerc 39(8):1388–1400
65. Johnson AK, Cunningham JT, Thunhorst RL (1996) Integrative role of the lamina terminalis in the regulation of cardiovascular and body fluid homeostasis. Clin Exp Pharmacol Physiol 23(2):183–191
66. Johnson AK, Gross PM (1993) Sensory circumventricular organs and brain homeostatic pathways. FASEB J Off Publ Fed Am Soc Exp Biol 7(8):678–686
67. Johnson AK, Thunhorst RL (2007) The neuroendocrinology, neurochemistry and molecular biology of thirst and salt appetite. Handb Neurochem Mol Neurobiol Behav Neurochem Neuroendocrinol Mol Neurobiol 3:641–687
68. Jorm AF (2001) Association of hypotension with positive and negative affect and depressive symptoms in the elderly. Br J Psychiatry 178(6):553–555
69. Kalivas PW, Alesdatter JE (1993) Involvement of N-methyl-D-aspartate receptor stimulation in the ventral tegmental area and amygdala in behavioral sensitization to cocaine. J Pharmacol Exp Ther 267(1):486–495
70. Kaunitz H (1956) Causes and consequences of salt consumption. Nature 178(4543):1141–1144
71. Keil LC, Summy-Long J, Severs WB (1975) Release of vasopressin by angiotensin II. Endocrinology 96(4):1063–1065
72. Kelley AE (2004) Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning. Neurosci Biobehav Rev 27(8):765–776
73. Kleinewietfeld M et al (2013) Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature 496(7446):518–522
74. Lee CT et al (2006) Serum- and glucocorticoid-inducible kinase (SGK) is a target of the MAPK/ERK signaling pathway that mediates memory formation in rats. Eur J Neurosci 23(5):1311–1320
75. Leshem M (1998) Salt preference in adolescence is predicted by common prenatal and infantile mineralofluid loss. Physiol Behav 63(4):699–704
76. Leshem M (2009) Biobehavior of the human love of salt. Neurosci Biobehav Rev 33(1):1–17
77. Leshem M (2011) Low dietary sodium is anxiogenic in rats. Physiol Behav 103(5):453–458
78. Leshem M (2013) The human penchant for deranged salt balance. In: De Luca LA, Johnson AK, Menani JV (eds) Neurobiology of body fluid homeostasis: transduction and integration (series IV: frontiers in neuroscience). Taylor and Francis, Boca Raton, p 1–22
79. Leshem M, Abutbul A, Eilon R (1999) Exercise increases the preference for salt in humans. Appetite 32(2):251–260
80. Liedtke WB et al (2011) Relation of addiction genes to hypothalamic gene changes subserving genesis and gratification of a classic instinct, sodium appetite. Proc Natl Acad Sci 108(30):12509
81. Lind RW, Johnson AK (1982) Subfornical organ-median preoptic connections and drinking and pressor responses to angiotensin II. J Neurosci Off J Soc Neurosci 2(8):1043–1051
82. Loriaux AL, Roitman JD, Roitman MF (2011) Nucleus accumbens shell, but not core, tracks motivational value of salt. J Neurophysiol 106(3):1537–1544
83. Lucas LR, Grillo CA, McEwen BS (2003) Involvement of mesolimbic structures in short-term sodium depletion: in situ hybridization and ligand-binding analyses. Neuroendocrinology 77(6):406–415
84. Lucas LR, Grillo CA, McEwen BS (2007) Salt appetite in sodium-depleted or sodium-replete conditions: possible role of opioid receptors. Neuroendocrinology 85(3):139–147
85. Lucas LR, Pompei P, McEwen BS (2000) Salt appetite in salt-replete rats: involvement of mesolimbic structures in deoxycorticosterone-induced salt craving behavior. Neuroendocrinology 71(6):386–395
86. MacGregor G, De Wardener HE (1998) Salt, diet and health. Cambridge University Press, Cambridge
87. Mameli M et al (2009) Cocaine-evoked synaptic plasticity: persistence in the VTA triggers adaptations in the NAc. Nat Neurosci 12(8):1036–1041
88. McCance RA (1936) Experimental sodium chloride deficiency in man. Proc R Soc Lond B Biol Sci 119(814):245–268
89. McEwen OR (1935) Salt loss as a common cause of ill-health in hot climates. Lancet 225(5826):1015
90. McKinley MJ (2013) Adaptive appetites for salted and unsalted food in rats: differential effects of sodium depletion, DOCA, and dehydration. Am J Physiol Regul Integr Comp Physiol 304(12):R1149–R1160
91. McKinley MJ et al (1999) The lamina terminalis and its role in fluid and electrolyte homeostasis. J Clin Neurosci Off J Neurosurg Soc Australas 6(4):289–301
92. Menani JV, Thunhorst RL, Johnson AK (1996) Lateral parabrachial nucleus and serotonergic mechanisms in the control of salt appetite in rats. Am J Physiol Regul Integr Comp Physiol 270(1):R162
93. Mifflin SW, Felder RB (1990) Synaptic mechanisms regulating cardiovascular afferent inputs to solitary tract nucleus. Am J Physiol 259(3 Pt 2):H653–H661
94. Mogenson GJ, Jones DL, Yim CY (1980) From motivation to action: functional interface between the limbic system and the motor system. Prog Neurobiol 14(2):69–97
95. Morris MJ, Na ES, Johnson AK (2008) Salt craving: the psychobiology of pathogenic sodium intake. Physiol Behav 94(5):709–721
96. Morris MJ, Na ES, Johnson AK (2010) Mineralocorticoid receptor antagonism prevents hedonic deficits induced by a chronic sodium appetite. Behav Neurosci 124(2):211
97. Morris MJ et al (2006) The effects of deoxycorticosterone-induced sodium appetite on hedonic behaviors in the rat. Behav Neurosci 120(3):571–578
98. Moss KN (1923) Some effects of high air temperatures and muscular exertion upon colliers. Proc R Soc Lond B Containing Papers Biol Charact 95:181–200
99. Mozaffarian D et al (2014) Global sodium consumption and death from cardiovascular causes. N Engl J Med 371(7):624–634
100. Na ES, Morris MJ, Johnson AK (2012) Opioid mechanisms that mediate the palatability of and appetite for salt in sodium replete and deficient states. Physiol Behav 106:164–170
101. Na ES et al (2007) The neural substrates of enhanced salt appetite after repeated sodium depletions. Brain Res 1171:104–110
102. Naray-Fejes-Toth A, Fejes-Toth G (2000) The sgk, an aldosterone-induced gene in mineralocorticoid target cells, regulates the epithelial sodium channel. Kidney Int 57(4):1290–1294
103. Nestler EJ (2001) Molecular basis of long-term plasticity underlying addiction. Nat Rev Neurosci 2(2):119–128
104. Nestler EJ, Barrot M, Self DW (2001) DeltaFosB: a sustained molecular switch for addiction. Proc Natl Acad Sci U S A 98(20):11042–11046
105. Nestler EJ, Hyman SE (2010) Animal models of neuropsychiatric disorders. Nat Neurosci 13(10):1161–1169
106. Olds J, Milner P (1954) Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. J Comp Physiol Psychol 47(6):419
107. Papp M, Willner P, Muscat R (1991) An animal model of anhedonia: attenuation of sucrose consumption and place preference conditioning by chronic unpredictable mild stress. Psychopharmacology 104(2):255–259
108. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. Academic Press, San Diego
109. Peart WS (1965) The renin-angiotensin system. Pharmacol Rev 17(2):143–182
110. Peciña S, Berridge KC (2000) Opioid site in nucleus accumbens shell mediates eating and hedonic ‘liking’ for food: map based on microinjection Fos plumes. Brain Res 863(1–2):71–86
111. Pereira DTB, Menani JV, De Luca LA Jr (2010) FURO/CAP: a protocol for sodium intake sensitization. Physiol Behav 99(4):472–481
112. Phillips MI (1987) Functions of angiotensin in the central nervous system. Annu Rev Physiol 49:413–435
113. Potts WTW, Parry G (1964) Osmotic and ionic regulation in animals. In: International series of monographs on pure and applied biology. Division: Zoology, vol 19. Pergamon Press, Oxford, p 423
114. Richter CP (1936) Increased salt appetite in adrenalectomized rats. Am J Physiol Leg Content 115(1):155–161
115. Robinson MJF, Berridge KC (2013) Instant transformation of learned repulsion into motivational “wanting”. Curr Biol 23(4):282–289
116. Roitman MF, Wheeler RA, Carelli RM (2005) Nucleus accumbens neurons are innately tuned for rewarding and aversive taste stimuli, encode their predictors, and are linked to motor output. Neuron 45(4):587–597
117. Roitman MF et al (1997) Dopamine and sodium appetite: antagonists suppress sham drinking of NaCl solutions in the rat. Behav Neurosci 111(3):606
118. Roitman MF et al (2002) Induction of a salt appetite alters dendritic morphology in nucleus accumbens and sensitizes rats to amphetamine. J Neurosci 22(11):RC225
119. Roitman MF et al (2008) Real-time chemical responses in the nucleus accumbens differentiate rewarding and aversive stimuli. Nat Neurosci 11(12):1376
120. Ruhf AA, Starbuck EM, Fitts DA (2001) Effects of SFO lesions on salt appetite during multiple sodium depletions. Physiol Behav 74(4):629–636
121. Sakai RR, Nicolaidis S, Epstein AN (1986) Salt appetite is suppressed by interference with angiotensin II and aldosterone. Am J Physiol Regul Integr Comp Physiol 251(4):R762–R768
122. Sakai RR et al (1987) Salt appetite is enhanced by one prior episode of sodium depletion in the rat. Behav Neurosci 101(5):724
123. Sakai RR et al (1989) Prior episodes of sodium depletion increase the need-free sodium intake of the rat. Behav Neurosci 103(1):186
124. Schulkin J (1986) The evolution and expression of salt appetite. In: De Caro G, Epstein AN, Massi M (eds) The physiology of thirst and sodium appetite. Plenum, New York, pp 491–496
125. Seymour D et al (1980) Acute confusional states and dementia in the elderly: the role of dehydration/volume depletion, physical illness and age. Age Ageing 9(3):137–146
126. Smith KS et al (2009) Ventral pallidum roles in reward and motivation. Behav Brain Res 196(2):155–167
127. Takamata A et al (1994) Sodium appetite, thirst, and body fluid regulation in humans during rehydration without sodium replacement. Am J Physiol Regul Integr Comp Physiol 266(5):R1493–R1502
128. Tindell AJ et al (2006) Ventral pallidum firing codes hedonic reward: when a bad taste turns good. J Neurophysiol 96(5):2399–2409
129. Trujillo KA, Akil H (1991) Inhibition of morphine tolerance and dependence by the NMDA receptor antagonist MK-801. Science 251(4989):85–87
130. Watson SJ et al (1982) Dynorphin and vasopressin: common localization in magnocellular neurons. Science 216(4541):85–87
131. Weinberger MH et al (2001) Salt sensitivity, pulse pressure, and death in normal and hypertensive humans. Hypertension 37(2 Pt 2):429–432
132. Wilkins L, Richter CP (1940) A great craving for salt by a child with cortico-adrenal insufficiency. J Am Med Assoc 114(10):866–868
133. Yeomans MR, Blundell JE, Leshem M (2004) Palatability: response to nutritional need or need-free stimulation of appetite? Br J Nutr 92(Suppl 1):S3–S14
134. Yuste R, Bonhoeffer T (2001) Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24(1):1071–1089