Physiological state tunes mesolimbic signaling: lessons from sodium appetite and inspiration from Randall R. Sakai

Fortin, Samantha M.; Roitman, Mitchell F.

doi:10.1016/j.physbeh.2016.11.021

Cited by 11Neurotransmitter Receptor Influence on BehaviorRegulation of Appetite and ObesityOlfactory and Sensory Function Studies

Physiological state tunes mesolimbic signaling: lessons from sodium appetite and inspiration from Randall R. Sakai

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Fortin, Samantha M., Roitman, Mitchell F.·2017·Physiology & Behavior

DOI 10.1016/j.physbeh.2016.11.021PMC PMC5777138

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Abstract

Sodium deficit poses a life-threatening challenge to body fluid homeostasis and generates a sodium appetite - the behavioral drive to ingest sodium. Dr. Randall R. Sakai greatly contributed to our understanding of the hormonal responses to negative sodium balance and to the central processing of these signals. Reactivity to the taste of sodium solutions and the motivation to seek and consume sodium changes dramatically with body fluid balance. Here, we review studies that collectively suggest that sodium deficit recruits the mesolimbic system to play a role in the behavioral expression of sodium appetite. The recruitment of the mesolimbic system likely contributes to intense sodium seeking and reinforces sodium consumption observed in deficient animals. Some of the hormones that are released in response to sodium deficit act directly on both dopamine and nucleus accumbens elements. Moreover, the taste of sodium in sodium deficient rats evokes a pattern of dopamine and nucleus accumbens activity that is similar to responses to rewarding stimuli. A very different pattern of activity is observed in non-deficient rats. Given the well-characterized endocrine response to sodium deficit and its central action, sodium appetite becomes an ideal model for understanding the role of mesolimbic signaling in reward, reinforcement and the generation of motivated behavior.

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Sodium depletion causes a robust and highly specific motivation to consume sodium, such that salt solutions that are negative/aversive in the replete state become preferred/rewarding in sodium-depleted animals.
“Sodium depletion causes a robust and highly specific motivation to consume sodium, such that salt solutions that are negative/aversive in the replete state become preferred/rewarding in sodium-depleted animals”
From FGF21 and the physiological regulation of macronutrient preference (2020) · cites this paper as [21]

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A neural substrate of prediction and reward
Schultz, W., Dayan, P., & Montague, P. R. (1997) · Science · doi:10.1126/science.275.5306.1593 · Cited by 9,388 · see citing works
Molecular Mechanisms of Depression: Perspectives on New Treatment Strategies
Lang, U. E., & Borgwardt, S. (2013) · Cellular Physiology and Biochemistry · doi:10.1159/000350094 · Cited by 8,501 · see citing works
Heart Disease and Stroke Statistics—2015 Update: A Report From the American Heart Association
Mozaffarian, D., Benjamin, E. J., Go, A. S., Arnett, D. K., Blaha, M. J., Cushman, M., de Ferranti, S., Després, J.-P., Fullerton, H. J., Howard, V. J., et al. (2015) · Circulation · doi:10.1161/cir.0000000000000152 · Cited by 5,797 · see citing works
What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?
Berridge, K. C., & Robinson, T. E. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00019-8 · Cited by 4,127 · see citing works
Dopamine, learning and motivation.
Wise, R. A. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1406 · Cited by 3,379 · cited 1× · see citing works
“nucleus accumbens [NAc]; dorsal striatum) were first proposed to be involved in reinforcement processes after the seminal studies of Roy Wise and colleagues [30,31].”
Method
Ghrelin modulates the activity and synaptic input organization of midbrain dopamine neurons while promoting appetite
Abizaid, A., Liu, Z.-W., Andrews, Z. B., Shanabrough, M., Borok, E., Elsworth, J. D., Roth, R. H., Sleeman, M. W., Picciotto, M. R., Tschöp, M. H., et al. (2006) · Journal of Clinical Investigation · doi:10.1172/jci29867 · Cited by 984 · see citing works
Leptin Receptor Signaling in Midbrain Dopamine Neurons Regulates Feeding
Hommel, J. D., Trinko, R., Sears, R. M., Georgescu, D., Liu, Z.-W., Gao, X.-B., Thurmon, J. J., Marinelli, M., & DiLeone, R. J. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.023 · Cited by 902 · see citing works
A causal link between prediction errors, dopamine neurons and learning
Steinberg, E. E., Keiflin, R., Boivin, J. R., Witten, I. B., Deisseroth, K. A., & Janak, P. H. (2013) · Nature Neuroscience · doi:10.1038/nn.3413 · Cited by 879 · see citing works
Mesolimbic dopamine signals the value of work
Hamid, A., Pettibone, J. R., Mabrouk, O. S., Hetrick, V. L., Schmidt, R., Weele, C. M. V., Kennedy, R. T., Aragona, B. J., & Berke, J. D. (2015) · Nature Neuroscience · doi:10.1038/nn.4173 · Cited by 815 · see citing works
Alterations in the morphology of dendrites and dendritic spines in the nucleus accumbens and prefrontal cortex following repeated treatment with amphetamine or cocaine
Robinson, T. E., & Kolb, B. E. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00576.x · Cited by 726 · see citing works
Associative learning mediates dynamic shifts in dopamine signaling in the nucleus accumbens
Day, J. J., Roitman, M. F., Wightman, R. M., & Carelli, R. M. (2007) · Nature Neuroscience · doi:10.1038/nn1923 · Cited by 710 · see citing works
Persistent structural modifications in nucleus accumbens and prefrontal cortex neurons produced by previous experience with amphetamine
Robinson, T. E., & Kolb, B. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-21-08491.1997 · Cited by 704 · see citing works
Neuroleptic-Induced "Anhedonia" in Rats: Pimozide Blocks Reward Quality of Food
Wise, R. A., Spindler, J., de Wit, H., & Gerberg, G. J. (1978) · Science · doi:10.1126/science.566469 · Cited by 636 · see citing works
The taste reactivity test. II. Mimetic responses to gustatory stimuli in chronic thalamic and chronic decerebrate rats
Grill, H. J., & Norgren, R. (1978) · Brain Research · doi:10.1016/0006-8993(78)90569-3 · Cited by 588 · see citing works
GLP-1 Neurons in the Nucleus of the Solitary Tract Project Directly to the Ventral Tegmental Area and Nucleus Accumbens to Control for Food Intake
Alhadeff, A. L., Rupprecht, L. E., & Hayes, M. R. (2012) · Endocrinology · doi:10.1210/en.2011-1443 · Cited by 515 · see citing works
Hindbrain Neurons as an Essential Hub in the Neuroanatomically Distributed Control of Energy Balance
Grill, H. J., & Hayes, M. R. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.06.015 · Cited by 483 · see citing works
Nucleus Accumbens Neurons Are Innately Tuned for Rewarding and Aversive Taste Stimuli, Encode Their Predictors, and Are Linked to Motor Output
Roitman, M. F., Wheeler, R. A., & Carelli, R. M. (2005) · Neuron · doi:10.1016/j.neuron.2004.12.055 · Cited by 453 · see citing works
INCREASED SALT APPETITE IN ADRENALECTOMIZED RATS
Richter, C. P. (1936) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1936.115.1.155 · Cited by 448 · see citing works
Modulation of Brain Reward Circuitry by Leptin
Fulton, S. E., Woodside, B. C., & Shizgal, P. (2000) · Science · doi:10.1126/science.287.5450.125 · Cited by 421 · see citing works
Striatal dopamine neurotransmission: Regulation of release and uptake
Sulzer, D., Cragg, S. J., & Rice, M. E. (2016) · Basal Ganglia · doi:10.1016/j.baga.2016.02.001 · Cited by 382 · see citing works
DAncing past the DAT at a DA synapse
Cragg, S. J., & Rice, M. E. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.03.011 · Cited by 373 · see citing works
PRECLINICAL STUDY: Ghrelin stimulates locomotor activity and accumbal dopamine‐overflow via central cholinergic systems in mice: implications for its involvement in brain reward
Jerlhag, E., Egecioglu, E., Dickson, S. L., Andersson, M. A., Svensson, L., & Engel, J. A. (2006) · Addiction Biology · doi:10.1111/j.1369-1600.2006.00002.x · Cited by 352 · see citing works
Instant transformation of learned repulsion into motivational “wanting”
Robinson, M. J. F., & Berridge, K. C. (2013) · Current Biology · doi:10.1016/j.cub.2013.01.016 · Cited by 320 · see citing works
Dopaminergic correlates of motivated behavior: importance of drive
Wilson, C., Nomikos, G., Collu, M., & Fibiger, H. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-07-05169.1995 · Cited by 294 · see citing works
Insulin enhances striatal dopamine release by activating cholinergic interneurons and thereby signals reward
Stouffer, M. A., Woods, C. A., Patel, J. C., Lee, C. R., Witkovsky, P., Bao, L., Machold, R. P., Jones, K. T., de Vaca, S. C., Reith, M. E. A., et al. (2015) · Nature Communications · doi:10.1038/ncomms9543 · Cited by 286 · see citing works
Central regulation of sodium appetite
Geerling, J. C., & Loewy, A. D. (2007) · Experimental Physiology · doi:10.1113/expphysiol.2007.039891 · Cited by 275 · see citing works
Sodium depletion enhances salt palatability in rats
Berridge, K. C., Flynn, F. W., Schulkin, J., & Grill, H. J. (1984) · Behavioral Neuroscience · doi:10.1037/0735-7044.98.4.652 · Cited by 257 · cited 1× · see citing works
“However, in a sodium deplete state, the taste of concentrated NaCl becomes transformed to one that is appetitive, palatable [21] and reinforcing [15,22].”
Background
Insulin induces long-term depression of ventral tegmental area dopamine neurons via endocannabinoids
Labouèbe, G., Liu, S., Dias, C., Zou, H., Wong, J. C. Y., Karunakaran, S., Clee, S. M., Phillips, A. G., Boutrel, B., & Borgland, S. L. (2013) · Nature Neuroscience · doi:10.1038/nn.3321 · Cited by 239 · see citing works
Intracellular Signals Mediating the Food Intake-Suppressive Effects of Hindbrain Glucagon-like Peptide-1 Receptor Activation
Hayes, M. R., Leichner, T. M., Zhao, S., Lee, G., Chowansky, A., Zimmer, D. J., Jonghe, B. C. D., Kanoski, S. E., Grill, H. J., & Bence, K. K. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.02.001 · Cited by 234 · see citing works
Type I corticosteroid receptor‐like immunoreactivity in the rat CNS: Distribution and regulation by corticosteroids
Ahima, R. S., Krozowski, Z. S., & Harlan, R. E. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903130312 · Cited by 232 · see citing works
Microvascular specializations promoting rapid interstitial solute dispersion in nucleus tractus solitarius
Gross, P. M., Wall, K. M., Pang, J. J., Shaver, S. W., & Wainman, D. S. (1990) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1990.259.6.r1131 · Cited by 206 · see citing works
Mesolimbic Dopamine and the Regulation of Motivated Behavior
Salamone, J. D., Pardo, M., Yohn, S. E., López-Cruz, L., SanMiguel, N., & Correa, M. (2015) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2015_383 · Cited by 204 · see citing works
The hunger for salt: An anthropological, physiological and medical analysis-by
(1984) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(84)90037-9 · Cited by 198 · see citing works
Sodium deprivation alters neural responses to gustatory stimuli.
Contreras, R. J., & Frank, M. G. (1979) · The Journal of General Physiology · doi:10.1085/jgp.73.5.569 · Cited by 198 · see citing works
Aldosterone in the brain
Geerling, J. C., & Loewy, A. D. (2009) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.90399.2008 · Cited by 184 · see citing works
Ghrelin Acts as an Interface between Physiological State and Phasic Dopamine Signaling
Cone, J. J., McCutcheon, J. E., & Roitman, M. F. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4404-13.2014 · Cited by 181 · see citing works
Cost, Benefit, Tonic, Phasic
Niv, Y. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1390.018 · Cited by 179 · see citing works
Salt appetite is suppressed by interference with angiotensin II and aldosterone
Sakai, R. R., Nicolaı̈dis, S., & Epstein, A. N. (1986) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1986.251.4.r762 · Cited by 174 · see citing works
Inhibitions of Nucleus Accumbens Neurons Encode a Gating Signal for Reward-Directed Behavior
Taha, S. A., & Fields, H. L. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3227-05.2006 · Cited by 171 · see citing works
Basal and feeding-evoked dopamine release in the rat nucleus accumbens is depressed by leptin
Krügel, U., Schraft, T., Kittner, H., Kieß, W., & Illés, P. (2003) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2003.09.047 · Cited by 171 · see citing works
Behavioral and Electrophysiological Indices of Negative Affect Predict Cocaine Self-Administration
Wheeler, R. A., Twining, R. C., Jones, J. L., Slater, J. M., Grigson, P. S., & Carelli, R. M. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.024 · Cited by 166 · see citing works
Central gustatory lesions: II. Effects on sodium appetite, taste aversion learning, and feeding behaviors.
Flynn, F. W., Grill, H. J., Schulkin, J. A., & Norgren, R. (1991) · Behavioral Neuroscience · doi:10.1037//0735-7044.105.6.944 · Cited by 161 · see citing works
The Glucagon-Like Peptide 1 Analogue Exendin-4 Attenuates the Nicotine-Induced Locomotor Stimulation, Accumbal Dopamine Release, Conditioned Place Preference as well as the Expression of Locomotor Sensitization in Mice
Egecioglu, E., Engel, J. A., & Jerlhag, E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077284 · Cited by 158 · see citing works
Pimozide decreases the positive reinforcing effect of sham fed sucrose in the rat
Geary, N., & Smith, G. P. (1985) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(85)90528-3 · Cited by 156 · see citing works
Glucagon-like peptide 1-(7–36) amide acts at lateral and medial hypothalamic sites to suppress feeding in rats
Schick, R., Zimmermann, J., Walde, T. V., & SCHUSDZIARRA, V. (2003) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00479.2002 · Cited by 152 · see citing works
Aldosterone Target Neurons in the Nucleus Tractus Solitarius Drive Sodium Appetite
Geerling, J. C., Engeland, W. C., Kawata, M., & Loewy, A. D. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3115-05.2006 · Cited by 148 · see citing works
The hunger for salt. An anthropological, physiological and medical analysis
(1983) · General Pharmacology The Vascular System · doi:10.1016/0306-3623(83)90123-4 · Cited by 148 · see citing works
Taste preferences for sodium salts by adrenalectomized rats.
Nachman, M. (1962) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0041348 · Cited by 147 · see citing works
Amiloride Disrupts NaCl versus KCl Discrimination Performance: Implications for Salt Taste Coding in Rats
Spector, A. C., Guagliardo, N. A., & John, S. J. S. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-24-08115.1996 · Cited by 146 · see citing works
Sodium hunger; The search for a salty taste
(1992) · General Pharmacology The Vascular System · doi:10.1016/0306-3623(92)90329-i · Cited by 142 · see citing works
Dopaminergic modulation of striatal neurons, circuits, and assemblies
Surmeier, D. J., Carrillo‐Reid, L., & Bargas, J. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.08.051 · Cited by 141 · see citing works
Salt appetite is enhanced by one prior episode of sodium depletion in the rat.
Sakai, R. R., Fine, W. B., Epstein, A. N., & Frankmann, S. P. (1987) · Behavioral Neuroscience · doi:10.1037//0735-7044.101.5.724 · Cited by 139 · see citing works
Acquisition of sodium by rats: Interaction of innate mechanisms and latent learning.
Krieckhaus, E. E., & Wolf, G. (1968) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0025547 · Cited by 138 · see citing works
Synaptic plasticity in the mesolimbic dopamine system
Thomas, M. J., & Malenka, R. C. (2003) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1236 · Cited by 137 · see citing works
Excitability of Dopamine Neurons: Modulation and Physiological Consequences
White, F., Hu, X., Marinelli, M., & Rudick, C. N. (2006) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/187152706784111542 · Cited by 136 · see citing works
Taste responses in the nucleus tractus solitarius of sodium‐deprived rats.
Jacobs, K. M., Mark, G. P., & Scott, T. R. (1988) · The Journal of Physiology · doi:10.1113/jphysiol.1988.sp017387 · Cited by 132 · see citing works
Changes in gustatory nerve discharges with sodium deficiency: a single unit analysis
Contreras, R. J. (1977) · Brain Research · doi:10.1016/0006-8993(77)90162-7 · Cited by 131 · see citing works
Central gustatory lesions: II. Effects on sodium appetite, taste aversion learning, and feeding behaviors.
Flynn, F. W., Grill, H. J., Schulkin, J. A., et al. (1991) · Behavioral Neuroscience · doi:10.1037/0735-7044.105.6.944 · Cited by 124 · see citing works
Salt appetite is enhanced by one prior episode of sodium depletion in the rat.
Sakai, R. R., Fine, W. B., Epstein, A. N., et al. (1987) · Behavioral Neuroscience · doi:10.1037/0735-7044.101.5.724 · Cited by 122 · see citing works
The amygdala: Site of genomic and nongenomic arousal of aldosterone-induced sodium intake
Sakai, R. R., McEwen, B. S., Fluharty, S. J., & Ma, L. Y. (2000) · Kidney International · doi:10.1046/j.1523-1755.2000.00972.x · Cited by 120 · see citing works
Aldosterone-sensitive neurons in the nucleus of the solitary tract: Efferent projections
Geerling, J. C., & Loewy, A. D. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20993 · Cited by 111 · see citing works
Salt taste discrimination after bilateral section of the chorda tympani or glossopharyngeal nerves
Spector, A. C., & Grill, H. J. (1992) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1992.263.1.r169 · Cited by 110 · see citing works
Induction of a Salt Appetite Alters Dendritic Morphology in Nucleus Accumbens and Sensitizes Rats to Amphetamine
Roitman, M. F., Na, E. S., Anderson, G., Jones, T. A., & Bernstein, I. L. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-11-j0001.2002 · Cited by 107 · see citing works
The Extended Amygdala and Salt Appetite
Johnson, A. K., de Olmos, J. S., Pastuskovas, C. V., Zardetto‐Smith, A. M., & Vivas, L. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb09272.x · Cited by 101 · see citing works
The biopsychology of salt hunger and sodium deficiency
Hurley, S. W., & Johnson, A. K. (2015) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-014-1676-y · Cited by 88 · see citing works
Body fluid homeostasis in congestive heart failure and cirrhosis with ascites
Skorecki, K. L., & Brenner, B. M. (1982) · The American Journal of Medicine · doi:10.1016/0002-9343(82)90824-5 · Cited by 88 · see citing works
Ghrelin regulates phasic dopamine and nucleus accumbens signaling evoked by food‐predictive stimuli
Cone, J. J., Roitman, J. D., & Roitman, M. F. (2015) · Journal of Neurochemistry · doi:10.1111/jnc.13080 · Cited by 85 · see citing works
Hedonic and nucleus accumbens neural responses to a natural reward are regulated by aversive conditioningPreprint
Roitman, M. F., Wheeler, R. A., Tiesinga, P. H. E., Roitman, J. D., & Carelli, R. M. (2010) · Learning & Memory · doi:10.17615/f90b-8s20 · Cited by 81 · see citing works
Food Restriction Increases Glutamate Receptor-Mediated Burst Firing of Dopamine Neurons
Branch, S. Y., Goertz, R. B., Sharpe, A. L., Pierce, J., Roy, S., Ko, D., Paladini, C. A., & Beckstead, M. J. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5099-12.2013 · Cited by 81 · see citing works
The taste of table salt
Roper, S. D. (2015) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-014-1683-z · Cited by 80 · see citing works
Physiological state gates acquisition and expression of mesolimbic reward prediction signals
Cone, J. J., Fortin, S. M., McHenry, J. A., Stuber, G. D., McCutcheon, J. E., & Roitman, M. F. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1519643113 · Cited by 79 · see citing works
Sodium homeostasis in chronic decerebrate rats.
Grill, H. J., Schulkin, J. A., & Flynn, F. W. (1986) · Behavioral Neuroscience · doi:10.1037//0735-7044.100.4.536 · Cited by 67 · see citing works
Dependence of adrenalectomy-induced sodium appetite on the action of angiotensin II in the brain of the rat.
Sakai, R. R., & Epstein, A. N. (1990) · Behavioral Neuroscience · doi:10.1037/0735-7044.104.1.167 · Cited by 66 · see citing works
Lesions of the central nucleus of the amygdala II: Effects on intraoral NaCl intake
Seeley, R. J., Galaverna, O., Schulkin, J. A., Epstein, A. N., & Grill, H. J. (1993) · Behavioural Brain Research · doi:10.1016/0166-4328(93)90147-i · Cited by 61 · see citing works
Leptin Signaling in the Medial Nucleus Tractus Solitarius Reduces Food Seeking and Willingness to Work for Food
Kanoski, S. E., Alhadeff, A. L., Fortin, S. M., Gilbert, J. R., & Grill, H. J. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.235 · Cited by 61 · see citing works
Richter and sodium appetite: from adrenalectomy to molecular biology
Krause, E. G., & Sakai, R. R. (2007) · Appetite · doi:10.1016/j.appet.2007.01.015 · Cited by 54 · see citing works
Nucleus accumbens shell, but not core, tracks motivational value of salt
Loriaux, A. L., Roitman, J. D., & Roitman, M. F. (2011) · Journal of Neurophysiology · doi:10.1152/jn.00153.2011 · Cited by 54 · see citing works
Immediate acceptance of sodium salts by sodium deficient rats
Handal, P. J. (1965) · Psychonomic Science · doi:10.3758/bf03343156 · Cited by 54 · see citing works
FoxP2 expression defines dorsolateral pontine neurons activated by sodium deprivation
Geerling, J. C., Stein, M. K., Miller, R. L., Shin, J.-W., Gray, P. A., & Loewy, A. D. (2010) · Brain Research · doi:10.1016/j.brainres.2010.11.028 · Cited by 52 · see citing works
FoxP2 brainstem neurons project to sodium appetite regulatory sites
Shin, J.-W., Geerling, J. C., Stein, M. K., Miller, R. L., & Loewy, A. D. (2011) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2011.05.003 · Cited by 51 · see citing works
Sodium homeostasis in chronic decerebrate rats.
Grill, H. J., Schulkin, J. A., & Flynn, F. W. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.4.536 · Cited by 51 · see citing works
Amiloride-sensitive sodium signals and salt appetite: multiple gustatory pathways
Roitman, M. F., & Bernstein, I. L. (1999) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1999.276.6.r1732 · Cited by 50 · see citing works
Dopamine and sodium appetite: Antagonists suppress sham drinking of NaC1 solutions in the rat.
Roitman, M. F., Schafe, G. E., Thiele, T. E., & Bernstein, I. L. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.3.606 · Cited by 49 · see citing works
Sodium depletion and aldosterone decrease dopamine transporter activity in nucleus accumbens but not striatum
Roitman, M. F., Patterson, T. A., Sakai, R. R., Bernstein, I. L., & Figlewicz, D. P. (1999) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1999.276.5.r1339 · Cited by 46 · see citing works
Sensitization of salt appetite is associated with increased "wanting" but not "liking" of a salt reward in the sodium-deplete rat.
Clark, J. J., & Bernstein, I. L. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.1.206 · Cited by 45 · see citing works
Disorders of Sodium and Water Balance
Harring, T. R., Deal, N., & Kuo, D. C. (2014) · Emergency Medicine Clinics of North America · doi:10.1016/j.emc.2014.01.001 · Cited by 43 · see citing works
Reciprocal cross-sensitization between amphetamine and salt appetite
Clark, J. J., & Bernstein, I. L. (2004) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2004.05.002 · Cited by 43 · see citing works
Bilateral dopaminergic lesions in the ventral tegmental area of rats influence sucrose intake, but not umami and amino acid intake
Shibata, R., Kameishi, M., Kondoh, T., & Torii, K. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.01.002 · Cited by 41 · see citing works
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Fortin, S. M., Cone, J. J., Ng-Evans, S., McCutcheon, J. E., & Roitman, M. F. (2015) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0725s70 · Cited by 40 · see citing works
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Wolf, G. (1967) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1967.213.6.1433 · Cited by 39 · see citing works
Salt Appetite in Salt-Replete Rats: Involvement of Mesolimbic Structures in Deoxycorticosterone-Induced Salt Craving Behavior
Lucas, L., Pompei, P., & McEwen, B. S. (2000) · Neuroendocrinology · doi:10.1159/000054559 · Cited by 38 · see citing works
Dopamine and sodium appetite: Antagonists suppress sham drinking of NaCl solutions in the rat.
Roitman, M. F., Schafe, G. E., Thiele, T. E., & Bernstein, I. L. (1997) · Behavioral Neuroscience · doi:10.1037/0735-7044.111.3.606 · Cited by 37 · see citing works
Role of experience in relationship between sodium deficiency and rate of bar pressing for salt.
Quartermain, D., Miller, N. E., & Wolf, G. (1967) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0024611 · Cited by 36 · see citing works
Salt Appetite in Sodium-Depleted or Sodium-Replete Conditions: Possible Role of Opioid Receptors
Lucas, L., Grillo, C. A., & McEwen, B. S. (2007) · Neuroendocrinology · doi:10.1159/000102536 · Cited by 33 · see citing works
Local inputs to aldosterone-sensitive neurons of the nucleus tractus solitarius
Sequeira, S. M., Geerling, J. C., & Loewy, A. D. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.05.059 · Cited by 32 · see citing works
Sodium appetite in the sham-drinking rat after chorda tympani nerve transection
Frankmann, S. P., Sollars, S. I., & Bernstein, I. L. (1996) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1996.271.2.r339 · Cited by 30 · see citing works
Neurotransmitter Transporters: Target for Endocrine Regulation
Figlewicz, D. P., Patterson, T. A., Zavosh, A., Brot, M. D., Roitman, M. F., & Szot, P. (1999) · Hormone and Metabolic Research · doi:10.1055/s-2007-978749 · Cited by 30 · see citing works
Area postrema projects to FoxP2 neurons of the pre-locus coeruleus and parabrachial nuclei: Brainstem sites implicated in sodium appetite regulation
Stein, M. K., & Loewy, A. D. (2010) · Brain Research · doi:10.1016/j.brainres.2010.08.085 · Cited by 26 · see citing works
Appetitive changes during salt deprivation are paralleled by widespread neuronal adaptations in nucleus accumbens, lateral hypothalamus, and central amygdala
Tandon, S., Simon, S. A., & Nicolelis, M. A. L. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00236.2012 · Cited by 20 · see citing works
Anion Size Does Not Compromise Sodium Recognition by Rats After Acute Sodium Depletion.
Geran, L. C., & Spector, A. C. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.1.178 · Cited by 19 · see citing works
Low-dose furosemide modulates taste responses in the nucleus of the solitary tract of the rat
Cho, Y. K., Smith, M. E., & Norgren, R. (2004) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00090.2004 · Cited by 18 · see citing works
Running to the taste of salt in mineralocorticoid-treated rats
Schulkin, J. A. (1985) · Hormones and Behavior · doi:10.1016/0018-506x(85)90038-8 · Cited by 17 · see citing works
Differential changes in central monoaminergic metabolism during first and multiple sodium depletions in rats
Frankmann, S. P., Broder, L., Dokko, J. H., & Smith, G. P. (1994) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(94)90167-8 · Cited by 15 · see citing works
Gastric afferents project to the aldosterone-sensitive HSD2 neurons of the NTS
Shin, J.-W., & Loewy, A. D. (2009) · Brain Research · doi:10.1016/j.brainres.2009.08.098 · Cited by 12 · see citing works
Parabrachial lesions in rats disrupt sodium appetite induced by furosemide but not by calcium deprivation
Grigson, P. S., Colechio, E. M., Power, M. L., Schulkin, J. A., & Norgren, R. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.11.070 · Cited by 4 · see citing works
Differential effects of mineralocorticoid and angiotensin II on incentive and mesolimbic activity
Grafe, L. A., & Flanagan‐Cato, L. M. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.12.002 · Cited by 4 · see citing works

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Hulme, O., Morville, T., & Gutkin, B. (2019) · Physics of Life Reviews · doi:10.1016/j.plrev.2019.07.005 · Cited by 30 · see citing works
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Salt Taste, Nutrition, and Health
(2020) · MDPI eBooks · doi:10.3390/books978-3-03936-466-4

Authors: Fortin, S. M., & Roitman, M. F.
Affiliations: University of Illinois Chicago (US)
Corresponding author: Roitman, Mitchell F.
ORCID: Fortin, Samantha M.
Roitman, Mitchell F.
Venue: Physiology & Behavior
Publisher: Elsevier BV
Published: 2017-09
Volume: 178
Pages: 21-27
ISSN: 0031-9384 (ISSN-L)
DOI: 10.1016/j.physbeh.2016.11.021
PMC: PMC5777138
OpenAlex: W2550322372
Cited by: 11
References: 105
Citations by year: 2026: 1 · 2023: 1 · 2020: 4 · 2019: 1 · 2018: 4
FWCI: 0.18
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Physiology & Behavior (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute on Drug Abuse (R01DA025634)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
Keywords: sodium appetite, sodium deficiency, mesolimbic system, fluid homeostasis, dopamine, nucleus accumbens, sodium taste, reward, reinforcement, motivated behavior
MeSH terms: Animals, Appetite, Humans, Limbic System, Sodium, Dietary, Water-Electrolyte Balance

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Physiological state tunes mesolimbic signaling: lessons from sodium appetite and inspiration from Randall R. Sakai

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