Abstract
The homeostatic need for sodium is one of the strongest motivational drives known in animals. Although the brain regions involved in the sensory detection of sodium levels have been mapped relatively well, data about the neural basis of the motivational properties of salt appetite, including a role for midbrain dopamine cells, have been inconclusive. Here, we employed a combination of fiber photometry, behavioral pharmacology and c-Fos immunohistochemistry to study the involvement of the mesocorticolimbic dopamine system in salt appetite in rats. We observed that sodium deficiency affected the responses of dopaminergic midbrain neurons to salt tasting, suggesting that these neurons encode appetitive properties of sodium. We further observed a significant reduction in the consumption of salt after pharmacological inactivation of the nucleus accumbens (but not the medial prefrontal cortex), and microstructure analysis of licking behavior suggested that this was due to decreased motivation for, but not appreciation of salt. However, this was not dependent on dopaminergic neurotransmission in that area, as infusion of a dopamine receptor antagonist into the nucleus accumbens did not alter salt appetite. We conclude that the nucleus accumbens, but not medial prefrontal cortex, is important for the behavioral expression of salt appetite by mediating its motivational component, but that the switch in salt appreciation after sodium depletion, although detected by midbrain dopamine neurons, must arise from other areas.
Highlights
In order to obtain all nutrients necessary for survival, organisms need to make adaptive food choices based on their homeostatic needs[1,2]
In an attempt to substantiate the findings of ref.[22], that showed that sodium deprivation did not change baseline activity of ventral tegmental area (VTA) DA neurons, we analyzed c-Fos immunoreactivity in a coronal slice of the midbrain that included the VTA and substantia nigra (Fig. 1a; n = 21)
Region-of-interest analysis showed no significant differences in the number of c-Fos positive cells in the VTA (Fig. 1c), the substantia nigra pars compacta (SNc; Fig. 1d), or the substantia nigra pars reticulata (SNr; Fig. 1e)
Summary
In order to obtain all nutrients necessary for survival, organisms need to make adaptive food choices based on their homeostatic needs[1,2]. A remarkable observation that illustrates the innate drive for sodium is that rats normally experience a hypertonic sodium solution as aversive, but that this solution is experienced as positive and consumed in high amounts when rats are low on sodium, a phenomenon known as salt appetite[4,5,8,9] Such a switch in the experience of a flavor from aversive to appetitive, driven by a homeostatic need, is a prime example of how adaptive the interaction between sensory and reward systems can be in order to maintain homeostasis and ensure survival. Given its role in processing rewarding and aversive stimuli[14,15], a logical candidate for the mediation of salt appetite is the mesocorticolimbic dopamine (DA) system, consisting of DA neurons in the ventral tegmental area (VTA) projecting to the nucleus accumbens (NAc) and medial prefrontal cortex (mPFC). We hypothesized that VTA DA neurons may respond differently to salty solutions during a normal versus sodium-depleted state, and that these changes in DA cell responsiveness are important for the expression of behaviors associated with salt appetite
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