Adaptive Behavior Without New Learning: Salt Appetite and the Ventral Pallidum
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Material below summarizes the article Optogenetic Inhibition of Ventral Pallidum Neurons Impairs Context-Driven Salt-Seeking, published on May 11, 2017, in JNeurosci and authored by Stephen E. Chang, Elizabeth B. Smedley, Katherine J. Stansfield, Jeffrey J. Stott, and Kyle S. Smith.
Our behavior is strongly influenced by the environmental cues around us. For example, cues associated with rewards, such as food, money, and drugs, can predict the availability of the rewards, and they can also acquire rewarding properties themselves. The acquisition of these cue-triggered behaviors is often considered to be the result of experience with the particular cue and its associated outcome.
However, changes in behavior can also occur without prior experience when physiological needs change.
A striking example of this process is the salt appetite phenomenon. This occurs when animals encounter a new state of bodily salt depletion. In this state, they are able to immediately seek out salt even when it was not very rewarding previously. Importantly, this adaptive salt-seeking behavior occurs before rats have ever tasted salt in the depleted state, and therefore they have never experienced salt as enjoyable. Moreover, the sudden increase in salt-seeking following sodium depletion also occurs to subsequent encounters with salt-paired cues despite never having tasted salt in the sodium-depleted state.
A primary brain region for mediating reward seeking is the ventral pallidum (VP). Neural activity in the VP has been shown to track the changes in value associated with salt and salt-paired cues before and after rats have been depleted of bodily sodium. However, it was not known whether the VP or any brain region was needed for this kind of nutrient seeking under new deprivation states.
To address this question, we used optogenetics to inhibit the VP when rats would normally seek salt. This method allowed us to transiently reduce VP activity during behavior. To assess the level of salt-seeking behavior, we developed a novel conditioned place preference procedure wherein different environmental contexts were learned to contain either salt or sugar.
On separate days, rats were able to enter one of two chambers that contained access to the desirable sugar or the less desirable salt. The sugar- and salt-paired chambers were connected by another chamber that served as the starting point of each training day. Importantly, rats had access to only one of sugar- or salt-paired chambers on each training day.
Following training, rats were given a baseline test session in which they were allowed to freely explore both the sugar- and salt-paired chambers in the absence of sugar or salt. Following re-training, rats were then depleted of bodily sodium by injecting a diuretic (furosemide) and maintained on salt-free food. Now depleted of bodily sodium, rats were given access to both the sugar- and salt-paired chambers in the absence of sugar or salt. During this key test of salt seeking, the VP was inhibited. Subsequently, rats were given another test session identical to the previous test session, except now sugar and salt were made available to consume.
We found a remarkably specific effect: Optogenetically inhibiting the VP reduced the normal elevation in time spent in the salt-paired chamber following sodium depletion. This effect was specific to inhibiting the anterior/central VP, while inhibiting the posterior VP had no effect. Anterior/central VP inhibition had minimal effects, while posterior VP inhibition had no effect on the elevation in salt consumption following sodium depletion once it was made available.
Collectively, these results show that the brain processes mediating deficit-driven reward seeking versus reward consumption to replenish those deficits are neurally dissociable, and that VP activity is particularly critical for the former phenomenon.
In comparison to the large amount of research being conducted on reinforcement learning, which involves iterative updating in predictions of reward based on experience, adaptive reward seeking like salt appetite that occurs in the absence of new learning opportunities has received little attention in neuroscience. Along with the neural activity measures showing how salt seeking is encoded in the VP and other brain areas, these results help set the stage for investigating brain circuits that are needed for adaptive reward seeking to occur.
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Optogenetic Inhibition of Ventral Pallidum Neurons Impairs Context-Driven Salt-Seeking. Stephen E. Chang, Elizabeth B. Smedley, Katherine J. Stansfield, Jeffrey J. Stott and Kyle S. Smith. JNeurosci May 2017 DOI: 10.1523/JNEUROSCI.2968-16.2017