While many studies have investigated the neuroscience behind how an animal learns to achieve a goal, such as obtaining water when thirsty, none have understood how animals choose between a number of competing needs – until now.

A study, published Sept. 27 in the journal Nature, used advanced techniques developed by the researchers to track the brain’s dopamine reward system and found – for the first time ­– this system flexibly retunes toward the most important goal when faced with multiple competing needs.

In the study, when a lonely and thirsty male zebra finch encountered a female, his thirst waned and he instead focused his attention on her, a shift reflected in the dopamine system. 

Along with expanding our understanding of how dopamine neurons and pathways influence complex behavior, the finding may also inform the development of new artificial intelligence designs that mimic neural networks and dopamine reward systems.

“What we did that was new to my knowledge, is we were less interested in how an animal achieves a given objective and more interested in what happens when multiple objectives are on the table,” said Jesse Goldberg, associate professor of neurobiology and behavior and Robert R. Capranica Fellow in the College of Arts and Sciences and senior author of the study. Andrea Roeser, Ph.D. ‘23 and Vikram Gadagkar, Ph.D. ‘13, a former postdoctoral researcher, both past members of Goldberg’s lab, are co-first authors.

For more than a century, researchers have been studying relationships between dopamine and learning. Dopamine neurons fire in response to rewards meeting diverse needs such as hunger, thirst, loneliness, language, and song learning, to name a few. Upon receiving a reward, such as water when thirsty, dopamine neurons exhibit a burst in activity. All drugs of addiction work through this system, Goldberg said. In Parkinson’s disease, dopamine neurons lose their function.

Previous research in Goldberg’s lab found that when young zebra finches learn songs, dopamine neurons fire when the birds unexpectedly hit the right note, and the neurons are suppressed when they are disappointed by hitting a bad note.

“The problem that bothered me after that discovery was: How can a bird use the same system and same learning signals for singing when it also wants to get food?” Goldberg said. “It seemed that this single system was being asked to do too much.”

In the current study, Roeser developed a technique using optical recording methods and an engineered virus. Genes in the virus drove the expression of fluorescent dopamine sensors, such that the tissue fluoresced in proportion to dopamine levels. Optical fibers placed in the brain were then able to measure dopamine levels rising and falling as birds sang songs, courted females, and drank water. While a previous system using electrodes let researchers measure dopamine signals for up to 30 minutes, this new method allowed them to measure neuron activity for up to four hours straight over weeks.

“It was a key technical advance that enabled the discovery,” Goldberg said.

In experiments, Goldberg and colleagues isolated male zebra finches, which are social animals, and also made them thirsty. The male had been trained to recognize that a flashing light meant it could peck a spout and get a drink, and when the bird was alone, the cue triggered both a large dopamine signal and water retrieval. But when the female was added to the cage, the male ignored the cue and the dopamine signal ceased.

“It’s kind of intuitive, but hadn’t explicitly been shown before, that courtship reduces the need for thirst,” Goldberg said. “And that’s important because in a complex and natural environment priorities change as new opportunities arise.” The shift was reflected in both the bird’s behavior and in the dopamine signal, he said.

During courtship the male sings to impress the female, and the researchers wondered how the dopamine system might respond to the male’s evaluation of his own song, where stakes are higher in order to impress the female. Surprisingly, they found that the male’s dopamine system for evaluating his own song was turned off, as was his water reward signal.

The authors then hypothesized that maybe the dopamine system was retuning as the animal shifted its attention to the female’s behavior. And they found that, indeed, when females called back in response to singing males, big activations were observed in the specific part of the male’s dopamine system dedicated to social communication. “Both thirst and self-evaluation associated dopamine signals were turned off during courtship, and instead, that same signal was driven by her positive feedback,” Goldberg said.

Goldberg hypothesizes that females are giving males cues for what she likes during courtship singing. And over the course of an courtship period with multiple males, the female may be able to determine which male adopts her advice on what works. “On the basis of that type of interaction she could suss out not just his fitness but his commitment, specifically to her,” Goldberg said.       

These learning centers of the brain dynamically retune on moment by moment timescales, as an animal changes its priorities in response to new opportunities in the environment, Goldberg said.

The study was funded by the National Institutes of Health.     

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