The Neurobiology Of Changing Priorities In A Songbird

When a thirsty and lonely male zebra finch changes his mind from getting a drink of water to prioritizing courtship, his dopamine-releasing brain cells reflect his new intensions

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What happens in the brain when we change our mind to refocus our priorities? If people’s brains work like a zebra finch brain (which they seem to), dopamine-releasing brain cells are the secret.

Dopamine is a type of neurotransmitter. It’s made in your brain and acts as a chemical messenger that communicates between brain cells and also between nerve cells in your brain and in other parts of your body. Dopamine is an important player in the “reward center” — it’s often referred to as the “feel-good” hormone because it gives you a sense of pleasure or accomplishment.

Dopamine neurons “fire” by releasing dopamine when a variety of diverse needs are met. Upon receiving a reward, such as a drink of water when thirsty, dopamine neurons show a burst in activity. All drugs of addiction — and junk food too — work through this system in people. In contrast, dopamine neurons lose their function in people with a movement disorder like Parkinson’s disease.

Previous research found that when young male zebra finches, Taeniopygia guttata, learn and practice their songs, their dopamine neurons fire when the bird produces the correct note thereby providing an internal reward signal but their dopamine neurons are suppressed when the bird produces an incorrect note.

“Dopamine seems to function as an internal error signal, helping the bird to realize that it has made a blunder and did not quite replicate the song it had memorized,” said co-lead author of the study, Vikram Gadagkar, an assistant professor of neuroscience at Columbia University’s Zuckerman Institute and an assistant professor of neuroscience at Columbia’s Vagelos College of Physicians and Surgeons.

In songbirds, dopamine neurons respond to rewards from meeting a bird’s many needs such as drinking water or practicing his song, but what happens in a bird’s brain when he changes his mind to pursue a new opportunity?

“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?” said the senior co-author of the study, songbird neurophysiologist Jesse Goldberg, associate professor of neurobiology and behavior and Robert R. Capranica Fellow in the College of Arts and Sciences at Cornell University.

“It seemed that this single system was being asked to do too much.”

To investigate this fundamental question, co-lead author of the new study, Andrea Roeser, developed a cutting-edge methodology for using optical recording and a specially engineered virus to track a bird’s dopamine reward system. Dr Roeser, who was a PhD Candidate in Professor Goldberg’s lab at Cornell when this work was done, designed a system where the virus drove the expression of fluorescent dopamine sensors so the tissue would fluoresce in proportion to dopamine expression levels. Optical fibers placed in the brain measured dopamine levels rising and falling as birds sang, courted females, and drank water. Whilst a previous system using electrodes allowed 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,” Professor Goldberg said.

In this study, Dr Roeser, Professor Gadagkar, Professor Goldberg and collaborators placed male zebra finches, which are social birds, into isolation and made them thirsty. The male had been trained to respond to a flashing light that meant it could peck a water spout to get a drink. When the bird was alone, the light cue triggered both a large dopamine signal and water drinking. But surprisingly, when a female was introduced to the cage, the male ignored the cue and the dopamine signal ceased.

“The males stop worrying about anything else and, for the first time, we have found signs of that re-prioritization in the behavior of specific brain cells,” Professor Gadagkar said.

“It’s kind of intuitive, but hadn’t explicitly been shown before, that courtship reduces the need for thirst,” Professor Goldberg added. “And that’s important because in a complex and natural environment priorities change as new opportunities arise.”

By changing his mind from drinking water to interacting with a female, the lonely male zebra finch’s decision was reflected in his dopamine system, which flexibly retuned toward meeting this most important goal in the face of multiple competing needs.

“Our findings could help explain what our brains are doing when they shift gears as different opportunities arise and as our priorities change,” Professor Gadagkar observed.

Interacting with a female was always the most important priority for a male zebra finch. Dr Roeser, Professor Gadagkar, Professor Goldberg and collaborators found that whenever courtship became part of the mix, replete with the external reward of a female calling in response to the male’s song, the dopamine-based error signals that are linked to seeking water or song rehearsal were suppressed.

“We think this is the first demonstration of a socially driven shift of dopaminergic error signals,” Professor Gadagkar reported. “The big idea here is that your self-evaluation system, which you’re using to learn when you’re practicing, might be dialed down or switched off when you’re performing and your dopamine system instead becomes primed to receiving social feedback.”

But how did these competing choices work? The study found that water reward signals were routed to one particular region of the brain whilst reward signals driven by the presence of a female were routed to a different part of the brain.

“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,” Professor Goldberg explained.

Additionally, dopamine reward signals were driven by female calls that were timed to coincide with the male’s courtship song, leading Professor Goldberg to propose that females are giving males cues for what she likes during courtship singing. During the course of a courtship period with multiple males, the female may be identifying which male adopts her advice.

“On the basis of that type of interaction she could suss out not just his fitness but his commitment, specifically to her,” Professor Goldberg explained.

In addition to expanding our understanding of how dopamine neurons and pathways influence complex behavior, these findings may also inform the development of new artificial intelligence designs that mimic neural networks and dopamine reward systems.

“A big question for us now is whether these systems may be widely at play when it comes to learning many kinds of behaviors, including speaking, singing, playing an instrument and all kinds of behaviors where learning depends on internal self evaluations,” Professor Gadagkar elaborated. “Now, I want to know if this same circuitry might be much more general-purpose than anyone previously had thought.”

Source:

Andrea Roeser and Vikram Gadagkar, Anindita Das, Pavel A. Puzerey, Brian Kardon & Jesse H. Goldberg (2023). Dopaminergic error signals retune to social feedback during courtship, Nature | doi:10.1038/s41586-023-06580-w

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