Study reframes amygdala as the sophisticated learning arbiter

A Dartmouth study challenges the conventional view that the amygdala-the two-sided structure deep in the brain involved in emotion, learning, and decision making-is simply the brain's primitive "fear center," reflexively driving us to avoid the things we fear, from high places and tight spaces to spiders and large crowds.

The researchers report in Nature Communications that the amygdala is far more complex, acting as a sophisticated arbiter to help the brain choose between competing strategies for learning and decision-making.

"Historically, the amygdala has been studied from the perspective of fear learning, and it has been generalized to reward learning," says Jae Hyung Woo, a PhD candidate in the psychological and brain sciences and the study's first author. "Our main hypothesis was that it must have other functions given its extensive connections to the rest of the brain."

The amygdala's other functions seem to surface under uncertainty, when the brain is faced with two kinds of learning strategies in pursuing a reward. In the study, the researchers give the example of brewing a cup of coffee with an unfamiliar machine.

Under an action-based approach, you could try what you did the last time you operated a similar machine and press the button that worked before. Under a stimulus-based approach, by contrast, you could focus on a defining feature, like the machine's blinking light, and select that feature.

"People have labeled the amygdala as an emotional fear system, but there is nothing really primitive in the brain, even when you talk about this area," says Alireza Soltani, the study's senior author and associate professor of psychological and brain sciences at Dartmouth. 

"The key distinction is whether learning should be tied to a motor action or the identity of the stimulus," Soltani says. "Action-based learning involves considering the specific motor movements that can lead to a reward, while stimulus-based learning can be more flexible because it allows you to evaluate and select a desired stimulus without immediately considering the actions needed to get there."

Because these two learning modes happen simultaneously, the researchers hypothesized that there should be a region in the brain that mediates between them to choose the path most likely to lead to the better outcome. A damaged amygdala appears to disrupt this mediation process, the researchers found, suggesting that it plays this critical role.

The research team developed computational models based on reinforcement learning to track how the brain assigns weight to action and stimulus-based learning strategies when it's unclear which strategy is best-suited for the task. They found that the amygdala pivots between the two systems at the start, but that as it gathers more information, it picks the system with the more reliable model.

When the amygdala was damaged, however, they found that arbitration became more random as the brain struggled to update its assessment of which learning system would be most useful. The brain also tended to default toward action-based learning from the outset, they found, impairing its ability to arbitrate between the two systems. As a result, behavior became more rigid overall.

"A healthy amygdala promotes exploration between alternative models and as a result, can make you choose something you wouldn't otherwise choose, and you can learn from that," Soltani says.

"Ultimately, successful learning involves finding a more reliable model," he says. Their results could help explain why previous studies found that amygdala damage impaired stimulus learning in some cases but improved it in others.

One of the brain's oldest regions, the amygdala is critical for survival by detecting threats in the environment and triggering an immediate response. As the brain evolved, other systems may have connected to it, giving the amygdala a more nuanced and deliberate role in decision making.

"The fact that the amygdala controls so many systems in the brain and has many connections suggests that it's actually doing something more critical than just signaling fear and emotion," Woo says. "We're not saying the amygdala isn't about fear. We're reframing its role as a mediator between multiple learning systems."

The team's findings could have implications for how we treat phobias and other anxiety disorders. Some people handle their fear of spiders by simply avoiding them, showing a bias toward stimulus-learning. "The fear is tied to the stimulus, making the response rigid and difficult to override," says Soltani.

The research suggests that shifting attention away from a fear-provoking stimulus and toward an action-based exploration mode could be more effective. For example, instead of focusing on the spider, and trying to convince yourself it's not so threatening (a stimulus-based approach), you could think about reframing the situation through a set of repeated actions, perhaps placing a cup over the spider and then approaching it.

"In this way, the amygdala, one of the brain's arbitrators, can favor action-based learning, which is a more reliable predictor of the outcome (no harm). This promotes exploration and flexibility, helping to overcome fear even when the stimulus initially carries strong negative associations," says Soltani.

The research team is now analyzing recordings of neural activity in the prefrontal cortex during different tasks to understand how neurons interact during the arbitration process. In collaboration with researchers at UCLA, they're also conducting experiments with rats to examine specific neural pathways between the amygdala and prefrontal cortex.

Woo and Soltani collaborated with researchers at the National Institute of Mental Health.