Ask a Neuroscientist: Fear, Reward and the Decision Making Tug-of-War

Photo of a snake pit from the Disney Indiana Jones ride
© 2008 Joe Penniston CC BY-NC-ND 2.0

Mike asks:

"If neurons are the driving force behind thoughts, actions and emotions, is it simply the case people lean towards one decision over another when more neurons are activated in a particular brain region? 

For example, let's say someone was deathly afraid of snakes and given an opportunity to walk through a snake enclosure. The fear response would be "no" and easy to decide. Conversely, if the same person was offered a winning lottery ticket worth a million dollars, their response would likely be "yes". 

My question centers around what happens when someone is faced with a decision that both greatly terrifies them and [also is] something they really want? What causes the brain to lean more towards fear or reward? Are more neurons firing in one region of the brain more than others, or is something else going on?"

Mike, that’s a great question that gets at some of the most fundamental puzzles in the neuroscience of decision making. We live most of our lives poised between the carrot of desire and whip of fear, but how do our brains balance these great motivators? How do you determine that your desire for another donut is less than your fear of appearing gluttonous, or that your fear of public speaking is no match for your desire for applause? In the specific scenario you asked about, our ophidiophobic protagonist is offered a million dollars to walk through a terrifying snake enclosure. How is fear balanced against desire to make this decision? And what goes on in the brain as it is made?

Well, for starters, we know that the brain has separate centers specialized in processing fearful and rewarding experiences. Decades of research have shown that a deep brain region called the amygdala is crucial for learning to recognize and respond to frightening stimuli, while another area called the nucleus accumbens is at the center of brain’s reward system, which uses the neurotransmitter dopamine to reinforce actions that lead to positive outcomes. Together, these systems work to steer you away from danger and lure you towards pleasurable activities (not just the obvious drugs, sex & rock’n’roll type of pleasures, but also more elevated experiences like bonding with friends over a beer, getting kudos from your boss, or hearing a friend tell you you look fantastic today). 

Both of these brain systems are powerful drivers of behavior, and we have them in common with many other creatures. They evolved to keep animals safe and healthy, and they generally do their jobs well. So to some extent, your decision about whether to face the hall of snakes is going to be related to how intensely the prospect of a stroll among the serpents activates your amygdala vs. how excited your nucleus accumbens gets when you think about the million dollar prize.

Image of the pathways for rewarding stimuli in the brain

However, this isn’t the whole story. We (meaning humans and other primates) are also endowed with advanced “executive” brain regions, centered in the prefrontal cortex, that weigh experience, context, objectives and values along with emotional factors. The PFC circuitry can inhibit us from acting out of instinctive desires (like resisting the impulse to reach for a cookie straight out of the oven) or fears (like keeping yourself from flinching when you get a shot at the doctor’s office) when we know such actions would be inappropriate. (You may not be surprised to learn that the PFC’s ability to inhibit impulsive behavior is one of the brain functions particularly impaired by alcohol consumption.)  *

So when you are deciding whether to brave the hall of snakes, your prefrontal cortex is going to be involved in trying to temper your fear of the snakes and evaluate your excitement about the money you may gain. These circuits can take into account whether the snakes are behind glass and ask whether you’re sure that $1 million check is for real. Is the fear you’re feeling justified? What’s the real risk, and what’s the real payoff? Are there people watching who will judge you for not taking the risk?

Okay, so you have executive brain systems centered in the prefrontal cortex that play an important role in decision making by evaluating competing emotional motivations and the specific context of the decision. But your original question was not just where do we make decisions (with what part of the brain), but how do we make decisions – how does the firing of neurons actually take fear and desire into account to produce a decisive choice among different possible actions? 

This is a challenging question that neuroscientists are still struggling to answer, in part because the number of variables influencing most decisions is very large and difficult to control in scientific studies. As with any active and exciting area of research, the partial answers and tentative theories that scientists are exploring now may well be proven wrong in a few years. Still, to satisfy your curiosity, let me tell you one of these current theories, which is based on a number of experiments where researchers recorded the activity of neurons in monkeys trained to make very simple types of decisions. These studies suggest that big groups of hundreds or thousands of neurons in the PFC and other executive regions represent competing choices in the patterns of their electrical activity. As evidence accumulates in favor of a particular decision, that pattern of activity will eventually “win out” over the others and the monkey will go ahead and make the corresponding choice. Some recent studies have even been able to decode what decision a monkey is about to make from recordings of these patterns of activity and even detect when the monkey seems to change its mind, as the neurons' activities shift first towards one pattern and then towards another in a sort of neuronal tug of war. **

These experiments involved extremely simple types of decisions about things like the pattern of dots moving on a screen or the frequency of a vibration on the monkey’s fingertip, and so the patterns of neural activity that seemed to represent the monkey’s decision were driven by these sensory inputs alone. In more complex decisions, perhaps brain activity representing memory, values, instincts, and objectives comes together in these decision making centers of the brain and influence the competing patterns of activity representing different potential decisions. In the case of the scenario of snakes vs. cash, the neurons would weigh immediate sensory evidence (how big are the snakes, are they behind glass, how big is the reward), memories of past experience (your first, terrifying encounter with a snake), imagination of the future (all the things you can buy with that cash prize) as well as personal values (be brave! be safe! don’t be foolish! take risks!), to finally settle on one pattern of activity that will set your ultimate actions in motion. ***

I hope this has helped you understand how brain regions responsible for emotional reactions and executive control interact to help guide us to balanced decisions. Your question really brings us to the edge of what we know about the neuroscience of decision making, but as technology and scientific ideas advance, keep an eye out for major new discoveries that will give much better answers to big questions like this in the years to come.


* It’s worth noting that the PFC’s role in decision making not to simply shut down emotional reactions, but more to  adjust their influence according to context (since the cheering that is appropriate at a sporting event is not usually acceptable at a business meeting). In fact, people who have suffered damage to their brains' emotional centers do not become cool, collected decision machines. Instead, they are paralyzed by the simplest choices, presumably because without a fundamental emotional sense of what is “good” and what is “bad,” every infinitesimal detail of a choice seems equally relevant to the decision at hand. 

** These experiments are very difficult to design and interpret, partly because we still don’t have very good techniques for recording the thousands of neurons involved in these kinds of decisions all at once. Instead of looking at the whole picture, researchers have to be content with using statistics and computer modeling to extract meaning from fragments of much larger patterns of brain activity. As technology improves, hopefully scientists will be able to better understand the whole picture of the relationship between neural activity and decisions.

*** Actually, your original focus on extremes of fear and desire brings up one last side note. Most decision making research has focused on very simple choices just because they’re easier to study, so it’s not as clear how the PFC deals with really extreme emotions. Snake phobias are a particularly challenging example. Some researchers think that the fear of snakes (as well as spiders and other creepy-crawlies) may be instinctive, genetically encoded in the amygdala’s fear circuitry, but a paralyzing phobia is probably also connected to some past experience that trained the amygdala to equate the sight of slithering serpents with a sense of immense impending danger. If you’re seriously phobic, seeing a snake can trigger a deer-in-the-headlights frozen paralysis or the overwhelming impulse to run away. These are ancient  defensive responses that kept our ancestors alive, and they’re pretty hard to reason with. The mental paralysis induced by extreme fear may actually override the executive brain, making it impossible to think clearly about the fact that the snakes are safe behind glass or to give your imagination of all the things you could do with that million dollars equal weight against that overpowering dread. But exactly how powerful fear has to be to override the promise of reward? That too waits on the science of tomorrow.

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