In the face of uncertainty, the brain chooses randomness as the best strategy

Past experience is usually a reliable guide for making decisions, but in unpredictable and challenging situations, it might make more sense to take risks. A study published by Cell Press September 25th in the journal Cell shows that, in competitive situations, rats abandon their normal tactic of using past experience to make decisions and instead make random choices when their competitor is hard to defeat. This switch in strategy is controlled by a dedicated brain circuit, indicating that the brain can actively disengage from its past experiences and enter a random decision-making mode when it provides a competitive edge. These findings may have implications for human disorders such as depression, in which even ordinary decision-making is viewed as ineffective.

"We discovered that animals can get stuck in a random mode of behavior that in a way resembles learned helplessness, which has been linked to depression and is triggered when repeated efforts prove to be ineffective," said senior study author Alla Karpova of the Janelia Farm Research Campus. "Our findings may shed light on the origins of learned helplessness and the associated impairments in strategic decision-making."

The brain has evolved to optimize behavioral choices by using all available information acquired from past experience. However, when animals encounter new and unpredictable situations, such as a novel environment or prey that moves erratically, it might be more beneficial to instead vary behavior randomly.

To find out if this is indeed the case, Karpova and her team trained rats to stick their nose in one of two ports, or holes in a wall, to potentially receive a sugary Kool-Aid reward. Meanwhile, the animals were monitored by a computer-simulated competitor, which was programmed to analyze past behavior to predict future choices. The rats received juice at the port they selected only if their choice differed from that predicted by the computer. When faced with a weak competitor, the animals made choices based on past experience, as usual. But when a sophisticated competitor used complex algorithms to make strong predictions based on subtle behavioral patterns, the rats actively ignored past experience and instead selected the reward port at random.

To find out whether this shift in strategy is regulated by a specific part of the brain, the authors zeroed in on the anterior cingulate cortex, a brain structure involved in using experience to make decisions. Indeed, when the researchers manipulated the activity of neurons that release a stress hormone called norepinephrine into the anterior cingulate cortex, they were able to reverse the rats' behavioral strategies. Stimulation of these neurons caused rats to abandon the experience-based strategy and behave randomly in situations when this was not expected. By contrast, inhibition of norepinephrine release caused rats to rely on the experience-based strategy even when faced with the challenging competitor.

"The findings suggest that changes in activity in the anterior cingulate cortex could prevent erroneous beliefs from guiding decisions and promote exploratory behavior when environmental rules are uncertain," Karpova says. "But sometimes these changes in neural activity can go too far and become maladaptive, resulting in learned helplessness or even depression. In those cases, suppression of norepinephrine release into the anterior cingulate cortex may serve as an effective therapy to restore strategic decision-making."