The Neuroscience of Feeling Surprised by Unpredictability

Two new studies shed light on how the brain responds to being surprised.

Posted Nov 26, 2020

Christian Dorn/Pixabay
Source: Christian Dorn/Pixabay

Over the past year, numerous Psychology Today blog posts (here, here, here) and countless memes have framed the predictable monotony of day-to-day life during COVID-19 quarantines and stay-at-home advisories through the lens of Bill Murray's plight in the 1993 movie Groundhog Day. Surely, you've experienced the mind-numbing boredom that accompanies the predictability of a humdrum daily routine that doesn't offer any surprises.

What's happening in the brain when everything becomes predictable in a 'Groundhog Day' way versus times when the brain is surprised by something unexpected? Two new (and very different) studies help to answer this question.

Brainwave Frequencies Downplay What's Predictable and Highlight Unpredictability 

The first study (Bastos et al., 2020) led by neuroscientists at MIT shows how the feedforward and feedback flow of different brainwave frequencies allows the brain to spotlight what's surprising and downplay what's predictable. This research in monkeys suggests that predictability and unpredictability may be reflected in specific brainwave rhythms and "predictive routing." These findings were published on Nov. 23 in Proceedings of the National Academy of Sciences.

The human and nonhuman primate brain continuously scan the environment for novel stimuli and quickly identify sensory inputs that deviate from predictions (i.e., prediction errors). To pinpoint how this works, MIT researchers from Earl Miller's Lab at The Picower Institute for Learning and Memory had monkeys perform a working memory task with changing stimulus predictability. At the same time, the neural spikes and oscillations in various cortical areas were recorded.

The researchers found that "predictability modulated the patterns of feedforward/feedback flow, cortical layers, and oscillations used to process a visual stimulus."

More specifically, Bastos et al. found that predictability enhanced alpha (8 to 14 Hz) or beta (15 to 30 Hz) brainwave power in all of the cortical areas they monitored during stimulus processing. On the flip side, unpredictable stimuli were "associated with increases in spiking and in gamma-band (40 to 90 Hz) power/connectivity that fed forward up the cortical hierarchy via superficial-layer cortex." These findings led to the coining of a new theoretical framework they call "predictive routing."

"Our results suggest a hierarchical layer and frequency-specific framework for top-down vs. bottom-up processing related to stimulus predictability. We interpret the results in a framework we call predictive routing," the authors explain. "Together, these results suggest that predictive coding may stem from rhythmic interactions between lower frequency rhythms in deep cortical layers that signal predictions and inhibit the superficial-layer gamma and spiking in the sensory pathways that match those predictions."

"The key element of this new model is that prediction can be accomplished by selectively inhibiting routes of information flow that carry predictable information," lead author André Bastos said in a news release

"Our paper shows that predictive coding can work without specialized circuits for detecting mismatches between predictions and reality," senior author Earl Miller added. "These interactions between beta and gamma are happening all over the cortex. And it's not generic—it targets the processing of specific stimuli."

Nina Garman/Pixabay
Source: Nina Garman/Pixabay

Surprise Widens Pupils, Activates Dopamine-Related Brain Regions, and Boosts Long-Term Memory

The second recent surprise vs. predictability study (Antony et al., 2020) by neuroscientists at Princeton University shows how being surprised is associated with unique neural signatures indexed by pupil dilation, activation of subcortical dopamine-related brain regions, reinforced learning, and more vivid long-term memories. These findings were published on Nov. 25 in the journal Neuron.

"As events in the world unfold, the brain rapidly adjusts its predictions of what will happen next. Of course, our predictions are not always correct—and when they are inaccurate, we often experience surprise (i.e., unsigned prediction error)," the authors explain. "Surprise is theorized to be critical for learning and memory, updating our beliefs about the structure of the world, and demarcating events in the continuous flow of time."

For this research, lead author James Antony and his Princeton Neuroscience Institute colleagues investigated the neural signatures of surprise by observing twenty self-identified basketball fans as each person watched the last five minutes of nine different NCAA March Madness games from 2012. Older basketball games were chosen to increase the odds that study participants (mostly undergraduate students) wouldn't have seen the plays or know what to expect.

As participants watched each basketball game's finale, neural activity was monitored via fMRI and pupil diameter was measured using eye-tracking technology.

"Watching sports is a great paradigm for perception and prediction of events because these predictions are quantifiable," Antony said in a news release. "Also, although sports are not relevant for survival, they tap into deep human nature in terms of excitement and social bonding."

Surprise also correlates with subjective enjoyment and a sense of reward. "Casual fans typically prefer games with high uncertainty and surprise to combat boredom. In many circumstances, subjects find tasks to be less boring when events are not perfectly predictable," the authors note. "Moreover, although people typically prefer certainty about outcomes that are instrumental for survival, in domains with non-instrumental information, such as narratives, music, and sports, people tend to prefer violations of their expectations, suggesting that surprise is often a rewarding affective experience."

During moments of surprise, the researchers observed notable brain activity changes in the prefrontal cortex accompanied by pupil dilation, which indicates a surge of activity in dopamine-related reward centers.

"We speculate that similar latent belief states underlie people's responses to real-world events in other domains, including fiction, film, and the news—people are elated (or dismayed) in proportion to their surprise at breaking-news stories or sudden narrative swings and are more likely to consume exciting forms of media with many twists and turns," Antony et al. conclude. "Moreover, people's longest-lasting memories are formed in precisely those moments when their beliefs substantially shift. Future studies should continue to leverage naturalistic stimuli with quantifiable latent variables to investigate how humans respond to their ever-changing world."

References

André M. Bastos, Mikael Lundqvist, Ayan S. Waite, View ORCID ProfileNancy Kopell, and Earl K. Miller. "Layer and Rhythm Specificity for Predictive Routing." PNAS (First published: November 23, 2020) DOI: 10.1073/pnas.2014868117

James W. Antony, Thomas H. Hartshorne, Ken Pomeroy, Todd M. Gureckis, Uri Hasson, Samuel D. McDougle, Kenneth A. Norman. "Behavioral, Physiological, and Neural Signatures of Surprise during Naturalistic Sports Viewing." Neuron (First published: November 25, 2020) DOI: 10.1016/j.neuron.2020.10.029