Scientific Understanding of Consciousness
Hippocampus Association Memory for Decisions
Science 12 October 2012: Vol. 338 no. 6104 pp. 270-273
Preference by Association: How Memory Mechanisms in the Hippocampus Bias Decisions
G. Elliott Wimmer, Daphna Shohamy
Department of Psychology, Columbia University, New York, NY 10027, USA.
Every day people make new choices between alternatives that they have never directly experienced. Yet, such decisions are often made rapidly and confidently. Here, we show that the hippocampus, traditionally known for its role in building long-term declarative memories, enables the spread of value across memories, thereby guiding decisions between new choice options. Using functional brain imaging in humans, we discovered that giving people monetary rewards led to activation of a preestablished network of memories, spreading the positive value of reward to nonrewarded items stored in memory. Later, people were biased to choose these nonrewarded items. This decision bias was predicted by activity in the hippocampus, reactivation of associated memories, and connectivity between memory and reward regions in the brain. These findings explain how choices among new alternatives emerge automatically from the associative mechanisms by which the brain builds memories. Further, our findings demonstrate a previously unknown role for the hippocampus in value-based decisions.
Decisions are sometimes guided by direct past experience: If a choice led to a good outcome in the past, people are likely to make that same choice again. This process is known to depend on reward learning mechanisms in the striatum. But frequently in life, we have to decide between options we have never considered before. It has been suggested that such decisions could be guided by associative memory, however, surprisingly little is known about how this process happens.
We investigated the mechanism by which neural circuits for memory modulate value and guide decisions about new choice options. Our central hypothesis was that the hippocampus enables the positive value of reward to spread across associated memories, thereby increasing the value of items that were never rewarded. Specifically, we hypothesized that receiving reward can lead to two simultaneous and interactive processes: (i) the direct learning of stimulus-reward associations in the striatum and (ii) the spread of reward to associated items stored in memory via the hippocampus.
Our hypothesis is grounded in two essential features of how the hippocampus builds memories. First, the hippocampus encodes relationships between items and events that appear together, forming an associative link between them. Second, because of this associative link, when a person later encounters one item, the hippocampus can complete the pattern and automatically reactivate the neural representation of the other item, allowing the integration of old memories with new ones.
We reasoned that these features of memory formation in the hippocampus could provide a mechanism by which reward experiences can systematically change the value of items that were never rewarded: These items gain a positive value merely by association. If so, this mechanism predicts that later, when confronted with a decision, people will be biased to choose items that were never rewarded in the past. By emphasizing the associative nature of processes in the hippocampus, regardless of awareness, this mechanism further predicts that the hippocampus might bias value even when associations are not explicitly remembered.
To test our prediction that reward will spread across associated memories, we used functional magnetic resonance imaging to measure brain responses during a learning and decision task designed to test how associative memory biases decisions between new choice options. First, we had participants (n = 28) build new associative memories by exposing them to regularities between pairs of neutral stimuli. These regularities were encoded incidentally while participants performed a cover task
These results indicate that reward can spread to bias the value of options that were themselves never directly rewarded. This finding provides insight into how people are biased by past experience to make new decisions between options that were never previously rewarded: Networks of associations in memory, formed across many different experiences, can result in the spread of value across associations.
The idea that memory and decision-making are intertwined has deep roots in behavioral theories of both memory and decision-making, yet there has been very little evidence for an underlying mechanism. Understanding the mechanism by which value spreads among related memories in the brain may help to explain why people sometimes develop seemingly ungrounded preferences for or against particular things, places, or people. Although we highlight how transfer of past experience can guide behavior in a changing environment, this same mechanism may also lead to seemingly irrational choices, consistent with social and cognitive theories regarding the role of associative memory in decision-making heuristics.
The finding that the hippocampus supports the spread of value provides several new insights into the neural bases of both memory and decision-making. First, our findings extend the role of the hippocampus beyond memory per se, demonstrating that the hippocampus contributes directly to value assignment and decision-making.
Second, although in humans the hippocampus is traditionally associated with explicit declarative memory, our results indicate that transfer of value by the hippocampus is not driven by conscious awareness. Thus, our results suggest that the hippocampus contributes to an automatic assessment of value, perhaps performing a function similar to Bayesian inference about value.
Finally, though it is known that memory can support decisions by retrieving relevant information at the time of decision-making, our results demonstrate an alternative mechanism whereby the hippocampus dynamically modulates value representations during learning itself. This mechanism allows value to spread and bias decisions without effortful retrieval at the time of decision.
Understanding how associative memory biases decisions provides insight into critical open questions in decision-making research. Although reward learning models have been successfully applied to many aspects of behavior, these models cannot account for the full diversity of animal and human decision-making. The uncovering of a neural mechanism by which associative memory biases decision-making sheds light on how value generalizes across experience, with implications for both adaptive behaviors and maladaptive behaviors such as addiction.
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