The simple act of choosing influences declarative memory

Abstract

Individuals value the opportunity to make choices and exert control over their environment. This perceived sense of agency has been shown to have broad influences on cognition, including preference, decision-making, and valuation. However, it is unclear whether perceived control influences memory. Using a combined behavioral and functional magnetic resonance imaging approach, we investigated whether imbuing individuals with a sense of agency over their learning experience influences novel memory encoding. Participants encoded objects during a task that manipulated the opportunity to choose. Critically, unlike previous work on active learning, there was no relationship between individuals' choices and the content of memoranda. Despite this, we found that the opportunity to choose resulted in robust, reliable enhancements in declarative memory. Neuroimaging results revealed that anticipatory activation of the striatum, a region associated with decision-making, valuation, and exploration, correlated with choice-induced memory enhancements in behavior. These memory enhancements were further associated with interactions between the striatum and hippocampus. Specifically, anticipatory signals in the striatum when participants are alerted to the fact that they will have to choose one of two memoranda were associated with encoding success effects in the hippocampus on a trial-by-trial basis. The precedence of the striatal signal in these interactions suggests a modulatory relationship of the striatum over the hippocampus. These findings not only demonstrate enhanced declarative memory when individuals have perceived control over their learning but also support a novel mechanism by which these enhancements emerge. Furthermore, they demonstrate a novel context in which mesolimbic and declarative memory systems interact.

Keywords: agency; choice; fMRI; hippocampus; memory; striatum.

Figure 1.

Overview of the choice encoding task. Participants had to press a button to remove occluder screens and reveal to-be encoded objects. In the choice condition (top), participants were able to decide which occluder screen to remove. In the fixed condition (bottom), participants were instructed to select the red button. Before the encoding phase, a condition cue appeared that informed the upcoming trial type. L, Left; R, right.

Figure 2.

Choice influences declarative memory. At a 24 h test, object recognition was better for old objects presented in the choice compared with the fixed condition. Objects from both conditions were endorsed as old more often than novel foils.

Figure 3.

Cue-evoked striatal activation correlates with choice memory. a, Choice cues were associated with greater left striatal activation compared with fixed cues. b, The striatal activation identified from the choice > fixed cue was used for an across-participants, brain-behavior correlation. Striatal activation to choice cues correlates with later object memory in the choice condition, although there is no relationship between striatal activation to fixed cues and object memory in the fixed condition. This relationship was significantly stronger than the correlation between striatal activation and memory in the fixed condition.

Figure 4.

Encoding-success activations are equivalent across conditions. a, Activations that predicted successful memory encoding during the encoding phase collapsed across conditions. b, Conjunction analysis of activations that predict successful memory encoding during the encoding phase in the choice and fixed conditions, respectively.

Figure 5.

Cue-evoked striatal activation interacts with the hippocampus during successful memory encoding. On a trial-by-trial basis, correlations between cue-evoked activation in the left (L) striatum and encoding-related activation in the right (R) hippocampus was associated with successful memory encoding in the choice, but not fixed, condition. R, Remembered trials; F, forgotten trials.