Not what U expect: Effects of Prediction Errors on Episodic Memory.

The characterization of the relationship between predictions and one-shot episodic encoding poses an important challenge for memory research. On the one hand, events that are compatible with our previous knowledge are thought to be remembered better than incompatible ones. On the other hand, unexpected situations, by virtue of their surprise, are known to cause enhanced learning. Several theoretical accounts try to solve this apparent paradox by conceptualizing prediction error (PE) as a continuum ranging from low PE (for expectation matching events) to high PE (for expectation mismatching ones). Under such framework, the relationship between PE and memory encoding would be described by a U-shape function with higher memory performance for extreme levels of PE and lower memory for middle levels of PE. In this study we used a gradual manipulation of the strength of association between scenes and objects to render different levels of PE and then tested for episodic memory of the (mis)matching events. In two experiments, and in contrast to what was anticipated, recognition memory as a function of PE followed an inverted U-shape, with higher performance for intermediate levels of PE. Furthermore, in two additional experiments we showed the relevance of explicit predictions at encoding to reveal such inverted U pattern, thus providing the boundary conditions of the effect. We discuss our current findings in the light of the uncertainty in the environment and the importance of the operations underlying encoding tasks.

Neural Mechanisms of Learning are Critically Dependent on Sleep

Sleep supports memory consolidation as well as next-day learning. The Active Systems account of offline consolidation suggests that sleep-associated memory processing paves the way for new learning, but empirical evidence in support of this idea is scarce. Using a within-subjects, crossover design, we assessed behavioural and electrophysiological indices of episodic encoding after a night of sleep or total sleep deprivation in healthy adult humans (aged 18-25 years), and investigated whether the behavioural measures were predicted by the overnight consolidation of episodic associations formed the previous day. Sleep supported memory consolidation and next-day learning, as compared to sleep deprivation. However, the magnitude of this sleep-associated consolidation benefit did not significantly predict the ability to form novel memories after sleep. Interestingly, sleep deprivation prompted a qualitative change in the neural signature of encoding: whereas 12-20 Hz beta desynchronization - an established EEG marker of successful encoding - was observed after sleep, sleep deprivation disrupted beta desynchrony during successful learning. Taken together, our findings suggest that effective learning mechanisms are critically dependent on sleep, but not necessarily sleep-associated consolidation.

Developmental changes in story-evoked responses in the neocortex and hippocampus

How does the representation of naturalistic life events change with age? Here we analyzed fMRI data from 415 children and adolescents (5 - 19 years) as they watched a narrative movie. In addition to changes in the degree of inter-subject correlation (ISC) with age in sensory and medial parietal regions, we used a novel measure (between-groups ISC) to reveal age-related shifts in the responses across the majority of the neocortex. Over the course of development, brain responses became more discretized into stable and coherent events, and shifted earlier in time to anticipate upcoming event transitions. However, hippocampal responses to event boundaries actually decreased with age, suggesting a shifting division of labor between episodic encoding processes and schematic event representations between the ages of 5 and 19.

The hippocampus shows an own-age bias during unfamiliar face viewing

The present study investigated the neural correlates of the own-age bias for face recognition in a repetition suppression paradigm. Healthy young and older adults viewed upright and inverted unfamiliar faces. Some of the upright faces were repeated following one of two delays (lag 0 or lag 11). Repetition suppression effects were observed in bilateral fusiform cortex, with no evidence of an own-age bias. By contrast, the right anterior hippocampus showed an own-age bias (greater activity for own- than other-age faces) when viewing an unfamiliar face for the first time. Given the importance of the hippocampus to episodic memory encoding, we conjecture that the increased hippocampal activity for own-age relative to other-age faces reflects differential engagement of neural processes supporting the episodic encoding of faces and might provide insight into the processes giving rise to own-age biases in face recognition memory.

Statistical prediction of the future impairs episodic encoding of the present

Memory is typically thought of as enabling reminiscence about past experiences. However, memory also informs and guides processing of future experiences. These two functions of memory are often at odds: Remembering specific experiences from the past requires storing idiosyncratic properties that define particular moments in space and time, but by definition such properties will not be shared with similar situations in the future and thus may not be applicable to future situations. We discovered that, when faced with this conflict, the brain prioritizes prediction over encoding. Behavioral tests of recognition and source recall showed that items allowing for prediction of what will appear next based on learned regularities were less likely to be encoded into memory. Brain imaging revealed that the hippocampus was responsible for this interference between statistical learning and episodic memory. The more that the hippocampus predicted the category of an upcoming item, the worse the current item was encoded. This competition may serve an adaptive purpose, focusing encoding on experiences for which we do not yet have a predictive model.

Dopamine is associated with prioritization of reward-associated memories in Parkinson’s disease

Patients with Parkinson’s disease have reduced reward sensitivity related to dopaminergic neuron loss, which is associated with impairments in reinforcement learning. Increasingly, however, dopamine-dependent reward signals are recognized to play an important role beyond reinforcement learning. In particular, it has been shown that reward signals mediated by dopamine help guide the prioritization of events for long-term memory consolidation. Meanwhile, studies of memory in patients with Parkinson’s disease have focused on overall memory capacity rather than what is versus what isn’t remembered, leaving open questions about the effect of dopamine replacement on the prioritization of memories by reward and the time-dependence of this effect. The current study sought to fill this gap by testing the effect of reward and dopamine on memory in patients with Parkinson’s disease. We tested the effect of dopamine modulation and reward on two forms of long-term memory: episodic memory for neutral objects and memory for stimulus-value associations. We measured both forms of memory in a single task, adapting a standard task of reinforcement learning with incidental episodic encoding events of trial-unique objects. Objects were presented on each trial at the time of feedback, which was either rewarding or not. Memory for the trial-unique images and for the stimulus-value associations, and the influence of reward on both, was tested immediately after learning and 2 days later. We measured performance in Parkinson’s disease patients tested either ON or OFF their dopaminergic medications and in healthy older control subjects. We found that dopamine was associated with a selective enhancement of memory for reward-associated images, but that it did not influence overall memory capacity. Contrary to predictions, this effect did not differ between the immediate and delayed memory tests. We also found that while dopamine had an effect on reward-modulated episodic memory, there was no effect of dopamine on memory for stimulus-value associations. Our results suggest that impaired prioritization of cognitive resource allocation may contribute to the early cognitive deficits of Parkinson’s disease.