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In the current study, we are not aware of previous reports of midbrain-hippocampal interactions. However, some data from our lab suggest that midbrain activity predicts spatial pattern typicality in the hippocampus. This prior work showed that midbrain activation patterns predict pattern typicality in the hippocampus, and that midbrain activity in turn predicts hippocampal pattern typicality. The present study extended that work by showing that midbrain activation is associated with hippocampal pattern typicality, and that the effect of midbrain activation on hippocampal pattern typicality accounts for its effect on subsequent memory. The link between midbrain activity and the stability of hippocampal pattern typicality as a mechanism for midbrain modulation of memory is thus supported.
The findings of the current study may provide insight into why midbrain activity is related to subsequent memory. In the current study, we operationalized putative midbrain-hippocampus interactions as patterns of typicality in the hippocampus. This measure captures how much a particular pattern departs from the typical pattern for a given individual and trial, and may be more sensitive to midbrain regulation of memory than the centroid approach typically used in MVPA studies. This measure of convergence offers several possible mechanistic interpretations. First, pattern typicality may reflect the degree to which a state is experienced as novel and thus, perhaps, more disruptive to subsequent memory formation. Prior work suggests that novelty, and more generally, variations in arousal, may alter memory33,34,35,36 and recent work has linked arousal to temporal dynamics of BOLD response in the hippocampus37. Second, pattern typicality may reflect increased efficiency of memory formation. Increased typicality may be associated with decreased deviation from a prototypical pattern, indicating decreased reliance on experience to shape subsequent memories. Further work is needed to determine how such a shift in typicality relates to learning-related brain activity, and how it impacts future memory. Third, pattern convergence may reflect a means of improving the reliability of encoding and subsequent memory formation. In this case, the degree to which a participant engages the hippocampus in a given state (or experiences it as novel) is known to influence the extent of subsequent memory formation38. The current work shows that the degree to which a pattern converges on a prototypical pattern is positively associated with subsequent memory, consistent with such a mechanism. Further work is needed to determine whether midbrain-induced changes in pattern convergence at encoding benefit memory formation.
Our current results can be interpreted as a paradigm for a higher-order mechanism for memory modulation. Certainly, our findings support the hypothesis that the hippocampus is a site of the formation and storage of episodic memory. Memory formation has been proposed to consist of multiple parallel processing stages, with encoding the stage that ultimately shapes the memory trace, and consolidation a stage that supports the durable storage of the memory trace98. It is well known that hippocampal activation during memory formation is associated with good memory. Our results further support the notion that a mechanism capable of influencing this stage is modulated by neuromodulatory input. It is also possible that the hippocampus is a site of information storage and replay. It is known that the hippocampus can be activated during the retrieval of recently learned information and replay of previously encoded information can be observed in the hippocampus while individuals are awake15,99. It has also been hypothesized that replay may provide a means for pattern completion and recovery of previously learned information when memory consolidation is impaired60. The role of neuromodulators in influencing such processes is currently unknown, and may be an important avenue for future research. There is evidence that cognitively active states can influence hippocampal activity in the context of replay, with the hippocampus engaging in a more persistent replay mode while in states for which new information is required to be consolidated100,101. Our findings would suggest that such states may be associated with the formation of more convergent hippocampal representations. That such states can be instantiated by neuromodulation may therefore provide a computational mechanism for shaping such processes. 827ec27edc