Review
How the hippocampus preserves order: the role of prediction and context

https://doi.org/10.1016/j.tics.2014.12.004Get rights and content

Highlights

  • The hippocampus shows a forward prediction signal with sequence repetition.

  • Encoding novel sequences is facilitated by shared context.

  • Stability in hippocampal activation patterns across items relates to the successful encoding of temporal relationships between those items.

Remembering the sequence of events is critical for deriving meaning from our experiences and guiding behavior. Prior investigations into the function of the human hippocampus have focused on its more general role in associative binding, but recent work has focused on understanding its specific role in encoding and preserving the temporal order of experiences. In this review we summarize recent work in humans examining hippocampal contributions to sequence learning. We distinguish the learning of sequential relationships through repetition from the rapid, episodic acquisition of sequential associations. Taken together, this research begins to clarify the link between hippocampal representations and the preservation of the order of events.

Section snippets

Sequences in memory

Much of our experience is perceived and understood through the sequences of events that occur. Episodic memory, which allows us to relive events from our past, is defined by the recovery of the unique context in which the event occurred [1]. The context can, but need not always, include spatial details and various forms of temporal detail including how the event unfolded in time. Furthermore, many of our everyday experiences are repeated sequences of highly similar events, such as one's morning

Laying the groundwork

Theoretical models have proposed various potential mechanisms by which hippocampal processes could bridge temporally disparate events into coherent, bound associative memories. One proposal is that context-sensitive cells may develop from background neural firing in the hippocampal subregion CA3 due to its recurrent excitatory connections [9]. Associations formed between cells coding items in a sequence and these background context cells could result in indirect associations between items that

Two routes to sequence learning?

It is important to consider that there may be multiple cognitive and neural mechanisms that support hippocampal sequence learning. In particular, we suggest that there may be a distinction between single-trial or episodic sequence encoding and the representation of a well-learned, repeated, predictable sequence because each re-exposure to a sequence may modify the learned representation. Thus, recent work examining changes in hippocampal activation as a function of many sequence repetitions is

Sequence learning through repetition

There is now growing evidence that the human hippocampus is sensitive to repeating sequences. Prior fMRI work across various sequence learning paradigms has shown that hippocampal activation is generally enhanced during sequence learning 26, 27, 28 and a recent case study showed that a patient with complete loss of the bilateral hippocampus and some surrounding cortex failed to show learning of even simple sequential associations despite showing intact item memory [29].

Recent fMRI work has

Episodic sequence encoding

One particular challenge for the development of theoretical approaches to understanding the mechanisms of sequence memory formation is that, outside the laboratory setting, sequence memory is often formed even after a single exposure and hence repetition as a necessary component of learning is not viable. In paradigms testing the free recall of once-presented sequences, one of the most ubiquitous findings is the tendency for recall to exhibit temporal clustering [43], meaning that recall

Concluding remarks

Here we have reviewed emerging evidence characterizing human hippocampal involvement in sequence learning. We draw a possible distinction between sequence learning that may involve extracting temporal regularities through multiple repetitions and rapid, novel episodic sequence encoding. Further, we propose that the underlying processes and representations by which sequence information is acquired in these two cases may be biased by their learning context. On the one hand, episodic sequence

Acknowledgments

This work was supported by the National Institute of Mental Health (R01 – MH074692) and the National Science Foundation (DGE – 0813964).

Glossary

Delay conditioning
conditioning in which the conditioned and unconditioned stimuli overlap in time.
Place cells
hippocampal neurons that fire when an animal is at a particular location in space.
Replay
sequential pattern of hippocampal place cell responses during offline periods that corresponds to the response pattern during a prior experience.
Temporal context
defined by the temporal context model [22] as a slowly drifting representation that binds to and updates with each newly encountered item.

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