Memory on time

doi:10.1016/j.tics.2012.12.007

Trends in Cognitive Sciences

Volume 17, Issue 2, February 2013, Pages 81-88

https://doi.org/10.1016/j.tics.2012.12.007 Get rights and content

Considerable recent work has shown that the hippocampus is critical for remembering the order of events in distinct experiences, a defining feature of episodic memory. Correspondingly, hippocampal neuronal activity can ‘replay’ sequential events in memories and hippocampal neuronal ensembles represent a gradually changing temporal context signal. Most strikingly, single hippocampal neurons – called time cells – encode moments in temporally structured experiences much as the well-known place cells encode locations in spatially structured experiences. These observations bridge largely disconnected literatures on the role of the hippocampus in episodic memory and spatial mapping, and suggest that the fundamental function of the hippocampus is to establish spatio-temporal frameworks for organizing memories.

Section snippets

The temporal organization of memory

The idea that everyday memories are organized in time dates from at least Aristotle, and Tulving emphasized temporal organization when he introduced the modern conception of episodic memory as distinct from semantic memory. Furthermore, many studies have identified the hippocampus as a core brain area that supports the capacities for recollection (e.g., [3]) and episodic memory [4]. Therefore, it stands to reason that the hippocampus might play an important role in the temporal organization of

The hippocampus plays an essential role in memory for the order of events within episodes

The role of the hippocampus in the temporal organization of memory has been examined in two general paradigms, memory for serial order within lists and performance in disambiguating overlapping event sequences. The earliest studies on memory for serial order showed that amnesic patients of various etiologies were impaired in reproducing the ordering of 15 words, but the deficit was attributed to potential compromise of the functionality of prefrontal cortex, for which damage also resulted in a

The hippocampus plays an essential role in disambiguation of overlapping memories

Many of our experiences overlap with the contents of events that occur in sequential experiences. For example, we often walk through common streets on the way to different locations and we often visit with the same people to have diverse discussions, yet we usually are able to recall each ordered experience distinctly. The role of the hippocampus in disambiguating overlapping sequences has been studied in rats trained on odor sequences that overlapped (Figure 1a), implemented as a series of

Neuronal networks in the hippocampus ‘replay’ sequences of events in memories

There is substantial evidence that hippocampal neural ensembles represent the order of events from previous experiences. Much of the data come from studies where rats repetitively traverse the same route through space, during which hippocampal place cells (see Glossary) activate sequentially. In this paradigm, numerous studies have reported forward and reverse ‘replays’ of the place cell sequences, both when animals are asleep and during periods of quiet wakefulness (e.g., [26]). Hippocampal

How do neuronal networks in the hippocampus organize events in time?

Two kinds of models have been proposed to explain the underlying neural representation that supports the temporal organization of hippocampal sequence representations. Neuronal ensembles might represent temporal order by constructing a firing chain via enhancements of direct connections between neurons that represent temporally adjacent events 32, 33 or hippocampal ensembles might represent a gradually evolving temporal context to which memories are bound at appropriate times 34, 35, 36.

Time cells and place cells

Many studies have provided considerable evidence that the activity of hippocampal neurons signal an animal's location within an environment – these neurons are called place cells (reviewed in [39,45]). There is strong evidence of spatial representation by hippocampal neurons in humans, as well 57, 58. How can the observations on temporal representation by the hippocampus be reconciled with its well-known role in spatial representation? There are two main features of time cells and place cells

Concluding remarks

There is a wealth of evidence from diverse experimental approaches in humans and animals that the hippocampus plays a central role in the temporal organization of memories and supports the disambiguation of overlapping episodes. Ensembles of hippocampal time cells may represent a gradually changing temporal context signal that integrates information across events and thereby both separates distinct episodes and defines the temporal structure within each unique episode. The evolving hippocampal

Acknowledgments

This work was supported by NIMH grant MH095297.

Glossary

Context cells: theoretical neurons whose activity bridges between events and therefore could link their representations in order. These may pre-exist or arise independent of specific events, or could arise as an integration of event information over periods of time.
Long-term potentiation (LTP): the enhancement of efficacy of the synaptic connections between neurons; occurs as a result of repetitive combined pre-synaptic and post-synaptic activation.
Place cells: neurons in the hippocampus that fire

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Trends in Cognitive Sciences

ReviewMemory on time

Section snippets

The temporal organization of memory

The hippocampus plays an essential role in memory for the order of events within episodes

The hippocampus plays an essential role in disambiguation of overlapping memories

Neuronal networks in the hippocampus ‘replay’ sequences of events in memories

How do neuronal networks in the hippocampus organize events in time?

Time cells and place cells

Concluding remarks

Acknowledgments

Glossary

Neuropsychologia

Neuron

Behav. Brain Res.

Neuron

Trends Neurosci.

Neuron

Trends Neurosci.

Behav. Brain Res.

Neuron

Neuron

Neuron

Neuron

Curr. Opin. Neurobiol.

Neuron

Neuron

Précis of Elements of Episodic Memory

Behav. Brain Sci.

The medial temporal lobe and recognition memory

Annu. Rev. Neurosci.

Differential effects of early hippocampal pathology on episodic and semantic memory

Science

Memory for single items, word pairs, and temporal order of different kinds in a patient with selective hippocampal lesions

Cogn. Neuropsychol.

Bilateral hippocampal pathology impairs topographical and episodic memory but not visual pattern matching

Hippocampus

Spatial and temporal episodic memory retrieval recruit dissociable functional networks in the human brain

Learn. Mem.

A specific role of the human hippocampus in recall of temporal sequences

J. Neurosci.

An unexpected sequence of events: mismatch detection in the human hippocampus

PLoS Biol.

Medial temporal lobe contributions to episodic sequence encoding

Cereb. Cortex

Differential encoding mechanisms for subsequent associative recognition and free recall

J. Neurosci.

Critical role of the hippocampus in memory for sequences of events

Nat. Neurosci.

The role of the hippocampus in memory for the temporal order of a sequence of odors

Behav. Neurosci.

Cognitive mechanisms of memory for order in rhesus monkeys

Hippocampus

Review
Memory on time