Details, gist and schema: hippocampal–neocortical interactions underlying recent and remote episodic and spatial memory

doi:10.1016/j.cobeha.2017.07.016

Current Opinion in Behavioral Sciences

Volume 17, October 2017, Pages 114-123

https://doi.org/10.1016/j.cobeha.2017.07.016 Get rights and content

Highlights

•
The nature of a memory trace, not its age, determines its hippocampal dependence.
•
Remote memories rich in perceptual detail still engage the hippocampus (HPC).
•
Ventromedial prefrontal cortex (vmPFC) represents schemas.
•
Anterior HPC represents the gist of spatial and episodic memories.
•
Posterior HPC and posterior neocortex mediate fine-grained detailed representations.

Memories are complex and dynamic, continuously transforming with time and experience. In this paper, we review evidence of the neural basis of memory transformation for events and environments with emphasis on the role of hippocampal–neocortical interactions. We argue that memory transformation from detail-rich representations to gist-like and schematic representation is accompanied by corresponding changes in their neural representations. These changes can be captured by a model based on functional differentiation along the long-axis of the hippocampus, and its functional connectivity to related posterior and anterior neocortical structures, especially the ventromedial prefrontal cortex (vmPFC). In particular, we propose that perceptually detailed, highly specific representations are mediated by the posterior hippocampus and neocortex, gist-like representations by the anterior hippocampus, and schematic representations by vmPFC. These representations can co-exist and the degree to which each is utilized is determined by its availability and by task demands.

Introduction

It is well established that the hippocampus is needed for the acquisition and retention of recently acquired spatial and episodic (or context-dependent) memory [1, 2, 3, 4•, 5, 6]. There is also a consensus that these types of memory are not stored in the hippocampus as such. The memory trace, or engram, consists of an integrated hippocampal–cortical ensemble of neurons, with the hippocampus binding information and providing the sparsely distributed code ‘pointing to’ to the cortical (and subcortical) neurons where information about the content and conscious experience of the memory is represented [7].

What is the nature of the sparse code that is represented in the hippocampus? Many alternatives have been proposed, leading to debates about the role of the hippocampus in consolidation [3, 4•, 5, 8, 9, 10, 11, 12, 13] and the types of memories dependent on hippocampal function [1, 2, 14, 15, 16, 17, 18, 19, 20]. By one view, the hippocampus is a temporary memory structure that is implicated in retention and retrieval only until the identical memory is consolidated in extra-hippocampal structures in the neocortex [9, 10, 21]. An alternative view, provided by the Trace Transformation Theory, and the Multiple Trace Theory from which it is derived, is that the hippocampus continues to be implicated in retention and retrieval of perceptually-rich, detailed memories, in perpetuity [3, 4•, 5, 22]. This framework predicts that the specificity of a memory, namely its gist and perceptual features, remain hippocampally-dependent, but memories can also be transformed with time and experience to more schematic or semantic representations, which become independent of the hippocampus.

Gist refers to the central features of a particular episode (story line), and is distinct from schema, which refer to ‘adaptable associative networks of knowledge extracted over multiple similar experiences’ [23, 24], capturing similarities across particular episodes. Thus, a gist representation may not be richly detailed but is still specific to a single episode (‘my tenth birthday party’), while a schema is a more abstract representation based on multiple similar episodes or memories (birthday parties in general). Crucially, schema, gist and detailed representations are not mutually exclusive. These differing representations may co-exist and support one another or may be preferentially retrieved at the expense of the other(s) based on the particular demands of a task. Thus, it is the quality or nature of the memory representation, rather than its age, that determines whether it is dependent on the hippocampus.

In this review we discuss primarily recent evidence supporting the hippocampus's role in the representation of perceptually-rich memories including episodes and scenes, how some of these memories are transformed with time and experience, relinquishing their hippocampal representation, and how this evidence informs theories of memory systems and hippocampal function (see [4•, 5, 23, 24, 25, 26, 27, 28] for previous reviews in humans and rodents). In the second section, we discuss evidence for functional differentiation along the long-axis of the hippocampus. In the third section, we propose how such differentiation relates to the questions above concerning the nature of hippocampal and neocortical memory representations. Throughout, we consider transformations to include forgetting of perceptual and contextual details, distortions, extraction of statistical regularities among instances, and assimilation to schemas while preserving the central elements (gist and schema) of the memory.

Section snippets

The nature of episodic and spatial memory representations as revealed in studies on memory consolidation and transformation

Extensive hippocampal damage typically impairs memory for specific episodes no matter how long ago they were acquired [29, 30], but more nuanced patterns of deficits are revealed in individuals with partial damage. Medial temporal lobe epilepsy (mTLE) that affects the hippocampus leads to autobiographical memory loss extending back to early childhood [31]. To investigate the nature of this loss, St-Laurent et al. [32^•] had people with mTLE and healthy controls retrieve detailed memories of

Specialization along the longitudinal axis of the hippocampus: Gist and detailed representations mediated by anterior and posterior hippocampus

As we noted, the type and specificity of memories may influence activity levels along the long-axis of the hippocampus during memory encoding and retrieval, based on anterior–posterior differences in functional neural organization, such as receptive field size, the distribution of hippocampal subfields, and their connections to other brain regions [4•, 64, 65]. Recent evidence suggests that in humans, as in rodents [66], the pHPC represents more fine-grained, local (spatial) features of the

Interactions of aHPC, pHPC and vmPFC in support of spatial and episodic memory representations varying in detail

Thus, we suggest that differences in the detail-richness of scenes and episodes lead to differential recruitment of the aHPC and pHPC. Differential involvement of the aHPC and pHPC, as well as their connectivity to neocortical structures, such as posterior neocortex and vmPFC, may help, therefore, to better characterize the representations associated with spatial and episodic memory, and their interactions during retrieval of recent and remote memory (see Figure 2 for illustration). With a

Conclusion

We have reviewed evidence that the hippocampus is involved in long-term memory for detailed representations episodic and spatial memory (for possible behavioural consequences of this shared dependence, see Box 2). A challenge for future research is in differentiating among schematic, gist-like and detailed representations in both spatial and episodic memory and linking them specifically to the neural regions proposed. In keeping with the nomenclature proposed in our paper, we acknowledge that

Conflict of interest statement

Nothing declared.

Acknowledgements

We gratefully acknowledge Buddhika Bellana, Iva Brunec, Melanie Sekeres, Asaf Gilboa, Gordon Winocur, and two anonymous reviewers for their helpful comments on previous versions of this manuscript. This work was supported by the Canadian Institutes of Health Research (Grant #: MOP 49566).

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Details, gist and schema: hippocampal–neocortical interactions underlying recent and remote episodic and spatial memory

Highlights

Introduction

Section snippets

The nature of episodic and spatial memory representations as revealed in studies on memory consolidation and transformation

Specialization along the longitudinal axis of the hippocampus: Gist and detailed representations mediated by anterior and posterior hippocampus

Interactions of aHPC, pHPC and vmPFC in support of spatial and episodic memory representations varying in detail

Conclusion

Conflict of interest statement

Acknowledgements

Behav Brain Res

Behav Neurosci

Neuropsychologia

Cold Spring Harb. Perspect. Biol.

Nat Rev Neurosci

Neuron

Behav Brain

Nat Neurosci

Annu Rev Psychol

J Neurosci

Neuropsychologia

Trends Cogn Sci

Neuropsychologia

Front Hum Neurosci

Nat Rev Neurosci

Trends Cogn Sci

Hippocampus

J Cogn Neurosci

Nat Rev Neurosci

Nat Rev Neurosci

Cereb Cortex

J Neurosci

Neuroimage Clin

Elife

The Hippocampus as a Cognitive Map

The hippocampus and space revisited

Hippocampus

Memory transformation and systems consolidation

J Int Neuropsychol Soc

Episodic memory and beyond: the hippocampus and neocortex in transformation

Annu Rev Psychol

Memory formation and long-term retention in humans and animals: convergence towards a transformation account of hippocampal–neocortical interactions

Neuropsychologia

The primate hippocampal formation: evidence for a time-limited role in memory storage

Science

The medial temporal lobe memory system

Science

Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus

J Neurosci

Memory consolidation, retrograde amnesia and the hippocampal complex

Curr Opin Neurobiol

The hippocampus: a manifesto for change

J Exp Psychol Gen

The construction system of the brain

Philos Trans R Soc Lond B: Biol Sci

Deconstructing episodic memory with construction

Trends Cogn Sci

Is the rodent hippocampus just for “place”?

Curr Opin Neurobiol

The neuroscience of remote memory

Curr Opin Neurobiol

What is a memory schema? A historical perspective on current neuroscience literature

Neuropsychologia

Schema representation in patients with ventromedial PFC lesions

J Neurosci

Mechanisms of memory consolidation and transformation

Cognitive Neuroscience of Memory Consolidation

The medial temporal lobe and the attributes of memory

Trends Cogn Sci

Systems consolidation and the content of memory

Neurobiol Learn Mem

Episodic memory: from mind to brain

Annu Rev Psychol

What's new with the amnesic patient H.M.?

Nat Rev Neurosci

Remote episodic memory deficits in patients with unilateral temporal lobe epilepsy and excisions

J Neurosci

The perceptual richness of complex memory episodes is compromised by medial temporal lobe damage

Hippocampus

The retrieval of perceptual memory details depends on right hippocampal integrity and activation