1. Neuroscience

Memory: How the brain constructs dreams

Deep inside the temporal lobe of the brain, the hippocampus has a central role in our ability to remember, imagine and dream.
https://doi.org/10.7554/eLife.58874
Share this article
Cite this article
  1. Erin J Wamsley
(2020)
Memory: How the brain constructs dreams
eLife 9:e58874.
https://doi.org/10.7554/eLife.58874
  2. Download BibTeX
  3. Download .RIS
  1. Erin J Wamsley  Is a corresponding author
  1. Department of Psychology and Program in Neuroscience, Furman University, United States

Our most vivid dreams are a remarkable replication of reality, combining disparate objects, actions and perceptions into a richly detailed hallucinatory experience. How does our brain accomplish this? It has long been suspected that the hippocampus contributes to dreaming, in part due to its close association with memory: according to one estimate, about half of all dreams contain at least one element originating from a specific experience while the subject was awake (Fosse et al., 2003). Although these dreams are rarely a faithful replication of any one memory, fragments of various recent experiences intermingle with other memories (usually related remote and semantic memories) to create a novel dream. Given all this, one might guess that dreams are created by those regions of the brain responsible for memory. However, studies dating back to the 1960s have suggested that patients with a damaged hippocampus still dream (Torda, 1969a; Torda, 1969b; Solms, 2014) and, somewhat amazingly, such patients can have dreams involving recent experiences of which they have no conscious memory (Stickgold et al., 2000)!

But are the dreams of patients with damage to hippocampus truly ‘normal’? Or alternatively, might such damage, while not preventing dreams, alter the form in which they are expressed? Indeed, there is reason to think that the hippocampus supports crucial aspects of dream construction beyond the simple insertion of memories. Recent work in the cognitive neurosciences has established that the hippocampus, in addition to being involved in the formation of memories, is also part of a brain system that is involved in using memory to construct novel imagined scenarios and simulate possible future events (Hassabis et al., 2007; Hassabis and Maguire, 2009; Schacter and Addis, 2007). As a result, patients without a hippocampus find it difficult to imagine scenes that are coherent, possibly because the hippocampus is responsible for combining different elements of memory into a spatially coherent whole.

Now, in eLife, Eleanor Maguire of University College London (UCL) and colleagues – including Goffredina Spanò as first author – report that the dreams of four amnesia patients lacking a hippocampal memory system do not have the richness of detail found in most dreams (Spanò et al., 2020). Besides reporting substantially fewer dreams than the patients in a control group, the four patients with amnesia also reported dreams that were markedly less detailed: their dreams contained fewer details of spatial location (e.g., descriptions like ‘behind the bar’ or ‘to my left I can see’) and fewer sensory details. These observations support the emerging view that dreams are generated by networks in the brain similar to the networks that are involved in recalling memories and constructing imagined scenarios during wakefulness (Fox et al., 2013; Graveline and Wamsley, 2015). Like memory and imagination, a vivid dream requires the construction of detailed, memory-based imagined scenes – and this process appears to rely on the hippocampus.

These observations partially echo the reports of Clara Torda from more than a half century ago, who characterized the dreams of amnesia patients as ‘shorter’, ‘simpler’, ‘repetitious’ and ‘stereotyped’ (Torda, 1969a). But Torda’s papers were written before the invention of noninvasive methods for imaging the brain, so it is not completely clear which structures may have been damaged in her patients. In contrast, the patients in the work of Spanò et al. all have well-characterized lesion sites with damage restricted solely to the hippocampus. This allows us to confidently attribute their impoverished dreams to the loss of the hippocampus itself, rather than to other regions of nearby temporal lobe which might also have a role in dreaming.

As with many studies of rare neurological patients, the latest work must be interpreted with caution due to the small sample size. For example, patient dreams were not significantly shorter than control dreams, leading to an apparently selective deficit in specific types of details reported (such as spatial details and sensory details), rather than a general deficit in the length of the dream. On average, however, the control dreams contained more than twice the number of informative words as the patient dreams, and the lack of a statistical difference between the two groups may be a mere artifact of the low sample size.

Nonetheless, these observations and a handful of similar studies are helping us to understand how the hippocampus contributes to the dreaming process. The work of Spanò et al. – who are based at UCL, the Royal Free Hospital in London, University Hospital Bonn and the universities of Arizona and Oxford – suggests hippocampal damage disrupts dreaming in ways that mirror how it also disrupts imagination. This suggests that, rather than being an entirely distinct phenomenon, dreaming is a part of a continuum of spontaneous, constructive thought and imagery continuously generated across the sleep and waking states.

References

    1. Graveline YM
    2. Wamsley EJ
    (2015) Dreaming and waking cognition
    Translational Issues in Psychological Science 1:97–105.
    https://doi.org/10.1037/tps0000018
    1. Hassabis D
    2. Maguire EA
    (2009) The construction system of the brain
    Philosophical Transactions of the Royal Society B: Biological Sciences 364:1263–1271.
    https://doi.org/10.1098/rstb.2008.0296

Article and author information

Author details

  1. Erin J Wamsley

    Erin J Wamsley is in the Department of Psychology and Program in Neuroscience, Furman University, Greenville, United States
    For correspondence
    erin.wamsley@furman.edu
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4465-3890

Publication history

  1. Version of Record published:

Copyright

© 2020, Wamsley

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 49,990
    views
  • 825
    downloads
  • 3
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Erin J Wamsley
(2020)
Memory: How the brain constructs dreams
eLife 9:e58874.
https://doi.org/10.7554/eLife.58874

Categories and tags

Research organism

    1. Related to

    Dreaming with hippocampal damage

    Goffredina Spanò, Gloria Pizzamiglio ... Eleanor A Maguire
  2. Further reading

Further reading

    1. Neuroscience

    Dreaming with hippocampal damage

    Goffredina Spanò, Gloria Pizzamiglio ... Eleanor A Maguire
    Short Report

    The hippocampus is linked with both sleep and memory, but there is debate about whether a salient aspect of sleep – dreaming – requires its input. To address this question, we investigated if human patients with focal bilateral hippocampal damage and amnesia engaged in dreaming. We employed a provoked awakening protocol where participants were woken up at various points throughout the night, including during non-rapid eye movement and rapid eye movement sleep, to report their thoughts in that moment. Despite being roused a similar number of times, dream frequency was reduced in the patients compared to control participants, and the few dreams they reported were less episodic-like in nature and lacked content. These results suggest that hippocampal integrity may be necessary for typical dreaming to occur, and aligns dreaming with other hippocampal-dependent processes such as episodic memory that are central to supporting our mental life.

    1. Neuroscience

    Associative plasticity of granule cell inputs to cerebellar Purkinje cells

    Rossella Conti, Céline Auger
    Research Article

    Granule cells of the cerebellum make up to 175,000 excitatory synapses on a single Purkinje cell, encoding the wide variety of information from the mossy fibre inputs into the cerebellar cortex. The granule cell axon is made of an ascending portion and a long parallel fibre extending at right angles, an architecture suggesting that synapses formed by the two segments of the axon could encode different information. There are controversial indications that ascending axon (AA) and parallel fibre (PF) synapse properties and modalities of plasticity are different. We tested the hypothesis that AA and PF synapses encode different information, and that the association of these distinct inputs to Purkinje cells might be relevant to the circuit and trigger plasticity, similar to the coincident activation of PF and climbing fibre inputs. Here, by recording synaptic currents in Purkinje cells from either proximal or distal granule cells (mostly AA and PF synapses, respectively), we describe a new form of associative plasticity between these two distinct granule cell inputs. We show for the first time that synchronous AA and PF repetitive train stimulation, with inhibition intact, triggers long-term potentiation (LTP) at AA synapses specifically. Furthermore, the timing of the presentation of the two inputs controls the outcome of plasticity and induction requires NMDAR and mGluR1 activation. The long length of the PFs allows us to preferentially activate the two inputs independently, and despite a lack of morphological reconstruction of the connections, these observations reinforce the suggestion that AA and PF synapses have different coding capabilities and plasticity that is associative, enabling effective association of information transmitted via granule cells.

    1. Neuroscience

    Stable sequential dynamics in prefrontal cortex represents subjective estimation of time

    Yiting Li, Wenqu Yin ... Baoming Li
    Research Article

    Time estimation is an essential prerequisite underlying various cognitive functions. Previous studies identified ‘sequential firing’ and ‘activity ramps’ as the primary neuron activity patterns in the medial frontal cortex (mPFC) that could convey information regarding time. However, the relationship between these patterns and the timing behavior has not been fully understood. In this study, we utilized in vivo calcium imaging of mPFC in rats performing a timing task. We observed cells that showed selective activation at trial start, end, or during the timing interval. By aligning long-term time-lapse datasets, we discovered that sequential patterns of time coding were stable over weeks, while cells coding for trial start or end showed constant dynamism. Furthermore, with a novel behavior design that allowed the animal to determine individual trial interval, we were able to demonstrate that real-time adjustment in the sequence procession speed closely tracked the trial-to-trial interval variations. And errors in the rats’ timing behavior can be primarily attributed to the premature ending of the time sequence. Together, our data suggest that sequential activity maybe a stable neural substrate that represents time under physiological conditions. Furthermore, our results imply the existence of a unique cell type in the mPFC that participates in the time-related sequences. Future characterization of this cell type could provide important insights in the neural mechanism of timing and related cognitive functions.