Complementary roles of human hippocampal subregions during retrieval of spatiotemporal context

Milagros S. Copara, Abdul S. Hassan, Colin T. Kyle, Laura A. Libby, Charan Ranganath, Arne D. Ekstrom

Research output: Contribution to journalArticle

38 Citations (Scopus)

Abstract

Current evidence strongly supports the central involvement of the human medial temporal lobes (MTL) in storing and retrieving memories for recently experienced events. However, a critical remaining question regards exactly how the hippocampus and surrounding cortex represents spatiotemporal context defining an event in memory. Competing accounts suggest that this process may be accomplished by the following: (1) an overall increase in neural similarity of representations underlying spatial and temporal context, (2) a differentiation of competing spatiotemporal representations, or (3) a combination of the two processes, with different subregions performing these two functions within the MTL. To address these competing proposals, we used high-resolution functional magnetic resonance imaging targeting the MTL along with a multivariate pattern similarity approach with 19 participants. While undergoing imaging, participants performed a task in which they retrieved spatial and temporal contextual representations from a recently learned experience. Results showed that successfully retrieving spatiotemporal context defining an episode involved a decrease in pattern similarity between putative spatial and temporal contextual representations in hippocampal subfields CA2/CA3/DG, whereas the parahippocampal cortex (PHC) showed the opposite pattern. These findings could not be accounted for by differences in univariate activations for complete versus partial retrieval nor differences in correlations for correct or incorrect retrieval. Together, these data suggest that the CA2/CA3/DG serves to differentiate competing contextual representations, whereas the PHC stores a comparatively integrated trace of scene-specific context, both of which likely play important roles in successful episodic memory retrieval.

Original languageEnglish (US)
Pages (from-to)6834-6842
Number of pages9
JournalJournal of Neuroscience
Volume34
Issue number20
DOIs
StatePublished - 2014

Fingerprint

Temporal Lobe
Episodic Memory
Hippocampus
Magnetic Resonance Imaging

Keywords

  • Episodic memory
  • High-res fMRI
  • Hippocampus
  • Multivariate pattern analysis
  • Parahippocampal cortex
  • Spatiotemporal

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Copara, M. S., Hassan, A. S., Kyle, C. T., Libby, L. A., Ranganath, C., & Ekstrom, A. D. (2014). Complementary roles of human hippocampal subregions during retrieval of spatiotemporal context. Journal of Neuroscience, 34(20), 6834-6842. https://doi.org/10.1523/JNEUROSCI.5341-13.2014

Complementary roles of human hippocampal subregions during retrieval of spatiotemporal context. / Copara, Milagros S.; Hassan, Abdul S.; Kyle, Colin T.; Libby, Laura A.; Ranganath, Charan; Ekstrom, Arne D.

In: Journal of Neuroscience, Vol. 34, No. 20, 2014, p. 6834-6842.

Research output: Contribution to journalArticle

Copara, MS, Hassan, AS, Kyle, CT, Libby, LA, Ranganath, C & Ekstrom, AD 2014, 'Complementary roles of human hippocampal subregions during retrieval of spatiotemporal context', Journal of Neuroscience, vol. 34, no. 20, pp. 6834-6842. https://doi.org/10.1523/JNEUROSCI.5341-13.2014
Copara, Milagros S. ; Hassan, Abdul S. ; Kyle, Colin T. ; Libby, Laura A. ; Ranganath, Charan ; Ekstrom, Arne D. / Complementary roles of human hippocampal subregions during retrieval of spatiotemporal context. In: Journal of Neuroscience. 2014 ; Vol. 34, No. 20. pp. 6834-6842.
@article{78bdae1bdbbe443fb5d691561d6f61cf,
title = "Complementary roles of human hippocampal subregions during retrieval of spatiotemporal context",
abstract = "Current evidence strongly supports the central involvement of the human medial temporal lobes (MTL) in storing and retrieving memories for recently experienced events. However, a critical remaining question regards exactly how the hippocampus and surrounding cortex represents spatiotemporal context defining an event in memory. Competing accounts suggest that this process may be accomplished by the following: (1) an overall increase in neural similarity of representations underlying spatial and temporal context, (2) a differentiation of competing spatiotemporal representations, or (3) a combination of the two processes, with different subregions performing these two functions within the MTL. To address these competing proposals, we used high-resolution functional magnetic resonance imaging targeting the MTL along with a multivariate pattern similarity approach with 19 participants. While undergoing imaging, participants performed a task in which they retrieved spatial and temporal contextual representations from a recently learned experience. Results showed that successfully retrieving spatiotemporal context defining an episode involved a decrease in pattern similarity between putative spatial and temporal contextual representations in hippocampal subfields CA2/CA3/DG, whereas the parahippocampal cortex (PHC) showed the opposite pattern. These findings could not be accounted for by differences in univariate activations for complete versus partial retrieval nor differences in correlations for correct or incorrect retrieval. Together, these data suggest that the CA2/CA3/DG serves to differentiate competing contextual representations, whereas the PHC stores a comparatively integrated trace of scene-specific context, both of which likely play important roles in successful episodic memory retrieval.",
keywords = "Episodic memory, High-res fMRI, Hippocampus, Multivariate pattern analysis, Parahippocampal cortex, Spatiotemporal",
author = "Copara, {Milagros S.} and Hassan, {Abdul S.} and Kyle, {Colin T.} and Libby, {Laura A.} and Charan Ranganath and Ekstrom, {Arne D.}",
year = "2014",
doi = "10.1523/JNEUROSCI.5341-13.2014",
language = "English (US)",
volume = "34",
pages = "6834--6842",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "20",

}

TY - JOUR

T1 - Complementary roles of human hippocampal subregions during retrieval of spatiotemporal context

AU - Copara, Milagros S.

AU - Hassan, Abdul S.

AU - Kyle, Colin T.

AU - Libby, Laura A.

AU - Ranganath, Charan

AU - Ekstrom, Arne D.

PY - 2014

Y1 - 2014

N2 - Current evidence strongly supports the central involvement of the human medial temporal lobes (MTL) in storing and retrieving memories for recently experienced events. However, a critical remaining question regards exactly how the hippocampus and surrounding cortex represents spatiotemporal context defining an event in memory. Competing accounts suggest that this process may be accomplished by the following: (1) an overall increase in neural similarity of representations underlying spatial and temporal context, (2) a differentiation of competing spatiotemporal representations, or (3) a combination of the two processes, with different subregions performing these two functions within the MTL. To address these competing proposals, we used high-resolution functional magnetic resonance imaging targeting the MTL along with a multivariate pattern similarity approach with 19 participants. While undergoing imaging, participants performed a task in which they retrieved spatial and temporal contextual representations from a recently learned experience. Results showed that successfully retrieving spatiotemporal context defining an episode involved a decrease in pattern similarity between putative spatial and temporal contextual representations in hippocampal subfields CA2/CA3/DG, whereas the parahippocampal cortex (PHC) showed the opposite pattern. These findings could not be accounted for by differences in univariate activations for complete versus partial retrieval nor differences in correlations for correct or incorrect retrieval. Together, these data suggest that the CA2/CA3/DG serves to differentiate competing contextual representations, whereas the PHC stores a comparatively integrated trace of scene-specific context, both of which likely play important roles in successful episodic memory retrieval.

AB - Current evidence strongly supports the central involvement of the human medial temporal lobes (MTL) in storing and retrieving memories for recently experienced events. However, a critical remaining question regards exactly how the hippocampus and surrounding cortex represents spatiotemporal context defining an event in memory. Competing accounts suggest that this process may be accomplished by the following: (1) an overall increase in neural similarity of representations underlying spatial and temporal context, (2) a differentiation of competing spatiotemporal representations, or (3) a combination of the two processes, with different subregions performing these two functions within the MTL. To address these competing proposals, we used high-resolution functional magnetic resonance imaging targeting the MTL along with a multivariate pattern similarity approach with 19 participants. While undergoing imaging, participants performed a task in which they retrieved spatial and temporal contextual representations from a recently learned experience. Results showed that successfully retrieving spatiotemporal context defining an episode involved a decrease in pattern similarity between putative spatial and temporal contextual representations in hippocampal subfields CA2/CA3/DG, whereas the parahippocampal cortex (PHC) showed the opposite pattern. These findings could not be accounted for by differences in univariate activations for complete versus partial retrieval nor differences in correlations for correct or incorrect retrieval. Together, these data suggest that the CA2/CA3/DG serves to differentiate competing contextual representations, whereas the PHC stores a comparatively integrated trace of scene-specific context, both of which likely play important roles in successful episodic memory retrieval.

KW - Episodic memory

KW - High-res fMRI

KW - Hippocampus

KW - Multivariate pattern analysis

KW - Parahippocampal cortex

KW - Spatiotemporal

UR - http://www.scopus.com/inward/record.url?scp=84900437377&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84900437377&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.5341-13.2014

DO - 10.1523/JNEUROSCI.5341-13.2014

M3 - Article

VL - 34

SP - 6834

EP - 6842

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 20

ER -