Temporal integration of narrative information in a hippocampal amnesic patient

Default network regions appear to integrate information over time windows of 30 ​s or more during narrative listening. Does this long-timescale capability require the hippocampus? Amnesic behavior suggests that regions other than the hippocampus can independently support some online processing when...

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Main Authors: Xiaoye Zuo, Christopher J. Honey, Morgan D. Barense, Davide Crombie, Kenneth A. Norman, Uri Hasson, Janice Chen
Format: Article
Language:English
Published: Elsevier 2020-06-01
Series:NeuroImage
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811920301452
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spelling doaj-452e1d4ceb084c5fae356355a21ba8562021-02-15T04:12:24ZengElsevierNeuroImage1095-95722020-06-01213116658Temporal integration of narrative information in a hippocampal amnesic patientXiaoye Zuo0Christopher J. Honey1Morgan D. Barense2Davide Crombie3Kenneth A. Norman4Uri Hasson5Janice Chen6Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD, 21218, USA; Corresponding author.Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD, 21218, USADepartment of Psychology, University of Toronto, Toronto, Ontario, M5S 3G3, Canada; Rotman Research Institute, Baycrest Hospital, Toronto, Ontario, M5S 3G3, CanadaDepartment of Biology II - Neurobiology, Ludwig Maximilian University of Munich, Großhaderner Str. 2, 82152, Planegg, GermanyPrinceton Neuroscience Institute, Princeton University, Princeton, NJ, 08544, USA; Department of Psychology, Princeton University, Princeton, NJ, 08544, USAPrinceton Neuroscience Institute, Princeton University, Princeton, NJ, 08544, USA; Department of Psychology, Princeton University, Princeton, NJ, 08544, USADepartment of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, MD, 21218, USADefault network regions appear to integrate information over time windows of 30 ​s or more during narrative listening. Does this long-timescale capability require the hippocampus? Amnesic behavior suggests that regions other than the hippocampus can independently support some online processing when input is continuous and semantically rich: amnesics can participate in conversations and tell stories spanning minutes, and when tested immediately on recently heard prose they are able to retain some information. We hypothesized that default network regions can integrate the semantically coherent information of a narrative across long time windows, even in the absence of an intact hippocampus. To test this prediction, we measured BOLD activity in the brain of a hippocampal amnesic patient (D.A.) and healthy control participants while they listened to a 7 min narrative. The narrative was played either in its intact form, or as a paragraph-scrambled version, which has been previously shown to interfere with the long-range temporal dependencies in default network activity. In the intact story condition, D.A.’s moment-by-moment BOLD activity spatial patterns were similar to those of controls in low-level auditory cortex as well as in some high-level default network regions (including lateral and medial posterior parietal cortex). Moreover, as in controls, D.A.’s response patterns in medial and lateral posterior parietal cortex were disrupted when paragraphs of the story were presented in a shuffled order, suggesting that activity in these areas did depend on information from 30 ​s or more in the past. Together, these results suggest that some default network cortical areas can integrate information across long timescales, even when the hippocampus is severely damaged.http://www.sciencedirect.com/science/article/pii/S1053811920301452
collection DOAJ
language English
format Article
sources DOAJ
author Xiaoye Zuo
Christopher J. Honey
Morgan D. Barense
Davide Crombie
Kenneth A. Norman
Uri Hasson
Janice Chen
spellingShingle Xiaoye Zuo
Christopher J. Honey
Morgan D. Barense
Davide Crombie
Kenneth A. Norman
Uri Hasson
Janice Chen
Temporal integration of narrative information in a hippocampal amnesic patient
NeuroImage
author_facet Xiaoye Zuo
Christopher J. Honey
Morgan D. Barense
Davide Crombie
Kenneth A. Norman
Uri Hasson
Janice Chen
author_sort Xiaoye Zuo
title Temporal integration of narrative information in a hippocampal amnesic patient
title_short Temporal integration of narrative information in a hippocampal amnesic patient
title_full Temporal integration of narrative information in a hippocampal amnesic patient
title_fullStr Temporal integration of narrative information in a hippocampal amnesic patient
title_full_unstemmed Temporal integration of narrative information in a hippocampal amnesic patient
title_sort temporal integration of narrative information in a hippocampal amnesic patient
publisher Elsevier
series NeuroImage
issn 1095-9572
publishDate 2020-06-01
description Default network regions appear to integrate information over time windows of 30 ​s or more during narrative listening. Does this long-timescale capability require the hippocampus? Amnesic behavior suggests that regions other than the hippocampus can independently support some online processing when input is continuous and semantically rich: amnesics can participate in conversations and tell stories spanning minutes, and when tested immediately on recently heard prose they are able to retain some information. We hypothesized that default network regions can integrate the semantically coherent information of a narrative across long time windows, even in the absence of an intact hippocampus. To test this prediction, we measured BOLD activity in the brain of a hippocampal amnesic patient (D.A.) and healthy control participants while they listened to a 7 min narrative. The narrative was played either in its intact form, or as a paragraph-scrambled version, which has been previously shown to interfere with the long-range temporal dependencies in default network activity. In the intact story condition, D.A.’s moment-by-moment BOLD activity spatial patterns were similar to those of controls in low-level auditory cortex as well as in some high-level default network regions (including lateral and medial posterior parietal cortex). Moreover, as in controls, D.A.’s response patterns in medial and lateral posterior parietal cortex were disrupted when paragraphs of the story were presented in a shuffled order, suggesting that activity in these areas did depend on information from 30 ​s or more in the past. Together, these results suggest that some default network cortical areas can integrate information across long timescales, even when the hippocampus is severely damaged.
url http://www.sciencedirect.com/science/article/pii/S1053811920301452
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