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...
Main Authors: | , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Elsevier
2020-06-01
|
Series: | NeuroImage |
Online Access: | http://www.sciencedirect.com/science/article/pii/S1053811920301452 |
id |
doaj-452e1d4ceb084c5fae356355a21ba856 |
---|---|
record_format |
Article |
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 |
work_keys_str_mv |
AT xiaoyezuo temporalintegrationofnarrativeinformationinahippocampalamnesicpatient AT christopherjhoney temporalintegrationofnarrativeinformationinahippocampalamnesicpatient AT morgandbarense temporalintegrationofnarrativeinformationinahippocampalamnesicpatient AT davidecrombie temporalintegrationofnarrativeinformationinahippocampalamnesicpatient AT kennethanorman temporalintegrationofnarrativeinformationinahippocampalamnesicpatient AT urihasson temporalintegrationofnarrativeinformationinahippocampalamnesicpatient AT janicechen temporalintegrationofnarrativeinformationinahippocampalamnesicpatient |
_version_ |
1724269280406536192 |