Movement-related theta rhythm in humans: coordinating self-directed hippocampal learning.
The hippocampus is crucial for episodic or declarative memory and the theta rhythm has been implicated in mnemonic processing, but the functional contribution of theta to memory remains the subject of intense speculation. Recent evidence suggests that the hippocampus might function as a network hub...
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2012-01-01
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| Series: | PLoS Biology |
| Online Access: | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1001267&type=printable |
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| author | Raphael Kaplan Christian F Doeller Gareth R Barnes Vladimir Litvak Emrah Düzel Peter A Bandettini Neil Burgess |
| author_facet | Raphael Kaplan Christian F Doeller Gareth R Barnes Vladimir Litvak Emrah Düzel Peter A Bandettini Neil Burgess |
| author_sort | Raphael Kaplan |
| collection | DOAJ |
| description | The hippocampus is crucial for episodic or declarative memory and the theta rhythm has been implicated in mnemonic processing, but the functional contribution of theta to memory remains the subject of intense speculation. Recent evidence suggests that the hippocampus might function as a network hub for volitional learning. In contrast to human experiments, electrophysiological recordings in the hippocampus of behaving rodents are dominated by theta oscillations reflecting volitional movement, which has been linked to spatial exploration and encoding. This literature makes the surprising cross-species prediction that the human hippocampal theta rhythm supports memory by coordinating exploratory movements in the service of self-directed learning. We examined the links between theta, spatial exploration, and memory encoding by designing an interactive human spatial navigation paradigm combined with multimodal neuroimaging. We used both non-invasive whole-head Magnetoencephalography (MEG) to look at theta oscillations and Functional Magnetic Resonance Imaging (fMRI) to look at brain regions associated with volitional movement and learning. We found that theta power increases during the self-initiation of virtual movement, additionally correlating with subsequent memory performance and environmental familiarity. Performance-related hippocampal theta increases were observed during a static pre-navigation retrieval phase, where planning for subsequent navigation occurred. Furthermore, periods of the task showing movement-related theta increases showed decreased fMRI activity in the parahippocampus and increased activity in the hippocampus and other brain regions that strikingly overlap with the previously observed volitional learning network (the reverse pattern was seen for stationary periods). These fMRI changes also correlated with participant's performance. Our findings suggest that the human hippocampal theta rhythm supports memory by coordinating exploratory movements in the service of self-directed learning. These findings directly extend the role of the hippocampus in spatial exploration in rodents to human memory and self-directed learning. |
| format | Article |
| id | doaj-art-7c06af2a66f14fa98e2f21535f424156 |
| institution | Kabale University |
| issn | 1544-9173 1545-7885 |
| language | English |
| publishDate | 2012-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj-art-7c06af2a66f14fa98e2f21535f4241562025-08-20T03:46:42ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852012-01-01102e100126710.1371/journal.pbio.1001267Movement-related theta rhythm in humans: coordinating self-directed hippocampal learning.Raphael KaplanChristian F DoellerGareth R BarnesVladimir LitvakEmrah DüzelPeter A BandettiniNeil BurgessThe hippocampus is crucial for episodic or declarative memory and the theta rhythm has been implicated in mnemonic processing, but the functional contribution of theta to memory remains the subject of intense speculation. Recent evidence suggests that the hippocampus might function as a network hub for volitional learning. In contrast to human experiments, electrophysiological recordings in the hippocampus of behaving rodents are dominated by theta oscillations reflecting volitional movement, which has been linked to spatial exploration and encoding. This literature makes the surprising cross-species prediction that the human hippocampal theta rhythm supports memory by coordinating exploratory movements in the service of self-directed learning. We examined the links between theta, spatial exploration, and memory encoding by designing an interactive human spatial navigation paradigm combined with multimodal neuroimaging. We used both non-invasive whole-head Magnetoencephalography (MEG) to look at theta oscillations and Functional Magnetic Resonance Imaging (fMRI) to look at brain regions associated with volitional movement and learning. We found that theta power increases during the self-initiation of virtual movement, additionally correlating with subsequent memory performance and environmental familiarity. Performance-related hippocampal theta increases were observed during a static pre-navigation retrieval phase, where planning for subsequent navigation occurred. Furthermore, periods of the task showing movement-related theta increases showed decreased fMRI activity in the parahippocampus and increased activity in the hippocampus and other brain regions that strikingly overlap with the previously observed volitional learning network (the reverse pattern was seen for stationary periods). These fMRI changes also correlated with participant's performance. Our findings suggest that the human hippocampal theta rhythm supports memory by coordinating exploratory movements in the service of self-directed learning. These findings directly extend the role of the hippocampus in spatial exploration in rodents to human memory and self-directed learning.https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1001267&type=printable |
| spellingShingle | Raphael Kaplan Christian F Doeller Gareth R Barnes Vladimir Litvak Emrah Düzel Peter A Bandettini Neil Burgess Movement-related theta rhythm in humans: coordinating self-directed hippocampal learning. PLoS Biology |
| title | Movement-related theta rhythm in humans: coordinating self-directed hippocampal learning. |
| title_full | Movement-related theta rhythm in humans: coordinating self-directed hippocampal learning. |
| title_fullStr | Movement-related theta rhythm in humans: coordinating self-directed hippocampal learning. |
| title_full_unstemmed | Movement-related theta rhythm in humans: coordinating self-directed hippocampal learning. |
| title_short | Movement-related theta rhythm in humans: coordinating self-directed hippocampal learning. |
| title_sort | movement related theta rhythm in humans coordinating self directed hippocampal learning |
| url | https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.1001267&type=printable |
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