Neural Representation of Overlapping Path Segments and Reward Acquisitions in the Monkey Hippocampus
Disambiguation of overlapping events is thought to be the hallmark of episodic memory. Recent rodent studies have reported that when navigating overlapping path segments in the different routes place cell activity in the same overlapping path segments were remapped according to different goal locati...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-09-01
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| Series: | Frontiers in Systems Neuroscience |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fnsys.2019.00048/full |
| _version_ | 1811274120670740480 |
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| author | Rafael Vieira Bretas Rafael Vieira Bretas Jumpei Matsumoto Hiroshi Nishimaru Yusaku Takamura Etsuro Hori Taketoshi Ono Hisao Nishijo |
| author_facet | Rafael Vieira Bretas Rafael Vieira Bretas Jumpei Matsumoto Hiroshi Nishimaru Yusaku Takamura Etsuro Hori Taketoshi Ono Hisao Nishijo |
| author_sort | Rafael Vieira Bretas |
| collection | DOAJ |
| description | Disambiguation of overlapping events is thought to be the hallmark of episodic memory. Recent rodent studies have reported that when navigating overlapping path segments in the different routes place cell activity in the same overlapping path segments were remapped according to different goal locations in different routes. However, it is unknown how hippocampal neurons disambiguate reward delivery in overlapping path segments in different routes. In the present study, we recorded monkey hippocampal neurons during performance of three virtual navigation (VN) tasks in which a monkey alternately navigated two different routes that included overlapping path segments (common central hallway) and acquired rewards in the same locations in overlapping path segments by manipulating a joystick. The results indicated that out of 106 hippocampal neurons, 57 displayed place-related activity (place-related neurons), and 18 neurons showed route-dependent activity in the overlapping path segments, consistent with a hippocampal role in the disambiguation of overlapping path segments. Moreover, 75 neurons showed neural correlates to reward delivery (reward-related neurons), whereas 56 of these 75 reward-related neurons showed route-dependent reward-related activity in the overlapping path segments. The ensemble activity of reward-related neurons represented reward delivery, locations, and routes in the overlapping path segments. In addition, ensemble activity patterns of hippocampal neurons more distinctly represented overlapping path segments than non-overlapping path segments. The present results provide neurophysiological evidence of disambiguation in the monkey hippocampus, consistent with a hippocampal role in episodic memory, and support a recent computational model of “neural differentiation,” in which overlapping items are better represented by repeated retrieval with competitive learning. |
| first_indexed | 2024-04-12T23:13:22Z |
| format | Article |
| id | doaj.art-d89b3e0f77314f67995b427a98b94ab5 |
| institution | Directory Open Access Journal |
| issn | 1662-5137 |
| language | English |
| last_indexed | 2024-04-12T23:13:22Z |
| publishDate | 2019-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Systems Neuroscience |
| spelling | doaj.art-d89b3e0f77314f67995b427a98b94ab52022-12-22T03:12:45ZengFrontiers Media S.A.Frontiers in Systems Neuroscience1662-51372019-09-011310.3389/fnsys.2019.00048476918Neural Representation of Overlapping Path Segments and Reward Acquisitions in the Monkey HippocampusRafael Vieira Bretas0Rafael Vieira Bretas1Jumpei Matsumoto2Hiroshi Nishimaru3Yusaku Takamura4Etsuro Hori5Taketoshi Ono6Hisao Nishijo7System Emotional Science, Graduate School of Medicine and Pharmaceutical University, University of Toyama, Toyama, JapanSymbolic Cognitive Development, Center for Biosystems Dynamics Research, RIKEN, Kobe, JapanSystem Emotional Science, Graduate School of Medicine and Pharmaceutical University, University of Toyama, Toyama, JapanSystem Emotional Science, Graduate School of Medicine and Pharmaceutical University, University of Toyama, Toyama, JapanSystem Emotional Science, Graduate School of Medicine and Pharmaceutical University, University of Toyama, Toyama, JapanSystem Emotional Science, Graduate School of Medicine and Pharmaceutical University, University of Toyama, Toyama, JapanSystem Emotional Science, Graduate School of Medicine and Pharmaceutical University, University of Toyama, Toyama, JapanSystem Emotional Science, Graduate School of Medicine and Pharmaceutical University, University of Toyama, Toyama, JapanDisambiguation of overlapping events is thought to be the hallmark of episodic memory. Recent rodent studies have reported that when navigating overlapping path segments in the different routes place cell activity in the same overlapping path segments were remapped according to different goal locations in different routes. However, it is unknown how hippocampal neurons disambiguate reward delivery in overlapping path segments in different routes. In the present study, we recorded monkey hippocampal neurons during performance of three virtual navigation (VN) tasks in which a monkey alternately navigated two different routes that included overlapping path segments (common central hallway) and acquired rewards in the same locations in overlapping path segments by manipulating a joystick. The results indicated that out of 106 hippocampal neurons, 57 displayed place-related activity (place-related neurons), and 18 neurons showed route-dependent activity in the overlapping path segments, consistent with a hippocampal role in the disambiguation of overlapping path segments. Moreover, 75 neurons showed neural correlates to reward delivery (reward-related neurons), whereas 56 of these 75 reward-related neurons showed route-dependent reward-related activity in the overlapping path segments. The ensemble activity of reward-related neurons represented reward delivery, locations, and routes in the overlapping path segments. In addition, ensemble activity patterns of hippocampal neurons more distinctly represented overlapping path segments than non-overlapping path segments. The present results provide neurophysiological evidence of disambiguation in the monkey hippocampus, consistent with a hippocampal role in episodic memory, and support a recent computational model of “neural differentiation,” in which overlapping items are better represented by repeated retrieval with competitive learning.https://www.frontiersin.org/article/10.3389/fnsys.2019.00048/fullhippocampusplace cellsnavigationoverlappingdisambiguationneural differentiation |
| spellingShingle | Rafael Vieira Bretas Rafael Vieira Bretas Jumpei Matsumoto Hiroshi Nishimaru Yusaku Takamura Etsuro Hori Taketoshi Ono Hisao Nishijo Neural Representation of Overlapping Path Segments and Reward Acquisitions in the Monkey Hippocampus Frontiers in Systems Neuroscience hippocampus place cells navigation overlapping disambiguation neural differentiation |
| title | Neural Representation of Overlapping Path Segments and Reward Acquisitions in the Monkey Hippocampus |
| title_full | Neural Representation of Overlapping Path Segments and Reward Acquisitions in the Monkey Hippocampus |
| title_fullStr | Neural Representation of Overlapping Path Segments and Reward Acquisitions in the Monkey Hippocampus |
| title_full_unstemmed | Neural Representation of Overlapping Path Segments and Reward Acquisitions in the Monkey Hippocampus |
| title_short | Neural Representation of Overlapping Path Segments and Reward Acquisitions in the Monkey Hippocampus |
| title_sort | neural representation of overlapping path segments and reward acquisitions in the monkey hippocampus |
| topic | hippocampus place cells navigation overlapping disambiguation neural differentiation |
| url | https://www.frontiersin.org/article/10.3389/fnsys.2019.00048/full |
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