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Role of the Hippocampus in Distinct Memory Traces: Timing of Match and Mismatch Enhancement Revealed by Intracranial Recording

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Abstract

A previous functional magnetic resonance imaging study reported evidence for parallel memory traces in the hippocampus: a controlled match signal detecting matches to internally-generated goal states and an automatic mismatch signal identifying unpredicted perceptual novelty. However, the timing information in this process is unknown. In the current study, facilitated by the high spatial and temporal resolution of intracranial recording from human patients, we confirmed that the left posterior hippocampus played an important role in the goal match enhancement effect, in which combinations of object identity and location were involved. We also found that this effect happened within 520 ms to 735 ms after the probe onset, ~150 ms later than the perceptual mismatch enhancement found bilaterally in both the anterior and posterior hippocampus. More specifically, the latency of the perceptual mismatch enhancement effect of the right hippocampus was positively correlated with the performance accuracy. These results suggested that the hippocampus is crucial in working memory if features binding with location are involved in the task and the goal match enhancement effect happens after perceptual mismatch enhancement, implying the dissociation of different components of working memory at the hippocampus. Moreover, single trial decoding results suggested that the intracranial field potential response in the right hippocampus can classify the match or switch task. This is consistent with the findings that the right hippocampal activity observed during the simulation of the future events may reflect the encoding of the simulation into memory.

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Acknowledgements

We thank the patients for their cooperation in this study. We also thank Gabriel Kreiman, Jedediah Singer and Kun Hu for their assistance and support. Many thanks to the doctors and nurses in Beijing Functional Neurosurgery Institute for their cooperation, especially Xueyuan Wang, Xi Zhang, Cuiping Xu, and Chang Liu. We also acknowledge Fenghuachangtai Company for providing the device for ECoG recording. This work was supported by grants from the Ministry of Science and Technology of China (2015CB351701 and 2012CB825500), the National Natural Science Foundation of China (91132302), and the Chinese Academy of Sciences (XDB2010001 and XDB2050001).

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Authors and Affiliations

  1. Beijing Institute of Functional Neurosurgery, Xuanwu Hospital, Capital Medical University, Beijing, 100053, China

    Bing Ni, Tao Yu, Hongwei Zhu & Yongjie Li

  2. State Key Laboratory of Brain and Cognitive Science, Institute of Biophysics, The Innovation Center of Excellence on Brain Science, Chinese Academy of Sciences, Beijing, 100101, China

    Ruijie Wu & Zuxiang Liu

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  1. Bing Ni
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Correspondence to Ruijie Wu.

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Ni, B., Wu, R., Yu, T. et al. Role of the Hippocampus in Distinct Memory Traces: Timing of Match and Mismatch Enhancement Revealed by Intracranial Recording. Neurosci. Bull. 33, 664–674 (2017). https://doi.org/10.1007/s12264-017-0172-8

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  • DOI: https://doi.org/10.1007/s12264-017-0172-8

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