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Research Articles, Behavioral/Cognitive

Hippocampal Theta and Episodic Memory

Joseph H. Rudoler, Nora A. Herweg and Michael J. Kahana
Journal of Neuroscience 25 January 2023, 43 (4) 613-620; DOI: https://doi.org/10.1523/JNEUROSCI.1045-22.2022
Joseph H. Rudoler
1Computational Memory Lab, Department of Psychology, University of Pennsylvania, Philadelphia, Pennsylvania 19104
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Nora A. Herweg
1Computational Memory Lab, Department of Psychology, University of Pennsylvania, Philadelphia, Pennsylvania 19104
2Department of Neuropsychology, Institute of Cognitive Neuroscience, Faculty of Psychology, Ruhr University Bochum, 44780 Bochum, Germany
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Michael J. Kahana
1Computational Memory Lab, Department of Psychology, University of Pennsylvania, Philadelphia, Pennsylvania 19104
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Abstract

Computational models of rodent physiology implicate hippocampal theta as a key modulator of learning and memory (Buzsáki and Moser, 2013; Lisman and Jensen, 2013), yet human hippocampal recordings have shown divergent theta correlates of memory formation. Herweg et al. (2020) suggest that decreases in memory-related broadband power mask narrowband theta increases. Their survey also notes that the theta oscillations appear most prominently in contrasts that isolate memory retrieval processes and when aggregating signals across large brain regions. We evaluate these hypotheses by analyzing human hippocampal recordings captured as 162 neurosurgical patients (n = 86 female) performed a free recall task. Using the Irregular-Resampling Auto-Spectral Analysis (IRASA) to separate broad and narrowband components of the field potential, we show that (1) broadband and narrowband components of theta exhibit opposite effects, with broadband signals decreasing and narrowband theta increasing during successful encoding; (2) whereas low-frequency theta oscillations increase before successful recall, higher-frequency theta and alpha oscillations decrease, masking the positive effect of theta when aggregating across the full band; and (3) the effects of theta on memory encoding and retrieval do not differ between reference schemes that accentuate local signals (bipolar) and those that aggregate signals globally (whole-brain average). In line with computational models that ascribe a fundamental role for hippocampal theta in memory, our large-scale study of human hippocampal recordings shows that 3–4 Hz theta oscillations reliably increase during successful memory encoding and before spontaneous recall of previously studied items.

SIGNIFICANCE STATEMENT Analyzing recordings from 162 participants, we resolve a long-standing question regarding the role of hippocampal theta oscillations in the formation and retrieval of episodic memories. We show that broadband spectral changes confound estimates of narrowband theta activity, thereby accounting for inconsistent results in the literature. After accounting for broadband effects, we find that increased theta activity marks successful encoding and retrieval of episodic memories, supporting rodent models that ascribe a key role for hippocampal theta in memory function.

  • fractal
  • hippocampus
  • memory
  • oscillations
  • theta

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The Journal of Neuroscience: 43 (4)
Journal of Neuroscience
Vol. 43, Issue 4
25 Jan 2023
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Hippocampal Theta and Episodic Memory
Joseph H. Rudoler, Nora A. Herweg, Michael J. Kahana
Journal of Neuroscience 25 January 2023, 43 (4) 613-620; DOI: 10.1523/JNEUROSCI.1045-22.2022

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Hippocampal Theta and Episodic Memory
Joseph H. Rudoler, Nora A. Herweg, Michael J. Kahana
Journal of Neuroscience 25 January 2023, 43 (4) 613-620; DOI: 10.1523/JNEUROSCI.1045-22.2022
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Keywords

  • fractal
  • hippocampus
  • memory
  • oscillations
  • theta

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