A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning
Abstract
The theta rhythm appears in the rat hippocampal electroencephalogram during exploration and shows phase locking to stimulus acquisition. Lesions that block theta rhythm impair performance in tasks requiring reversal of prior learning, including reversal in a T-maze, where associations between one arm location and food reward need to be extinguished in favor of associations between the opposite arm location and food reward. Here, a hippocampal model shows how theta rhythm could be important for reversal in this task by providing separate functional phases during each 100-300 msec cycle, consistent with physiological data. In the model, effective encoding of new associations occurs in the phase when synaptic input from entorhinal cortex is strong and long-term potentiation (LTP) of excitatory connections arising from hippocampal region CA3 is strong, but synaptic currents arising from region CA3 input are weak (to prevent interference from prior learned associations). Retrieval of old associations occurs in the phase when entorhinal input is weak and synaptic input from region CA3 is strong, but when depotentiation occurs at synapses from CA3 (to allow extinction of prior learned associations that do not match current input). These phasic changes require that LTP at synapses arising from region CA3 should be strongest at the phase when synaptic transmission at these synapses is weakest. Consistent with these requirements, our recent data show that synaptic transmission in stratum radiatum is weakest at the positive peak of local theta, which is when previous data show that induction of LTP is strongest in this layer.
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The theta rhythm is thought to be important for organizing disparate memory tasks.
“The theta rhythm is thought to be important for organizing disparate memory tasks (Lisman and Idiart, 1995; Hasselmo et al., 2002; Hasselmo, 2005; Lisman and Jensen, 2013; Siegle and Wilson, 2014)”
From Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit (2016) · cites this paper as Hasselmo et al., 2002
Phase preferential firing may aid information processing tasks by providing order and allowing multiple channels of information to be processed in parallel.
“In turn, phase preferential firing may aid information processing tasks by providing order and allowing multiple channels of information to be processed in parallel (Jensen and Lisman, 2000; Hasselmo et al., 2002; Womelsdorf et al., 2007; Schomburg et al., 2014; Jeewajee et al., 2014; Maris et al., 2016).”
From Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit (2016) · cites this paper as Hasselmo et al., 2002
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- Authors
- Hasselmo, M. E., Bodelón, C., & Wyble, B. P.
- Affiliations
- Boston University (US)
- Department of Psychology, Program in Neuroscience and Center for BioDynamics, Boston University, Boston, MA 02215, U.S.A.
- Corresponding author
- Hasselmo, Michael E.
- Bodelón, Clara
- ORCID
- Hasselmo, Michael E.
- Venue
- Neural Computation
- Publisher
- MIT Press
- Published
- 2002-04-01
- Volume
- 14
- Issue
- 4
- Pages
- 793-817
- ISSN
- 0899-7667 (ISSN-L)
- 1530-888X
- OpenAlex
- W2152372327
- Cited by
- 875
- References
- 60
- Citations by year
- 2026: 57 · 2025: 56 · 2024: 44 · 2023: 38 · 2022: 43 · 2021: 51 · 2020: 44 · 2019: 36 · 2018: 36 · 2017: 44 · 2016: 30 · 2015: 37 · 2014: 48 · 2013: 36 · 2012: 26
- FWCI
- 13.91
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neural Computation (publishedVersion)
- PubMed (publishedVersion)
- Kent Academic Repository (University of Kent) (submittedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (MH 60013, MH61492, R01MH061492)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- hippocampal theta rhythm, reversal learning, spatial learning, T-maze, long-term potentiation, depotentiation, entorhinal cortex, CA3, synaptic transmission, stratum radiatum, memory encoding, memory retrieval, extinction, phase locking
- MeSH terms
- Algorithms, Animals, Electroencephalography, Hippocampus, Learning, Membrane Potentials, Memory, Models, Neurological, Neuronal Plasticity, Psychomotor Performance, Reversal Learning, Theta Rhythm, Entorhinal Cortex, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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