Sleep-Dependent θ Oscillations in the Human Hippocampus and Neocortex
Open accessAbstract
Hippocampal theta waves recorded during rapid eye movement (REM) sleep are thought to play a critical role in memory consolidation in lower mammals, but previous attempts to detect similar theta oscillations in the human hippocampus have been unsuccessful. Using subdural and depth recordings from epileptic patients, we now report the first evidence of state-dependent hippocampal theta waves (4-7 Hz) in humans. Unlike the continuous theta in rodents, however, these oscillations were consistently observed during REM sleep in short (approximately 1 sec) bursts and during transitions to wake in longer epochs. Theta waves were also observed in the basal temporal lobe and frontal cortex during transitions from sleep to wake and in quiet wakefulness but not in REM, and they were not coherent with hippocampal theta oscillations. The absence of functional coupling between neocortex and hippocampus during theta periods indicates that multiple theta generators exist in the human brain, and that they are dynamically regulated by brain state. Gamma oscillations were also present during REM theta bursts, but the fluctuations in gamma power were not associated with theta phase, pointing out another significant difference between rodent and human theta properties. Together, these findings suggest that the generation mechanisms of theta oscillations in humans might have evolved from tonic to phasic in hippocampus during REM sleep and extended from hippocampus to cortex, where they appear in certain wakefulness-related states.
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Compared with wakefulness or SWS, EEG activity during REM sleep shows reduced coherence between limbic-hippocampal and neocortical circuitry in a wide range of frequencies including theta and gamma.
“Compared with wakefulness or SWS, EEG activity during REM sleep shows reduced coherence between limbic-hippocampal and neocortical circuitry in a wide range of frequencies including theta and gamma (51,174,293).”
From About Sleep's Role in Memory (2013) · cites this paper as [174]
The Results report that hippocampal–neocortical coherence was absent regardless of brain state, rather than reduced specifically during REM sleep relative to wakefulness or SWS. The cited passage concerns theta-range oscillations and does not establish the claimed comparison across frequencies including gamma. (LLM, conf=0.88)
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Experimental — accuracy not yet measuredThe theta rhythm is directly connected with some areas engaged in memory processing and represents an EEG marker of hippocampal activity.
“the theta rhythm is directly connected with some areas engaged in memory processing and, in particular, it represents an EEG marker of hippocampal activity”
From The Functional Role of Dreaming in Emotional Processes (2019) · cites this paper as Cantero et al., 2003
The Introduction (page not provided) describes theta oscillations as a prominent feature of the hippocampus and says they have been hypothesized to participate in memory encoding and retrieval. The Discussion (page not provided) reports independent, state-dependent hippocampal and cortical theta generators, so it does not establish that theta generally marks hippocampal activity or is directly connected across memory-related areas. (LLM, conf=0.85)
Experimental — accuracy not yet measuredTheta rhythm may be considered as the local field potential that represents an electrophysiological marker of hippocampal activity both during awake behavior and REM sleep.
“Theta rhythm may be considered as the local field potential (LFP) that represents an electrophysiological marker of hippocampal activity (Rutishauser et al., 2010), both during awake behavior and REM sleep (Klimesch, 1996; Cantero et al., 2003).”
From EEG oscillations during sleep and dream recall: state- or trait-like individual differences? (2015) · cites this paper as Cantero et al., 2003
The Results report hippocampal theta bursts during REM sleep and during transitions from sleep to waking. They also state that none of the three patients with hippocampal-depth electrodes showed these oscillations during quiet wakefulness. Thus Cantero et al. support the REM-sleep portion, but their findings do not establish hippocampal theta during awake behavior generally; the LFP-marker wording is cited to a different source. (LLM, conf=0.88)
Experimental — accuracy not yet measured
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“It has been hypothesized that the theta rhythm is directly connected with some areas engaged in memory processing and, in particular, it represents an EEG marker of hippocampal activity (Klimesch, 1996; Cantero et al., 2003; Rutishauser et al., 2010) modulating neuronal changes in hippocampal formation and in neocorti…”
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- Authors
- Cantero, J. L., Atienza, M., Stickgold, R., Kahana, M. J., Madsen, J. R., & Kocsis, B.
- Affiliations
- Harvard University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2003-11-26
- Volume
- 23
- Issue
- 34
- Pages
- 10897-10903
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6740994
- OpenAlex
- W2132486749
- Cited by
- 312
- References
- 48
- Citations by year
- 2026: 3 · 2025: 14 · 2024: 12 · 2023: 9 · 2022: 13 · 2021: 10 · 2020: 12 · 2019: 10 · 2018: 13 · 2017: 15 · 2016: 16 · 2015: 15 · 2014: 15 · 2013: 31 · 2012: 22
- FWCI
- 5.37
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministerio de Ciencia y Tecnología
- National Institutes of Health
- National Institute of Mental Health (R01MH062525, MH-61975, MH-48832, MH-062525, R01MH048832, R01MH061975)
- National Institute on Drug Abuse (R01DA011744, DA-11744)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- hippocampal theta oscillations, REM sleep, sleep-wake transition, memory consolidation, neocortex, frontal cortex, gamma oscillations, theta-gamma coupling, epilepsy patients
- MeSH terms
- Adolescent, Adult, Biological Clocks, Child, Electrodes, Implanted, Epilepsy, Hippocampus, Humans, Male, Sleep, Theta Rhythm, Wakefulness, Neocortex
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