Cited by 4Sleep and Wakefulness ResearchMemory and Neural MechanismsNeural dynamics and brain function

Firing Activities of REM- and NREM-Preferring Neurons Are Differently Modulated by Fast Network Oscillations and Behavior in the Hippocampus, Prelimbic Cortex, and Amygdala

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Kajiya, Risa, Miyawaki, Hiroyuki, Nakahara, Hirokazu, Mizuseki, Kenji·2025·eneuro

Abstract

Sleep consists of two alternating states—rapid eye movement (REM) and non-REM (NREM) sleep. Neurons adjust their firing activity based on brain state, however, the extent to which this modulation varies across neurons and brain regions remains poorly understood. This study analyzed previously acquired 17-h continuous recordings of single-unit activity and local field potentials in the ventral hippocampal CA1 region, prelimbic cortex layer 5, and basolateral nucleus of the amygdala of fear-conditioned rats. The findings indicate that more than half of the neurons fired faster during REM sleep than during NREM sleep, although a notable subset of neurons exhibited the opposite preference, firing preferentially during NREM sleep. During sleep, the overall firing activity of both REM- and NREM-preferring neurons decreased. However, fast network oscillations, including hippocampal sharp-wave ripples (SWRs), amygdalar high-frequency oscillations, cortical ripples, and cortical spindles, differentially modulated REM- versus NREM-preferring neurons. During wakefulness, REM-preferring neurons fired more slowly but were more intensely activated by SWRs and shock presentations than NREM-preferring neurons. Moreover, during fast network oscillations in sleep, neurons with similar REM/NREM preferences exhibited stronger within- and cross-regional coactivation than those with differing preferences. Conversely, during awake SWRs in fear conditioning sessions, neurons with different REM/NREM preferences showed stronger interregional coactivation than those with similar preferences. These findings suggest that the distinct activity patterns of REM- and NREM-preferring neurons, potentially reflecting different roles in memory, affect local and global networks differently, thereby balancing experience-dependent network modifications with sleep-dependent homeostatic regulation of neuronal excitability.

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Crossref · 10.1523/eneuro.0575-24.2025

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  • The rate of action potential firing reportedly increases only modestly (<1.3-fold) in the retrosplenial cortex and primary visual cortex, while decreasing in motor and somatosensory cortices during REM sleep.

    “However, the rate of action potential firing reportedly increases only modestly (<1.3-fold) in the retrosplenial cortex (RSC) and primary visual cortex (V1), while decreasing in motor and somatosensory cortices during REM sleep61–63.”

    From Energy paradox in REM sleep: balancing supply and consumption in brain metabolism (2026) · cites this paper as [62]

    The Results section reports REM-related firing in ventral CA1, prelimbic cortex, and basolateral amygdala, not the four cortical areas named in the claim. Searches for retrosplenial cortex, somatosensory cortex, and the <1.3-fold figure found no passage in our copy establishing the claimed regional pattern. (LLM, conf=0.75)

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Authors
Kajiya, R., Miyawaki, H., Nakahara, H., & Mizuseki, K.
Affiliations
Osaka City University (JP)
Corresponding author
  • Miyawaki, Hiroyuki
  • Mizuseki, Kenji
Venue
eneuro
Published
2025-05
Volume
12
Issue
5
Pages
ENEURO.0575-24.2025
ISSN
2373-2822 (ISSN-L)
OpenAlex
W4410392806
Cited by
4
References
84
Citations by year
2026: 3 · 2025: 1
FWCI
2.28
Type
journal article
Language
en
Open access
Locations
  • eNeuro (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Institutional Repositories DataBase (IRDB) (submittedVersion)
Funders
  • MEXT | Japan Society for the Promotion of Science (24H00862, 24K02340, 23H04681, 22K19483, 21H00209, 25H02508)
  • Japan Agency for Medical Research and Development (JP24wm0625216)
  • Brain Science Foundation
  • Asahi Glass Foundation
  • Shimadzu Science Foundation
  • Life Science Foundation of Japan
  • Astellas Foundation for Research on Metabolic Disorders
  • Takeda Science Foundation
  • Naito Foundation
  • Sumitomo Foundation
  • Sumitomo Electric group CSR Foundation
  • Ichiro Kanehara Foundation for the Promotion of Medical Sciences and Medical Care
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords
REM sleep, NREM sleep, sleep-dependent memory consolidation, hippocampal CA1, prelimbic cortex, basolateral amygdala, sharp-wave ripples, high-frequency oscillations, sleep spindles, fear conditioning, single-unit activity, local field potentials, network oscillations
MeSH terms
Action Potentials, Amygdala, Animals, Conditioning, Classical, Fear, Hippocampus, Male, Neurons, Sleep Stages, Sleep, REM, Wakefulness, Rats, Sprague-Dawley, Prefrontal Cortex, Rats

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