Cited by 14Neural dynamics and brain functionMemory and Neural MechanismsSleep and Wakefulness Research

Enhancement of hippocampal-thalamocortical temporal coordination during slow-frequency long-duration anterior thalamic spindles

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Alizadeh, Zahra, Azimi, Amin, Ghorbani, Maryam·2022·The Journal of Neuroscience

Published version of a preprint

Abstract

Temporal nesting of cortical slow oscillations, thalamic spindles, and hippocampal ripples indicates multiregional neuronal interactions required for memory consolidation. However, how the thalamic activity during spindles organizes hippocampal dynamics remains largely undetermined. We analyzed simultaneous recordings of anterodorsal thalamus and CA1 in male mice to determine the contribution of thalamic spindles in cross-regional synchronization. Our results indicated that temporal hippocampo-thalamocortical coupling was more enhanced during slower and longer thalamic spindles. Additionally, spindles occurring closer to slow oscillation trough were more strongly coupled to ripples. We found that the temporal association between CA1 spiking/ripples and thalamic spindles was stronger following spatial exploration compared with baseline sleep. We further developed a hippocampal-thalamocortical model to explain the mechanism underlying the duration and frequency-dependent coupling of thalamic spindles to hippocampal activity. Our findings shed light on our understanding of the functional role of thalamic activity during spindles on multiregional information transfer. SIGNIFICANCE STATEMENT The contribution of thalamic spindles with differential properties to cross-regional synchronization and information transfer still remains poorly understood. Using simultaneous anterodorsal thalamic and hippocampal recordings from naturally sleeping mice before and after exploration, we found strong coupling of CA1 units to anterodorsal thalamic spindles and increase of this coupling following spatial experience. We further showed that the temporal coupling of CA1 units and hippocampal ripples with thalamic spindles and the spindle-associated modulation of CA1 units with ripples were stronger for spindles with slower frequency of oscillations. Our experimental as well as computational findings using a hippocampal-thalamocortical model provide the first demonstration that spindle frequency and duration can provide valuable information about the underlying multiregional interactions essential for memory consolidation computations.

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Crossref · 10.1523/jneurosci.2515-21.2022

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  • The anterior thalamus might be specifically involved in coordinating hippocampal memory replay with thalamocortical activity.

    “The anterior thalamus might be specifically involved in coordinating hippocampal memory replay with thalamocortical activity.189”

    From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [189]

    The Abstract and Discussion report that anterodorsal thalamic spindles are temporally coupled with CA1 activity and hippocampal ripples, with stronger coupling after spatial exploration. This supports a possible coordinating role, but the paper measures spiking and ripples, not hippocampal memory replay itself. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • Sleep spindles are associated with signs of increased synchronization between hippocampal and neocortical activity in both mice and humans.

    “Indeed, sleep spindles have been found to be associated with signs of increased synchronization between hippocampal and neocortical activity in both mice 189 and humans.34”

    From Sleep—A brain-state serving systems memory consolidation (2023) · cites this paper as [189]

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Authors
Alizadeh, Z., Azimi, A., & Ghorbani, M.
Affiliations
  • Ferdowsi University of Mashhad (IR)
  • Institute for Advanced Studies in Basic Sciences (IR)
Corresponding author
Ghorbani, Maryam
Venue
The Journal of Neuroscience
Published
2022-08-15
Volume
42
Issue
38
Pages
7222-7243
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W4291618525
Cited by
14
References
89
Citations by year
2026: 1 · 2025: 4 · 2024: 2 · 2023: 7
FWCI
1.68
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
Keywords
hippocampal ripples, slow oscillations, CA1, memory consolidation, spatial exploration, sleep

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