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Functional MRI reveals brain-wide actions of thalamically-initiated oscillatory activities on associative memory consolidation

Author

Listed:
  • Xunda Wang

    (The University of Hong Kong
    The University of Hong Kong)

  • Alex T. L. Leong

    (The University of Hong Kong
    The University of Hong Kong)

  • Shawn Z. K. Tan

    (The University of Hong Kong)

  • Eddie C. Wong

    (The University of Hong Kong
    The University of Hong Kong)

  • Yilong Liu

    (The University of Hong Kong
    The University of Hong Kong)

  • Lee-Wei Lim

    (The University of Hong Kong)

  • Ed X. Wu

    (The University of Hong Kong
    The University of Hong Kong
    The University of Hong Kong)

Abstract

As a key oscillatory activity in the brain, thalamic spindle activities are long believed to support memory consolidation. However, their propagation characteristics and causal actions at systems level remain unclear. Using functional MRI (fMRI) and electrophysiology recordings in male rats, we found that optogenetically-evoked somatosensory thalamic spindle-like activities targeted numerous sensorimotor (cortex, thalamus, brainstem and basal ganglia) and non-sensorimotor limbic regions (cortex, amygdala, and hippocampus) in a stimulation frequency- and length-dependent manner. Thalamic stimulation at slow spindle frequency (8 Hz) and long spindle length (3 s) evoked the most robust brain-wide cross-modal activities. Behaviorally, evoking these global cross-modal activities during memory consolidation improved visual-somatosensory associative memory performance. More importantly, parallel visual fMRI experiments uncovered response potentiation in brain-wide sensorimotor and limbic integrative regions, especially superior colliculus, periaqueductal gray, and insular, retrosplenial and frontal cortices. Our study directly reveals that thalamic spindle activities propagate in a spatiotemporally specific manner and that they consolidate associative memory by strengthening multi-target memory representation.

Suggested Citation

  • Xunda Wang & Alex T. L. Leong & Shawn Z. K. Tan & Eddie C. Wong & Yilong Liu & Lee-Wei Lim & Ed X. Wu, 2023. "Functional MRI reveals brain-wide actions of thalamically-initiated oscillatory activities on associative memory consolidation," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37682-8
    DOI: 10.1038/s41467-023-37682-8
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    1. N. K. Logothetis & O. Eschenko & Y. Murayama & M. Augath & T. Steudel & H. C. Evrard & M. Besserve & A. Oeltermann, 2012. "Hippocampal–cortical interaction during periods of subcortical silence," Nature, Nature, vol. 491(7425), pages 547-553, November.
    2. Jinhee Baek & Sukchan Lee & Taesup Cho & Seong-Wook Kim & Minsoo Kim & Yongwoo Yoon & Ko Keun Kim & Junweon Byun & Sang Jeong Kim & Jaeseung Jeong & Hee-Sup Shin, 2019. "Neural circuits underlying a psychotherapeutic regimen for fear disorders," Nature, Nature, vol. 566(7744), pages 339-343, February.
    3. S. M. Purcell & D. S. Manoach & C. Demanuele & B. E. Cade & S. Mariani & R. Cox & G. Panagiotaropoulou & R. Saxena & J. Q. Pan & J. W. Smoller & S. Redline & R. Stickgold, 2017. "Characterizing sleep spindles in 11,630 individuals from the National Sleep Research Resource," Nature Communications, Nature, vol. 8(1), pages 1-16, August.
    4. Anuck Sawangjit & Carlos N. Oyanedel & Niels Niethard & Carolina Salazar & Jan Born & Marion Inostroza, 2018. "The hippocampus is crucial for forming non-hippocampal long-term memory during sleep," Nature, Nature, vol. 564(7734), pages 109-113, December.
    5. Dheeraj S. Roy & Young-Gyun Park & Minyoung E. Kim & Ying Zhang & Sachie K. Ogawa & Nicholas DiNapoli & Xinyi Gu & Jae H. Cho & Heejin Choi & Lee Kamentsky & Jared Martin & Olivia Mosto & Tomomi Aida , 2022. "Brain-wide mapping reveals that engrams for a single memory are distributed across multiple brain regions," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    6. Nikos K. Logothetis & Jon Pauls & Mark Augath & Torsten Trinath & Axel Oeltermann, 2001. "Neurophysiological investigation of the basis of the fMRI signal," Nature, Nature, vol. 412(6843), pages 150-157, July.
    7. Randolph F. Helfrich & Janna D. Lendner & Bryce A. Mander & Heriberto Guillen & Michelle Paff & Lilit Mnatsakanyan & Sumeet Vadera & Matthew P. Walker & Jack J. Lin & Robert T. Knight, 2019. "Bidirectional prefrontal-hippocampal dynamics organize information transfer during sleep in humans," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    8. Charles W. Dickey & Anna Sargsyan & Joseph R. Madsen & Emad N. Eskandar & Sydney S. Cash & Eric Halgren, 2021. "Travelling spindles create necessary conditions for spike-timing-dependent plasticity in humans," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
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