Post-training cerebellar cortical activity plays an important role for consolidation of memory of cerebellum-dependent motor learning

Okamoto, Tatsuo; Shirao, Tomoaki; Shutoh, Fumihiro; Suzuki, Toshinori; Nagao, Soichi

doi:10.1016/j.neulet.2011.08.056

Cited by 36 publications

(30 citation statements)

References 28 publications

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“…Although several theoretical models have addressed the question of how multiple plasticity mechanisms work together in cerebellar motor learning (11)(12)(13)(14), none has explicitly taken the memory consolidation process during posttraining periods into consideration. Our model reproduced previously reported oculomotor behavioral data obtained from wild-type mice (8)(9)(10). Notably, the simulated nuclear long-term memory formed mostly after training and relatively little during training, consistent with the hypothesis of posttraining memory consolidation.…”

supporting

confidence: 86%

“…Fig. 2B plots the OKR gain before the daily training against the training period (day) in the simulation results and experimental data (9). The simulated OKR gain increased linearly day by day and the slope became steeper with the delay.…”

Section: Significancementioning

confidence: 99%

“…Infusion of the GABA A receptor agonist, muscimol, to the cerebellar cortex immediately after training disrupts memory transfer (9). Muscimol infusion suppresses firing of PCs by the activation of GABA A receptors on PCs, and thereby VN is released from PC inhibition.…”

Section: Significancementioning

confidence: 99%

“…This MarrAlbus-Ito hypothesis (2, 3), however, has been challenged since Miles and Lisberger's proposal (4) that long-term potentiation (LTP) at mossy fiber-vestibular nuclear neuron (MF-VN) synapses, not LTD at PF-PC synapses, underlies vestibuloocular reflex (VOR) gain adaptation (4)(5)(6)(7). In a recent study on optokinetic response (OKR) gain adaptation, we found evidence that might resolve the controversy: LTD at PF-PC synapses (PF-LTD) and LTP at MF-VN synapses (MF-LTP) play different roles in OKR adaptation (8)(9)(10). Namely, PF-LTD accounts for short-term memory in PCs during 1-h training, whereas MF-LTP forms long-term memory in VN after the 1-h training that accumulates during repeated trials of 1-h training.…”

mentioning

confidence: 99%

“…Namely, PF-LTD accounts for short-term memory in PCs during 1-h training, whereas MF-LTP forms long-term memory in VN after the 1-h training that accumulates during repeated trials of 1-h training. It thus appears as if short-term memory formed in PCs during 1-h training is transferred to VN after training to consolidate as long-term memory (8)(9)(10).…”

mentioning

confidence: 99%

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Modeling memory consolidation during posttraining periods in cerebellovestibular learning

Yamazaki¹,

Nagao

Lennon

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Long-term depression (LTD) at parallel fiber-Purkinje cell (PF-PC) synapses is thought to underlie memory formation in cerebellar motor learning. Recent experimental results, however, suggest that multiple plasticity mechanisms in the cerebellar cortex and cerebellar/vestibular nuclei participate in memory formation. To examine this possibility, we formulated a simple model of the cerebellum with a minimal number of components based on its known anatomy and physiology, implementing both LTD and long-term potentiation (LTP) at PF-PC synapses and mossy fibervestibular nuclear neuron (MF-VN) synapses. With this model, we conducted a simulation study of the gain adaptation of optokinetic response (OKR) eye movement. Our model reproduced several important aspects of previously reported experimental results in wild-type and cerebellum-related gene-manipulated mice. First, each 1-h training led to the formation of short-term memory of learned OKR gain at PF-PC synapses, which diminished throughout the day. Second, daily repetition of the training gradually formed long-term memory that was maintained for days at MF-VN synapses. We reproduced such memory formation under various learning conditions. Third, long-term memory formation occurred after training but not during training, indicating that the memory consolidation occurred during posttraining periods. Fourth, spaced training outperformed massed training in long-term memory formation. Finally, we reproduced OKR gain changes consistent with the changes in the vestibuloocular reflex (VOR) previously reported in some genemanipulated mice.cerebellum | plasticity | memory consolidation | posttraining period | Marr-Albus-Ito theory L ong-term depression (LTD) at parallel fiber-Purkinje cell (PF-PC) synapses in the cerebellar cortex has been thought to be the major mechanism of motor learning (1). This MarrAlbus-Ito hypothesis (2, 3), however, has been challenged since Miles and Lisberger's proposal (4) that long-term potentiation (LTP) at mossy fiber-vestibular nuclear neuron (MF-VN) synapses, not LTD at PF-PC synapses, underlies vestibuloocular reflex (VOR) gain adaptation (4-7). In a recent study on optokinetic response (OKR) gain adaptation, we found evidence that might resolve the controversy: LTD at PF-PC synapses (PF-LTD) and LTP at MF-VN synapses (MF-LTP) play different roles in OKR adaptation (8-10). Namely, PF-LTD accounts for short-term memory in PCs during 1-h training, whereas MF-LTP forms long-term memory in VN after the 1-h training that accumulates during repeated trials of 1-h training. It thus appears as if short-term memory formed in PCs during 1-h training is transferred to VN after training to consolidate as long-term memory (8-10).To investigate the mechanisms of this memory transfer and posttraining consolidation, we conducted a computer simulation study using a simple theoretical model of the cerebellovestibular system including both LTD and LTP at PF-PC synapses and MF-VN synapses. Although several theoretical models have addressed the question of ...

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supporting

confidence: 86%

Section: Significancementioning

confidence: 99%

Section: Significancementioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

See 3 more Smart Citations

Modeling memory consolidation during posttraining periods in cerebellovestibular learning

Yamazaki¹,

Nagao

Lennon

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Glial modulation of the parallel memory formation

Kanaya

Ito

Morizawa

et al. 2023

Glia

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Actions from glial cells could affect the readiness and efficacy of learning and memory. Using a mouse cerebellar-dependent horizontal optokinetic response motor learning paradigm, short-term memory (STM) formation during the online training period and long-term memory (LTM) formation during the offline rest period were studied. A large variability of online and offline learning efficacies was found. The early bloomers with booming STM often had a suppressed LTM formation and late bloomers with no apparent acute training effect often exhibited boosted offline learning performance. Anion channels containing LRRC8A are known to release glutamate. Conditional knockout of LRRC8A specifically in astrocytes including cerebellar Bergmann glia resulted in a complete loss of STM formation while the LTM formation during the rest period remained. Optogenetic manipulation of glial activity by channelrhodopsin-2 or archaerhodopsin-T (ArchT) during the online training resulted in enhancement or suppression of STM formation, respectively.STM and LTM are likely to be triggered simultaneously during online training, but LTM is expressed later during the offline period. STM appears to be volatile and the achievement during the online training is not handed over to LTM. In addition, we found that glial ArchT photoactivation during the rest period resulted in the augmentation of LTM formation. These data suggest that STM formation and LTM formation are parallel separate processes. Strategies to weigh more on the STM or the LTM could depend on the actions of the glial cells.

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Role of the Cerebellum in the Acquisition and Consolidation of Memory of Motor Learning

Nagao

2021

Contemporary Clinical Neuroscience

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Post-training cerebellar cortical activity plays an important role for consolidation of memory of cerebellum-dependent motor learning

Cited by 36 publications

References 28 publications

Modeling memory consolidation during posttraining periods in cerebellovestibular learning

Modeling memory consolidation during posttraining periods in cerebellovestibular learning

Glial modulation of the parallel memory formation

Role of the Cerebellum in the Acquisition and Consolidation of Memory of Motor Learning

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