Role of Cerebellar Cortical Protein Synthesis in Transfer of Memory Trace of Cerebellum-Dependent Motor Learning

Okamoto, Tatsuo; Endo, Shogo; Shirao, Tomoaki; Nagao, Soichi

doi:10.1523/jneurosci.1151-11.2011

Cited by 65 publications

(73 citation statements)

References 48 publications

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“…In addition, a recent study has shown that the blockade of protein synthesis in the Fl with anisomycin abolished HOKR adaptation during spaced but not massed training (12). This is consistent with our study that showed rapid structural modifications in the Fl after spaced training, considering that new protein synthesis is necessary for the restructuring of synapses (2).…”

Section: Discussionsupporting

confidence: 93%

“…We also observed a selective influence of the spacing on retention but not acquisition of memory in HOKR adaptation (Fig. 1), which is consistent with the results of a previous study that was performed using a similar model (12). Thus, the spacing effect appears to occur selectively on acquisition or retention of memory depending on learning paradigms.…”

Section: Discussionsupporting

confidence: 91%

“…1F). A previous study using HOKR showed no significant difference in retention between 1-h and 24-h intervals (12). These results indicate that 1-h interval is critical and sufficient for maximal facilitation of memory retention in HOKR adaptation.…”

Section: Discussionsupporting

confidence: 44%

“…A previous study has reported spacing effect on the retention but not on the acquisition of HOKR adaptation (12). Resting intervals of 60 min or longer resulted in a similar retention of HOKR gain after 24 h. Therefore, we tested resting intervals shorter or equal to 60 min within a constant total amount of training to study the effects of various temporal features of the stimulus on HOKR adaptation.…”

Section: Memory Retention But Not Acquisition Is Dependent On the Lenmentioning

confidence: 96%

“…Training trials that include resting intervals between them (spaced training) produce stronger and longer-lasting memories than do the same number of trials with no intervals (massed training) (9). The spacing effect has been observed in a variety of explicit and implicit memory tasks (10)(11)(12)(13), and the molecular mechanisms supporting this phenomenon have been reported (14)(15)(16)(17)(18). Various intracellular signaling molecules such as CREB (19), mitogen-activated protein (MAP) kinase (20,21), and PKA (22,23) underlie the spacing effect and are implicated in the remodeling of neuronal structures (23).…”

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confidence: 99%

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Distinct kinetics of synaptic structural plasticity, memory formation, and memory decay in massed and spaced learning

Aziz

Wang

Kesaf

et al. 2013

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

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Long-lasting memories are formed when the stimulus is temporally distributed (spacing effect). However, the synaptic mechanisms underlying this robust phenomenon and the precise time course of the synaptic modifications that occur during learning remain unclear. Here we examined the adaptation of horizontal optokinetic response in mice that underwent 1 h of massed and spaced training at varying intervals. Despite similar acquisition by all training protocols, 1 h of spacing produced the highest memory retention at 24 h, which lasted for 1 mo. The distinct kinetics of memory are strongly correlated with the reduction of floccular parallel fiber-Purkinje cell synapses but not with AMPA receptor (AMPAR) number and synapse size. After the spaced training, we observed 25%, 23%, and 12% reduction in AMPAR density, synapse size, and synapse number, respectively. Four hours after the spaced training, half of the synapses and Purkinje cell spines had been eliminated, whereas AMPAR density and synapse size were recovered in remaining synapses. Surprisingly, massed training also produced long-term memory and halving of synapses; however, this occurred slowly over days, and the memory lasted for only 1 wk. This distinct kinetics of structural plasticity may serve as a basis for unique temporal profiles in the formation and decay of memory with or without intervals. cerebellar motor learning | AMPA receptor reduction | synapse shrinkage and elimination D uring learning, memories are formed in a specific population of neuronal circuits and are consolidated for persistence (1, 2). These memory processes are supported by discrete subcellular events such as reversible modifications in the efficacy of synaptic transmission (3-5) or persistent structural modifications in the size and number of synaptic connections (6-8). However, how these synaptic modifications relate to the dynamics of formation and decay of memories in behaving animals remains elusive. Memory formation and its persistence are also sensitive to the temporal features of stimulus presentation, as observed in the well-known "spacing effect." Training trials that include resting intervals between them (spaced training) produce stronger and longer-lasting memories than do the same number of trials with no intervals (massed training) (9). The spacing effect has been observed in a variety of explicit and implicit memory tasks (10-13), and the molecular mechanisms supporting this phenomenon have been reported (14-18). Various intracellular signaling molecules such as CREB (19), mitogen-activated protein (MAP) kinase (20, 21), and PKA (22, 23) underlie the spacing effect and are implicated in the remodeling of neuronal structures (23). In vitro studies showed that spaced stimuli induced the protrusion of new filopodia (20) and the recruitment of new synapses (24) in hippocampal neurons. However, despite the existence of numerous behavioral and molecular studies, no conjoint study has elucidated the synaptic correlates that underpin the expression of the spacing effect du...

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Section: Discussionsupporting

confidence: 93%

Section: Discussionsupporting

confidence: 91%

Section: Discussionsupporting

confidence: 44%

Section: Memory Retention But Not Acquisition Is Dependent On the Lenmentioning

confidence: 96%

mentioning

confidence: 99%

See 3 more Smart Citations

Distinct kinetics of synaptic structural plasticity, memory formation, and memory decay in massed and spaced learning

Aziz

Wang

Kesaf

et al. 2013

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

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Efficacy of spaced learning in adaptation of optokinetic response

Pham

Kim

et al. 2020

Brain and Behavior

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Optokinetic reflex (OKR) and vestibulo-ocular reflex (VOR) complement each other to minimize the retinal slip of images within the physiological range of head movement, and OKR allows the eyeball to follow image in motion with the same direction while the head remains stationary. Neural circuits for basic OKR observed in untrained naïve animals are composed of closed-loop structures including nucleus reticularis tegmenti pontis, vestibular nuclei, and oculomotor nuclei. Continuous oscillation of optokinetic drum for a few hours enhances the OKR gain (short-term adaptation of OKR; Ito, 2006; Shutoh

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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 Cerebellar Cortical Protein Synthesis in Transfer of Memory Trace of Cerebellum-Dependent Motor Learning

Cited by 65 publications

References 48 publications

Distinct kinetics of synaptic structural plasticity, memory formation, and memory decay in massed and spaced learning

Distinct kinetics of synaptic structural plasticity, memory formation, and memory decay in massed and spaced learning

Efficacy of spaced learning in adaptation of optokinetic response

Glial modulation of the parallel memory formation

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