Glial modulation of the parallel memory formation

Abstract

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.

Plastic vasomotion entrainment

“…We have shown above that the frequency-locked vasomotion in the cortex also got entrained with repeated training sessions ( Figure 3 ). It has been shown that HOKR performance increase relies on the neuronal and glial activity in the cerebellar flocculus ( Kanaya et al, 2023 ). We next evaluated whether the plasticity of the vasomotion dynamics in the flocculus correlates with the HOKR performance increase.…”

“…It is possible that vasomotion enhancement may increase the meta-plasticity and provide a basis for efficient neuronal plasticity to occur. In the cerebellum, neuron-to-astrocyte (or Bergmann glia) ( Matsui et al, 2005 ; Matsui and Jahr, 2004 ; Matsui and Jahr, 2003 ) and astrocyte-to-neuron ( Beppu et al, 2021 ; Beppu et al, 2014 ; Sasaki et al, 2012 ) signaling pathways have been identified and such neuron-astrocyte interaction has been shown to be essential for the online HOKR learning to occur ( Kanaya et al, 2023 ). Late offline HOKR learning was dependent in part on the phagocytosis activity of astrocytes ( Morizawa et al, 2022 ).…”

“…In fiber photometry experiments, the eye movements were simultaneously recorded. The method of recording and analyzing eye movement was previously described in detail ( Kanaya et al, 2023 ). During the HOKR experiments, the mouse was exposed to white noise sounds, which helped keep the mouse alert.…”

“…The horizontally oscillating visual pattern that was used in this study is known to induce optokinetic response (HOKR). Repeated exposure to such a pattern results in an increased amplitude of the HOKR eye movement ( Ito, 1982 ; Kanaya et al, 2023 ; Waespe and Henn, 1977 ). Neuronal circuit plasticity required for the HOKR learning takes place in the flocculus region of the cerebellum.…”

Plastic vasomotion entrainment

“…It is possible that vasomotion enhancement may increase the meta-plasticity and provide a basis for efficient neuronal plasticity to occur. In the cerebellum, neuron-to-astrocyte (or Bergmann glia) (Matsui et al, 2005; Matsui and Jahr, 2004, 2003) and astrocyte-to-neuron (Beppu et al, 2021, 2014; Sasaki et al, 2012) signaling pathways have been identified and such neuron-astrocyte interaction has been shown to be essential for the online HOKR learning to occur (Kanaya et al, 2023). Late offline HOKR learning was dependent in part on the phagocytosis activity of astrocytes (Morizawa et al, 2022).…”