---
_id: '1919'
abstract:
- lang: eng
text: 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.
acknowledgement: his work was supported by Solution Oriented Research for Science
and Technology (R.S.), Core Research for Evolutional Science and Technology, Japan
Science and Technology Agency (Y.F.), and Grants-in-Aid for Scientific Research
on Priority Areas-Molecular Brain Sciences 16300114 (to R.S.) and 18022043 (to Y.F.).
author:
- first_name: Wajeeha
full_name: Aziz, Wajeeha
last_name: Aziz
- first_name: Wen
full_name: Wang, Wen
last_name: Wang
- first_name: Sebnem
full_name: Kesaf, Sebnem
id: 401AB46C-F248-11E8-B48F-1D18A9856A87
last_name: Kesaf
- first_name: Alsayed
full_name: Mohamed, Alsayed
last_name: Mohamed
- first_name: Yugo
full_name: Fukazawa, Yugo
last_name: Fukazawa
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
citation:
ama: Aziz W, Wang W, Kesaf S, Mohamed A, Fukazawa Y, Shigemoto R. Distinct kinetics
of synaptic structural plasticity, memory formation, and memory decay in massed
and spaced learning. PNAS. 2014;111(1):E194-E202. doi:10.1073/pnas.1303317110
apa: Aziz, W., Wang, W., Kesaf, S., Mohamed, A., Fukazawa, Y., & Shigemoto,
R. (2014). Distinct kinetics of synaptic structural plasticity, memory formation,
and memory decay in massed and spaced learning. PNAS. National Academy
of Sciences. https://doi.org/10.1073/pnas.1303317110
chicago: Aziz, Wajeeha, Wen Wang, Sebnem Kesaf, Alsayed Mohamed, Yugo Fukazawa,
and Ryuichi Shigemoto. “Distinct Kinetics of Synaptic Structural Plasticity, Memory
Formation, and Memory Decay in Massed and Spaced Learning.” PNAS. National
Academy of Sciences, 2014. https://doi.org/10.1073/pnas.1303317110.
ieee: W. Aziz, W. Wang, S. Kesaf, A. Mohamed, Y. Fukazawa, and R. Shigemoto, “Distinct
kinetics of synaptic structural plasticity, memory formation, and memory decay
in massed and spaced learning,” PNAS, vol. 111, no. 1. National Academy
of Sciences, pp. E194–E202, 2014.
ista: Aziz W, Wang W, Kesaf S, Mohamed A, Fukazawa Y, Shigemoto R. 2014. Distinct
kinetics of synaptic structural plasticity, memory formation, and memory decay
in massed and spaced learning. PNAS. 111(1), E194–E202.
mla: Aziz, Wajeeha, et al. “Distinct Kinetics of Synaptic Structural Plasticity,
Memory Formation, and Memory Decay in Massed and Spaced Learning.” PNAS,
vol. 111, no. 1, National Academy of Sciences, 2014, pp. E194–202, doi:10.1073/pnas.1303317110.
short: W. Aziz, W. Wang, S. Kesaf, A. Mohamed, Y. Fukazawa, R. Shigemoto, PNAS 111
(2014) E194–E202.
date_created: 2018-12-11T11:54:43Z
date_published: 2014-01-07T00:00:00Z
date_updated: 2021-01-12T06:54:04Z
day: '07'
department:
- _id: RySh
doi: 10.1073/pnas.1303317110
intvolume: ' 111'
issue: '1'
language:
- iso: eng
main_file_link:
- open_access: '1'
url: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3890840/
month: '01'
oa: 1
oa_version: Submitted Version
page: E194 - E202
publication: PNAS
publication_status: published
publisher: National Academy of Sciences
publist_id: '5175'
scopus_import: 1
status: public
title: Distinct kinetics of synaptic structural plasticity, memory formation, and
memory decay in massed and spaced learning
type: journal_article
user_id: 4435EBFC-F248-11E8-B48F-1D18A9856A87
volume: 111
year: '2014'
...
---
_id: '1920'
abstract:
- lang: eng
text: Cerebellar motor learning is suggested to be caused by long-term plasticity
of excitatory parallel fiber-Purkinje cell (PF-PC) synapses associated with changes
in the number of synaptic AMPA-type glutamate receptors (AMPARs). However, whether
the AMPARs decrease or increase in individual PF-PC synapses occurs in physiological
motor learning and accounts for memory that lasts over days remains elusive. We
combined quantitative SDS-digested freeze-fracture replica labeling for AMPAR
and physical dissector electron microscopy with a simple model of cerebellar motor
learning, adaptation of horizontal optokinetic response (HOKR) in mouse. After
1-h training of HOKR, short-term adaptation (STA) was accompanied with transient
decrease in AMPARs by 28% in target PF-PC synapses. STA was well correlated with
AMPAR decrease in individual animals and both STA and AMPAR decrease recovered
to basal levels within 24 h. Surprisingly, long-termadaptation (LTA) after five
consecutive daily trainings of 1-h HOKR did not alter the number of AMPARs in
PF-PC synapses but caused gradual and persistent synapse elimination by 45%, with
corresponding PC spine loss by the fifth training day. Furthermore, recovery of
LTA after 2 wk was well correlated with increase of PF-PC synapses to the control
level. Our findings indicate that the AMPARs decrease in PF-PC synapses and the
elimination of these synapses are in vivo engrams in short- and long-term motor
learning, respectively, showing a unique type of synaptic plasticity that may
contribute to memory consolidation.
acknowledgement: This work was supported by Solution-Oriented Research for Science
and Technology from the Japan Science and Technology Agency; Ministry of Education,
Culture, Sports, Science and Technology of Japan Grant 16300114 (to R.S.).
author:
- first_name: Wen
full_name: Wang, Wen
last_name: Wang
- first_name: Kazuhiko
full_name: Nakadate, Kazuhiko
last_name: Nakadate
- first_name: Miwako
full_name: Masugi Tokita, Miwako
last_name: Masugi Tokita
- first_name: Fumihiro
full_name: Shutoh, Fumihiro
last_name: Shutoh
- first_name: Wajeeha
full_name: Aziz, Wajeeha
last_name: Aziz
- first_name: Etsuko
full_name: Tarusawa, Etsuko
last_name: Tarusawa
- first_name: Andrea
full_name: Lörincz, Andrea
last_name: Lörincz
- first_name: Elek
full_name: Molnár, Elek
last_name: Molnár
- first_name: Sebnem
full_name: Kesaf, Sebnem
id: 401AB46C-F248-11E8-B48F-1D18A9856A87
last_name: Kesaf
- first_name: Yunqing
full_name: Li, Yunqing
last_name: Li
- first_name: Yugo
full_name: Fukazawa, Yugo
last_name: Fukazawa
- first_name: Soichi
full_name: Nagao, Soichi
last_name: Nagao
- first_name: Ryuichi
full_name: Shigemoto, Ryuichi
id: 499F3ABC-F248-11E8-B48F-1D18A9856A87
last_name: Shigemoto
orcid: 0000-0001-8761-9444
citation:
ama: Wang W, Nakadate K, Masugi Tokita M, et al. Distinct cerebellar engrams in
short-term and long-term motor learning. PNAS. 2014;111(1):E188-E193. doi:10.1073/pnas.1315541111
apa: Wang, W., Nakadate, K., Masugi Tokita, M., Shutoh, F., Aziz, W., Tarusawa,
E., … Shigemoto, R. (2014). Distinct cerebellar engrams in short-term and long-term
motor learning. PNAS. National Academy of Sciences. https://doi.org/10.1073/pnas.1315541111
chicago: Wang, Wen, Kazuhiko Nakadate, Miwako Masugi Tokita, Fumihiro Shutoh, Wajeeha
Aziz, Etsuko Tarusawa, Andrea Lörincz, et al. “Distinct Cerebellar Engrams in
Short-Term and Long-Term Motor Learning.” PNAS. National Academy of Sciences,
2014. https://doi.org/10.1073/pnas.1315541111.
ieee: W. Wang et al., “Distinct cerebellar engrams in short-term and long-term
motor learning,” PNAS, vol. 111, no. 1. National Academy of Sciences, pp.
E188–E193, 2014.
ista: Wang W, Nakadate K, Masugi Tokita M, Shutoh F, Aziz W, Tarusawa E, Lörincz
A, Molnár E, Kesaf S, Li Y, Fukazawa Y, Nagao S, Shigemoto R. 2014. Distinct cerebellar
engrams in short-term and long-term motor learning. PNAS. 111(1), E188–E193.
mla: Wang, Wen, et al. “Distinct Cerebellar Engrams in Short-Term and Long-Term
Motor Learning.” PNAS, vol. 111, no. 1, National Academy of Sciences, 2014,
pp. E188–93, doi:10.1073/pnas.1315541111.
short: W. Wang, K. Nakadate, M. Masugi Tokita, F. Shutoh, W. Aziz, E. Tarusawa,
A. Lörincz, E. Molnár, S. Kesaf, Y. Li, Y. Fukazawa, S. Nagao, R. Shigemoto, PNAS
111 (2014) E188–E193.
date_created: 2018-12-11T11:54:43Z
date_published: 2014-01-07T00:00:00Z
date_updated: 2021-01-12T06:54:05Z
day: '07'
department:
- _id: RySh
doi: 10.1073/pnas.1315541111
intvolume: ' 111'
issue: '1'
language:
- iso: eng
main_file_link:
- open_access: '1'
url: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3890858/
month: '01'
oa: 1
oa_version: Submitted Version
page: E188 - E193
publication: PNAS
publication_status: published
publisher: National Academy of Sciences
publist_id: '5174'
scopus_import: 1
status: public
title: Distinct cerebellar engrams in short-term and long-term motor learning
type: journal_article
user_id: 4435EBFC-F248-11E8-B48F-1D18A9856A87
volume: 111
year: '2014'
...