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Memory formation orchestrates the wiring of adult-born hippocampal neurons into brain circuits

Petsophonsakul, Petnoi; Richetin, Kevin; Andraini, Trinovita; Roybon, Laurent LU and Rampon, Claire (2017) In Brain Structure and Function 222(6). p.2585-2601
Abstract

During memory formation, structural rearrangements of dendritic spines provide a mean to durably modulate synaptic connectivity within neuronal networks. New neurons generated throughout the adult life in the dentate gyrus of the hippocampus contribute to learning and memory. As these neurons become incorporated into the network, they generate huge numbers of new connections that modify hippocampal circuitry and functioning. However, it is yet unclear as to how the dynamic process of memory formation influences their synaptic integration into neuronal circuits. New memories are established according to a multistep process during which new information is first acquired and then consolidated to form a stable memory trace. Upon recall,... (More)

During memory formation, structural rearrangements of dendritic spines provide a mean to durably modulate synaptic connectivity within neuronal networks. New neurons generated throughout the adult life in the dentate gyrus of the hippocampus contribute to learning and memory. As these neurons become incorporated into the network, they generate huge numbers of new connections that modify hippocampal circuitry and functioning. However, it is yet unclear as to how the dynamic process of memory formation influences their synaptic integration into neuronal circuits. New memories are established according to a multistep process during which new information is first acquired and then consolidated to form a stable memory trace. Upon recall, memory is transiently destabilized and vulnerable to modification. Using contextual fear conditioning, we found that learning was associated with an acceleration of dendritic spines formation of adult-born neurons, and that spine connectivity becomes strengthened after memory consolidation. Moreover, we observed that afferent connectivity onto adult-born neurons is enhanced after memory retrieval, while extinction training induces a change of spine shapes. Together, these findings reveal that the neuronal activity supporting memory processes strongly influences the structural dendritic integration of adult-born neurons into pre-existing neuronal circuits. Such change of afferent connectivity is likely to impact the overall wiring of hippocampal network, and consequently, to regulate hippocampal function.

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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Adult hippocampal neurogenesis, Dendritic spine, Fear conditioning, Learning, Memory
in
Brain Structure and Function
volume
222
issue
6
pages
2585 - 2601
publisher
Springer
external identifiers
  • scopus:85008465382
  • wos:000406778700009
ISSN
1863-2653
DOI
10.1007/s00429-016-1359-x
language
English
LU publication?
yes
id
f73c2248-f0b7-4790-9186-0d90cf46c1b9
date added to LUP
2017-02-13 13:12:16
date last changed
2018-01-07 11:49:27
@article{f73c2248-f0b7-4790-9186-0d90cf46c1b9,
  abstract     = {<p>During memory formation, structural rearrangements of dendritic spines provide a mean to durably modulate synaptic connectivity within neuronal networks. New neurons generated throughout the adult life in the dentate gyrus of the hippocampus contribute to learning and memory. As these neurons become incorporated into the network, they generate huge numbers of new connections that modify hippocampal circuitry and functioning. However, it is yet unclear as to how the dynamic process of memory formation influences their synaptic integration into neuronal circuits. New memories are established according to a multistep process during which new information is first acquired and then consolidated to form a stable memory trace. Upon recall, memory is transiently destabilized and vulnerable to modification. Using contextual fear conditioning, we found that learning was associated with an acceleration of dendritic spines formation of adult-born neurons, and that spine connectivity becomes strengthened after memory consolidation. Moreover, we observed that afferent connectivity onto adult-born neurons is enhanced after memory retrieval, while extinction training induces a change of spine shapes. Together, these findings reveal that the neuronal activity supporting memory processes strongly influences the structural dendritic integration of adult-born neurons into pre-existing neuronal circuits. Such change of afferent connectivity is likely to impact the overall wiring of hippocampal network, and consequently, to regulate hippocampal function.</p>},
  author       = {Petsophonsakul, Petnoi and Richetin, Kevin and Andraini, Trinovita and Roybon, Laurent and Rampon, Claire},
  issn         = {1863-2653},
  keyword      = {Adult hippocampal neurogenesis,Dendritic spine,Fear conditioning,Learning,Memory},
  language     = {eng},
  month        = {01},
  number       = {6},
  pages        = {2585--2601},
  publisher    = {Springer},
  series       = {Brain Structure and Function},
  title        = {Memory formation orchestrates the wiring of adult-born hippocampal neurons into brain circuits},
  url          = {http://dx.doi.org/10.1007/s00429-016-1359-x},
  volume       = {222},
  year         = {2017},
}