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

Brain Struct Funct. 2017 Aug;222(6):2585-2601. doi: 10.1007/s00429-016-1359-x. Epub 2017 Jan 6.

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, 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.

Keywords: Adult hippocampal neurogenesis; Dendritic spine; Fear conditioning; Learning; Memory.

MeSH terms

  • Animals
  • Behavior, Animal*
  • Conditioning, Psychological
  • Dendritic Spines / metabolism
  • Dendritic Spines / physiology
  • Electric Stimulation
  • Fear
  • Genes, Reporter
  • Green Fluorescent Proteins / biosynthesis
  • Green Fluorescent Proteins / genetics
  • Hippocampus / cytology
  • Hippocampus / metabolism
  • Hippocampus / physiology*
  • Luminescent Proteins / biosynthesis
  • Luminescent Proteins / genetics
  • Male
  • Memory*
  • Mice, Inbred C57BL
  • Neural Pathways / metabolism
  • Neural Pathways / physiology
  • Neuroanatomical Tract-Tracing Techniques
  • Neurogenesis*
  • Neurons / metabolism
  • Neurons / physiology*
  • Red Fluorescent Protein
  • Time Factors

Substances

  • Luminescent Proteins
  • enhanced green fluorescent protein
  • Green Fluorescent Proteins