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The microbiota regulate neuronal function and fear extinction learning.

Coco Chu1, Mitchell H Murdock2,3,4, Deqiang Jing3,4,5

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The gut microbiota is crucial for fear extinction learning in mice, influencing brain development and function. Microbial signals are needed in both early life and adulthood for healthy brain function and behavior.

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Area of Science:

  • Neuroscience
  • Microbiology
  • Behavioral Science

Background:

  • Multicellular organisms host a complex microbiota influencing host physiology and behavior.
  • Microbiota alterations are linked to neuropsychiatric disorders, but underlying mechanisms are unclear.
  • Fear extinction learning is a key cognitive process modulated by host behavior.

Purpose of the Study:

  • To investigate the role of the microbiota in fear extinction learning.
  • To elucidate the mechanisms by which the microbiota influences neuronal activity and behavior.
  • To identify microbiota-derived signals critical for brain development and function.

Main Methods:

  • Manipulation of microbiota in antibiotic-treated and germ-free adult mice.
  • Single-nucleus RNA sequencing of the medial prefrontal cortex.
  • Transcranial two-photon imaging to assess neuronal activity and dendritic spine remodeling.
  • Metabolomic analysis to identify key microbial metabolites.

Main Results:

  • Microbiota manipulation in adult mice led to significant deficits in fear extinction learning.
  • Gene expression in the medial prefrontal cortex was altered in various cell types.
  • Deficits were associated with impaired dendritic spine remodeling and reduced neuronal activity.
  • A critical neonatal developmental window for microbiota-derived signals was identified.
  • Four downregulated metabolites in germ-free mice were linked to neuropsychiatric disorders.

Conclusions:

  • Microbiota-derived signals are essential for fear extinction learning during both early postnatal development and adulthood.
  • Microbial metabolites may directly influence brain function and behavior.
  • Findings have implications for understanding how diet, infection, and lifestyle impact brain health and neuropsychiatric disorder susceptibility.