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Chronic Stress Induces Coordinated Cortical Microcircuit Cell-Type Transcriptomic Changes Consistent With Altered

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Chronic stress alters gene expression in specific brain cells, leading to coordinated changes in neural circuits and potentially impacting mood disorders. This study reveals how stress reorganizes the cortical microcircuit, affecting pyramidal and interneurons.

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Area of Science:

  • Neuroscience
  • Molecular Biology
  • Genomics

Background:

  • Cortical microcircuits process information via excitatory pyramidal (PYR) cells and inhibitory interneurons expressing somatostatin (SST), parvalbumin, or vasoactive intestinal peptide.
  • Major depressive disorder and chronic stress are linked to impaired PYR cell morphology and reduced SST cell markers, but coordinated microcircuit changes remain unclear.

Purpose of the Study:

  • To investigate the transcriptomic effects of unpredictable chronic mild stress (UCMS) on distinct microcircuit cell types in the mouse medial prefrontal cortex.
  • To understand how UCMS affects anxiety- and depressive-like behaviors and their correlation with cellular and molecular changes.

Main Methods:

  • Exposure of C57BL/6 mice to UCMS or control conditions for 5 weeks.
  • Assessment of anxiety- and depressive-like behaviors.
  • Laser microdissection of medial prefrontal cortex microcircuit cell types followed by RNA sequencing and differential gene expression analysis.

Main Results:

  • UCMS induced significant behavioral changes indicative of increased emotionality.
  • Unique differentially expressed genes were identified in each cell type post-UCMS, with dysregulation in presynaptic functions, oxidative stress, metabolism, and translation.
  • A shift towards increased transcriptomic coordination between PYR, SST, and parvalbumin cells was observed under UCMS, with PYR cells adopting a hub-like role.

Conclusions:

  • UCMS leads to cell-specific deficits and microcircuit-wide synaptic reorganization.
  • A shift in the regulation of the cortical excitation-inhibition balance occurs, suggesting enhanced coordinated regulation of PYR cells by SST and parvalbumin interneurons.
  • These findings offer insights into the cellular and circuit-level mechanisms underlying stress-induced behavioral changes and potential therapeutic targets.