Microglia regulate motor neuron plasticity via reciprocal fractalkine and adenosine signaling

Alexandria B. Marciante, Arash Tadjalli, Maria Nikodemova, Kayla A. Burrowes, Jose Oberto, Edward K. Luca, Yasin B. Seven, Jyoti J. Watters, Tracy L. Baker and Gordon S. Mitchell ()
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Alexandria B. Marciante: University of Florida
Arash Tadjalli: University of Florida
Maria Nikodemova: University of Florida
Kayla A. Burrowes: University of Florida
Jose Oberto: University of Florida
Edward K. Luca: University of Florida
Yasin B. Seven: University of Florida
Jyoti J. Watters: University of Florida
Tracy L. Baker: University of Florida
Gordon S. Mitchell: University of Florida

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract We report an important role for microglia in regulating neuroplasticity within phrenic motor neurons. Brief episodes of low oxygen (acute intermittent hypoxia; AIH) elicit a form of respiratory motor plasticity known as phrenic long-term facilitation (pLTF) that is regulated by the balance of competing serotonin vs adenosine-initiated cellular mechanisms. Serotonin arises from brainstem raphe neurons, but the source of adenosine is unknown. We tested if hypoxic episodes initiate phrenic motor neuron to microglia fractalkine signaling that evokes extracellular adenosine formation using a well-defined neurophysiology preparation in male rats. With moderate AIH, phrenic motor neuron adenosine 2A receptor activation undermines serotonin-dominant pLTF whereas severe AIH induces pLTF by the adenosine-dependent mechanism. Consequently, phrenic motor neuron fractalkine knockdown, microglial fractalkine receptor inhibition, and microglial ablation enhance moderate AIH, but suppress severe AIH-induced pLTF. We conclude, microglia play important roles in healthy spinal cords, regulating plasticity in motor neurons responsible for breathing.

Date: 2024
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DOI: 10.1038/s41467-024-54619-x

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