Abstract
Perineuronal nets (PNNs) surrounding fast-spiking, parvalbumin (PV) interneurons provide excitatory:inhibitory balance, which is impaired in several disorders associated with altered diurnal rhythms, yet few studies have examined diurnal rhythms of PNNs or PV cells. We measured the intensity and number of PV cells and PNNs labeled with Wisteria floribunda agglutinin (WFA) and also the oxidative stress marker 8-oxo-deoxyguanosine (8-oxo-dG) in rat prelimbic medial prefrontal cortex (mPFC) at Zeitgeber times (ZT) ZT0 (lights-on, inactive phase), ZT6 (mid-inactive phase), ZT12 (lights-off, active phase), and ZT18 (mid-active phase). Relative to ZT0, the intensities of PNN and PV labeling were increased in the dark (active) phase compared with the light (inactive) phase. The intensity of 8-oxo-dG was decreased from ZT0 at all times (ZT6,12,18). We also measured GAD 65/67 and vGLUT1 puncta apposed to PV cells with and without PNNs. There were more excitatory puncta on PV cells with PNNs at ZT18 vs. ZT6, but no changes in PV cells without PNNs and no changes in inhibitory puncta. Whole-cell slice recordings in fast-spiking (PV) cells with PNNs showed an increased ratio of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor:N-methyl-D-aspartate receptor (AMPA: NMDA) at ZT18 vs. ZT6. The number of PV cells and PV/PNN cells containing orthodenticle homeobox 2 (OTX2), which maintains PNNs, showed a strong trend toward an increase from ZT6 to ZT18. Diurnal fluctuations in PNNs and PV cells are expected to alter cortical excitatory:inhibitory balance and provide new insights into treatments for diseases impacted by disturbances in sleep and circadian rhythms.
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Data availability
Data are available upon request from the corresponding author.
Code availability
Available for download at https://pipsqueak.ai.
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Acknowledgements
The authors would like to thank Dr. Megan Slaker, Ryan P. Todd, Monica Chang, and Nathan Allen for help with earlier stages of the experiments and Jonathan Ramos for assistance with analysis.
Funding
This work was funded by Washington State University Alcohol and Drug Abuse Research Program, NIH GM134789 (JHH); NIH DA033404 (BAS), DA040965 (BAS, TEB, SAA); NIH NS078498 (JPW); NIH P30 NS061800 (SAA); and Agence Nationale de la Recherche ANR-18-CE16-0013–01 (AP and AAD).
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JHH, AEE, ETJ, and DH conducted experiments and analyzed data; PNB analyzed data; JPW performed statistical analyses and contributed to writing the manuscript; AD and AP contributed to writing the manuscript; and SAA, TEB, and BAS contributed to writing the manuscript, and designed and directed the experiments.
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JHH and BAS are listed as inventors of the Washington State University analysis program, Pipsqueak™. JHH is a majority stake holder in Rewire Neuro, Inc., the licensing partner of the Pipsqueak™ technology. The authors do not perceive these relationships to have had an influence on this report.
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All procedures were performed in accordance with the National Institutes of Health's Guidelines for the Care and Use of Laboratory Animals and with approval from the Institutional Animal Care and Use Committee at Legacy Research Institute and Washington State University.
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Harkness, J.H., Gonzalez, A.E., Bushana, P.N. et al. Diurnal changes in perineuronal nets and parvalbumin neurons in the rat medial prefrontal cortex. Brain Struct Funct 226, 1135–1153 (2021). https://doi.org/10.1007/s00429-021-02229-4
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DOI: https://doi.org/10.1007/s00429-021-02229-4