Visualizing the lipid dynamics role in infrared neural stimulation using stimulated Raman scattering

Infrared neural stimulation (INS) uses pulsed infrared light to yield label-free neural stimulation with broad experimental and translational utility. Despite its robust demonstration, INS’s mechanistic and biophysical underpinnings have been the subject of debate for more than a decade. The role of...

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Bibliographic Details
Published in:Biophysical journal 2022-04, Vol.121 (8), p.1525-1540
Main Authors: Adams, Wilson R., Gautam, Rekha, Locke, Andrea, Masson, Laura E., Borrachero-Conejo, Ana I., Dollinger, Bryan R., Throckmorton, Graham A., Duvall, Craig, Jansen, E. Duco, Mahadevan-Jansen, Anita
Format: Article
Language:English
Subjects:
Lipid Bilayers
Nonlinear Optical Microscopy
Optical Imaging
Spectrum Analysis, Raman - methods
Vibration
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Summary:Infrared neural stimulation (INS) uses pulsed infrared light to yield label-free neural stimulation with broad experimental and translational utility. Despite its robust demonstration, INS’s mechanistic and biophysical underpinnings have been the subject of debate for more than a decade. The role of lipid membrane thermodynamics appears to play an important role in how fast IR-mediated heating nonspecifically drives action potential generation. Direct observation of lipid membrane dynamics during INS remains to be shown in a live neural model system. We used hyperspectral stimulated Raman scattering microscopy to study biochemical signatures of high-speed vibrational dynamics underlying INS in a live neural cell culture model. The findings suggest that lipid bilayer structural changes occur during INS in vitro in NG108-15 neuroglioma cells. Lipid-specific signatures of cell stimulated Raman scattering spectra varied with stimulation energy and radiation exposure. The spectroscopic observations agree with high-speed ratiometric fluorescence imaging of a conventional lipophilic membrane structure reporter, 4-(2-(6-(dibutylamino)-2-naphthalenyl)ethenyl)-1-(3-sulfopropyl)pyridinium hydroxide. The findings support the hypothesis that INS causes changes in the lipid membrane of neural cells by changing the lipid membrane packing order. This work highlights the potential of hyperspectral stimulated Raman scattering as a method to safely study biophysical and biochemical dynamics in live cells.
ISSN:0006-3495
1542-0086
DOI:10.1016/j.bpj.2022.03.006