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. 2023 Sep 1:15:1208274.
doi: 10.3389/fnagi.2023.1208274. eCollection 2023.

Reduced biophotonic activities and spectral blueshift in Alzheimer's disease and vascular dementia models with cognitive impairment

Zhuo Wang  1   2   3 , Zhipeng Xu  1 , Yi Luo  4 , Sisi Peng  1 , Hao Song  1 , Tian Li  1 , Jiaxin Zheng  1 , Na Liu  2 , Shenjia Wu  1 , Junxia Zhang  5 , Lei Zhang  1 , Yuan Hu  1 , Yanping Liu  1 , Dongwei Lu  1 , Jiapei Dai  2 , Junjian Zhang  1
Affiliations

Reduced biophotonic activities and spectral blueshift in Alzheimer's disease and vascular dementia models with cognitive impairment

Zhuo Wang et al. Front Aging Neurosci. .

Abstract

Background: Although clinically, Alzheimer's disease (AD) and vascular dementia (VaD) are the two major types of dementia, it is unclear whether the biophotonic activities associated with cognitive impairments in these diseases share common pathological features.

Methods: We used the ultraweak biophoton imaging system (UBIS) and synaptosomes prepared by modified percoll method to directly evaluate the functional changes in synapses and neural circuits in AD and VaD model animals.

Results: We found that biophotonic activities induced by glutamate were significantly reduced and spectral blueshifted in synaptosomes and brain slices. These changes could be partially reversed by pre-perfusion of the ifenprodil, a specific antagonist of the GluN2B subunit of N-methyl-D-aspartate receptors (NMDARs).

Conclusion: Our findings suggest that AD and VaD pathology present similar but complex changes in biophotonic activities and transmission at synapses and neural circuits, implying that communications and information processing of biophotonic signals in the brain are crucial for advanced cognitive functions.

Keywords: Alzheimer’s disease; biophotonic activity; cognitive impairment; spectral blueshift; synaptic dysfunction; synaptosome; vascular dementia.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Spectral detection of biophotonic activity. (A) Photon spectral images are obtained from three known-wavelength lasers (405 nm, 532 nm, 650 nm) under conditions of normal (up planes) and ultraweak (down planes) light intensities, showing one zero-order fringe and two first-grade fringes. The two first-grade fringes present a trend away from the zero-order fringe from short to long wavelengths. Scale bar: 0.5 cm. (B) There are linear relationships between the wavelengths and fringe distances ΔLc, ΔLmin, ΔLmax of three lasers under conditions of normal (left plane) and ultraweak (right plane) light intensities. (C) Representative biophoton spectral images in WT, 3xTg-AD and 3xTg-AD + ifenprodil groups. Scale bar: 0.5 cm. (D) The spectral range represented by λmin, λave, and λmax in WT, 3xTg-AD and 3xTg-AD + ifenprodil groups. n = 6 animals per group. (E) Representative biophoton spectral images in sham, 2VO and 2VO + ifenprodil groups. Scale bar: 0.5 cm. (F) The spectral range represented by λmin, λave, and λmax in sham, 2VO and 2VO + ifenprodil groups. n = 6 animals per group. The data in (D,F) were presented as means ± SEMs and analyzed by one-way ANOVA. ***p < 0.001; ###p < 0.001.
Figure 2
Figure 2
Cognitive impairments in AD and VaD model animals. (A) The discrimination ratio of NOR test in WT and 3xTg-AD groups. n = 12. (B) The escape latency (left plane) and time in target quadrant (right plane) of MWM test in WT and 3xTg-AD groups. n = 12. (C) Representative swimming track of WT and 3xTg-AD groups during the probe trial. (D) The discrimination ratio of NOR test in sham and 2VO groups. n = 12. (E) The escape latency (left plane) and time in target quadrant (right plane) of MWM test in sham and 2VO groups. n = 12. (F) The representative swimming track of sham and 2VO groups during the probe trial. The platform in (C,F) were located in the northwest quadrant. The data in (A,B,D,E) were presented as means ± SEMs and analyzed by Student’s t test. **p < 0.01; ***p < 0.001.
Figure 3
Figure 3
Changes in biophoton emission of synaptosomes after perfusion with glutamate or glutamate + ifenprodil. (A) Representative electron microscopy images of the synaptosomes prepared from WT, 3xTg-AD, sham and 2VO groups. Scale bar: 500 nm. (B) Experimental scheme for the study of biophton emission induced by 50 mM glutamate or pre-perfusion with 10 μM ifenprodil. (C) Representative real-time images of biophoton emission of hippocampal synaptosomes in WT, 3xTg-AD and 3xTg-AD + ifenprodil groups. Each row of representative images from left to right corresponded to positioning, initiation, maintenance, washing, and reapplication periods. Scale bar: 0.5 cm. (D) Representative real-time images of biophoton emission of hippocampal synaptosomes in sham, 2VO and 2VO + ifenprodil groups. Scale bar: 0.5 cm. (E) The dynamic changes of biophoton emission (left plane) and average values every 30 min (right plane) from synaptosomes in WT, 3xTg-AD and 3xTg-AD + ifenprodil groups were represented by relative gray values (RGVs). n = 6 animals per group. (F) The dynamic changes of biophoton emission (left plane) and average values every 30 min (right plane) from synaptosomes in sham, 2VO and 2VO + ifenprodil groups were represented by RGVs. n = 6 animals per group. (G) RGVs of hippocampal synaptosomes in WT, 3xTg-AD and 3xTg-AD + ifenprodil groups during initiation, maintenance, washing, and reapplication periods, respectively. n = 6 animals per group. (H) RGVs of hippocampal synaptosomes in sham, 2VO and 2VO + ifenprodil groups during initiation, maintenance, washing, and reapplication periods, respectively. n = 6 animals per group. The data in (E–H) were presented as means ± SEMs and analyzed by one-way ANOVA. **p < 0.01; ***p < 0.001; #p < 0.05; ##p < 0.01; ###p < 0.001; no significance, p > 0.05.
Figure 4
Figure 4
Changes of biophoton transmission in brain slices. (A) Representative real-time images of biophoton transmission of brain slices in WT, 3xTg-AD and 3xTg-AD + ifenprodil groups. Each row of representative images from left to right corresponded to positioning, initiation, maintenance, washing, and reapplication periods. Scale bar: 0.5 cm. (B) Representative real-time images of biophoton transmission of brain slices in sham, 2VO and 2VO + ifenprodil groups. Scale bar: 0.5 cm. (C) The dynamic changes of biophoton emission (left plane) and average values every 30 min (right plane) from brain slices in WT, 3xTg-AD and 3xTg-AD + ifenprodil groups were represented by RGVs. n = 6 animals per group. (D) The dynamic changes of biophoton emission (left plane) and average values every 30 min (right plane) from brain slices in sham, 2VO and 2VO + ifenprodil groups were represented by RGVs. n = 6 animals per group. (E) RGVs of brain slices in WT, 3xTg-AD and 3xTg-AD + ifenprodil groups during initiation, maintenance, washing, and reapplication periods, respectively. n = 6 animals per group. (F) RGVs of brain slices in sham, 2VO and 2VO + ifenprodil groups during initiation, maintenance, washing, and reapplication periods, respectively. n = 6 animals per group. The data in (C–F) were presented as means ± SEMs and analyzed by one-way ANOVA. **p < 0.01; ***p < 0.001; #p < 0.05; ##p < 0.01; ###p < 0.001; no significance, p > 0.05.
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