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Link to original content: http://pubmed.ncbi.nlm.nih.gov/38638979/
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. 2024 Apr 6;10(8):e29090.
doi: 10.1016/j.heliyon.2024.e29090. eCollection 2024 Apr 30.

FNDC5/irisin mediates the protective effects of Innovative theta-shaking exercise on mouse memory

Runhong Yao  1 , Kouji Yamada  2 , Sho Izawa  2 , Takumi Kito  3 , Hirohide Sawada  4 , Takeshi Chihara  4 , Naoki Aizu  2 , Daiki Iwata  4 , Kazuhiro Nishii  2
Affiliations

FNDC5/irisin mediates the protective effects of Innovative theta-shaking exercise on mouse memory

Runhong Yao et al. Heliyon. .

Abstract

As a passive motion and non-invasive treatment, theta-shaking exercise is considered an alternative to traditional active exercise for slowing down brain ageing. Here, we studied the influence of theta-shaking exercise on fibronectin type III domain containing 5/irisin (FNDC5/irisin) in the anterior nucleus of the thalamus, hippocampus, and medial prefrontal cortex (ATN-HPC-MPFC). Further, we assessed memory in senescence-accelerated prone mice (SAMP-10 mice) using a behavioural test to confirm the protective effect of theta-shaking exercise against age-related memory decline. SAMP-10 mice were subjected to theta-shaking exercise for 9-30 weeks. Mice then performed the T-maze test and passive avoidance task. Immunohistochemical analysis and ELISA were used to assess FNDC5/irisin, nerve growth factor (NGF), and neurotrophin 4/5 (NT4/5) expression in the ATN-HPC-MPFC. In the shaking group, FNDC5 was locally upregulated within the hippocampus and MPFC area rather than exhibiting even distribution throughout brain tissue. Irisin levels were generally higher in the control group. Meanwhile, hippocampal NGF levels were significantly higher in the shaking group, with no differences noted in neurotrophin levels. Theta-shaking preserved normal neurons in certain sub-regions. However, no beneficial changes in neuronal density were noted in the ATN. Theta-shaking exercise positively affects memory function in SAMP-10 mice. FNDC5 upregulation and higher levels of NGF, along with the potential involvement of irisin, may have contributed to the preservation of normal neuronal density in the hippocampus and MPFC subregions.

Keywords: FNDC5/Irisin; Hippocampus; Medial prefrontal cortex; Shaking exercise; Theta oscillation.

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Conflict of interest statement

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Figures

Fig. 1
Fig. 1
Study timeline. All the mice were acclimated for 1 week. The theta-shaking exercise was initiated when the mice were 9 weeks old. Behavioural tests were performed at 8, 20, and 30 weeks. Brain tissue was obtained after the last behavioural test.
Fig. 2
Fig. 2
ATN–HPC–MPFC diagram. The anterior nucleus of the dorsal thalamus is also observed. The hippocampus is divided into seven parts: the dentate gyrus (DG: upstream and downstream), cornu ammonis field 3 (CA3: proximal and distal), cornu ammonis field 1 (CA1: proximal and middle distal), and the subiculum. The medial prefrontal cortex (MPFC) is divided into two parts (the dorsal and ventral rostral). ATN, anterior thalamic nuclei, DG, dentate gyrus; CA3, cornu ammonis field 3; CA1, cornu ammonis field1; DR, dorsal rostral; VR, ventral rostra.
Fig. 3
Fig. 3
Short-term memory assessment through a spontaneous alternation T-maze test. The shaking group (20W) differed significantly from the control. No significant differences were observed at 30W. Grey line: control group, purple line: theta-shaking group (*p < 0.05 and **p < 0.01).
Fig. 4
Fig. 4
Passive avoidance task. Both groups exhibited age-related long-term memory decline. Grey line: control group, purple line: theta-shaking group (*p < 0.05 and **p < 0.01).
Fig. 5
Fig. 5
Histomorphological analysis of the ATN–HPC–MPFC circuit. (A) Quantification of FNDC5 staining in the ATN–HPC–MPFC circuit. (A-a) FNDC5-positive neurons are present in sagittal brain sections. (A-b) Abnormal neuron counts in sagittal brain sections. (A-c) Neuron counts in sagittal brain sections. Grey bars: control group, purple bars: theta-shaking group (*p < 0.05 and **p < 0.01; paired Student's t-test; two-sided). (B) Photomicrographs of FNDC5 staining in the ATN–HPC–MPFC circuit. Neuronal morphology, staining patterns, nucleus positioning, and structural integrity were assessed to identify and characterise abnormal neurons. ATN: anterior thalamic nuclei; HPC: hippocampus; MPFC: medial prefrontal cortex; FNDC5: fibronectin type III domain containing 5; DG: dentate gyrus; CA3: cornu ammonis field 3; CA1: cornu ammonis field 1; DR: dorsal rostral; VR: ventral rostral.
Fig. 6
Fig. 6
Effects of theta-shaking exercise on irisin protein levels in the hippocampus and wide-area brain. A significantly higher expression was present in the wide-area brain (p = 0.022) and local hippocampus control group (p < 0.01). Grey bars: control group, purple bars: theta-shaking group. (*p < 0.05 and **p < 0.01; paired Student's t-test; two-sided, n = 7 control mice, 7 shaking mice). The experiments were repeated twice with similar results.
Fig. 7
Fig. 7
Effects of theta-shaking exercise on NGF levels in the hippocampus and wide-area brain. A significant increase occurred in NGF in the theta-shaking group (p = 0.038). Grey bars: control group, purple bars: theta-shaking group (*p < 0.05, paired Student's t-test; two-sided, n = 7 control mice, 7 shaking mice). The experiments were repeated twice with similar results. NGF, nerve growth factor.
Fig. 8
Fig. 8
Effects of the theta-shaking exercise on NT4/5 levels in the hippocampus and wide-area brain. No changes in NT4/5 were detected in the wide-area brain or hippocampus in either group. Grey bars: control group, purple bars: theta-shaking group (paired Student's t-test; two-sided, n = 7 control, 7 shaking). The experiments were repeated twice with similar results. NT4/5: neurotrophin 4/5.
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