Modulatory effect of aerobic physical activity on synaptic ultrastructure in the old mouse hippocampus

Patrizia Fattoretti, Manuela Malatesta, Barbara Cisterna, Chiara Milanese, Carlo Zancanaro

Research output: Contribution to journalArticle

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Abstract

Aerobic physical exercise (APE) leads to improved brain functions. To better understand the beneficial effect of APE on the aging brain, a morphometric study was carried out of changes in hippocampal synapses of old (> 27 months) Balb/c mice undergoing treadmill training (OTT) for 4 weeks in comparison with old sedentary (OS), middle-aged sedentary (MAS) and middle-aged treadmill training (MATT) mice. The inner molecular layer of the hippocampal dentate gyrus (IMLDG) and the molecular stratum of Ammon's horn1 neurons (SMCA1) were investigated. The number of synapses per cubic micron of tissue (numeric density, Nv), overall synaptic area per cubic micron of tissue (surface density, Sv), average area of synaptic contact zones (S), and frequency (%) of perforated synapses (PS) were measured in electron micrographs of ethanol-phosphotungstic acid (E-PTA) stained tissue. Data were analyzed with analysis of variance (ANOVA). In IMLDG, an effect of age was found for Nv and Sv, but not S and %PS. Similar results were found for exercise and the interaction of age and exercise. In post hoc analysis Nv was higher (60.6% to 75.1%; p < 0.001) in MATT vs. MAS, OS and OTT. Sv was higher (32.3% to 54.6%; p < 0.001) in MATT vs. MAS, OS and OTT. In SMCA1, age affected Nv, Sv and %PS, but not S. The effect of exercise was significant for Sv only. The interaction of age and exercise was significant for Nv, Sv and %PS. In post hoc analysis Nv was lower in OS vs. MAS, MATT and OTT (-26.1% to -32.1%; p < 0.038). MAS and OTT were similar. Sv was lower in OS vs. MAS, MATT and OTT (-23.4 to -30.3%, p < 0.004). MAS and OTT were similar. PS frequency was higher in OS vs. MAS, MATT and OTT (48.3% to +96.6%, p < 0.023). APE positively modulated synaptic structural dynamics in the aging hippocampus, possibly in a region-specific way. The APE-associated reduction in PS frequency in SMCA1 of old mice suggests that an increasing complement of PS is a compensatory phenomenon to maintain synaptic efficacy. In conclusion, the modulation of synaptic plasticity by APE gives quantitative support to the concept that APE protects from neurodegeneration and improves learning and memory in aging.

Original languageEnglish
Article number141
JournalFrontiers in Aging Neuroscience
Volume10
Issue numberMAY
DOIs
Publication statusPublished - May 16 2018

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Hippocampus
Synapses
Exercise
Parahippocampal Gyrus
Dentate Gyrus
Phosphotungstic Acid
Neuronal Plasticity
Brain
Analysis of Variance
Ethanol
Learning
Electrons
Neurons

Keywords

  • Aging
  • Exercise
  • Hippocampus
  • Physical activity
  • Synaptic morphology

ASJC Scopus subject areas

  • Ageing
  • Cognitive Neuroscience

Cite this

Modulatory effect of aerobic physical activity on synaptic ultrastructure in the old mouse hippocampus. / Fattoretti, Patrizia; Malatesta, Manuela; Cisterna, Barbara; Milanese, Chiara; Zancanaro, Carlo.

In: Frontiers in Aging Neuroscience, Vol. 10, No. MAY, 141, 16.05.2018.

Research output: Contribution to journalArticle

Fattoretti, Patrizia ; Malatesta, Manuela ; Cisterna, Barbara ; Milanese, Chiara ; Zancanaro, Carlo. / Modulatory effect of aerobic physical activity on synaptic ultrastructure in the old mouse hippocampus. In: Frontiers in Aging Neuroscience. 2018 ; Vol. 10, No. MAY.
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