Whole Body Vibration Improves Spatial Memory, Anxiety-Like Behavior, and Motor Performance in Aged Male and Female Rats

Abstract

Aging is a progressive process leading to functional decline in many domains. Recent studies have shown that physical exercise (PE) has a positive influence on the progression of age-related functional decline, including motor and brain functions. Whole body vibration (WBV) is a form of passive stimulation by mechanical vibration platforms, which offers an alternative for PE interventions, especially for aged individuals. WBV has been demonstrated to mimic the beneficial effects of PE on the musculoskeletal system, as well on the central nervous system. However, preclinical data with aged rodents are very limited. Hence, the purpose of this experiment was to investigate the effects of a 5-week WBV intervention with an aged animal model on memory functions, anxiety-related behavior, and motor performance. The 18-month old male (N = 14) and female (N = 14) Wistar rats were divided into two groups, namely, vibration and pseudo-vibration. Animals underwent a 5-week WBV intervention protocol with low intensity (frequency of 30 Hz and amplitude of 50-200 μm) stimulation. After 5 weeks, the following cognitive and motor tests were administered: open-field, novel and spatial object recognition, grip-hanging, and balance-beam. WBV-treated rats showed a decrease in their anxiety level in the open field test compared with those in the pseudo-treated controls. In addition, WBV-treated male animals showed significantly increased rearing in the open-field test compared to their pseudo controls. Spatial memory was significantly improved by WBV treatment, whereas WBV had no effect on object memory. Regarding motor performance, both grip strength and motor coordination were improved by WBV treatment. Our results indicate that WBV seems to have comparable beneficial effects on age-related emotional, cognitive, and motor decline as what has been reported for active PE. No striking differences were found between the sexes. As such, these findings further support the idea that WBV could be considered as a useful alternative for PE in case active PE cannot be performed due to physical or mental issues.

Keywords: healthy aging; muscle strength; object recognition; open field activity; passive physical exercise.

FIGURE 1

Experimental design. The 18-month-old male and female rats underwent 5 weeks of whole body vibration intervention with a single daily session of 10 min exposure, five times per week. After 5 weeks, a test battery was performed to assess anxiety-like behavior, memory functions, and motor performance. The used MarodyneLiv plate is depicted in the upper left corner.

FIGURE 2

Novel and spatial object recognition test battery was performed to assess spatial and object memory. The test series consisted of four separated phases. Phase 1: rat was placed into the empty test box for 3 min to get familiarized to the test environment. Phase 2: two identical objects were placed into the test box in parallel position, and the rat was familiarized to the objects for 3 min. Phase 3: spatial object recognition: after cleaning, the two same objects were placed back in diagonal position, and the rat was allowed to explore the objects for 3 min. Phase 4: novel object recognition: after cleaning, objects were placed back in the diagonal position; however, one of the familiar objects was replaced by a novel object, and the rat was allowed to explore the objects for 3 min.

FIGURE 3

The effects of whole body vibration on exploratory and anxiety-related behavior in the open field test in aged male and female rats. Data are presented as percentage of wall vs. non-wall time (i.e., they are reciprocal of each other). All animals spent more than 50% of the total time in the wall zone. Vibration-treated animals showed a strong tendency (p = 0.077) of decreased time spent in the wall zone and increased time spent in the center zone (A). The number of crossings significantly increased in the female animals (B). Time spent with rearing increased significantly in the vibration-treated male group compared with the pseudo-treated male group (C). Two-way ANOVA was used for analyzing these results. Pseudo-whole body vibration (n = 14, 7 females and 7 males); whole body vibration (n = 14, 7 females and 7 males). F, F statistical value; I, main effect of intervention (vibration/pseudo vibration); S, main effect of sex (male/female); I*S, interaction effect of intervention and sex. Data are depicted as mean ± SEM. *p < 0.05 and **p < 0.01.

FIGURE 4

Effects of whole body vibration on spatial memory in the spatial object relocation test. Preference time (A) and relocated object bouts (B) were significantly increased in vibration treated groups compared with control groups. Two-way ANOVA was used for analyzing these results. Pseudo whole body vibration (n = 14, 7 females and 7 males) and whole body vibration (n = 13, 7 females and 6 males). Dotted line: reference line of 50% for random exploration. F, F statistical value; I, main effect of intervention (vibration/pseudo vibration); S, main effect of sex (male/female); I*S, interaction effect of intervention and sex. Data are depicted as mean ± SEM. *p < 0.05.

FIGURE 5

Effects of whole body vibration on object memory in the novel object recognition test. Preference time and number of novel object bouts had no significant difference among all groups (A,B). Preference time showed significant difference in the female animals compared with the 50% of chance level (A). Two-way ANOVA was used for the analysis of group interactions, and the independent sample t-test was used for comparison to the chance level. Pseudo whole body vibration (n = 10, 6 females and 4 males) and whole body vibration (n = 11, 6 females and 5 males). Dotted line: reference line of 50% for random exploration. F, F statistical value; I, main effect of intervention (vibration/pseudo vibration); S, main effect of sex (male/female); I*S, interaction effect of intervention and sex. Data are depicted as mean ± SEM. *p < 0.05.

FIGURE 6

Effects of whole body vibration on motor performance in the grip hanging (A) and balance beam (B) tests. Hanging time was significantly increased in vibration-treated animals compared to the pseudo vibration-treated animals (A). Walking time on the beam (B) was significantly decreased in vibration-treated animals compared with the pseudo vibration-treated animals, as well in the female animals compared with the male animals. Grip hanging/balance beam: pseudo whole body vibration (n = 13/13, 7/7 females and 6/6 males) and whole body vibration (n = 14/14, 7/7 females and 7/7 males). F, F statistical value; I, main effect of intervention (vibration/pseudo vibration); S, main effect of sex (male/female); I*S, interaction effect of intervention and sex. Data are depicted as mean ± SEM. *p < 0.05 and ***p < 0.001.