Social isolation improves the performance of rodents in a novel cognitive flexibility task

Abstract

Background: Social isolation, i.e., the deprivation of social contact, is a highly stressful circumstance that affects behavioral and functional brain development in social animals. Cognitive flexibility, one of the essential executive brain function that facilitates survival problem solving, was reported to be impaired after social isolation rearing. However, most of the previous studies have focused on the constrained aspect of flexibility and little is known about the unconstrained aspect. In the present study, the unconstrained cognitive flexibility of Kunming mice (Mus musculus, Km) reared in isolation was examined by a novel digging task. The exploratory behavior of the mice was also tested utilizing the hole-board and elevated plus maze tests to explain the differences in cognitive flexibility between the mice reared socially and in isolation.

Results: The results demonstrated that the isolated mice had a higher success rate in solving the novel digging problem and showed a higher rate of exploratory behavior compared with the controls. Linear regression analysis revealed that the time it took the mice to solve the digging problem was negatively associated with exploratory behavior.

Conclusions: The data suggest that social isolation rearing improves unconstrained cognitive flexibility in mice, which is probably related to an increase in their exploratory behavior. Such effects may reflect the behavioral and cognitive evolutionary adaptations of rodents to survive under complex and stressful conditions.

Fig. 1

Schematic diagram of the testing apparatus for unconstrained cognitive flexibility viewed from above (a) and from the side (b). Dimensions of the apparatus was 50 cm × 10 cm × 25 cm (l × w × h). A removable plexiglas wall separated one-third of the apparatus to make a start box. When the wall was removed, the test area was exposed, consisting of a ramp leading to the reward pot at the end of the apparatus. A panel was placed in the middle of the ramp making 4 cm of open space at the bottom of the ramp. For the digging task on test day, the ramp was covered by sawdust to a height of 6 cm from the bottom to restrict access to the reward pot

Fig. 2

Cumulative proportion of mice reared under different conditions that solved the novel digging task. The success rate of the isolated mice (iso, black line) was significant higher than the mice reared socially (soc, gray line) (Cox’s F-test, P = 0.038)

Fig. 3

Comparison of exploratory behavior of mice reared under different conditions in the hole board test. a: box plots show the distribution of latency to first head dip (HD) of mice in socially reared (soc) and isolation-reared (iso) groups. Solid lines in the boxes are median lines; dashed lines in the boxes are mean lines. b: the distribution of rearing activity (RE) and HDs of mice in socially reared (gray circles) and isolation-reared groups (black circles). The triangles show the mean values of the RE and HDs of mice and the error bars indicate the standard deviations

Fig. 4

Comparison of exploratory behavior of mice reared socially (gray circles) and in isolation (black circles) in the elevated plus maze test. a: the distribution of ΔE and ΔT of mice in the two groups which were calculated according to the times the mice entering into open and closed arms in the elevated plus maze and the time the mice stayed there (see Methods for details). The dashed lines indicate the zero of ΔE and ΔT. b: the distribution of RE and HDs of mice in the two groups. The triangles show the mean values and the error bars indicate the standard deviations

Fig. 5

Relationship of time that mice spent in the novel digging task to the exploratory behavior level detected utilizing the hole board (HB) (a, b, c and d) and elevated plus maze (EPM) (e and f) tests. Solid lines, regression lines; R², determination coefficient; P, significant level