Short-term social isolation induces depressive-like behaviour and reinstates the retrieval of an aversive task: mood-congruent memory in male mice?

Abstract

Background: Although mood-congruent memory (MCM), or the tendency to recall information consistent with one's mood, is a robust phenomenon in human depression, to our knowledge, it has never been demonstrated in animals.

Methods: Mice were subjected to social isolation (SI) or crowding for 12 hours and had their depressive-like behaviour (evaluated by the forced swim, tail suspension, sucrose preference and splash tests) or their serum corticosterone concentrations evaluated. In addition, we determined the temporal forgetting curve of the plus-maze discriminative avoidance task (PM-DAT) and examined the effects of SI or crowding on memory retrieval in the PM-DAT. Finally, we verified the effects of metyrapone pretreatment on reinstatement of memory retrieval or on the increase of corticosterone levels induced by SI.

Results: Twelve hours of SI produced depressive-like behaviour, enhanced corticosterone concentration and reinstated retrieval of a forgotten discriminative aversive (i.e., negatively valenced) task. Depressive-like behaviour was critical for this facilitative effect of SI because 12 hours of crowding neither induced depressive-like behaviour nor enhanced retrieval, although it increased corticosterone levels at the same magnitude as SI. However, corticosterone increase was a necessary condition for MCM in mice, in that the corticosterone synthesis inhibitor metyrapone abolished SI-induced retrieval reinstatement.

Limitations: Our study did not investigate the effects of the social manipulations proposed here in a positively valenced task.

Conclusion: To our knowledge, the present paper provides the first evidence of MCM in animal models.

Fig. 1

Duration of immobility (s) in the forced swim test presented by mice that were socially isolated (SI), crowded or kept in their home cages (control) for 12 hours. Data are reported as means and standard errors. *p < 0.05 compared with the other 2 groups (1-way analysis of variance and Tukey test).

Fig. 2

(A) Latency (s) to the first immobility episode and (B) duration of immobility (s) in the tail suspension test presented by mice that were socially isolated (SI), crowded or kept in their home cages (control) for 12 hours. Data are reported as means and standard errors. *p < 0.05 compared with the other 2 groups (1-way analysis of variance and Tukey test).

Fig. 3

(A) Latency (s) to the first grooming episode and (B) duration of grooming (s) in the splash test presented by mice that were socially isolated (SI), crowded or kept in their home cages (control) for 12 hours. Data are reported as means and standard errors. *p < 0.05 compared with the other 2 groups (1-way analysis of variance and Tukey test).

Fig. 4

Percentage of sucrose consumption in the sucrose preference test presented by mice that were socially isolated (SI), crowded or kept in their home cages (control) for 12 hours. Data are reported as means and standard errors. *p < 0.05 compared with the other 2 groups (1-way analysis of variance and Tukey test).

Fig. 5

Time spent in the aversive and nonaversive enclosed arms of the plus-maze discriminative avoidance task apparatus in the (A) training and (B) test sessions by mice subjected to the test session 7, 15 or 30 days after the training session. Data are reported as means and standard errors. *p < 0.05 compared with the time spent in the nonaversive enclosed arm (2-way analysis of variance and Tukey test).

Fig. 6

Time spent in the aversive and nonaversive enclosed arms of the plus-maze discriminative avoidance task apparatus for all of the groups — control, socially isolated (SI) and crowded in the test session, respectively — in the (A) training and (B) test sessions, as well as (C) the total number of entries into all arms of the apparatus during the test session. Data are reported as means and standard errors. *p < 0.05 compared with the time spent in the nonaversive enclosed arm; †p < 0.05 compared with the time spent in the aversive enclosed arm of the other groups and ‡p < 0.05 compared with the other 2 groups (panel C, 1-way analysis of variance and Tukey test).

Fig. 7

Time spent in the aversive and nonaversive enclosed arms of the of the plus-maze discriminative avoidance task apparatus by all of the groups — control, socially isolated (SI) animals treated with vehicle and SI animals treated with metyrapone in the test session —in the (A) training and (B) test sessions, as well as (C) the total number of entries into all of the arms of the apparatus in the test session. Data are reported as means and standard errors. *p < 0.05 compared with the time spent in the nonaversive enclosed arm (panels A and B, 2-way analysis of variance and Tukey test). †p < 0.05 compared with the control group (panel C, 1-way analysis of variance and Tukey test).