Sex differences in the effects of social and physical environment on novelty-induced exploratory behavior and cocaine-stimulated locomotor activity in adolescent rats

Abstract

Many factors influence the rewarding effects of drugs such as cocaine. The present study was done to determine whether social and environmental factors alter behavior in adolescent male and female rats. On postnatal day (PND) 23, rats were housed in one of several same-sex conditions. Both social (number of rats per cage) and environmental (availability of toys) factors were manipulated. Socially isolated rats were housed alone (1 rat/cage) in an environment that either was impoverished (with no toys; II) or enriched (with toys; IE). Standard housing for these studies was social and impoverished, which was 2 rats/cage with no toys (SI2). Other rats were housed 2/cage with toys (SE2), or 3/cage with (SE3) or without (SI3) toys. On PND 37, novelty-induced locomotor activity was measured for 30min. On PND 44-46, locomotor activity in response to an injection of 5mg/kg cocaine was measured for 60min each day. For male rats, only social conditions altered novelty-induced activity. Males housed in groups of three had the most activity, compared to pair-housed and isolated rats. For females, social and environmental enrichment interacted to alter novelty-induced activity. In contrast to males, isolated females had increased activity, compared to group-housed females. Further, isolated females in impoverished environments had more activity than isolated females in enriched environments and group-housed females in impoverished environments. The effect of environmental enrichment on cocaine-stimulated locomotor activity was altered depending upon the number of rats living in a cage for males. For females, only social conditions altered cocaine-stimulated behavior, with activity increasing with the number of rats in the cage, regardless of environmental enrichment. These data show that social and environmental enrichment differentially alter novelty-induced and cocaine-stimulated locomotor activity in adolescent male and female rats.

Fig. 1

Response to a novel environment on PND 37 (two weeks after housing) of male adolescent rats housed under different conditions, expressed as mean ± SEM. (A) Distance traveled in 30 min and (B) time (secs) spent in the center of the chamber/30 min. The rats were not habituated to the locomotor chambers (i.e. testing began immediately after the rats were placed in the chambers for the first time and the sessions lasted 30 min). The SE3 and SI3 groups (3 rats/cage with or without toys, n=26 and 23, respectively) exhibited significantly higher levels of activity than any of the other groups tested. II = isolated impoverished (n=22; 1 rat/cage, no toys); SI2 = social impoverished (n=16; 2 rats/cage with no toys – this is our standard housing condition); IE = isolated enriched (n=16; 1 rat/cage with toys); SE2 = social enriched 2 (n=8; 2/cage with toys). *significant difference from isolated rats or rats housed 2/cage (p ≤ 0.05).

Fig. 2

Response to a novel environment on PND 37 (two weeks after housing) of female adolescent rats housed under different conditions, expressed as mean ± SEM. (A) Distance traveled in 30 min and (B) time (secs) spent in the center of the chamber/30 min. The rats were not habituated to the locomotor chambers (i.e. testing began immediately after the rats were placed in the chambers for the first time and the sessions lasted 30 min). (A) The II group exhibited significantly higher levels of activity than any of the other groups tested. (B) Both the II and SI2 rats spent more time exploring the center of the test chamber than any of the other groups. II = isolated impoverished (one rat/cage without toys, n=24) IE = isolated enriched (n=24; one rat/cage with toys); SI2 = social impoverished 2 (n=16; 2/cage without toys); SE2 = social enriched 2 (n=16; 2/cage with toys); SI3 = social impoverished 3 (n=24; 3 rats/cage, no toys); SE3 = social enriched 3 (n=24; 3 rats/cage, with toys). #significant difference from isolated impoverished rats (p ≤ 0.05).

Fig. 3

Baseline locomotor activity on PND 43 in (A) male rats and (B) female rats. In males, there was a significant interaction between social and environmental housing conditions. Post-hoc tests showed that environmental enrichment decreased activity only in the rats housed 3/cage, but did not have a significant effect in rats housed alone or in pairs. In females, there was a significant effect of environment in that impoverished rats had higher levels of activity overall compared to enriched rats, but no effect of social housing and no social × environmental interaction.

Fig. 4

The effect of 5 mg/kg of cocaine on locomotor activity in male adolescent rats (PND 44-46) habituated to the test chamber after housing in different social/environmental conditions. Rats were housed (A) one/cage (II vs IE); (B) two/cage (SI2 vs SE2); and (C) three/cage (SI3 vs SE3). Data are presented as mean ± SEM total distance traveled during a 60 min session after habituation as a percent of baseline distance traveled on PND 43. *significant difference vs impoverished rats over 3 days of testing (p<0.05).

Fig. 5

The effect of 5 mg/kg of cocaine on locomotor activity in female adolescent rats (PND 44-46) habituated to the test chamber after housing in different social/environmental conditions. Rats were housed (A) one/cage (II vs IE); (B) two/cage (SI2 vs SE2); and (C) three/cage (SI3 vs SE3). Data are presented as mean ± SEM total distance traveled during a 60 min session after habituation as a percent of baseline distance traveled on PND 43.