A Novel Cooperative Behavior Assay in Rats Reveals Distinct Social Coordination Strategies of Increasing Complexity and Social Reciprocity Deficits in a Model of Fragile X Syndrome

Abstract

Cooperative behavior, the ability of individuals to coordinate their actions toward shared goals, is fundamental to survival and social success across species. However, the mechanisms supporting cooperation and disruptions leading to social deficits in neurodevelopmental disorders such as autism spectrum disorder remain poorly understood. To address these questions, we developed a novel cooperation task in which rat pairs had to visit matching reward wells on paired spatial mazes under deterministic and probabilistic reward contingencies, utilizing dyads of littermate wild-type (WT) and Fmr1 knock-out ( Fmr1 ) rats, a model of Fragile X Syndrome. Both WT and Fmr1 male rat pairs exhibited dynamic turn-taking with mixed leader–follower behavior for cooperation; however, WT pairs achieved significantly greater cooperation success than Fmr1 pairs. WT and Fmr1 pairs both successfully utilized a simple follower-tracking-leader strategy, resulting in slower asynchronous transitions between reward wells, with Fmr1 pairs more reliant on this reactive strategy. WT rat pairs also exhibited a more efficient and flexible predictive cooperation strategy, requiring anticipation and coordination of optimal transition patterns with peers, resulting in faster synchronous transitions. Fmr1 rats were unable to utilize this more efficient social reciprocity strategy of higher complexity, leading to deficits in adapting to the probabilistic reward condition and in cooperative behavior. These findings reveal distinct strategies of varying complexity for cooperation, demonstrating the existence of a complex predictive social reciprocity strategy in WT rats and its disruption in a rat autism model, providing a foundation for investigating mechanisms underlying social interactions with relevance to neurodevelopmental disorders.