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Abstract Although macaques and marmosets are both primates of choice for studying the brain mechanisms of cognition, they differ in key aspects of anatomy and behavior. Interestingly, recent connectomic analysis revealed that strong top-down projections from the prefrontal cortex to the posterior parietal cortex, present in macaques and important for executive function, are absent in marmosets. Here, we propose a consensus mapping that bridges the two species’ cortical atlases and allows for direct area-to-area comparison of their connectomes, which are then used to build comparative computational large-scale modeling of the frontoparietal circuit for working memory. We found that the macaque model exhibits resilience against distractors, a prerequisite for normal working memory function. By contrast, the marmoset model is sensitive to distractibility commonly observed behaviorally in this species. Surprisingly, this contrasting trend can be swapped by scaling intrafrontal and frontoparietal connections. Finally, the relevance to primate ethology and evolution is discussed. Graphical Abstract HighlightsConsensus mapping allows for directly comparing macaque and marmoset connectomes.Connectomes and spine counts constrain large-scale models of working memory.The marmoset model is susceptible to distraction, but not the macaque.Our results capture real life difference with regard to distraction.