In humans, frontal lesions result in deficits of social and emotional behavior that are often surprising in the presence of intact language and other cognitive skills. The connections between the motivation and memory functions of limbic cortex and the motor planning functions of frontal neocortex must be fundamental to meeting the daily challenges of self-regulation. The connectional architecture of limbic and neocortical networks suggests a model of function. The densely interconnected paralimbic cortices may serve to maintain a global motivational context within which specific actions are articulated and sequenced within frontal neocortical networks. The paralimbic networks represent the visceral and kinesthetic information that is integral to the representation of the bodily self. In a general sense, the implicit self-representation within paralimbic networks may shape the significance of perceptions and the motivational context for developing actions. The network architecture of the frontal lobe reflects the dual limbic origins of frontal cortex, in the dorsal archicortical and ventral paleocortical structures. In this paper, we speculated that these two limbic-cortical pathways apply different motivational biases to direct the frontal lobe representation of working memory. The dorsal limbic mechanisms projecting through the cingulate gyrus may be influenced by hedonic evaluations, social attachments, and they may initiate a mode of motor control that is holistic and impulsive. In contrast, the ventral limbic pathway from the amygdala to orbital frontal cortex may implement a tight, restricted mode of motor control that reflects adaptive constraints of self-preservation. In the human brain, hemispheric specialization appears to have led to asymmetric elaborations of the dorsal and ventral pathways. Understanding the inherent asymmetries of corticolimbic architecture may be important in interpreting the increasing evidence that the left and right frontal lobes contribute differently to normal and pathological forms of self-regulation.