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For more than two decades, research focusing on both clinical and non-clinical populations has suggested a key role for specific regions in the regulation of self-conscious emotions. It is speculated that both the expression and the interpretation of self-conscious emotions are critical in humans for action planning and response, communication, learning, parenting, and most social encounters. Empathy, Guilt, Jealousy, Shame, and Pride are all categorized as self-conscious emotions, all of which are crucial components to one’s sense of self. There has been an abundance of evidence pointing to the right Fronto-Temporal involvement in the integration of cognitive processes underlying the expression of these emotions. Numerous regions within the right hemisphere have been identified including the right temporal parietal junction (rTPJ), the orbitofrontal cortex (OFC), and the inferior parietal lobule (IPL). In this review, we aim to investigate patient cases, in addition to clinical and non-clinical studies. We also aim to highlight these specific brain regions pivotal to the right hemispheric dominance observed in the neural correlates of such self-conscious emotions and provide the potential role that self-conscious emotions play in evolution.