The experience of emotion comprises not only feelings but also behavioral expression, internal awareness, and the body’s physiological response. However, it remains unclear how the brain integrates these disparate aspects of emotion. Here, we used focal infrared neural stimulation (INS) of a sensory gateway (medial pulvinar [PM]) to map functional connections in cingulate, insula, and amygdala, using ultra-high-field 7T functional magnetic resonance imaging. Within each area, we find that PM-connected sites are patchy and mesoscale (millimeter scale) in size. Moreover, connections evoked from sequential stimulation sites in PM evoke topographic activations within areal subregions. We suggest mesoscale functional connections link the limbic axes of motor expression (cingulate), interoception (insula), and emotion-related processing (amygdala) and that the limbic system is fundamentally quite orderly at the mesoscale. Our results underscore the importance of millimeter-scale precision and organization in the diagnosis and treatment of affective disorders.