Cingulate cortex in the three limbic subsystems

Abstract

Broca's (1878) definition of the limbic lobe referred to its being located at the edge of the cerebral cortex, and Papez (1937) and MacLean (1990) welded a series of medial surface structures into what we now know as the limbic system. The last four decades of research have provided a wealth of detailed information on the connectivity and functions of the limbic system and one can only conclude that it is not a uniform and single system. The cingulate cortex itself has three major divisions: anterior primarily for emotion, middle mainly for response selection and feedback-guided decision making, and posterior/retrosplenial cortices for visuospatial orientation and assessing the self-relevance of objects and events. Each of these divisions has a different cytoarchitecture and set of connections. The cingulate observations lead to a new framework of limbic organization: three limbic subsystems that include the amygdala, orbitofrontal cortex, the insula, the hippocampus, and, of course, the cingulate cortex. This concept is expanded in terms of connectivity among them and the underlying functions of each subsystem. The three limbic subsystems considered here are the "anterior emotional subsystem," the "middle sensorimotor subsystem," and the "posterior cognitive spatial map subsystem" for localizing personally relevant objects and episodes. A defining characteristic of the anterior emotional subsystem is its input from the amygdala. Another interesting outcome of this analysis is that the middle hippocampus and anterior midcingulate cortex share a role in approach-avoidance decision making suggesting a potential for connectional synergy. Thus, the concept of "a" limbic system needs radical revision to accommodate a minimum of three limbic subsystems. As this approach was initiated by the three-part composition of the cingulate cortex, a finer-grain analysis of the cingulate region shows that six limbic subsystems may be a more accurate reflection of limbic organization.

Keywords: Amygdala; Connections; Emotion; Hippocampus; Insula; Orbitofrontal cortex; Response selection; Visuospatial orientation.