Adaptive control of functional connectivity: dorsal and ventral limbic divisions regulate the dorsal and ventral neocortical networks

Abstract

The connectional anatomy of the primate cortex is now well-defined by the Structural Model, in which adjacent cortical areas are interconnected in an organized network hierarchy of communication and control. The computational theory of “active inference” can be aligned with this architecture, proposing that predictions descend from higher association areas to be updated by ascending prediction errors from lower (i.e. primary) sensory and motor areas. Given the connectivity, the limbic networks at the apex of the cerebral hierarchy must then be responsible for the most general expectancies, which are propagated through the hierarchy to organize the multiple component network levels of experience and behavior. Anatomical evidence suggests that there are dual limbic divisions, reflecting archicortical (dorsal) and paleocortical (ventral) derivations, resulting in fundamentally different neural mechanisms for managing expectancies across the corticolimbic hierarchy. In the functional connectivity literature, the dorsal attention network is seen to provide top-down or endogenous control of attention, whereas the ventral attention network provides stimulus bound or exogenous attentional control. We review evidence indicating that the dorsal, archicortical division of the limbic system provides a feedforward, impulsive, endogenous mode of motive control, whereas the ventral, paleocortical limbic division provides feedback constraint linked to exogenous events.