The neural basis of imagination: An evolutionary perspective

The study of imagination has progressed due to its operationalization through a variety of behavioural tasks, initially designed for human participants and later adapted to non-human animals. However, this behavioural data has proven insufficient for inferring the level and scope of imagination in animals. To better understand human imagination, and its possible manifestations in animals, we trace here the evolutionary origin of the default mode network (DMN), which is central to human imagination. We show that the evolution of the DMN involved significant neural innovations at the base of the mammalian lineage: the emergence of the neocortex and a substantial reorganization of the hippocampus. These two structures underwent parallel evolution, including the emergence of a 3D organization, the establishment of a canonical microcircuit, a significant development of pyramidal neurons, and the emergence of dedicated compartments of granular neurons. We suggest that previous studies have underestimated the importance of hippocampal modifications in shaping the mammalian brain, especially considering its central role in studies of memory consolidation, replay and human imagination more generally. Looking beyond mammals, we expect to find a functionally similar network in birds, convergent with the mammalian DMN. We end with a discussion of findings that could be construed as indicators of imagination within and outside the mammalian clade and the relations of our extraordinary human imagination to language. • The default mode network (DMN) is consistently involved in imaginative tasks in humans • The two main architectural components of the DMN are the neocortex and hippocampus • Both structures underwent significant changes at the base of the mammalian lineage • These changes may have increased the imaginative abilities of the mammalian brain