Olfaction, navigation, and the origin of isocortex

Abstract

There are remarkable similarities between the brains of mammals and birds in terms of microcircuit architecture, despite obvious differences in gross morphology and development. While in reptiles and birds the most expanding component (the dorsal ventricular ridge) displays an overall nuclear shape and derives from the lateral and ventral pallium, in mammals a dorsal pallial, six-layered isocortex shows the most remarkable elaboration. Regardless of discussions about possible homologies between mammalian and avian brains, a main question remains in explaining the emergence of the mammalian isocortex, because it represents a unique phenotype across amniotes. In this article, we propose that the origin of the isocortex was driven by behavioral adaptations involving olfactory driven goal-directed and navigating behaviors. These adaptations were linked with increasing sensory development, which provided selective pressure for the expansion of the dorsal pallium. The latter appeared as an interface in olfactory-hippocampal networks, contributing somatosensory information for navigating behavior. Sensory input from other modalities like vision and audition were subsequently recruited into this expanding region, contributing to multimodal associative networks.

Keywords: hippocampus; isocortical evolution; olfaction; plasticity.

Figure 1

Phylogeny of fossil mammals. Critical phylogenetic nodes are shown in numbers. The inset provides a summary diagram of the different clades. Cynodonts are shown in purple. Node (1, blue) mammaliamorphs, a group of advanced cynodonts; (2, also blue) mammaliaforms. The common ancestor of modern mammals (crown mammals) is shown at the base of the green tree. This line gives rise to most mesozoic mammals (3, yellow) and to monotremes (4, green). The common ancestor of therians (marsupials and placentals) stays at the base of (5, blue) marsupials or metatherians and (6, red) placentals or eutherians. Note the dramatic extinction of mammalian lineages at the end of the Cretaceous, concomitant with the extinction of the dinosaurs. With permission from Luo (2007).

Figure 2

Olfactory projections to the hippocampus in birds, reptiles, and mammals. Based on Striedter (2015), with permission. CA1, Cornu Ammonis 1; CA3, Cornu Ammonis 3; Cx, Cortex; DG, Dentate gyrus; DLA, Dorsolateral anterior nucleus; DLAm, medial part of the dorsolateral anterior nucleus; DTh, Dorsal thalamus; HTh, Hypothalamus; ERCx, Entorhinal cortex; DCx, Dorsal cortex; DL, dorsolateral division of the hippocampus; DM, dorsomedial division of the hippocampus; DMCx, Dorsomedial cortex; LCx, Lateral cortex; N, Nidopallium; MCx, Medial cortex; OCx, Olfactory cortex; Sept, Septum; V, ventral division of the hippocampus (also named V-shaped area).

Figure 3

Connections between the olfactory cortex, the hippocampus and the frontal cortex in mammals. Note the thalamic olfactory projection that is relayed to the frontal cortex. Modified from Lynch (1986), Figure 8A, pp. 28, ©1986 Massachusetts Institute of Technology, by permission of The MIT Press.