A natural history of the frontal cortex

The frontal cortex of mammals has been the site of significant reshuffles during the about 310 million years of mammalian evolution. The existence of the frontal lobe is linked to the emergence of major cognitive and motor abilities, from the elaboration of efficient problem-solving strategies to the use of language in human. However, presenting the frontal lobe of the human cortex in an evolutionary perspective is a real challenge, almost a wager lost in advance. Reasons are the following. Although present in all the mammalian species known so far, the frontal lobe, and especially its prefrontal domain, is one of the most variable brain regions among mammalian species, even among individuals. The prefrontal cortex (PFC) exhibits a lot of variations not only in size (from 35% of the total brain volume in human to less than 4% in the cat for example [1]), but also in its connections, cell composition, branching pattern of neuronal processes, etc. Similar remarks can be made for other domains of the frontal cortex, including the motor and Broca's area for example. These variations do not fit with the phylogenetical position of the corresponding species, even in hominins, precluding any elaboration of a simple scenario of the evolution of the frontal cortex in mammals. Although disappointing at first glance, this observation points to the major influence of environment and lifestyle in shaping the functional anatomy of the frontal lobe during evolution. This has been rendered possible both by the extraordinary plasticity of the development of the frontal lobe, especially of the PFC, and by strong functional selection upon demanding environmental constraints. This is well exemplified by the discrepancies between overall brain volume and the size of the PFC in species like primates, cetaceans or carnivores [2]. Despite these large variations, some building principles seem to be at work to support the main functions of the frontal cortex. The frontal lobe includes the main motor area of the brain in all mammals, with different specializations. In contrast, the PFC is mostly an associative area receiving multimodal sensory cues and establishing connections with the basal ganglia, amygdala, insular and medial temporal cortex, all features conserved in mammals. Its orbito-frontal part is often defined by its afferent connections from the mediodorsal nucleus of thalamus. Then, it receives strong dopaminergic input from the mesocortical pathway, playing a crucial role in executive functions and motor planning. By definition, a PFC does not exist in species other than mammals, since only mammals have a six-layered cortical pallium. It is thus very striking that non-mammalian amniotes such as birds also display high cognitive flexibility and skills qualified as “intelligence”, and also often use languages in social communication, all functions that require a frontal cortex in mammals. In birds, and probably in other vertebrate species also, the same rules of functional organization of the pallium as those found for the mammalian cortex seem to operate and underlie similar sophisticated behaviors. In particular, the identification in some birds of a pallial structure exhibiting most of the main characteristics of the mammalian PFC is striking. Since this pallial structure is not homologous to the PFC in any respect, it strongly suggests that these executive structures have emerged independently during evolution [3]. Thus, very likely, similar functional constraints led the pallium of mammals and birds to converge on similar – yet independent – rules to build “executive” brain areas. Similar convergence holds true for the neural circuits underlying speech and languages, also in birds and primates. These types of convergences certainly exist in other groups of vertebrates such as teleost fishes. The frontal cortex is thus unique to mammals, but not the only one of its kind to have emerged during the evolution of the different vertebrate groups.