Collaboration between human neuropsychology and comparative neuroscience has generated invaluable contributions to our understanding of human brain evolution and function. Further cross-talk between these disciplines has the potential to continue to revolutionize these fields. Modern neuroimaging methods could be applied in a comparative context, yielding exciting new data with the potential of providing insight into brain evolution. Conversely, incorporating an evolutionary base into the theoretical perspectives from which we approach human neuropsychology could lead to novel hypotheses and testable predictions. In the spirit of these objectives, we present here a new theoretical proposal, the Inferential Brain Hypothesis, whereby the human brain is thought to be characterized by a shift from perceptual processing to inferential computation, particularly within the social realm. This shift is believed to be a driving force for the evolution of the large human cortex. (JINS, 2012, 18, 394–401)

The “radiator” theory of brain evolution is proposed to account for “mosaic evolution” whereby brain size began to increase rapidly in the genus Homo well over a million years after bipedalism had been selected for in early hominids. Because hydrostatic pressures differ across columns of fluid depending on orientation (posture), vascular systems of early bipeds became reoriented so that cranial blood flowed preferentially to the vertebral plexus instead of the internal jugular vein in response to gravity. The Hadar early hominids and robust australopithecines partly achieved this reorientation with a dramatically enlarged occipital/marginal sinus system. On the other hand, hominids in the gracile australopithecine through Homo lineage delivered blood to the vertebral plexus via a widespread network of veins that became more elaborate through time. Mastoid and parietal emissary veins are representatives of this network, and increases in their frequencies during hominid evolution are indicative of its development. Brain size increased with increased frequencies of mastoid and parietal emissary veins in the lineage leading to and including Homo, but remained conservative in the robust australopithecine lineage that lacked the network of veins. The brain is an extremely heatsensitive organ and emissary veins in humans have been shown to cool the brain under conditions of hyperthermia. Thus, the network of veins in the lineage leading to Homo acted as a radiator that released a thermal constraint on brain size. The radiator theory is in keeping with the belief that basal gracile and basal robust australopithecines occupied distinct niches, with the former living in savanna mosaic habitats that were subject to hot temperatures and intense solar radiation during the day.

The basal ganglia (BG) have received much attention during the last 3 decades mainly because of their clinical relevance. Our understanding of their structure, organisation and function in terms of chemoarchitecture, compartmentalisation, connections and receptor localisation has increased equally. Most of the research has been focused on the mammalian BG, but a considerable number of studies have been carried out in nonmammalian vertebrates, in particular reptiles and birds. The BG of the latter 2 classes of vertebrates, which together with mammals constitute the amniotic vertebrates, have been thoroughly studied by means of tract-tracing and immunohistochemical techniques. The terminology used for amniotic BG structures has frequently been adopted to indicate putative corresponding structures in the brain of anamniotes, i.e. amphibians and fishes, but data for such a comparison were, until recently, almost totally lacking. It has been proposed several times that the occurrence of well developed BG structures probably constitutes a landmark in the anamniote-amniote transition. However, our recent studies of connections, chemoarchitecture and development of the basal forebrain of amphibians have revealed that tetrapod vertebrates share a common pattern of BG organisation. This pattern includes the existence of dorsal and ventral striatopallidal systems, reciprocal connections between the striatopallidal complex and the diencephalic and mesencephalic basal plate (striatonigral and nigrostriatal projections), and descending pathways from the striatopallidal system to the midbrain tectum and reticular formation. The connectional similarities are paralleled by similarities in the distribution of chemical markers of striatal and pallidal structures such as dopamine, substance P and enkephalin, as well as by similarities in development and expression of homeobox genes. On the other hand, a major evolutionary trend is the progressive involvement of the cortex in the processing of the thalamic sensory information relayed to the BG of tetrapods. By using the comparative approach, new insights have been gained with respect to certain features of the BG of vertebrates in general, such as the segmental organisation of the midbrain dopaminergic cell groups, the occurrence of large numbers of dopaminergic cell bodies within the telencephalon itself and the variability in, among others, connectivity and chemoarchitecture. However, the intriguing question whether the basal forebrain organisation of nontetrapods differs essentially from that observed in tetrapods still needs to be answered.