Language, Paleoneurology, and the Fronto-Parietal System

摘要

Paleoneurology and the frontal lobes Broca's area has represented a major issue in evolutionary anthropology since the discovery of its association with language impairment. It was generally presumed that the whole frontal lobes had undergone important changes in our phylogenetic lineage, also because of their involvement in personality and executive functions. Accordingly, plenty of authors have declared so far that the fossil record supplies patent evidence of frontal lobe evolution, despite the fact that the fossil record, to date, has supplied none. In terms of frontal sulcal pattern, all human species display a similar scheme, at least from two million years (Tobias, 1987 ; Holloway, 1995 ). In terms of volume, there are still disagreements on whether or not humans and living apes share a similar allometric proportion of frontal cortex, and whether any minor difference may be statistically or functionally significant, (e.g., Semendeferi et al., 1997 ; Rilling, 2006 ; Barton and Venditti, 2013 ; Smaers, 2013 ; Gabi et al., 2016 ). If there are such critical uncertainties when dealing with living species, it can be easily imagined that these same issue can be particularly difficult to investigate in fossils, which can only provide information on the external gross anatomy of the brain and according to extremely reduced sample sizes. Many statements concerning the evolution of specific frontal cortical traits in fossil hominids are based on individual and fragmented cranial remains. Such punctual and partial information may be useful to delineate further hypotheses, but we don't have to forget that it can only provide incomplete and speculative perspectives (Bruner, 2013 ). These limitations may generate blurred frontiers between opinions (i.e., personal and subjective assessments) and hypotheses (perspectives that can be evaluated through experimental or quantitative approaches).An actual increase of the frontal or prefrontal cortex volume cannot be tested in fossils because of the many operational limits (like for example the localization of reliable boundaries). Apart from variation in absolute size, Neandertals and modern humans display relatively wider frontal lobes, when compared with other human species (Bruner and Holloway, 2010 ). In these two species, the breadth of the anterior fossa at the Broca's cap is larger, relative to the general brain width. Therefore, the term “wider” refers to endocranial proportions, and not necessarily to an absolute enlargement or expansion of the lobes. It is worth noting that modern humans and Neandertals are also the only hominids in which the frontal lobes lie entirely above the orbits (Bruner et al., 2014a ). The eyeball and the prefrontal cortex are separated by a tiny bony layer (this was the unfortunate principle of lobotomy), and these two districts exert reciprocal spatial constraints during morphogenesis. Orbits are anterior to the braincase in chimps, inferior to the frontal lobes in Neandertals and modern humans, and in an intermediate position in archaic humans (Bruner et al., 2014a ; Beaudet and Bruner, 2017 -Figure 1 ). Therefore, we cannot exclude that the lateral frontal widening displayed in modern humans and Neandertals could be a secondary structural consequence (lateral redistribution of the neural mass) of this vertical spatial limitation, with no functional meaning in terms of neural organization. Furthermore, in modern humans, the facial block (the bones forming the face) is much reduced when compared with earlier hominids or apes, and the temporal muscle is reduced accordingly (Cachel, 1978 ). The Broca's cap is adjacent to the temporal fossa, and the reduction of the muscle further decreases any possible lateral spatial constraints, if any. This does not mean that frontal widening in modern humans and Neandertals was not associated with true brain changes, but only that the influence of cranial architecture cannot be ruled out, and such frontal widening cannot be hence indisputably interpreted as evidence of change in brain organization. Figure 1 (Above) Projected parasagittal MRI slices (in red) showing the spatial relationship between the frontal cortex and upper face in modern humans, and projected midsagittal MRI slices (in blue) showing the parietal, occipital, and cerebellar areas. (Middle) Digital reconstruction of a chimp, of an African Middle Pleistocene fossil human, and of a modern human skull, showing the endocranial cavity (blue) and the orbital space (pink) (after Beaudet and Bruner, 2017 ). (Below) CT scout views of chimpanzees, Homo heidelbergensis and Homo sapiens , showing the position of the orbital boundaries; on the left, the thin-plate spline deformation pattern that separates chimps from modern humans, with fossil humans displaying an intermediate morphology (after Pereira-Pedro et al., 2017 ). The only specimen which goes against this structural hypothesis is the skull of Maba, found in China and dated to the tran