Paleoneurology deals with the study of brain anatomy in fossil species, as inferred from the morphology of their endocranial features. When compared with other living and extinct hominids, Homo sapiens is characterized by larger parietal bones and, according to the paleoneurological evidence, also by larger parietal lobes. The dorsal elements of the posterior parietal cortex (superior parietal lobules, precuneus, and intraparietal sulcus) may be involved in these morphological changes. This parietal expansion was also associated with an increase in the corresponding vascular networks, and possibly with increased heat loads. Only H. sapiens has a specific early ontogenetic stage in which brain form achieves such globular appearance. In adult modern humans, the precuneus displays remarkable variation, being largely responsible for the longitudinal parietal size. The precuneus is also much more expanded in modern humans than in chimpanzees. Parietal expansion is not influenced by brain size in fossil hominids or living primates. Therefore, our larger parietal cortex must be interpreted as a derived feature. Spatial models suggest that the dorsal and anterior areas of the precuneus might be involved in these derived morphological variations. These areas are crucial for visuospatial integration, and are sensitive to both genetic and environmental influences. This article reviews almost 20 years of my collaborations on human parietal lobe evolution, integrating functional craniology, paleoneurology, and evolutionary neuroanatomy.

Morphology is not only a study of material things and of the forms of material things, but has its dynamical aspect, under which we deal with the interpretation, in terms of force, of the operations of energy.

D’Arcy Wentworth Thompson

(On Growth and Form, 1942)

Traditionally, paleoneurology has been defined as the study of fossil endocasts, namely the casts of the cranial cavity in extinct species [Falk, 1987; Holloway et al., 2004]. The tight contact between brain and braincase, and the fact that the vault bones are largely shaped by the brain during growth, makes it possible to provide some inferences from skull (endocranial) morphology on brain anatomy [Bruner, 2017a]. This is particularly relevant when dealing with species for which we only have bone remains. Brain tissues do not fossilize, but the endocranial cavity can supply information on brain size and proportions, as well as on sulcal patterns, and in the past century these have been the most investigated paleoneurological features. On the endocranial wall, there are also the imprints of some vascular elements, such as the middle meningeal artery and the venous sinuses. The endocranial cavity provides this information by itself, but nonetheless paleoneurology (which should be more properly termed paleoneurobiology) largely deals with its positive mold, the endocranial cast. After all, we are primates, and we are used to relying on our eyes and hands to interact with our environment. That is why we prefer to have “something to see and to handle,” instead of an empty cavity. Of course, much information is lost from a real brain to its endocranial cast, which is a sort of geometrical model able to supply only some scattered information on cerebral gross cortical features and general proportions. Furthermore, the meninges and the cerebrospinal fluid are interposed between the cerebral cortex and the internal table of the braincase, separating their respective surfaces and smoothing the endocranial imprints, most of all in larger skulls [Kobayashi et al., 2014; Van Minh and Hamada, 2017]. Yet, despite these limitations, this is the only direct information we can have on the brains of extinct taxa and, therefore, deserves attention.

However, not every endocranial variation is due to brain anatomy. Even the word “brain” is a bit misleading and very general when dealing with morphology. Its size and shape depends on neurons but also upon glial cells, cerebrospinal fluid, and blood vessels. Furthermore, its form and geometry are not a real property of the organ itself, but are largely due to internal blood pressure and external meningeal tension [Moss and Young, 1960]. Additionally, the intimate spatial relationship between skull and brain makes influences between bone and cortex reciprocal, and the final phenotype is hence shaped by the effects of both soft and hard tissues. In terms of both ontogeny an phylogeny, skull and brain must co-evolve, following a principle of structural and functional balance [Richtsmeier et al., 2006; Bruner, 2015]. In the dorsal regions (vault), the brain largely molds the bones because its growth processes are compensated by bone deposition and modeling. However, in the ventral regions (base), the skull exerts important constraints on the brain form at the three endocranial fossae. The frontal lobes are constrained by the orbital structures, the temporal lobes are constrained by the facial block and by mandibular elements, and the cerebellum is constrained by the cranial base flexion. Therefore, when handling endocasts, paleoneurology must carefully consider not only brain anatomy but also the general spatial and morphogenetic relationships between skull and brain, so as to determine what changes of the brain form are due to brain evolution, and what are secondary outcomes due to cranial influences. Both kinds of variations are relevant in evolutionary anthropology, but only the former might possibly be associated with neural (and ultimately cognitive) variations.

Parietal lobes have interested paleoanthropologists for a long time. In the early days of the discipline, almost one century ago, Raymond Dart and Franz Weidenreich already mentioned morphological differences of the parietal region when studying australopithecines and Homo erectus, respectively. Ralph Holloway [1981] was probably the first to perform an endocranial shape analysis on living and fossil hominoids, evidencing a remarkable parietal variability among different species. In humans, distinctive parietal traits have been known since the first half of the 20th century also in neurobiology [Catani et al., 2017], and advances in the study of the parietal cortex have been stimulating and promising [Mountcastle, 1995]. Nonetheless, the posterior parietal cortex was, until recently, an “uncharted region” [Zilles and Palomero-Gallagher, 2001], and parietal lobes have never been taken into consideration when dealing with key changes in human evolution.

There could be at least 5 main reasons for this. First, a large part of the parietal cortex is not superficial but positioned under the cerebral surface (precuneus and intraparietal sulcus). These folds are more difficult to discern in terms of dissection and visualization, and they can pass unnoticed in many observations and surveys. Second, this deep position makes damage to these areas less compatible with survival after impairment. Functional damage – important in detecting an association between structure and function in the past centuries – is less easy to observe in these deep cortical areas when compared with lesions in other regions (e.g., language or personality alterations after frontal injury). Third, the parietal cortex is generally labeled with the elusive term “association cortex,” which denotes multiple and integrative functions. The parallel involvement of many distinct functions makes experiments and inferences less straightforward. Fourth, many parts of the parietal lobes are associated with visuospatial integration which, in general, refers to a set of functions traditionally interpreted as basic spatial management, something that was not expected to be involved in “higher” cognitive functions. Fifth, humans and nonhuman primates display many anatomical differences which often hamper a direct comparative approach. Patent inconsistencies between the monkey and human parietal cortical maps were described since Brodmann’s studies back in 1909 [Zilles and Palomero-Gallagher, 2001; Zilles and Amunts, 2010]. This lack of correspondence, instead of stimulating the study of these areas, may have paradoxically demoted interest in these cortical elements.

At the end of the 1990s, I began applying shape analysis and multivariate statistics to paleoanthropology and craniology, and it soon became apparent that parietal bone shape was characteristic in our own species. Parietal bone shape differences could have been only a matter of cranial architecture, but then I found similar results when working with endocasts, brains, or vessels. I was surprised to find an unexpected paucity of information on many cranial, cerebral, and vascular traits associated with parietal regions, so I began to investigate not only fossils but also living humans, not only hominoids but also other primates, not only evolutionary aspects but also medical ones, not only the isolated features but also their relationships. This article is hence a review of almost 20 years of my personal collaborations on the evolution of parietal anatomy, a long trail that did not aim to look for answers but instead search for proper questions.

The modern human skull has always been defined as “globular” when compared with extinct human species, which instead display a flatter braincase [Lieberman et al., 2002]. The frontal bone can partially contribute to this globular shape because of a more pronounced curvature of the frontal squama. However, there is no evolutionary evidence of macroscopic morphological changes in the modern human frontal lobes or in the frontal endocranial profile [Bookstein et al., 1999; Semendeferi et al., 2002; Bruner, 2017b], and therefore such frontal curvature is probably simply a spatial rearrangement due to the peculiar position of our face situated under the anterior cranial fossa [Beaudet and Bruner, 2017; Pereira-Pedro et al., 2017a]. Instead, shape analyses revealed that our globular vault is largely due to the size and proportions of the parietal bones [Bruner et al., 2004]. In fact, Homo sapiens has a parietal bone which is larger and more bulging than in any other human species [Bruner et al., 2011a]. This feature is not due to the large size of the braincase, and in fact the Neanderthals, with a similar cranial capacity, displayed short and flat parietal bones [Bruner, 2014]. The longitudinal size and curvature of the parietal bones do apparently not influence the position of other endocranial regions, but have an effect on the general orientation of the skull, thus influencing the general head position and its functional axis [Bruner et al., 2017a].

Moving from skull to brain, the boundaries of the parietal lobes can be tentatively recognized on endocasts [Pereira-Pedro and Bruner, 2018]. However, while morphometrics of the bone are based on fixed and recognizable craniometric landmarks (sutures), morphometrics of the lobe must be necessarily performed on anatomical inferences. Sulcal imprints are faint and smooth, and their localization is based on the experience of the anatomists. Nonetheless, the localization of cortical references on endocasts relies not only on the recognition of the specific grooves or bosses on the endocranial surface, but also on the relative position of other surrounding cortical elements. The use of sample or hemispheric averages can further limit this anatomical uncertainty, providing a rough but reasonable estimation of the position of the central sulcus, postcentral sulcus, parieto-occipital sulcus, intraparietal sulcus, supramarginal gyrus, and angular gyrus. According to such estimations, modern humans are not only characterized by larger parietal bones but also by larger parietal lobes (Fig. 1) [Bruner et al., 2003, 2018a; Bruner, 2004]. Spatially, this difference is apparently associated with the dorsal parts of the parietal cortex, possibly the superior parietal lobules or the intraparietal sulcus [Bruner, 2010]. A similar situation can be described when comparing the endocasts of living hominoids, with modern humans displaying a remarkable expansion of the superior parietal lobule (Fig. 2).

Fig. 1.

When compared with all the other fossil hominids, Homo sapiens’ rounded skull (a), in terms of midsagittal geometry (b), is largely due to absolute and relative enlargement of the parietal bone (c – digital replica of skull and endocast of an australopith, Sts5, and shape deformation associated with modern human cranial form). Some anatomical references of the parietal lobe (cs, central sulcus; pos, parieto-occipital sulcus; ips, intraparietal sulcus; smg, supramarginal gyrus; ag, angular gyrus) can be tentatively inferred on endocasts (d). When compared with more archaic human species like Homo erectus (e), Neanderthals display a lateral bulging of the dorsal parietal surface (LD: lateral dorsal areas), and modern humans are further characterized by a general longitudinal expansion of the same region (SD, sagittal dorsal areas). The former variation spatially matches the position of the intraparietal sulcus and superior parietal lobules, while the latter corresponds to the position of the superior parietal lobules and precuneus. Neanderthals and modern humans share a similar cranial capacity, but the latter shows a general enlargement of the parietal lobes (f – digital replica of skull and endocasts of the Neandertal Saccopastore 1, and shape deformation associated with modern human endocranial anatomy). Images after Bruner [2004, 2010, 2014] and Bruner et al. [2004, 2014a, 2015c].

Fig. 1.

When compared with all the other fossil hominids, Homo sapiens’ rounded skull (a), in terms of midsagittal geometry (b), is largely due to absolute and relative enlargement of the parietal bone (c – digital replica of skull and endocast of an australopith, Sts5, and shape deformation associated with modern human cranial form). Some anatomical references of the parietal lobe (cs, central sulcus; pos, parieto-occipital sulcus; ips, intraparietal sulcus; smg, supramarginal gyrus; ag, angular gyrus) can be tentatively inferred on endocasts (d). When compared with more archaic human species like Homo erectus (e), Neanderthals display a lateral bulging of the dorsal parietal surface (LD: lateral dorsal areas), and modern humans are further characterized by a general longitudinal expansion of the same region (SD, sagittal dorsal areas). The former variation spatially matches the position of the intraparietal sulcus and superior parietal lobules, while the latter corresponds to the position of the superior parietal lobules and precuneus. Neanderthals and modern humans share a similar cranial capacity, but the latter shows a general enlargement of the parietal lobes (f – digital replica of skull and endocasts of the Neandertal Saccopastore 1, and shape deformation associated with modern human endocranial anatomy). Images after Bruner [2004, 2010, 2014] and Bruner et al. [2004, 2014a, 2015c].

Close modal
Fig. 2.

A principal component analysis on endocranial 3D coordinates from hominoid endocasts using parietal lobe landmarks shows a PC1 (48% of the total variation) separating humans from all apes (above) because of parietal lobe enlargement (middle; red wireframe shows the shape change toward humans). If we consider only the parietal landmarks (below), PC1 (67%) separates again humans from apes because of the enlargement of the dorsal and anterior regions of the parietal lobe. In this example, endocasts from 1 representative individual of each species (adult males) were used, averaging 10 replicas and the 2 hemispheres, so as to limit uncertainty due to landmark localization (data after Pereira-Pedro and Bruner [2018]). Parietal landmarks: ab, angular boss; cs, central sulcus (midline estimation); ls, posterior end of the lateral sulcus; pos, parieto-occipital sulcus (midsagittal estimation); sb, supramarginal boss. Species: BON, Pan paniscus; CHIM, Pan troglodytes; GIB, Hylobates lar; GOR, Gorilla gorilla; HUM, Homo sapiens; ORA, Pongo pygmaeus; SIA, Symphalangus syndactylus. Morphometrics was computed with MorphoJ 1.06d [Klingenberg, 2011].

Fig. 2.

A principal component analysis on endocranial 3D coordinates from hominoid endocasts using parietal lobe landmarks shows a PC1 (48% of the total variation) separating humans from all apes (above) because of parietal lobe enlargement (middle; red wireframe shows the shape change toward humans). If we consider only the parietal landmarks (below), PC1 (67%) separates again humans from apes because of the enlargement of the dorsal and anterior regions of the parietal lobe. In this example, endocasts from 1 representative individual of each species (adult males) were used, averaging 10 replicas and the 2 hemispheres, so as to limit uncertainty due to landmark localization (data after Pereira-Pedro and Bruner [2018]). Parietal landmarks: ab, angular boss; cs, central sulcus (midline estimation); ls, posterior end of the lateral sulcus; pos, parieto-occipital sulcus (midsagittal estimation); sb, supramarginal boss. Species: BON, Pan paniscus; CHIM, Pan troglodytes; GIB, Hylobates lar; GOR, Gorilla gorilla; HUM, Homo sapiens; ORA, Pongo pygmaeus; SIA, Symphalangus syndactylus. Morphometrics was computed with MorphoJ 1.06d [Klingenberg, 2011].

Close modal

An increase in the size and proportions of the parietal bone can be explained as an increase in the underlying brain elements (larger parietal cortex) or, alternatively, as a spatial readjustment of the cranial architecture (i.e., flexion and curvature of the skull) with no major changes in brain proportions. However, in the case of an increase in the parietal lobe, the latter explication does not stand. A volumetric change of a specific cortical region cannot be interpreted as a geometric inflation due to spatial curvature and is more likely to be associated with the increase in some cerebral components (neurons, connections, glia, etc.) included within those boundaries.

Additional evidence comes from the vascular system: only H. sapiens has a complex and reticulated endocranial vascular network as far as we can see for the meningeal and diploic vessels [Bruner et al., 2005; Bruner and Sherkat, 2008; Rangel de Lázaro et al., 2016]. Vascular morphology can show important individual variation, and the mechanisms and factors involved in such diversity are still not known. However, all extinct human species display simpler vascular networks when compared with modern humans, with almost no anastomotic connections between the main branches. Apparently, vascular complexity does not depend on brain size, and it particularly concerns the parietal surface. This is relevant because the endocranial vascular system may have a central role in brain thermoregulation [Bruner et al., 2011b]. Numerical simulations showed that the dorsal parietal surface in more platycephalic species is important for endocranial heat exchange, and the bulging of the parietal region characteristic of modern humans can hence contribute to increase the heat load of the corresponding deeper cerebral areas [Bruner et al., 2012, 2014a].

Ontogenetic analysis of the endocranial form suggested that modern human brain globularity is achieved early postnatally [Neubauer et al., 2009] or even prenatally [Ponce de León et al., 2016]. Either way, it is due to a morphogenetic stage which is specific to H. sapiens and absent in chimps or Neanderthals [Gunz et al., 2010; Neubauer et al., 2010; Scott et al., 2014]. In sum, head and brain globularity in our species is largely due to parietal lobes and bones, and associated with a species-specific growth period. As far as the paleoneurological evidence can show, such morphological differences are definitely more apparent than many subtle or individual variations commonly debated in paleoanthropology or evolutionary neuroanatomy. They should deserve, at least, attention.

Parietal lobes are located below the parietal bones, although the respective size and positions may vary [Bruner et al., 2015a]. The parieto-occipital sulcus, separating the parietal and occipital cortex, is more stable in its cranial location, roughly close to the boundary between the parietal and occipital bones (lambda). In contrast, the position of the anterior boundary of the lobe (central sulcus and postcentral gyrus) is more variable, and it becomes relatively closer to the boundary of the frontal and parietal bones (bregma) in brains with larger parietal lobes. Although these positions and proportions are influenced by many factors and distinct ontogenetic processes, there is still a significant correlation between parietal bone and lobe length even among adult humans. In adults, the form of the parietal bone and lobe is integrated with the form of the occipital bone and lobe [Gunz and Harvati, 2007; Bruner et al., 2018b], and bulging of one of the two regions is associated with the flattening of the other. In contrast, the size of the parietal lobe is inversely correlated with the size of the frontal and temporal lobes, and not correlated with the size of the occipital cortex [Allen et al., 2002]. This may suggest more structural constraints with the occipital region and more functional constraints with frontal and temporal regions – an entangled morphogenetic position, indeed.

A key element of the dorsal parietal cortex is the precuneus, which displays remarkable morphological variability (Fig. 3). When dealing with the whole midsagittal brain geometry in adult humans, the most variable feature regards the precuneus longitudinal extension [Bruner et al., 2014b]. Namely, adult individuals show a noticeable anatomical diversity because of the length of the precuneus. Differences mainly deal with the dorsal regions, and enlargement of the precuneus is associated with increase in its cortical surface area [Bruner et al., 2015b]. Parietal lobes generally present larger size, more connections, and larger surface area in males than females, a difference associated with distinct visuospatial performance [Koscik et al., 2009]. Nonetheless, the overall precuneus morphology apparently does not depend on brain size, sex, hemisphere, or geographic ancestry [Bruner et al., 2017b]. The individual differences in sulcal variability may also be noticeable in these areas because of a variety of precuneal and subparietal sulci, and precuneus expansion is partially associated with additional folding elements [Bruner et al., 2017b]. Precuneus differences almost entirely occur along its longitudinal and vertical size and extensions, influencing the dorsal midsagittal morphology of the brain but not particularly the lateral (parasagittal) brain dimensions [Pereira-Pedro and Bruner, 2016]. Actually, precuneus lateral development (mainly due to the lateral extension of the subparietal sulcus) is less variable and does not apparently influence the external brain form.

Fig. 3.

The vertical extension of the precuneus (a) is responsible for the main coronal variation among adult humans, strictly influencing the height of the dorsal parietal cortex (b). The width of the precuneus (c) is, in contrast, less variable. The length of the dorsal part of the precuneus is also responsible for the main midsagittal brain shape differences among adult humans, because of variations in its cortical surface area (d). A similar shape change also represents the main difference between humans and chimps (e, f). Data after Bruner et al. [2014b], Pereira-Pedro and Bruner [2016], Bruner et al. [2017b]. Morphometrics was computed with PAST 2.17c [Hammer et al., 2001].

Fig. 3.

The vertical extension of the precuneus (a) is responsible for the main coronal variation among adult humans, strictly influencing the height of the dorsal parietal cortex (b). The width of the precuneus (c) is, in contrast, less variable. The length of the dorsal part of the precuneus is also responsible for the main midsagittal brain shape differences among adult humans, because of variations in its cortical surface area (d). A similar shape change also represents the main difference between humans and chimps (e, f). Data after Bruner et al. [2014b], Pereira-Pedro and Bruner [2016], Bruner et al. [2017b]. Morphometrics was computed with PAST 2.17c [Hammer et al., 2001].

Close modal

Interestingly, if we compare the midsagittal brain morphology in humans and chimpanzees, we also find that their main difference concerns the extension of the precuneus, which is much larger in our species [Bruner et al., 2017c]. This difference seems, again, to be localized in the dorsal and anterior part of the precuneus, a region that matches the area 7a according to Scheperjians et al. [2008]. This area includes the anterior portion of the medial surface of the precuneus but also the external dorsal surface of the superior parietal lobules.

In terms of spatial correspondence, the morphological changes associated with the precuneus at intra- and interspecific levels match the parietal bulging described in the endocranial evolution of modern humans [Bruner et al., 2014a].

It can be argued that modern human parietal expansion may be due to some intrinsic allometric trend of the brain and proportional scaling due to encephalization. However, the available evidence largely rejects this possibility. In fact, concerning the fossil record, Neanderthals had a brain size comparable with ours but no parietal longitudinal expansion [Bruner et al., 2003; Bruner, 2004; Gunz et al., 2010]. Concerning nonhuman primates, the precuneus is particularly variable within other species too, but there are no consistent differences in size and proportions between different species, including between species with very distinct brain size [Pereira-Pedro et al., 2017b]. Therefore, according to the converging evidence we have on extinct and extant species, we can conclude that the derived parietal proportions in H. sapiens are not due to general allometric effects associated with a large brain. It is worth noting that, when using apes as an allometric reference, humans display an expected parieto-occipital volume for their brain size [Semendeferi and Damasio, 2000] but smaller occipital volume [De Sousa et al., 2010] which, implicitly, should mean a larger parietal cortex.

In general, as expected after a visual inspection, humans and nonhuman primates display further differences in their whole parietal organization. The pattern of connections is distinct, notably at the inferior regions [Catani et al., 2017]. Although fossils have provided scanty evidence of gross morphological differences associated with the inferior parietal lobules, these areas are known to be specialized in humans as well [Bzdok et al., 2016]. The intraparietal sulcus is also far more complex in humans than in other primates, in terms of size and organization [Grefkes and Fink, 2005; Choi et al., 2006], and its evolutionary changes in our species are possibly related to tool use [Kastner et al., 2017]. The homology between humans and nonhuman primates for their parietal cortex is not clear, although the complexity of the intraparietal sulcus in H. sapiens may have displaced and repositioned internal and external folding regions, generating a lack of correspondence between human and nonhuman cortical topology [Zlatkina and Petrides, 2014]. It must be taken into account that most inferences are based on comparisons between humans and macaques, two lineages that are not closely related in terms of phylogeny, and that underwent separation and independent evolution for some 20 million years. Therefore, most results deal with only one genus of primates (Macaca) and in particular with one that is not related to human evolution. Many areas seem evolutionarily conserved in humans and macaques [Orban, 2016], but for those elements that are evolutionarily derived – in humans as well as in macaques – we still miss a comprehensive comparative scenario. Both modern humans and Neanderthals display a lateral bulging and widening of the dorsal parietal surface [Bruner et al., 2003], which could be tentatively interpreted as a cortical increase and outfold of the intraparietal cortex [Pereira-Pedro and Bruner, 2016].

Comparative data on the superior parietal lobule are still lacking. According to the parcellation proposed by Scheperjans et al. [2008], what we call superior lobule in humans is largely the outer extension of the anterior and posterior areas of the precuneus. This dorsal external surface has not been sufficiently investigated yet. At least three areas have been identified in the human dorsal region, but comparative data for nonhuman primates are lacking. These outer cortical folds are apparently involved in our derived parietal morphology, and future surveys should be specifically dedicated to investigate this issue.

The precuneus is involved in a functional integration of body and vision, bridging somatosensory and occipital signals [Cavanna and Trimble, 2006; Margulies et al., 2009; Zhang and Li, 2012; Freton et al., 2014]. Its anterior area deals mostly with body cognition, the posterior area with visual cognition, and the intermediate area integrates both signals. This process, generally named visuospatial integration, not only deals with body-environment physical coordination, but also with visual imaging [Land, 2014] and conscious self-centered memory recall [Fletcher et al., 1995]. Visual imagery is the basis for simulation and mental experiments. The body, in this sense, is used as a measure of physical space, but also in terms of chronological and social relationships (i.e., generating a chronological space and a social space according to an egocentric perspective) [Hills et al., 2015; Maister et al., 2015; Peer et al., 2015]. The intraparietal sulcus is also specialized in visuospatial capacities, particularly in eye-hand coordination [Grefkes and Fink, 2005; Tunik et al., 2007; Martin et al., 2011; Verhagen et al., 2012]. These visuospatial functions are relevant for all primates, but they are far more crucial for our species, which is characterized by complex tools and technology, visual symbols, and extensive social structure. Interestingly, potential early modern humans, dated at around 100–200,000 years ago, did not display larger parietal bones and lobes, suggesting that modern human phylogenetic origins may have preceded the evolution of a modern human brain form [Bruner and Pearson, 2013; Bruner et al., 2018a]. An inclusive survey suggested that, since the phylogenetic origin of our species, these changes may have followed a gradual pattern [Neubauer et al., 2018]. Paleoanthropologists find fossils with bulging parietal bones and lobes roughly since the same dates (≈50–100,000 years ago) archaeologists find distinctive modern cultural traits, like complex technology, larger social groups, and visual culture (paintings and ornamentation, for example). The exact timing and dynamics of these changes are not known, but, on an evolutionary and geological time scale, the two changes are almost matching. We should consider whether or not this is due to chance.

The case of Neanderthals merits attention, because paleoneurology, skeletal biology, ecology, and archaeology are supplying converging evidence on some aspects of their visuospatial behavior [see Bruner and Lozano, 2014, 2015 for a detailed discussion]. As we mentioned, although they had a similar or even larger brain volume than modern humans, they did not have large parietal lobes. At the same time, there is no evidence of a robust and complex visual culture, their social groups and territories were smaller, and there is not even any evidence of projectile technology (fine spears, spear throwers, or arrows). Also, according to the traces found on their front teeth, they largely relied on the mouth to handle their tools, more than any modern human population. This distinctive (and hazardous) degree of use of the mouth as a “third hand” may suggest that hand management may have been less efficient in dealing with their material culture [Bruner et al., 2016]. Hypotheses in cognitive archaeology cannot be tested to the same extent we can do in neontological fields, but all this evidence together points, independently, to possible limits in visuospatial resources and body cognition. This is not necessarily a verdict for extinction, and it may even suggest that their large brains may have had some distinct specializations that we did not evolve [Pearce et al., 2013]. Nonetheless, the comparison with Neanderthals further supports the hypothesis of derived – and probably enhanced – visuospatial cognition in modern humans, associated with body- environment management and body-tool functional specialization.

In the last 2 million years, our culture was not simply “object assisted” but instead “object dependent” [Plummer, 2004]. Our technology is actually part of our cognitive processes, and there are several theories in current neuroscience interpreting cognition as the result of integration between brain, body, and tools [Malafouris, 2010; Iriki and Taoka, 2012; Byrge et al., 2014]. In this sense, our parietal cortex and visuospatial functions can play a major role in the management of such interactions between the nervous system, the body interface, and technological resources [Bruner and Iriki, 2016]. Interestingly, a comprehensive analysis on neural circuits in primates evidenced major human changes in the genetic expression associated with the striatum, an element of the basal ganglia deeply involved in body management [Sousa et al., 2017].

Of course, the nature behind this association between form and function remains unclear. The parietal cortex is sensitive to genetic programming [Chen et al., 2012] but also to environmental influences, and its components are highly susceptible to training [Quallo et al., 2009]. At present, we ignore to what extent parietal differences between and within species are due to genes, culture, or to different kinds of feedback between both factors. Culture can influence phenotypic expression, but also genetic selection, through direct effects (autocatalysis) or indirect channeling of phenotypic plasticity [the so-called Baldwin effect; see for example Crispo, 2007]. Thus, although parietal differences begin now to be acknowledged in evolutionary neuroanatomy, their causes, factors and mechanisms still remain, at present, largely unexplained.

The parietal cortex has been largely neglected in evolutionary neuroanatomy (a case of “parietal neglect”!). The precuneus is a large cortical element but, despite an early and abandoned term quadrate lobule due to its square shape, it does not even have its own name, being defined in relation to something else (precuneus means anterior to the cuneus). Its broad designation includes some inferior areas which intermingle with the posterior cingulate and retrosplenial cortex. All this block, that bridges the parietal lobe with the cingulate cortex, is highly interconnected, but formed by distinct parts with distinct functions, and should be referred to as to posterior medial cortex [Bzdok et al., 2015]. The inferior areas are part of the default mode network and are crucial to functions that are integrated but distinct from those of the dorsal areas [Fransson and Marrelec, 2008; Margulies et al., 2009; Utevsky et al., 2014; Yang et al., 2014; Barks et al., 2015]. Therefore, probably the term precuneus should be strictly limited to the dorsal areas above the subparietal sulcus. I wonder whether the term quadrate lobule should also be rescued and used to indicate this region. It also remains to be established whether (or to what extent) the superior parietal lobule is part of the same element. Of course, the features described in this article should be integrated within a more comprehensive scenario. For example, we currently recognize the crucial importance of the frontoparietal system, these two regions being deeply interconnected by functional and connective networks [Jung and Haier, 2007; Caminiti et al., 2015].

The noticeable degree of morphological variation of the parietal lobes, and in particular of the precuneus, has been evidenced in distinct samples and through distinct methods. It is clear that there are differences between humans and other primates, and probably the same region displays a pronounced enlargement in H. sapiens compared with fossil human species. There are multiple and independent sources of evidence suggesting that the deep folds of the parietal cortex have undergone some specialization in modern humans. A mandatory future step is, therefore, to study the histological changes associated with these macroanatomical differences.

Geometrical models point to the dorsal and anterior areas as a main source of variation. Nonetheless, also the posterior (parieto-occipital) region may show human specialization for body-tool coordination and allocentric imaging [Hutchison et al., 2015; Sulpizio et al., 2016]. Enhanced morphological models can help to localize more specific areas involved in these volumetric variations in human fossils as well as in living primates.

The dorsal parietal cortex is largely involved in visuospatial integration, and future surveys should investigate possible functional or cognitive factors associated with its morphological diversity. Although differences in the parietal cortex are associated with visuospatial performance [Koscik et al., 2009], at present, there is no evidence correlating the overall precuneus morphology with traditional psychometric scores [Bruner et al., 2015b]. In this sense, and taking into account the cortical diversity of the precuneus, future neurofunctional analyses should consider more specific cortical areas and probably more targeted behavioral tasks.

Together with this “to-do” list, there is also a “not-to-do” list, which particularly refers to things that should be avoided when handling the fossil record. First, hypotheses should be tested through samples and not through specimens. Many paleoneurological traits display large intragroup variation and scarce intergroup differences. Therefore, individual fossils can hardly supply consistent support to promote or demote complex evolutionary scenarios. Second, quantitative analyses are necessary to provide a proper comparative framework. Descriptive studies should be restricted to preliminary and introductory surveys only. Third, speculations should be used with discretion and common sense, and quickly substituted by specific hypotheses that can be (at least partially) tested. Such hypotheses should be proposed and corroborated through multiple and independent lines of evidence, and not following specific or punctual results. Fourth, endocasts are valuable sources of information, but their general shape is the result of distinct factors (cranial and cerebral) and distinct elements (cortical areas). Therefore, overall shape analyses should be limited to preliminary geometrical surveys. More detailed morphometrics, based on anatomical boundaries, should be used to test specific hypotheses in evolutionary neuroanatomy [Bruner and Ogihara, 2018]. Fifth, more information is needed about modern human variation. Many paleoneurological traits are not even known, in terms of variability and function, in our species. Therefore, proper knowledge of large living samples is mandatory before we make inferences on a few fragmented bony remains.

Taking into account the many disputes and disagreements on subtle anatomical or statistical issues in paleoanthropology and evolutionary neuroanatomy, it is cu-rious how the large parietal differences have passed unnoticed, and they are not even mentioned in many scientific reviews. Nonetheless, at this time, neglecting such evidence seems to be unreasonable. Once the difference has been noticed, it should be investigated properly. And, if visuospatial functions have a major role in extending our “prosthetic” capacity in terms of space, time, technology, body cognition, and social perception, we should once more consider that brain evolution is basically a matter of anatomy, while cognitive evolution must deal with additional components (body and culture) that go beyond the neuronal content of a braincase.

I would like to thank Ashley Morhardt and Georg Striedter for giving me the opportunity to participate in the 29th Karger Workshop “From Fossils to Function: Integrative and Taxonomically Inclusive Approaches to Vertebrate Evolutionary Neuroscience.” Many and diverse studies on parietal evolution have been possible thanks to the collaboration with many people, including Giorgio Manzi, Ralph Holloway, Jim Rilling, Todd Preuss, Naomichi Ogihara, Manuel Martín-Loeches, Roberto Colom, Heidi Jacobs, Marina Lozano, Philipp Gunz, Simon Neubauer, Atsushi Iriki, Duilio Garofoli, Amélie Beaudet, Barbara Saracino, Fred Coolidge, Roberto Macchiarelli, and Xiujie Wu. I am particularly grateful to all the students who have supported and developed my laboratory over the years, namely Sofia Pereira-Pedro, Gizéh Rangel de Lázaro, José Manuel de la Cuétara, Annapaola Fedato, Alannah Pearson, María Silva Gago, Hideki Amano, and Stana Eisová. These research lines were primarily funded by the Proyecto Atapuerca (Spanish Government), coordinated by José María Bermudez de Castro, as well as by the Italian Institute of Anthropology and the Wenner-Gren Foundation.

The author declares no conflict of interest.

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