Journal of Archaeological Method and Theory (2021) 28:76–94

https://doi.org/10.1007/s10816-020-09500-8

Evolving Human Brains: Paleoneurology and the Fate

of Middle Pleistocene

Emiliano Bruner 1

Accepted: 15 December 2020 / Published online: 3 January 2021

# Springer Science+Business Media, LLC, part of Springer Nature 2021

Abstract
In the evolutionary radiation of the human genus, we have observed changes in both
brain size and proportions. Some of these morphological differences are thought to be
associated with functional variations, in physiological or cognitive aspects, while some
others are the secondary results of cortical or cranial structural constraints. Most archaic
human species, like Homo erectus and H. heidelbergensis, display larger brains when
compared with earlier hominids, but specializations in their cortical proportions, if there
are any, are difficult to recognize. In contrast, after or during Middle Pleistocene, more
derived species like H. sapiens and H. neanderthalensis show changes in overall brain
size but also in specific cerebral regions. Functions associated with body cognition,
visuospatial integration, tool use, language, and social structure may be involved in
these paleoneurological changes. Nonetheless, a proper evaluation of cognitive differ-
ences must take into account not only the cerebral components, but also the associated
mechanisms underlying technological extension. Brain-body prosthetic capacity can
have represented, indeed, a crucial adaptation to become obligatory tool users. These
processes involve both genetic and environmental effects, and they are probably
influent at phylogenetic (species) and historical (populations) level, bridging biological
and cultural factors through epigenetic feedbacks that are still poorly known and
scarcely investigated.

Keywords Human evolution . Endocasts . Parietal lobe . Prosthetic capacity . Body

cognition

* Emiliano Bruner
emiliano.bruner@cenieh.es

1
Centro Nacional de Investigación sobre la Evolución Humana, Paseo Sierra de Atapuerca 3,
09002 Burgos, Spain
Evolving Human Brains: Paleoneurology and the Fate of Middle... 77

“I was able to demonstrate (1936) that a preferential enlargement of the frontal

lobe in the course of human evolution, considered a certainty by the majority, in
reality is a legend. The brain expands mainly in its entirety and in all directions.
In addition, the most favored region is not the frontal lobe but the parietal lobe,
whilst the most privileged direction of expansion is not in breadth as Martin's
explanation implies but in height.” (Franz Weidenreich, 1941. The brain and its
role in the phylogenetic transformation of the human skull. Transactions of the
American Philosophical Society XXXI/V, p .331).

Human Paleoneurology

Paleoneurobiology deals with the study of brain anatomy and evolution in fossil species
(Holloway et al. 2004; Bruner 2017). The brain shapes the braincase during ontogeny,
leaving some information on the bones regarding its gross morphology, such as its
general size, proportions, sulcal patterns, or the traces of the meningeal vascular
channels. The endocast is a mould of the endocranial cavity, a positive cast of that
empty space, a cast that we generate to have a perceptual feedback of its forms and
features (Neubauer 2014; Holloway 2018). An endocast has exactly the same mor-
phology of its endocranial cavity, but we need such three-dimensional objects (real or
virtual) to acknowledge our visual—and even tactual—sensorial necessities. Of course,
an endocast is not a brain, but just a simulacrum of its gross external morphology. It
should neither be intended as “an object”, but rather as the final result of a process of
growth and development, based on multiple functional and structural relationships
between soft and hard tissues. Finally, it must not be interpreted as an autonomous
element, because it is part of a more comprehensive morphogenetic and evolutionary
system formed with the rest of the skull (Moss and Young 1960; Bastir et al. 2006;
Richtsmeier and Flaherty 2013; Bruner et al. 2015). Network analyses computed on
models of the human skull suggest that there are at least two main structural blocks,
namely the facial and neurocranial ones (Esteve-Altava et al. 2013; Esteve-Altava
2017). The ethmoid bone is a local facial hub, while the sphenoid connects the two
blocks, and the frontal and malar bones act as a structural hinge bridging the two
modules. Also, the brain, beyond its functional relationships, has a cortical topology
influenced by the spatial arrangement of its own parts (Hilgetag and Barbas 2006;
Tallinen et al. 2016; Bruner et al. 2018a). In this sense, it is worth noting that
gyrification, which is often used as a proxy for cortical complexity, increases back-
wards in the primate brain (Zilles et al. 1988, 1989). Also, taking into account the
spatial arrangement of the main sulcal elements, the posterior regions are more
integrated and complex than the anterior ones, the temporal lobes display an important
architectural burden, and the central lobe (between precentral and postcentral sulcus)
acts as a structural bridge between the anterior and posterior districts (Bruner et al.
2019). In the case of the brain-braincase balance and topology, a major role can be
described for the anterior fossa (influencing many distinct regions) and the parietal
bone (influenced by many distinct factors). Even a simplified network model taking
into account the spatial contact between the main gross cranial and cerebral region
(Fig. 1) is able to recognize an anterior block (face, frontal lobes, middle fossa, and
78 Bruner

cranial base) and a posterior block (the rest of the brain-skull system). According to this
simplified model, the anterior cranial fossa and the temporal lobes are the elements that
are more sensitive to global morphological changes. With this frame, it is hence
necessary to keep in mind that we cannot interpret any change in brain form as a
neural adaptation. Some brain changes are due to changes in the neural organization,
but others are due cortical or cranial topological and developmental constraints,
associated with no functional (cognitive) effects. For example, the above example
suggests that the morphology of the frontal lobes is sensitive to facial constraints and
that the temporal lobes are sensitive to both cranial and cerebral secondary adjustments.
All this information, in terms of direct evidence, is silent on the endocasts, and it
must be carefully investigated by integrating paleoneurology with comparative

Fig. 1 A simplified network model based on the spatial contact among main skull (grey/white) and brain (red)
elements (a, b). Temporal lobe and anterior fossa have the largest betweenness values (c: size and colour
intensity of the nodes), which means that they are positioned in between all the other elements. According to
the degree of connection (d: size of the nodes), two blocks can be identified (d: colours), an anterior one
(orange) including the face, the anterior cranial base, and the frontal lobes, and a posterior one (blue) including
the other elements. See Bruner et al. 2019 for further information. Networks and parameters were computed
with Gephi 0.9.2 (Bastian et al. 2009). The model includes the frontal lobe (FL), the central lobe (CL), the
parietal lobe (PL), the occipital lobe (OL) the temporal lobe (TL), the cerebellum (CE), the frontal squama
(FS), the parietal bone (PB), the occipital squama (OS), the temporal squama (TS), the anterior fossa (AF), the
middle fossa (MF), the posterior fossa (PF), the cranial base/clivus (CB), the orbital region (OR) the
ethmomaxillary complex (EM), and the mandible (MN)
Evolving Human Brains: Paleoneurology and the Fate of Middle... 79

morphometrics and evolutionary neuroanatomy (Bruner 2019). In fact, much informa-

tion is lost from a brain to an endocast, and this limitation must be taken into account.
Of course, this does not mean that we must reject the information they are able to
provide. Endocasts supply the only direct evidence on brain anatomy in extinct species
and, accordingly, they merit our attention.
A second limitation of paleontological fields in general regards the size and com-
position of the samples. Fossils provide anatomical information only on bones, and an
organism is definitely more than that. Furthermore, the fossil record is generally poor:
few bones, few individuals, few species. Individuals might not properly represent their
own species, and few specimens may not be enough to investigate variation (which is a
key factor in evolution). Moreover, few species might not properly represent the
phylogenetic diversity of their zoological group. All this results in limited statistical
resources. In paleoanthropology, statistical power is, at best, scarce. That is why many
scholars decide to rely on personal opinions and speculations to give the field a
narrative perspective, while many others decide that paleoanthropology is not a real
science and does not deserve attention. Between these two extremes (that is speculation
vs rejection), I believe there can be a fruitful optimization of the resources and methods.
Studies on fossils should rely, in this sense, on quantitative tools and multiple inde-
pendent evidence to evaluate at least some general hypotheses according to the
available evidence. This means being aware of the limitations, but also recognizing
the potentialities. Such a fine balance is not easy to acknowledge, but nobody ever said
that investigating human evolution was going to be an easy job.
This perspective review is aimed at presenting the current anatomical evidence for
brain evolution during and after Middle Pleistocene, mostly according to my own
works of the last 20 years. In particular, the changes described in the parietal cortex will
be discussed in terms of their possible association with visuospatial capacities, and with
those cognitive functions related to brain-body and body-tool integration. I will present
an integrated view bridging the evolution of the parietal lobes (and, in particular, of
their dorsal regions) with embodiment and technological extension.

Middle Pleistocene and Human Brain Evolution

Middle Pleistocene was a long and heterogeneous evolutionary moment for humans,
bracketing almost 700 ka and three continents. Certainly, we cannot be sure that the
scarce fossil record we have can really show what happened in such a huge chrono-
logical and geographical landscape (Fig. 2). In terms of brain size, we suppose there
were at least two independent human lineages, Homo erectus and H. heidelbergensis,
with the latter having a larger cranial capacity than the former, after a process of
encephalization and an increase of relative brain dimensions (Rightmire 2008). How-
ever, many scholars suspect that the taxonomic framework was far more complex, at
least separating H. heidelbergensis in one African and one European group. In this
latter case, the variability is furthermore quite difficult to interpret according to
traditional and homogeneous morphological parameters, and further taxonomic splits
are to be expected or speculated. However, if two human species are at least probable,
the existence of more taxa is possible but still not sufficiently clear in terms of
quantitative evidence, when considering the limitations of the species concept in
80 Bruner

palaeontology (Bruner 2013). H. heidelbergensis and H. erectus display several distinct

cranial features (Rightmire 2008; Stringer 2012), but their brain/endocast morphology
differs only in terms of average size, with no apparent or significant differences in brain
proportions or sulcal schemes (Bruner et al. 2015). Noticeable differences in their
overall brain morphology are not apparent, and any peculiar feature detected on the
specimens could be the result of idiosyncratic individual variation. Of course, this does
not mean that they had necessarily the same brains, but only that, with gross
endocranial morphology and small samples, it is not possible to recognize any consis-
tent dissimilarity. Like earlier humans, their endocasts display narrow frontal lobes, and
flat and short parietal lobes, mostly at the dorsal regions (Fig. 3). The occipital lobes
projected backward, the cerebellum was in a posterior position (largely below the
occipital cortex), and the vascular networks were rather simple, with almost no
anastomosis and with developed posterior branches (Grimaud-Hervé 1997). If these
two species did display some anatomical differences apart from brain size, it is
probably hard to tell. Namely, if they had evolved different brain proportions, such
differences must have been subtle. Interestingly, at least in terms of raw endocranial
metrics and proportions, the current fossil record suggests that the degree of variability
within H. erectus might have been comparable with the degree of variability among
modern humans (Bruner 2018a).
Whatever the taxonomy behind this scenario, it is clear that in the second half of the
Middle Pleistocene further evolutionary processes were taking place, and the group
assigned to H. heidelbergensis was probably undergoing a further selective shift towards
encephalization. The European and African populations were probably moving towards
two evolutionary alternatives, the two human species with larger brain size and a higher

Fig. 2 Main human species with a sufficient paleoneurological record (Ma: millions of years; ka: thousands of
years). Top left: digital reconstruction of skull and endocast of Homo ergaster KNM-ER3733
Evolving Human Brains: Paleoneurology and the Fate of Middle... 81

Fig. 3 Digital reconstruction of the endocast of Zhoukoudian XII, showing some major endocranial features
of Homo erectus. After Bruner et al. 2015

encephalization index, namely Neandertals (H. neanderthalensis) and modern humans

(H. sapiens), respectively in the two continents (Hublin 2009; Hublin et al. 2015).
At the evolutionary interface between more archaic smaller-brained morphotypes
(H. erectus and H. heidelbergensis) and more derived larger-brained morphotypes
(H. sapiens and H. neanderthalensis) we found specimens which are definitely hard
to interpret according to traditional linear models. Such difficulties are due to the
extreme paucity of fossils, and to the fact that they present a mosaic of features that
is not compatible with a gradual and progressive pattern of evolution.
In Europe, the sample from Sima de los Huesos, formerly ascribed to
H. heidelbergensis and dated between 300 and 430 ka, suggested an admixture of
primitive traits and derived Neandertal features, these latter mostly in the facial morphol-
ogy (Arsuaga et al. 1997, Arsuaga et al. 2014). Nonetheless, although the enlargement of
the parietal and temporal diameters may suggest early Neandertal characters (Poza-Rey
et al. 2019), their general endocranial appearance is plesiomorphic, with a narrow frontal
region and flat parietal surface (Bruner et al. 2003). A very similar situation can be found
in the Chinese skull from Maba, dated to around 300–130 ka, which presents Neandertal
traits in the upper face but more archaic features in the braincase (Fig. 4—Wu and Bruner
2016). The remarkable similarities between Sima de los Huesos in Spain and Maba in
China will probably deserve further attention. In contrast, in North Africa, the skull of
Jebel Irhoud, dated to 300 ka, displays a derived modern human facial morphology but a
Neandertal-like endocast (Fig. 5—Holloway 1981; Bruner and Pearson 2013; Hublin
et al. 2017). The reduced facial block increases the bulging of the frontal squama, but the
parietal morphology is generally comparable with the Neandertal morphotype. Such
evolutionary separation and independence of the face and braincase is not particularly
surprising, when taking into consideration the structural division in one anterior and one
posterior morphological block as described before, according to the anatomical analysis of
the topological networks of the human skull.
Therefore, at least considering these specimens, at the end of the Middle Pleistocene,
in Europe and Asia, we have some fossils with a Neandertal face and archaic braincase,
and in Africa, we have some fossils with a modern face and a Neandertal braincase, a
situation that is decidedly difficult to frame within a linear evolutionary scenario.
82 Bruner

Fig. 4 The skull of Maba (a) and the digital reconstruction of its endocast in superior (b) and posterior (c)
views, showing frontal narrowing and depression of the dorsal parietal region. The superposition (d) shows the
facial similarity between Maba (red) and Saccopastore 1 (white). After Wu and Bruner 2016

Big Brains: Modern Humans and Neandertals

Around 200–300 ka, we have the first evidence of a “Neandertal brain”. The skull of
Saccopastore 1, found in Rome (Italy) and dated between 120 and 250 ka, displays a
Neandertal endocast (Bruner and Manzi 2008). Also, the natural endocast from Gánovce,
found in Slovakia and dated to 105 ka, has a clear Neandertal appearance (Eisová et al.

Fig. 5 Cranial and endocranial moulds of Jebel Irhoud 1 (a). Comparing the midsagittal cranial profile (b), the
Jebel Irhoud (bold line) parietal shape is very similar to the Sima de los Huesos cranium 5 (thin line), although
this latter displays flatter frontal squama and a longer face. Analysing the endocranial form in three
dimensions, Jebel Irhoud (bold line) is more similar to the Neandertal average (c) than to the modern human
average (d), mostly because of the parietal morphology. After Bruner and Pearson 2013
Evolving Human Brains: Paleoneurology and the Fate of Middle... 83

2019). When compared with their ancestors, Neandertals had a larger brain size and higher
encephalization index. Nonetheless, they also had some different brain proportions, in
particular wider frontal lobes and wider parietal lobes (Bruner et al. 2003; Bruner 2004,
2014). Later “classic” Neandertals, around 50–70 ka, evolved an even larger brain size but
maintained a similar gross endocranial morphology (Fig. 6). As we have already men-
tioned, the modern human lineage could have evolved in the same period, in Africa, and
with a similar overall brain morphology (Bruner and Pearson 2013). If this is the case, it
remains to be investigated whether such common brain morphology between Neandertals
and early modern humans was associated with a common shared ancestor, or else if it is
the result of some parallel evolutionary change. Interestingly, Neandertals and early
modern humans did also share a very similar technology. Later H. sapiens, say around
100 ka, display instead a more globular brain form, a feature further stressed in late and
modern humans (Bruner et al. 2018b; Neubauer et al. 2018). The appearance of this
marked globular brain form roughly coincides with the period in which we begin finding a
full set of modern behaviours, including projectile technology, complex tools, and a
consistent graphic culture.
The first feature shared by Neandertals and modern humans is wide frontal lobes
(Bruner and Holloway 2010). Although it is tempting to associate this change to
functional aspects of the frontal lobes (like Broca’s area and language), it must be said
that this morphology could also be the result of cranial constraints (Fig. 7). Frontal
lobes in humans are not particularly large when compared with the ape proportions
(Semendeferi et al. 1997, 2002). Although humans probably have a more expanded and
connected prefrontal cortex (Smaers 2013), in terms of gross macroscopic appearance
the overall frontal proportions are then similar to the figure we can find in chimpanzees
or gorillas. If gross morphological frontal changes have not been found among
hominoids, it is unlikely that they can have evolved (and that, even so, can be revealed)

Fig. 6 The digital skull and endocast of Saccopastore 1 with the main features of the Neandertal brain form
(left), and the digital reconstruction of the natural endocasts from Gánovce (right). Both specimens suggest
that the Neandertal brain form dates at least to 100–200 ka. Images after Bruner 2014 and Eisová et al. 2019
84 Bruner

among human species. So, at present, we must assume that all hominoids (including
humans) share a similar gross proportion of frontal lobe, when differences in overall
brain size are acknowledged. However, modern humans and Neandertals are the only
human species in which the frontal lobes are positioned onto the orbital roof, generating
a spatial conflict between the brain and upper face (Beaudet and Bruner 2017; Pereira-
Pedro et al. 2017). Taking into consideration these two issues (i.e., similar gross
volumetric proportions but different shape and position), wider frontal lobes in modern
humans and Neandertals are likely to be a matter of lateral redistribution of the frontal
cortical mass, and not a primary change due to localized cortical expansion. Cortical
and functional changes cannot be excluded but, at present, cranial constraints cannot be
ruled out, and are likely to explain the frontal lobe morphology in these two taxa.
In addition, when compared with more archaic hominids, both Neandertals and
modern humans display an enlargement of the parietal cortex, albeit to a different
pattern and degree (Bruner 2018b). Neandertals display a lateral bulging of the dorsal
parietal region, which spatially matches the position of the superior parietal lobule or of
the intraparietal sulcus. Modern humans also show a similar widening of the parietal
lobe, but additionally, we also have a much longer parietal outline, spatially corre-
sponding with superior parietal lobules and precuneus (Bruner et al. 2014). In partic-
ular, when compared with Neandertals, modern humans display a geometric expansion
of the regions associated with the Jensen sulcus (on the inferior parietal lobule, between
the supramarginal and angular gyri) and with the parietal-occipital boundary (on the
superior parietal lobule)(Pereira-Pedro et al. 2020). In Neanderthals, in contrast, the
degree of parietal longitudinal extension is comparable with an archaic human pattern,
and interestingly, on their outer cranial surface, supernumerary ossicles reveal some
morphogenetic imbalance between brain and skull growth and development, suggest-
ing possible midsagittal constraints between a plesiomorph skull architecture and a big
brain (Manzi et al. 1996; Bruner 2014).
Modern humans have also been hypothesized to have longer temporal lobes,
expanded orbital cortex, and larger cerebella when compared with Neandertals
(Bastir et al. 2011; Gunz et al. 2019). Nonetheless, as mentioned earlier, these regions
have relevant structural constraints with the skull and cranial base, and inferences on
their gross morphological changes do require more caution. In contrast, a noticeable

Fig. 7 Archaic hominids display flat frontal squama and orbits that are partially anterior to the frontal lobes,
while in modern humans (and Neandertals) the frontal lobes lie onto the orbital roof. Therefore, frontal bulging
is probably a structural result of the brain-face spatial relationships. After Pereira-Pedro et al. 2017 and
Beaudet and Bruner 2017
Evolving Human Brains: Paleoneurology and the Fate of Middle... 85

correlation between orbit size and the size of the occipital lobe suggests that Neander-
tals might have had a larger occipital cortex, when compared with modern humans
(Pearce et al. 2013). The proportion of the parieto-occipital cortical block is rather
stable in apes and humans (Semendeferi and Damasio 2000) and therefore a relatively
larger occipital cortex is to be expected in association with a relatively smaller parietal
cortex. In this sense, the larger proportion of occipital cortex in Neandertals, if
confirmed, should be probably intended as a primitive human condition, and not as a
derived Neandertal-only feature.
A final note concerns hybridization between these two taxa. In primates, hybridiza-
tion does occur frequently between phylogenetically close species, and even between
genera (Holliday 2003; Jolly 2009). It is hence to be expected that Neandertals and
modern humans could, at least in principle, hybridize (as they apparently did;
Ackermann et al. 2019; Taylor and Larson 2019). However, phylogeny and taxonomy
are not about potentialities, but rather they concern the actual output of evolution
(Bruner 2013). Neandertal and modern human fossils are generally easy to distinguish,
because of a large set of cranial and post-cranial features (Tattersall 2007), and this
suggests they are the result of distinct and parallel processes of selection and adaptation.
In fact, taking into account the hypotheses on Neandertal genes introgression in modern
human populations, such admixture could have been so limited to suggest a strong and
effective demographic, behavioural or biological barrier (Currat and Excoffier 2011;
Overmann and Coolidge 2013). Taking also in consideration that such introgression
does not concern the whole species but only some geographical groups, it must be
intended as an issue dealing with population genetics more than with phylogeny.
Recently, Neandertal genes have been hypothesized to be correlated with the degree
of globularity (or, better, with the degree of non-globularity) of modern human brains,
although we still miss an interpretation on the possible functional or cognitive conse-
quence of such genetic influence (Gunz et al. 2019).

A Prosthetic Cognition

Parietal lobes are formed by association areas that are crucial to many distinct integrative
functions. They have many internal folds, blurred anatomical boundaries, and a noticeable
morphological diversity among primates. All these factors make them more difficult to
study in comparative and experimental neurobiology, when compared with other cortical
regions and, accordingly, their possible role in cognition and evolution were rather
neglected in the past century. The inferior lobules are involved in language comprehension
and calculations and, probably for this reason, they received more attention, and were soon
hypothesized to be derived in modern humans, when compared with other primates
(Bzdok et al. 2015, 2016; Kastner et al. 2017). The intraparietal sulcus is involved in
eye-hand coordination, is definitely larger and more complex in humans, and it is directly
involved in tool use (Grefkes and Fink 2005). Its internal extension is remarkable and,
apart from its main course, it may develop into many side branches. The supramarginal
gyrus and the angular gyrus, for example, are often separated by the sulcus of Jensen,
which is part of the intraparietal system (Zlatkina and Petrides 2014). Gross morphological
changes in this region can be, in some cases, the results of variations of the deep cortical
elements, possibly outfolding on the external brain surface.
86 Bruner

The anatomical organization and functions of the superior parietal lobules were
probably the most neglected issues. According to the cytoarchitectronic organization,
the superior lobule is likely to be the outer extension of the medial inter-hemispheric
cortex (Scheperjans et al. 2008), the precuneus, which is extremely variable among
adult humans and much larger in humans than in apes (Bruner et al. 2017a, b). The
precuneus is a bridge between body inputs (somatosensory cortex) and visual inputs
(occipital cortex), it integrates body and environment at physical, chronological and
social level, and it is involved in visual imaging and simulation, memory retrieval and
visuospatial integration (Fletcher et al. 1995; Cavanna and Trimble 2006; Freton et al.
2014; Land 2014). Instead of a separation between internal and external regions of the
superior and medial parietal cortex, cytoarchitecture suggests an antero-posterior sep-
aration, with the anterior area more involved in body cognition, the posterior area more
involved in visual cognition, and the middle area dedicated to the body-vision integra-
tion. The inferior regions of the precuneus fade into cortical areas which are part of the
default mode network. All these parietal regions have connections with many cortical
and subcortical areas, but are particularly connected with the prefrontal cortex (forming
a complex fronto-parietal system; Jung and Haier 2007; Caminiti et al. 2015) and with
the thalamus (cortico-thalamic pathways). Beside evolutionary differences in the size or
importance of these connections, the precuneus may also present some human-specific
tracts, bridging the parietal cortex with the cingulate region (Ardesch et al. 2019).
In general, we can state that parietal cortex is particularly involved in functions
associated with the management of the relationships between brain, body and environ-
ment (Bruner and Iriki 2016), and it supplies a global workspace for consciousness,
self-perception and autonoesis (Baars 2002; Coolidge 2014; Caminiti et al. 2015). Such
functions are directly involved in tool use and technology, so it is maybe not surprising
that they are derived in the most technological species ever to have evolved so far. But
this is even more intriguing when taking into consideration that body and tools can be
active elements of the cognitive process itself (Malafouris 2010a, 2013; Byrge et al.
2014). Theories collectively grouped under the label of “extended mind” interpret
cognition not as a product of the brain, but as a process generated by the integration
and interaction between brain, body, and technology. The brain “delegates” functions
to external components in order to enhance and evolve functions and capacities that go
beyond the organic possibility of the nervous system alone. Tools are, in this sense,
external elements that make it possible to offload and outsource information flow,
extending the process to out-of-the-body peripheral units (Kaplan 2012; Japyassú and
Laland 2017). In fact, tools are sensed as part of the body when handled, extending the
somatosentory capacity beyond the body as part of the brain’s body schemes (Maravita
and Iriki 2004; Cléry et al. 2015; Miller et al. 2019a, b). Although tools represent
crucial items in archaeology, the same perspective can be put forward for any element
of the material culture and, generally, for any cultural factor than can modify the
perception of the relationship between body and environment.
This approach is something rather new for our scientific culture based on reduc-
tionist approaches and on the undisputed centrality of the brain. Nonetheless, centrality
does not mean autonomy, and we must confess that our detailed knowledge on cell
structure and molecular dynamics have not been sufficient, at present, to explain our
cognitive capacities. Such perspectives in cognitive extension are difficult to be
accepted (because of the secular approval of “braincentric” views in Western cultures)
Evolving Human Brains: Paleoneurology and the Fate of Middle... 87

and difficult to test (because we currently lack proper methods and techniques to
analyse cognitive functions that may involve the integration of extra-body compo-
nents). Nonetheless, taking into account their strong theoretical basis, and considering
the failure of the alternative reductionist hypotheses, they surely deserve attention.
A proper agenda for theories in extended cognition would probably require three
steps. First, it must be evaluated whether or not tools are real parts of the system,
instead of a passive product of the brain. Often it is argued that a calculator, left on a
table, is not able to compute anything, but, admittedly, we must remember that a piece
of brain, left on a table, is not either. Therefore, we should try to avoid interpreting the
functional parts of the system only by a criterion of position (internal vs external) or
composition (organic vs inorganic). Second, if tools and the body are part of the
cognitive system, we should try to investigate the strength of this association and
dependence. Namely, we should consider how much this integration is responsible for
(and indispensable for) our cognitive machinery. This is, specifically, a matter of
understanding the degree of dependence between the parts involved. Third, if tools
and the body are parts of the cognitive system, we should investigate the possible
different roles of these components. Indeed, the fact that different elements may be all-
inclusive parts of the same system does not mean that they actually have the same roles
and functions. In sum, the agenda for extended cognition implies to test (i) if, (ii) to
what extent, and (iii) how body and tools are constituent parts of our cognitive system.
As anthropologists, we surely need to add a fourth point: to investigate where, when,
and how, within the evolutionary radiation of the human genus, this process did begin.
In particular, we should consider whether such a change in the brain-body-tool
relationships has occurred only in modern humans, in other human species, or gradu-
ally along distinct encephalization trajectories.
Despite the many controversies and disagreements on the origin and evolution of
tool use an tool making, it has been proposed that humans were occasional tool users
before 1.7 million years, habitual tool users between 1.7 and 0.3 million years, and
obligatory tool users in the last 300,000 years (Shea 2017). According to this hypoth-
esis, long stages of technological homogeneity were replaced by a noticeable degree
and rate of tool diversity in modern humans and Neandertals, associated with controlled
shaping and retouching, planning capacity, and learning behaviour based on social
complexity. Language could have been the factor triggering such cultural acceleration
at the end of the Middle Pleistocene. Obligatory tool use involves ecological and
cognitive specializations, and therefore, we can wonder whether differences in the
parietal cortex and prosthetic capacity can add further information on its evolutionary
onset. According to the paleoneurological evidence, Neandertals and early modern
humans can represent a first degree of body-tool specialization because of their partial
parietal development, while late modern humans could have evolved an additional
complexity of the body-tool cognition, as suggested by the further expansion of their
parietal cortex. In this case, although it can be statistically hard to detect behavioural
differences between early and late Homo sapiens (Shea 2011), the different degrees of
parietal expansion can witness actual differences in the general visuospatial capacities
(Bruner and Pearson 2013; Neubauer et al. 2018). In all cases, it is apparent that after
Middle Pleistocene “something happens”, in this sense.
Since ever, tool use has been interpreted as a crucial factor in human evolution, but
as a passive witness of increasing brain complexity and capacity. Instead, according to
88 Bruner

a perspective grounded in extended cognition, material culture and technological

extension could have a more direct and critical role, being archaeological remains of
the thinking minds, and not their mere by-product. Namely, we should interpret tools as
remnant pieces of the thinking hardware. It is here worth noting that, at least theoret-
ically, it can be proposed to distinguish objects and tools (Bruner and Gleeson 2019).
We can define a tool as an external functional element that is (i) mandatory to generate
and support a species’ ecological, cultural and cognitive capacity (Plummer 2004;
Malafouris 2010a, b; Shea 2017), (ii) that is biologically integrated into the body-
brain system (Maravita and Iriki 2004; Iriki and Taoka 2012; Miller et al. 2019a), and
(iii) that is part of a productive chain based on a propaedeutic operational sequence
(Muller et al. 2017). According to these criteria, as far as we know, only humans do
really use “tools”, while other animals simply make use of “objects”. We can wonder
whether object-using and tool-using may represent two distinct behavioural stages, or
else the extremes of a gradual capacity. Nonetheless, the cognitive and evolutionary
differences involved in the two concepts are patent. With this definition of tool and
technology in mind, we can employ the principles of cognitive extension not only to
fossil species but also to distinct modern populations, including different ethnic or
historical groups. Namely, if technology is a constituent part of cognition, distinct
technological toolkits would imply distinct cognitive machineries. This can generate
important cognitive differences between cultures or historical epochs, namely alterna-
tive and independent cognitive combinations that can be interesting to investigate
properly, as to disclose their respective behavioural features and constraints according
to a more comprehensive mental scenario.
In terms of evolution and adaptation, the integration of tools into the body scheme
and cognitive mechanisms requires a “prosthetic capacity”, namely the ability to
incorporate the object into the body somatosensorial unit and into the brain functional
relationships (Overmann 2015; Bruner and Gleeson 2019). This involves factors and
functions associated with body perception, space sensing, and haptic cognition (e.g.,
Tunik et al. 2007; Millar 2008; Turvey and Carello 2011; Ackerley and Kavounoudias
2015; Cléry et al. 2015). Therefore, we can wonder whether such prosthetic capacity
could have undergone a specific change or enhancement during human evolution,
associated with some genetic, developmental, or cultural reason (parietal lobe, neural
plasticity, visuospatial integration, etc.). Whatever genetic or physiological change able
to increase the potential to integrate body-tool and brain-tool functions will improve the
prosthetic capacity, the possibility to offload the information process, and the compe-
tence for delegating functions to external elements, trespassing the computational
limitations of the brain alone.

The Fate of the Middle Pleistocene

If the anatomical changes in the parietal cortex are due to a change in the body-tool
integration system, and if this system is involved in the offload of cognitive functions to
extra-body (exosomatic; sensu Shea 2017) components, it is clear that we will have to
rethink much of our past cognitive perspectives, which are still largely based on brain
self-sufficiency. Body cognition should be carefully reconsidered, also in cognitive
archaeology, a field in which we must rely on indirect traces of visuospatial behaviours
Evolving Human Brains: Paleoneurology and the Fate of Middle... 89

in order to make inferences on visuospatial functions (Bruner et al. 2018c). Actually, far
back towards the root of our family, we can even wonder whether the evolution of
bipedal locomotion, more than 3 million years ago, had enhanced the proprioceptive
and haptic potentialities of our earliest lineages. Bipedal posture partly or entirely
releases the locomotory constraints of the upper limb and probably involves a reorga-
nization of the gravitational and vestibular system. It has always been remarked that the
liberation of the hands from locomotion represents a hallmark for technological
evolution. However, this perspective was strictly interpreted in terms of a mechanical
system. Instead, it can be tentatively speculated that such changes can represent a
sensorial and propioceptive prerequisite to technological extension also in cognitive
terms. It is worth noting that also a parietal enlargement in australopiths has long been
hypothesized, following an enduring debate on their endocasts (e.g., Holloway et al.
2003).
There is no doubt that, after the Middle Pleistocene, at least two large-brained
human lineages underwent a noticeable specialization of their visuospatial and techno-
logical capacities. The lateral expansion of the parietal cortex and the complex culture
of Neandertals suggest a visuospatial enhancement, when compared with more archaic
human species, and these anatomical and cultural features look further improved—
dramatically—in modern humans (Bruner and Lozano 2014, 2015). Although the exact
timing of these changes is hard to verify because of the paucity of the fossil and
archaeological record, the parietal expansion of Neandertals and early modern humans
roughly coincide with the evolution of a “Mousterian” (prepared core) technology.
Similarly, the noticeable parietal bulging in later Homo sapiens roughly coincides with
the development of a behavioural modernity (including a further increase of tool
complexity, projectile tools, and a consistent graphic culture) (Bruner and Pearson
2013; Neubauer et al. 2018). In the case of Homo sapiens, the technological and
graphical skills reveal a powerful visuospatial sketchpad, which is a crucial part of
the working memory system (Coolidge and Wynn 2005).
Interestingly, the parietal cortex and body cognition are also involved in social
processes (Hills et al. 2015; Maister et al. 2015; Peer et al. 2015). In fact, body-
centred metrics and simulations are central to the management of the social environ-
ment, that is, the physical, chronological, mnemonic, and social spaces are handled
according to similar visual and body-based principles and mechanisms. Moreover, the
size of the association cortex in primates is proportional to the size of the social groups
(Dunbar 2012; Pearce et al. 2013), and hence, we must expect that the parietal
expansion in Neandertals and most of all in modern humans was likely associated with
changes in their social system. Technical and social environments are tightly associated
because of shared factors involving neural plasticity, visuospatial cognition, and
cultural transmission, and differences in these two aspects can be actually outstanding
when comparing modern humans and Neandertals (Lombard and Högberg 2021). In
both species, the increase of the social group size (as suggested by larger brains) and the
migration towards higher latitudes (which are characterized by a reduction of the
energetic resources) could have required the organization of fission-fusion societies,
based on splitting and re-aggregation of the social networks to regulate the demograph-
ic density (Grove et al. 2012). In modern humans, such social changes may have been
further integrated by a reduction of aggressive behaviours and an increase of cooper-
ative activities, through self-domestication (Bruner and Gleeson 2019; Wrangham
90 Bruner

2019). Finally, it must be also mentioned that the parietal lobes (in particular, the
precuneus) are involved in mind reading and mentalization (usually labelled with the
ambiguous and mysterious name of Theory of Mind), mostly when actions or episodic
memories are involved (Adenzato et al. 2019; Laillier et al. 2019). All these factors
cannot be disjointed from our unusual cultural and technological capacities, and their
intimate relationships with our evolutionary adaptations as toolmakers strengthen
further Herbert Spencer’s view of humans as the ultimate problem of biology and the
first problem of sociology.

Acknowledgments I would like to thank Marlize Lombard and Anders Högberg for inviting me to
contribute to this volume on Middle Stone Age and Middle Palaeolithic. I am grateful to the many friends,
students, and colleagues that have worked with me on the topics discussed in this article, including Sofia
Pereira-Pedro, Annapaola Fedato, María Silva Gago, Alannah Pearson, Stana Eisová, Amélie Beaudet, Xiujie
Wu, Naomichi Ogihara, James Rilling, Todd Preuss, Borja Esteve-Altava, Diego Rasskin-Gutman, Roberto
Colom, Manuel Martín-Loeches, and many others. Three anonymous reviewers provided very fruitful
comments to an early version of this article.

Funding My research is supported by the Spanish Government (PGC2018-093925-B-C31).

Compliance with Ethical Standards

Conflict of Interest The author declares that there is no conflict of interest.

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