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Dement Neuropsychol 2023;17:e20230078 View & Review

https://doi.org/10.1590/1980-5764-DN-2023-0078

The uniqueness of the human brain:


a review
José Eymard Homem Pittella1

ABSTRACT. The purpose of this review is to highlight the most important aspects of the anatomical and functional uniqueness
of the human brain. For this, a comparison is made between our brains and those of our closest ancestors (chimpanzees and
bonobos) and human ancestors. During human evolution, several changes occurred in the brain, such as an absolute increase in
brain size and number of cortical neurons, in addition to a greater degree of functional lateralization and anatomical asymmetry.
Also, the cortical cytoarchitecture became more diversified and there was an increase in the number of intracortical networks and
networks extending from the cerebral cortex to subcortical structures, with more neural networks being invested in multisensory
and sensory-motor-affective-cognitive integration. These changes permitted more complex, flexible and versatile cognitive
abilities and social behavior, such as shared intentionality and symbolic articulated language, which, in turn, made possible the
formation of larger social groups and cumulative cultural evolution that are characteristic of our species.
Keywords: Brain; Anatomy; Neurosciences; Human Evolution; Pan troglodytes.

A singularidade do cérebro humano: uma revisão


RESUMO. Esta revisão se propõe a relatar os aspectos mais importantes da singularidade anatômica e funcional do cérebro
humano. Para isso, faz-se uma comparação entre o nosso cérebro e os de nossos parentes evolutivos mais próximos (chimpanzés
e bonobos) e os ancestrais humanos. Durante a evolução humana ocorreu aumento absoluto do tamanho do cérebro e do
número de neurônios corticais cerebrais, maior grau de lateralização funcional e assimetria anatômica cerebral, citoarquitetura
cortical mais diversificada e aumento das redes neurais intracorticais e do córtex cerebral para as estruturas subcorticais
acompanhada de mudança em direção ao investimento de redes neurais na integração multissensorial e sensório-motora-
afetiva-cognitiva. Essas mudanças possibilitaram capacidades cognitivas e comportamentos sociais complexos, flexíveis e
versáteis, destacando-se a intencionalidade compartilhada e a linguagem articulada simbólica, que permitiram a formação de
grupos sociais maiores e a evolução cultural cumulativa característica de nossa espécie.
Palavras-chave: Encéfalo; Anatomia; Neurociências; Evolução Humana; Pan troglodytes..

INTRODUCTION our closest evolutionary relatives — great

T he purpose of this review was to inform


and comment on some anatomical and
functional aspects of the human brain — na-
apes, in particular chimpanzees and bono-
bos — have been incorporated and changed.
Therefore, information on the brains of these
ture’s most refined structure and, therefore, preceding species is necessary to help provide
the central component of human identity. answers to the question of human identity
Understanding the structure and function from a neuroscience perspective.
of the human brain is essential for answering What exactly makes our human brain
the question of why we are the species we are1. different from the brains of our human an-
Over the millions of years of evolution cestors and those of chimpanzees and bono-
of our brain, structures and neural networks bos? The questions to be asked are “is there
that were present in the brains of our hu- is any uniqueness in the human brain? If so,
man ancestors, as well as in the brains of what is it and at what level — macroscopic,

This review is part of a chapter of a book I have written titled “The Brain That Makes Us Humans”, published by Coopmed in 2021, and was also the subject of a
lecture presented by me on June 09, 2023, during the “Congress on Brain, Behavior and Emotions – BRAIN 2023”, held in Florianópolis, Brazil.
1
Universidade Federal de Minas Gerais, Faculdade de Medicina, Departamento de Anatomia Patológica e Medicina Legal, Belo Horizonte MG, Brazil.
Correspondence: José Eymard Homem Pittella; Email: jehpittella@hotmail.com.
Disclosure: The authors report no conflicts of interest.
Funding: none
Received on October 06, 2023; Accepted on October 12, 2023.

Pittella JEH.   The uniqueness of the human brain.   1


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Dement Neuropsychol 2023;17:e20230078

microscopic, or both — is it present? Is there any special number of neurons and glial cells, neuron body size,
anatomical arrangement or neural network in the con- dendritic arborization, axonal diameter, blood vessels,
nectome? Is there a greater number of brain neurons or and extracellular space.
a larger expansion or distinct architectural organization In general, brain size varies according to the animal’s
of the cerebral cortex in humans? On the other hand, if size and weight. The bigger the animal, the larger the
there is no uniqueness, are the differences between the size and weight of its brain tend to be, as it needs to
human brain and the brains of our ancestors and great control its body and make it function. An increase in
apes only quantitative?”. the relative brain size of a species, with brain volume ex-
These are the questions to be answered in this review, ceeding that expected for the species, will allow greater
based on the advances in neuroscience over the past de- cognitive capacity, as observed in humans.
cades and years. Throughout this review, the term “brain” On average, the weight of the adult human brain is
is used instead of encephalon, as the brain represents 1,400 g, ranging between 1,200 and 1,600 g. A smaller
the largest part of the encephalon (which includes, in percentage of weight values above or below these (rarely
addition to the brain, the brain stem and the cerebellum). over 2,000 g) is observed, with ample variation between
Thus, the topics described herein refer to brain structures individuals. In 1,130 adult and old age individuals of
and functions. For a better understanding of the text, both genders, brain weight varied from 1,720 to 900 g
the following topics are addressed herein2: (a variation of ~95%). This percent variation is related in
• Brain size and weight; part to gender (higher size and weight values in males,
• Number of cerebral cortex neurons; representing 9–12%) and body height6,7.
• Energy consumption by the brain; Starting at age 65, there is a 10/% reduction in average
• Cerebral functional and anatomical asymmetry; brain weight (and volume), with substantial individual
• Cerebral cortex expansion; variation. There is also a reduction in neuron size and den-
• Prefrontal cortex; dritic arborization responsible for neuronal connectivity,
• Connectome. although the number of neurons remains unchanged6.
A reduction of 0.45 to 0.5% in brain volume per year has
Brain size and weight been reported in other studies, starting at the age of 60
In terms of size, the human brain is three to four times years, as well as a reduction in thickness of the cerebral
larger than the brains of great apes. The frontal lobe cortex, and partial loss of axon myelin sheath8.
is the largest, followed by the parietal, temporal, and A study conducted with 42 chimpanzees raised in
occipital lobes3-5. Another difference between humans captivity (adolescents, adult, and aged, males and fe-
and great apes refers to frontal lobe position. Due to males) showed that an average brain weight of 389,9 g
its large expansion in humans, the frontal lobe became is reached in adolescence (ages 7 to 15 years), practically
positioned above the orbits (supraorbital position), the same as in young adults (ages 15–30 years), in which
leading to humans’ high, elevated forehead. In great average brain weight is 390 g. Individual variations have
apes, the frontal lobe is situated behind the orbits (ret- also been reported (458 to 308 g, a variation of almost
ro-orbital position), hence their low, slanted forehead. 50%), as well as a reduction in brain weight with age9.
In addition, because of its large expansion, the most In humans, the average brain weight (around 1,400 g)
anterior portion of the frontal lobe, referred to as the represents 2% of the body weight for a 70-kg individ-
prefrontal cortex, has acquired a more rounded contour ual, whereas in chimpanzees, brain weight averages
in humans, whereas it is more pointed in large apes, a 390 g, corresponding to approximately 0.7% of the
little less so in bonobos. Several factors contribute to average body weight for an adult male individual of 54
determining brain size in different species, such as the kg (Table 1).

Table 1. Average brain weight, average number of cerebral cortex neurons, and energy consumption by the brain of chimpanzees, Homo habilis, Homo
erectus, and Homo sapiens.
Chimpanzee Homo habilis Homo erectus Homo sapiens
Brain weight (g)* 390 (0.7%) 600-640+ 900-1,041+ 1,400 (2%)
Number of neurons (billions) 7.4 11 17 24
Energy consumption (%)§ 9-13 16 19-27
Notes: *Adult individual; +Cranial capacity in cm3; §% of energy consumption by the body at rest. The number of neurons in the human cerebral cortex (24 billion) estimated with basis on
the rules of proportionality to the number of neurons in the various brain structures of primates is much higher than the average obtained by counting with the isotropic fractionator method
(10.2 and 16.3 billion) and also when stereological methods are used (16.5 and 21 billion). See Table 2.

2   The uniqueness of the human brain.   Pittella JEH.


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Dement Neuropsychol 2023;17:e20230078

To compare the modern human brain with the brains brain neurons in human ancestors based on the rules
of our human ancestors, brain volume is estimated of proportionality to the number of neurons in the
based on the cranial capacity of fossilized skulls, which various cerebral structures of primates shows that the
is the volume of the inner space of the skull occupied by cerebral cortex of Australopithecus, Homo habilis, and
the brain. Comparison of the cranial capacity of Homo Homo erectus has respectively 9 billion, 11 billion, and
sapiens (1,350 cm3) with that of some of our ancestors 17 billion neurons, whereas the cerebral cortex of Homo
shows progressive volume increase during evolution: sapiens has 24 billion neurons16,17. This neuronal number
Australopithecus afarensis (413 cm3), Homo habilis (600- estimate for the human cerebral cortex is far larger than
640 cm3), and Homo erectus (900-1,041 cm3)10. the average number obtained by counting with the iso-
tropic fractionator method (10.2 and 16.3 billion) and
Number of cerebral cortex neurons by stereological methods (16.5 and 21 billion).
Knowledge of the cellular constitution of the brain is
very important for understanding its structure and Energy consumption by the brain
function. Differences in nerve system organization in The brain consumes a high amount of energy, requiring
terms of the number of cells in a region or structure, continuous access to glucose and oxygen transported
cellular architectural arrangement, and proportion to by the cerebral blood flow, which in humans represents
which a region or structure is dedicated to a particular 16% of cardiac output (the amount of blood pumped by
function can provide clues that help understand how the heart in 1 minute). Energy consumption by the brain
the brain is organized and how it functions11. varies according to age and gender, with larger amounts
The human brain has in average 86 billion neurons being consumed by young adults and women, and small-
(NeuN-positive cells) and 84 billion non-neuronal cells er amounts by men and the aged18. The extent to which
(NeuN-negative cells), most of which are glial cells12. the brain depends on constant blood supply is clearly
Of the total number of neurons, 16 billion (19%) are demonstrated when a person suffers cardiac arrest,
in the cerebral cortex. This proportion is similar to commonly secondary to myocardial infarction. Loss of
that observed in most mammal species (12 to 25%). consciousness occurs within approximately 15 seconds
Three studies conducted by different authors with a and, if cardiac reanimation is delayed, oxygen-glucose
variable number of adult and aged individuals of both deprivation will cause neuronal death in several regions
genders, using the (optical dissector) stereological and of the brain, particularly the cerebral cortex, four to
isotropic fractionator methods, showed that the cerebral seven minutes after cardiac arrest.
cortex contains between 10–25, 14.7–32, and 7.2–14.4 Compared to the great apes, humans consume more
billion neurons, respectively, the average number being energy and have a faster basal metabolic rate, which may
16.5, 21, and 10.2 billion, respectively. There was ample have favored evolution to a larger brain19. A though rep-
individual variation (100% or more) in all three studies, resenting only 2% of body weight, the adult human brain
with no differences between males and females6,13,14, and consumes 19 to 24% of the amount of energy required
no reduction in neuron numbers with age6,14. A neuronal by the human body at rest. This energy consumption
loss of about 10% was reported by Pakkenberg and Gun- rate is out of proportion to the relatively small mass
dersen13 (Table 2), yet no histopathological study was of the brain20. The brain of adult great apes requires far
made by these authors to exclude the presence of neu- less energy, with chimpanzees, for example, consuming
rodegenerative diseases that could explain neuronal loss. 9 to 13% of its total. It is admitted that the high energy
The number of neurons in the cerebral cortex of requirement of the human brain is attributable to its
humans is higher than that of chimpanzees (7.4 billion, large number of neurons17.
according to a study conducted with a single female A correlation is observed between, on the one
chimpanzee15). An estimation of the number of cortical hand, the areas of the carotid foramen in the skull and

Table 2. Recent neuron counting studies of the human cerebral cortex.


Number of Number of Average
Author Year Age (years) Method
cases neurons (billions) (billions)
Haug H 1997 111 20-110 S 10-25 16.5
Pakkenberg B, Gundersen H 1997 94 18-93 S 14.7-32 21
Azevedo FA et al. 2009 4 50-71 IF 16.3
Castro-Fonseca E et al. 2023 43 25-87 IF 7.2-14.4 10.2*
Abbreviations: S, Stereological; IF, Isotropic fractionator. Notes: *The cerebral cortex contains 23.8 billion non-neuronal cells, most of which are glial cells; See references.

Pittella JEH.   The uniqueness of the human brain.   3


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Dement Neuropsychol 2023;17:e20230078

transverse foramen of the cervical vertebrae through • petalias;


which the main arteries that irrigate the brain pass –— • downward displacement of the left occipital pole
the internal carotid arteries and the vertebral arteries, relative to the right occipital pole;
respectively — and, on the other hand, energy consump- • right-slanting of the medial surface of the occip-
tion by the brain, which seems to vary regardless of the ital lobe;
number of neurons. To explain these findings, it has been • asymmetry of the cerebral hemispheres in length,
proposed that a larger blood flow to the brain was required height, and width.
in humans, not because the brain became more expensive
in terms of energy, but rather because, as our ancestors Right-frontal and left-occipital petalias, which are
evolved, brain size increased in relation to body size21. present in 60% of the human population, consist of
forward displacement of the right-frontal pole and back-
Anatomical and functional asymmetry ward displacement of the left-occipital pole, commonly
Lateralization of the brain, with some brain functions observed in anatomical and neuroimaging studies.
tending to be served by only one of the brain hemi- Petalias of a similar or inverse pattern are identifiable
spheres, is present in several animal species and prob- in human ancestors10.
ably reflects an ancient evolutionary division between In vivo analysis using three-dimensional structural
the two hemispheres of functions that are essential magnetic resonance imaging of the brains of 91 humans
for survival, involving sensory and motor aspects22,23. and 78 chimpanzees showed that brain torque is specific
In modern humans, lateralization provided a solid of humans and absent in chimpanzees. In addition,
neural basis for the development of higher motor and the left hemisphere of the human brain is lower and
cognitive functions, such as using the hands as a tool, longer than the right hemisphere (lengths of 173.8 and
resulting in handedness (right-handed and left-handed 172.9 mm, respectively), whereas the cerebral hemi-
individuals, depending on which hand is preferably spheres of chimpanzees have equal dimensions. It is ad-
used), as well as lateralized brain control for speech mitted that these cerebral asymmetries in humans may
perception and production. These, in turn, led to the potentially correlate with the evolution of language27.
development of technology and more efficient forms
of communication and social interaction, respectively. Planum temporale
The left hemisphere of the brain has dominance This cortical area is in the lateral sulcus, posteriorly to
for language, particularly in right-handed individuals. the primary auditory cortex on the superior temporal
In 90-95% of humans, it is also dominant for using gyrus and is associated with language comprehension.
the right hand for gestural communications and tool In 65 to 70% of individuals, the left planum temporale
manipulation. Most left-handed individuals (78%) also is larger than its counterpart on the right, as demon-
show dominance of the left hemisphere for language. strated by Geschwind and Levitsky in a 1968 study of
The right hemisphere is dominant for music production a sample of 100 brains. This asymmetry is shared by
and visual spatial integration, which is the ability to rep- humans and all great apes28,29.
resent objects in three dimensions and, thus, estimate A study of the cytoarchitecture of the left planum
the distance between them24. Even though symbolic lan- temporale showed that its minicolumn arrangement,
guage is a cognitive and behavioral innovation unique with a larger spacing between minicolumns, as com-
to the human species, lateralization of the cortical areas pared to its counterpart on the right, in which the
associated with language in humans is also found in minicolumns are less spaced, is responsible for the
great apes, which suggests that language lateralization asymmetrical cortical surface of the human planum tem-
was already present in our last common ancestor. porale. This asymmetry is not present in chimpanzees
The main anatomical asymmetries in the human (see review30). A larger spacing between minicolumns
brain are brain torque, planum temporale, Broca area, equals a larger amount of neuropil, which, in turn, rep-
and arcuate fasciculus (which are related to language resents a higher number of dendrites, axon terminals,
evolution and speech production and perception), and and synapses, allowing for more refined processing by
the fusiform gyrus, involved in facial recognition. the minicolumns31-33.
A recent study of 98 individuals using structural
Brain torque magnetic resonance and diffusion tensor imaging
This consists of counterclockwise torsion of the cerebral during auditory perception of speech as reflected by
hemispheres, resulting in brain shape asymmetry, char- electroencephalography showed that the volume of the
acterized by several aspects25,26 such as: intra-neurite fraction, which indicates the density and

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Dement Neuropsychol 2023;17:e20230078

spatial dispersion of dendrites and axons, was larger in present in the left cerebral hemisphere of all humans.
the left planum temporale as compared to its right-size In the right cerebral hemisphere, however, this connec-
counterpart (2,081 mm3 x 1,645 mm3, respectively)34. tion is robust in 17.5% individuals, less robust in 20%
This means that the higher density and spatial disper- of individuals, and absent in the remaining 62.5%41,42.
sion of dendrites and axons in the left-right planum It is worth noting that, in both cerebral hemispheres,
temporale are associated with faster neural processing an indirect connection between Broca and Wernicke
of auditory speech perception. areas is provided by the arcuate fasciculus via an in-
termediary connection on the angular gyrus of the
Broca area inferior parietal lobule.
Located in the left inferior frontal gyrus, Broca area Projection of the three subdivisions — fronto-pari-
contains the speech motor programming (articulatory etal, temporal-parietal, and fronto-temporal — of the
code) that is relayed to the laryngeal motor cortex lo- arcuate fasciculus is well developed in humans, but quite
cated in the primary motor cortex behind Broca area, to reduced in chimpanzees43-46.
produce phonation in the larynx. In bonobos and chim-
panzees, too, vocalization is lateralized in the left cere- Fusiform gyrus
bral hemisphere. The volume and number of neurons The human right fusiform gyrus (in the lower portion
in Broca areas 44 and 45 of both cerebral hemispheres of the temporal and occipital lobes) is dominant in face
were analyzed in a small sample of 10 adult humans (5 recognition47. While integral, holistic face processing is
males and 5 females). In all 10 cases, the volume of area done in the dominant right fusiform gyrus and shared
44 was larger in the left hemisphere than in the right by chimpanzees (although not lateralized as in humans),
hemisphere, although this asymmetry was significant processing of individual facial features takes place in the
only in males. In 6 of these individuals (including all left fusiform gyrus48.
females), the volume of area 45 was significantly larger An interesting fact about the left fusiform gyrus is
in the left than in the right hemisphere35. that its neurons are larger, its minicolumns are wider,
In males, area 44 of the left hemisphere had a larger and its neuropil is more voluminous, as compared
number of neurons than its counterpart on the right. to those of the right fusiform gyrus dominant for
Although the total number of neurons in area 45 on the face perception. It seems, therefore, that the thinner
left side was larger than that on the right side in all 5 fe- minicolumnar arrangement and less neuropil in the
males, the difference was not significant. In males, there right fusiform gyrus are what make it dominant for
was no difference between the cerebral hemispheres in configurational face processing. This asymmetric cor-
the total number of neurons in area 45. New studies tical architectural pattern of the fusiform gyrus is not
with a larger sample of individuals are necessary to observed in chimpanzees.
corroborate these findings.
The cytoarchitecture of Broca area in humans and Cerebral cortex expansion
in its homologue in chimpanzees and bonobos exhibits Expansion of the cortical area of the brain, especially
large pyramidal neurons in layers III and V in all species the neocortex, occurred in all mammals, although it
studied. However, differences between the species are was particularly more intense and faster in primates.
observed in the volume occupied by the cell body of This expansion was both in absolute terms and relative
neurons and neuropil in the six cortical layers. Propor- to the rest of the brain, causing the human brain to
tional neuropil volume relative to cell body volume, acquire more folds and grooves, with the gyri becoming
which reflects the number of dendrites, axon termi- more tortuous14,49,50.
nals, and synapses required for information processing In addition to the primary sensory and motor areas
between neurons, is larger in humans as compared to shared with other mammals, the cerebral cortex of pri-
great apes36-40. mates acquired new cortical association areas (distinct
in terms of anatomy, cytoarchitecture, and function)
Arcuate fasciculus that were involved in higher order processing, allowing
This important curve-shaped (hence “arcuate”) fascic- for the integration of two or more senses (sight, hearing,
ulus connects areas of the inferior frontal and lateral body position in space), known as multimodal integra-
temporal areas, including Broca and Wernicke areas tion, and the generation of complex movements51.
responsible for speech and comprehension of spoken With regard to cortical cytoarchitecture, for exam-
and written language. A direct connection between ple, the neurons in association areas exhibit a larger
Broca and Wernicke areas by the arcuate fasciculus is number of synapses and a more complex dendritic

Pittella JEH.   The uniqueness of the human brain.   5


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Dement Neuropsychol 2023;17:e20230078

arborization. The superior and inferior parietal lobules represent information regardless of sensory stimula-
expanded greatly to include sensory-motor modules tion, i.e., our brain is capable of generating events that
that process and integrate information into motor are not taking place in the environment — the essence
commands, such as adjusting and fixing the eyes when of abstract thinking.
we see something interesting, reaching, grabbing, and
self-defense, allowing humans to acquire new skills, Prefrontal cortex
such as manipulating tools and using gestures for com- As mentioned earlier, the most recently evolved and
munication. A large cortical expansion occurred in the largest portion of the frontal lobe occupies the entire
temporal-parietal junction and posterior superior tem- front part of the frontal lobe — hence the name prefron-
poral sulcus, which contain areas involved in emotional tal cortex — and is one of the most important regions
face expression recognition, attention orientation, of the human brain. The prefrontal cortex is associated
theory of mind (the ability to infer the mental state of with cognitive and behavioral functions, emotional-cog-
others), and memory. This allowed rearrangement of nitive integration, working memory, executive func-
the cortical areas located in these regions and the ap- tions, decision-making, long-term planning, delayed
pearance of new functional cortical areas, contributing gratification, and impulsivity control56-60.
to an increase in human social skills52. Based on spatial location along the various geo-
The primary motor cortex, which is responsible metric planes — superior, inferior, anterior or ventral
for muscle action, became more specialized in the use (front), posterior or dorsal (back), lateral, medial — the
of arms, hands, and fingers, as well as in voluntary prefrontal cortex is divided into various areas with dis-
actions while walking, providing more advantages tinct functions: ventromedial prefrontal, ventrolateral,
to primates, especially humans. These functions dorsomedial, dorsolateral, frontopolar (frontal pole),
were further heightened by addition of the frontal orbitofrontal (above the orbits), and anterior cingulated
premotor and motor cortical areas of the anterior cortex (on the medial face of the cerebral hemispheres,
cingulate cortex, which are involved in movement above the corpus callosum)2,61.
planning. The prefrontal cortex in humans expand-
ed greatly in relation both to that of great apes and Volume of the cortical grey matter and subcortical
to the other regions of the brain, contributing to white matter of the prefrontal cortex of non-human
cognitive emotional control and social behavior and primates and humans
decision-making modulation53. A study of 60 humans, 29 chimpanzees, and 19 Old
The large expansion of the cerebral cortex in humans World monkeys showed that the volume of the cortical
in relation to non-humans and other mammal groups, grey matter of the human prefrontal cortex (which con-
unaccompanied by a significant increase in cortical tains neuron cell bodies, glial cells, and neuropil) and
thickness, is attributable to an increase in the number subcortical white matter was 1.9 times larger as com-
of minicolumns54. In humans, there has also been an pared to monkeys and 1.2 times larger as compared to
increase — in absolute terms and relative to the other chimpanzees. The subcortical white matter (containing
cortical layers — in the thickness of layers II and III, in nerve fibers entering and leaving the prefrontal cortex)
dendritic arborization size and complexity, as well as in was 2.4 times larger in humans as compared to monkeys
the size of the pyramidal neuron spines in these layers, and 1.7 times larger as compared to chimpanzees53.
with expansion of the cortico-cortical connections and These results suggest that the larger volume of the
improvement of the information processing and inte- human prefrontal cortex is due not only to its greater
gration capacity of these connections55. number of neurons (see below), but also to its larger
In short, expansion of the cerebral cortex was caused number of cortical synaptic connections, (probably)
by an increase in the number of neurons and synapses, higher number of axons per unit of area, and/or a larger
particularly in humans, in whom the neocortex oc- axon diameter.
cupies approximately 40% of the total brain volume,
a much larger proportion than that expected for the Number of neurons in the human prefrontal cortex
body weight of primates. Cerebral cortical expansion The frontal lobe contains 34% of the cerebral cortex
in humans has been to a large extent responsible for neurons, of which 85% are in the prefrontal cortex and
many of the behavioral specializations that are unique 15% in the primary motor cortex (on the precentral
to our species, such as fine hand motor control, cog- gyrus)14. These data indicate that, as the frontal lobe
nitive and social flexibility, and language production is the largest region of the brain, the prefrontal cortex
and comprehension, allowing humans to process and is the brain area with the largest number of cerebral

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cortex neurons. It should be noted that the premotor Over the past two decades, there has been a boom
and supplementary motor cortices were considered of in vivo studies of individuals, including humans and
by the authors of this study as being part of the pre- non-human primates, using structural and functional
frontal cortex. magnetic resonance and tensor diffusion imaging to
map distinct regions of the brain and their connectiv-
Cytoarchitecture of the prefrontal cortex in non-human ity patterns. Comparative analyses of the human con-
primates and humans nectome versus that of other species showed that the
A comparison of the cerebral cortical cytoarchitecture organization and spatial distribution of cortico-cortical
of humans versus great apes shows that Broca area and and cortico-subcortical fibers are similar in monkeys,
the anterior insular cortex of humans are 6 times larger chimpanzees, and humans. This similarity is attributed
than their homologues in chimpanzees, whereas the to selective pressures common to these primates, leading
primary motor cortex, primary somatosensory cortex, to a reduction in connectivity costs and, at the same time,
and primary visual cortex have similar sizes in both to more complex adaptive functions. Quatitative differ-
species62. These findings are in agreement with those ences, as well as differences in connectivity patterns, are
from other studies reporting thicker minicolumns and observed among the groups of primates.
a larger amount of neuropil in layer III of the human Several neural networks show similarity to those of
frontopolar cortex (indicating more refined neural humans, such as the corticospinal tract (which extends
processing) as compared to chimpanzees63. from the cerebral cortex to the spinal cord motor neu-
Similarly, the number of spines in the pyramidal rons responsible for the execution of muscle actions),
neurons of the human prefrontal cortex, which points connections of the limbic system involved in social be-
to the existence of synapses, is also larger as compared havior and emotion modulation (cingulum and fornix
to non-human primates, thus further supporting the bundle), and fasciculi that interconnect areas of the dif-
point of view that there was expansion of the prefrontal ferent brain lobes, allowing processing and integration
cortex in humans64. of information from association and primary sensory
and motor areas and forming an ample neural network
Connectome related to attention control45.
The different types of neurons and their synaptic con- Among these fasciculi, the following stand out:
nections at the micro- and macroscopic levels make • superior longitudinal fasciculus, which connects
up the neural networks known as connectome. At the the lateral frontal cortex to the lateral parietal
microscopic level, connections between the neurons are cortex;
made by synapses that convey information by means of • inferior longitudinal fasciculus, which connects
neurotransmitters. These synapses, identifiable under the temporal to the occipital lobe (the longitu-
an electronic microscope, are collectively known as the dinal name of these two fasciculi derives from
synaptome65,66. Studying the microscopic connections their direction relative to the main axis of these
of our nerve system is important, as the individual lobes)67;
neural identity of humans is thought to be defined by • inferior fronto-occipital fasciculus, which con-
our connectome. In other words, humans are different, nects the occipital lobe and, to a lesser degree, the
feel and think differently from other beings because the parietal and temporal lobes to the frontal lobe68.
neural synaptic connections are distinct and unique to
each of us, even though the human brain is admitted It is admitted, for example, that the inferior fron-
having hundreds of trillions of synapses. to-occipital fasciculus is related to visual information
Three-dimensional macroscopic visualization of processing and integration for basic communication
the connectome is possible using special magnetic res- acts between individuals of the same species, such as
onance techniques, such as diffusion tensor imaging producing distinct screams to alert when threatened
combined with tractography, allowing identification by different predators.
of the dominant orientation of the nerve fibers that Significant differences among primate species are
form the white matter tracts. In 2009, the U.S. National found, however, in connectivity of the multimodal as-
Institutes of Health launched the Human Connectome sociation areas, which is more elaborate in humans as
Project to initially map the brains of 1,200 adults us- compared to chimpanzees43. Examples are connections
ing the latest imaging technology. The data from this of the lateral parietal cortex, precuneus (superior, medi-
project are available on-line for laboratory analysis by al, and posterior portions of the parietal lobe), temporal
neuroscientists all over the world. cortex, inferior frontal cortex, and medial prefrontal

Pittella JEH.   The uniqueness of the human brain.   7


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Dement Neuropsychol 2023;17:e20230078

cortex, including important language processing tracts Also, there is preference for the human left ce-
such as the arcuate fasciculus, which, as mentioned rebral hemisphere to interconnect exclusively with
before, connects Broca and Wernicke areas responsible itself, particularly with the cortical areas involved in
for speech production and spoken and written language language and fine motor coordination, the latter being
comprehension42,44. related to using the hands to thread a needle, play a
During evolution, there has been a significant in- musical instrument or dissect an anatomical structure
crease in connectivity of the posterior middle temporal using a scalpel. In contrast, the cortical areas of the
gyrus and anterior portion of the left temporal lobe human right cerebral hemisphere associate with visu-
in humans as compared to chimpanzees. The poste- al-spatial processing and attention interact with both
rior middle temporal gyrus is involved in meaning cerebral hemispheres72.
attribution to words (semantics) and syntax process- Differences are also observed in the organization
ing (organizing words into phrases and sentences), of the superior longitudinal fasciculus, which, as men-
whereas the anterior portion of the temporal lobe is tioned before, connects the lateral frontal cortex with
associated with semantic representations of language. the lateral parietal cortex, the latter being considered
Connectivity of the posterior middle temporal gyrus by some anatomists to be distinct from the arcuate
was expanded in all three subdivisions of the arcuate fasciculus. In humans, as compared to chimpanzees,
fasciculus, particularly the parieto-temporal subdivi- there is greater connectivity of the superior longitudinal
sion, as well as in the middle longitudinal fasciculus. fasciculus with the lateral frontal cortex (dorsolateral
On the other hand, connectivity of the anterior portion prefrontal cortex and inferior frontal gyrus), more to
of the temporal lobe of humans also expanded in the the right in the latter, thus evidencing lateralization73.
inferior longitudinal fasciculus, middle longitudinal These differences may have implications for the evolu-
fasciculus, and uncinate fasciculus, the latter of which tion of some functions related to the frontal and parietal
connects the anterior portion of the temporal lobe to lobes, such as attention for comprehending and repro-
the orbitofrontal cortex45,46. ducing the details of an observed action, social learning,
Another important difference between humans and and use of tools.
non-human primates is in the motor control of speech A reduced proportion of connections (5.9%) seem
and vocalization by the laryngeal motor cortex. In to be specific to the human connectome, forming the
humans, the laryngeal motor cortex is in two areas of intra-hemispheric pathways (connecting different areas
the primary motor cortex (precentral gyrus): the face of the same cerebral hemisphere) related to multimodal,
representation area (dorsal laryngeal motor cortex) and unimodal, and primary (sensory and motor) association
the area underlying it (ventral laryngeal motor cortex). areas, with connections among these areas also being
The neurons of the laryngeal motor cortex make direct present43. Of the cortico-cortical intra-hemispheric
connections via the corticobulbar tract with the motor connections in the left cerebral hemisphere, 82.6%
neurons in the nucleus ambiguus (located in the brain (19 out of 23) are specific to humans and 50% (3 out
stem), facilitating control of the laryngeal muscles of 6) are specific to chimpanzees. As compared to the
and complex movement production in speech and connectome of chimpanzees, the human connectome
singing69,70. Compared to non-human primates, the exhibits relatively high levels of integration among
dorsal laryngeal motor cortex shows connectivity and functionally segregated brain systems, which allows for
synchronicity with motor control of the jaw, (especially greater precision in making a correct choice74.
for lowering of the jaw) during phonation71. There is also Based on data from the Human Connectome Project
greater connectivity with the adjacent temporoparietal and functional magnetic resonance studies, new cortical
cortex (inferior parietal lobule and superior temporal and subcortical functional neural networks have been
gyrus) responsible for more refined sensory and motor described as associated to:
processing and execution, which may have contributed • spatial navigation and identification and repre-
to better sensory and motor integration, resulting in sentation of events in a narrative;
more elaborate motor control of learned vocalizations • semantic categories of a higher order, such as in
such as speech and singing. processing and integrating meaning to a spoken,
In non-human primates, the laryngeal motor cor- heard or seen object (or another category); and
tex is in the premotor cortex and its neurons make • reward system75.
only indirect connections with the nucleus ambiguus,
restricting the production of vocalization patterns Individual differences are identified in the functional
learned voluntarily. connectome of humans at rest, which shows that some

8   The uniqueness of the human brain.   Pittella JEH.


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Dement Neuropsychol 2023;17:e20230078

neural networks are unique and stable, functioning as refined (*) and new (+) cognitive and behavioral
a neural fingerprint76. aspects, as compared to chimpanzees and bonobos
Provided below is a summary of the quantitative — the great apes that are our closest relatives from
anatomical changes in the human brain that have an evolutionary point of view — and our human an-
made it unique and allowed for the appearance of cestors (Chart 1)2,77.

Chart 1. Quantitative evolutionary changes in the anatomy of the human brain that resulted in its uniqueness.

• Absolute increase in brain size and in the number of neurons in the cerebral cortex;
• Anatomical and functional asymmetry;
• Expansion of the cerebral cortex in the association areas;
• More diversified cytoarchitecture of the cerebral cortex, with hemispheric asymmetry;
• Appearance of refined* and new+ cognitive and behavioral aspects:
o Reduction in reactive aggressiveness*
o Communication and cooperation for hunting, defense, and tool use*
Common understanding
o Shared intentionality+ Trusted collaboration

Experience sharing
o Symbolic articulated language+
o Formation of larger social groups and creation of artifacts, trade, art, science, philosophy and religion,
allowing for cumulative cultural evolution+

Examples of shared intentionality (collective work or activity performed jointly by a group of individuals):
sports teams, musicians of an orchestra, production of an opera, production of a film with actors, a military or
samba school parade.

REFERENCES
1. Sousa AMM, Meyer KA, Santpere G, Gulden FO, Sestan N. Evolution of years of cell counting. J Comp Neurol. 2016;524(18):3865-95. https://
the human nervous system function, structure, and development. Cell. doi.org/10.1002/cne.24040
2017;170(2):226-47. https://doi.org/10.1016/j.cell.2017.06.036 12. Azevedo FA, Carvalho LRB, Grinberg LT, Farfel JM, Ferretti REL, Leite
2. Pittella JE. O cérebro que nos faz humanos. Belo Horizonte: Folium; 2021. REP, et al. Equal numbers of neuronal and nonneuronal cells make the
3. Friedrich P, Forkel SJ, Amiez C, Balsters JH, Coulon O, Fan L, et al. human brain an isometrically scaled-up primate brain. J Comp Neurol
Imaging evolution of the primate brain: the next frontier? Neuroimage. 2009;513(5):532-41. https://doi.org/10.1002/cne.21974
2021;228:117685. https://doi.org/10.1016/j.neuroimage.2020.117685 13. Pakkenberg B, Gundersen HJ. Neocortical neuron number in humans:
4. DeCasien AR, Barton RA, Higham JP. Understanding the human brain: effect of sex and age. J Comp Neurol. 1997;384(2):312-20. PMID:
insights from comparative biology. Trends Cogn Sci. 2022;26(5):432-45. 9215725.
https://doi.org/10.1016/j.tics.2022.02.003 14. Castro-Fonseca E, Morais V, Silva CG, Wollner J, Freitas J, Mello-Neto
5. Garin CM, Garin M, Silenzi L, Jaffe R, Constantinides C. Multilevel atlas AF, et al. The influence of age and sex on the absolute cell numbers of
comparisons reveal divergent evolution of the primate brain. Proc Natl the human brain cerebral cortex. Cereb Cortex. 2023;33(13):8654-66.
Acad U S A. 2022;119(25):e2202491119. https://doi.org/10.1073/ https://doi.org/10.1093/cercor/bhad148
pnas.2202491119 15. Collins CE, Turner EC, Sawyer EK, Reed JL, Young NA, Flaherty DK, et al.
6. Haug H. The aging human cerebral cortex: morphometry of areal diffe- Cortical cell and neuron density estimates in one chimpanzee hemisphe-
rences and their functional meaning. In: Dani SU, Hori A, Walter GF, eds. re. Proc Natl Acad U S A. 2016;113(3):740-5. https://doi.org/10.1073/
Principles of neural aging. Amsterdam: Elsevier; 1997. p. 247-61. pnas.1524208113
7. Kaczkurkin AN, Raznahan A, Satterthwaite TD. Sex differences in the 16. Herculano-Houzel S, Kaas JH. Gorilla and orangutan brains conform to
developing brain: insights from multimodal neuroimaging. Neuropsycho- the primate scaling rules: implications for human evolution. Brain Behav
pharmacology. 2019;44(1):71-85. https://doi.org/10.1038/s41386-018- Evol. 2011;77(1):33-44. https://doi.org/10.1159/000322729
0111-z 17. Herculano-Houzel S. A vantagem humana: como o nosso cérebro se
8. Blinkouskaya Y, Caçoilo A, Gollamudi T, Jalalian S, Weickenmeier J. Brain tornou superpoderoso. São Paulo: Companhia das Letras; 2017.
aging mechanisms with mechanical manifestations. Mech Ageing Dev. 18. Xing CY, Tarumi T, Liu J, Zhang Y, Turner M, Riley J, et al. Dis-
2021;200:111575. https://doi.org/10.1016/j.mad.2021.111575 tribution of cardiac output to the brain across the adult lifespan.
9. Herndon JG, Tigges J, Anderson DC, Klumpp SA, McClure HM. Brain J Cereb Blood Flow Metab. 2017;37(8):2848-56. https://doi.or-
weight throughout the life span of the chimpanzee. J Comp Neurol. g/10.1177/0271678X16676826
1999;409(4):567-72. PMID: 10376740. 19. Pontzer H, Brown MH, Raichlen DA, Dunsworth H, Hare B, Walker K,
10. Tobias PV. Evolution of brain size, morphological restructuring and longevity et al. Metabolic acceleration and the evolution of human brain size and
in early hominids. In: Dani SU, Hori A, Walter GF, eds. Principles of neural life history. Nature. 2016;533(7603):390-2. https://doi.org/10.1038/
aging. Amsterdam: Elsevier; 1997. p. 153-74. nature17654
11. von Bartheld CS, Bahney J, Herculano-Houzel S. The search for true 20. Kuzawa CW, Chugani HT, Grossman LI, Lipovich L, Muzik O, Hof PR,
numbers of neurons and glial cells in the human brain: a review of 150 et al. Metabolic costs and evolutionary implications of human brain de-

Pittella JEH.   The uniqueness of the human brain.   9


View & Review
Dement Neuropsychol 2023;17:e20230078

velopment. Proc Natl Acad Sci U S A. 2014;111(36):13010-15. https:// areas in the human brain compared with chimpanzees. Proc Natl Acad Sci
doi.org/10.1073/pnas.1323099111 U S A. 2019;116(14):7101-6. https://doi.org/10.1073/pnas.1818512116
21. Boyer DM, Harrington AR. Scaling of bony canals for encephalic vessels 44. Eichert N, Verhagen L, Folloni D, Jbabdi S, Khrapitchev AA, Sibson NR,
in euarchontans: Implications for the role of the vertebral artery and brain et al. What is special about the human arcuate fasciculus? Lateralization,
metabolism. J Hum Evol. 2018;114:85-101. https://doi.org/10.1016/j. projections, and expansion. Cortex. 2019;118:107-15. https://doi.or-
jhevol.2017.09.003 g/10.1016/j.cortex.2018.05.005
22. Forrester GS, Todd BK. A comparative perspective on lateral biases 45. Byant KL, Li L, Eichert N, Mars RB. A comprehensive atlas of white matter
and social behavior. Prog Brain Res. 2018;238:377-403. https://doi. tracts in the chimpanzee. PLoS Biol. 2020;18(12):e3000971. https://doi.
org/10.1016/bs.pbr.2018.06.014 org/10.1371/journal.pbio.3000971
23. Güntürkün O, Ströckens F, Ocklenburg S. Brain lateralization: a com- 46. Sierpowska J, Bryant KL, Janssen N, Freches GB, Römkens M, Mangnus
parative perspective. Physiol Rev. 2020;100(3):1019-63. https://doi. M, et al. Comparing human and chimpanzee temporal lobe neuroanatomy
org/10.1152/physrev.00006.2019 reveals modifications to human language hubs beyond the frontotemporal
24. Kuhl PK, Damasio AR. A linguagem. In: Kandel ER, Schwartz JH, Jessell arcuate fasciculus. Proc Natl Acad Sci U S A. 2022;119(28):e2118295119.
TM, Siegelbaum AS, Hudspeth AJ, eds. Princípios de neurociências. 5a https://doi.org/10.1073/pnas.2118295119
ed. Porto Alegre: AMGH Editora; 2014. p. 1179-96. 47. Rossion B, Jacques C, Jonas J. Mapping face categorization in the human
25. Kong XZ, Mathias SR, Guadalupe T; ENIGMA Laterality Working Group, ventral occipitotemporal cortex with direct neural intracranial recordings.
Glahn DC, Franke B, et al. Mapping cortical brain asymmetry in 17,141 Ann N Y Acad Sci. 2018. https://doi.org/10.1111/nyas.13596
healthy individuals worldwide via the ENIGMA Consortium. Proc Natl 48. Moraes Jr R, Marinho de Sousa B, Fukusima S. Hemispheric specia-
Acad U S A. 2018;115(22):E5154-E5163. https://doi.org/10.1073/ lization in face recognition: from spatial frequencies to holistic/analytic
pnas.1718418115 cognitive processing. Psychol Neurosci. 2014;7(4),503-11. https://doi.
26. Zhao L, Matloff W, Shi Y, Cabeen RP, Toga AW. Mapping complex brain org/10.3922/j.psns. 2014.4.09.
torque components and their genetic architecture and phenomic asso- 49. Halley AC, Krubitzer L. Not all cortical expansions are the same: the
ciations in 24,112 individuals. Biol Psychiatry. 2022;91(8):753-68. https:// coevolution of the neocortex and the dorsal thalamus in mammals. Curr
doi.org/10.1016/j.biopsych.2021.11.002 Opin Neurobiol. 2019;56:78-86. doi: 10.1016/j.conb.2018.12.003.
27. Xiang L, Crow T, Roberts N. Cerebral torque is human specific and unre- 50. Namba T, Vaid S, Huttner WB. Primate neocortex development and evo-
lated to brain size. Brain Struct Funct. 2019;224(3):1141-50. https://doi. lution: conserved versus evolved folding. J Comp Neurol. 2019;527:1621-
org/10.1007/s00429-018-01818-0 32. doi: 10. 1002/cne.24606.
28. Geschwind N, Levitsky W. Human brain: left-right asymmetries in temporal 51. Kaas JH. The evolution of neocortex in primates. Prog Brain Res.
speech region. Science. 1968;161(3837):186-7. https://doi.org/10.1126/ 2012;195:91-102. doi: 10.1016/B978-0-444-53860-4.00005-2.
science.161.3837.186 52. Patel GH, Sestieri C, Corbetta M. The evolution of the temporoparietal
29. Witelson SF. Anatomic asymmetry in the temporal lobes: its documen- junction and posterior superior temporal sulcus. Cortex. 2019;118:38-50.
tation, phylogenesis, and relationship to functional asymmetry. Ann N Y doi: 10.1016/j. cortex.2019.01.026.
Acad Sci. 1977;299:328-54. https://doi.org/10.1111/j.1749-6632.1977. 53. Donahue CJ, Glasser MF, Preuss TM, Rilling JK, Van Essen DC.
tb41920.x Quantitative assessment of prefrontal cortex in humans relative to no-
30. Chance SA. The cortical microstructural basis of lateralized cogni- nhuman primates. PNAS. 2018;115(22):E5183-E5192. doi: 10.1073/
tion: a review. Front Psychol. 2014;5:820. https://doi.org/10.3389/ pnas.1721653115.
fpsyg.2014.00820 54. Rakic P. Evolution of the neocortex: perspective from developmen-
31. Buxhoeveden DP, Switala AE, Roy E, Litaker M, Casanova MF. Laterali- tal biology. Nat Rev Neurosci. 2009;10(10):724-35. doi: 10.1038/
zation of minicolumn structure in human planum temporale is absent in nrn2719.
nonhuman primate cortex. Brain Behav Evol. 2001;57:349-58. https:// 55. Galakhova AA, Hunt S, R. Wilbers R, Heyer DB, de Kock CPJ, Mans-
doi.org/10.1159/000047253 velder HD, et al. Evolution of cortical neurons supporting human cogni-
32. Buxhoeveden DP, Casanova MF. The minicolumn hypothesis in neuros- tion. Trends Cogn Sci. 2022;26(11):909-22. https://doi.org/10.1016/j.
cience. Brain. 2002;125 (5):935-51. https://doi.org/10.1093/brain/awf110 tics.2022.08.012.
33. Ruthig P, Schönwiesner M. Common principles in the lateralization of 56. Sapolsky, RM. Behave. The biology of humans at our best and worst.
auditory cortex structure and function for vocal communication in primates New York: Penguin Press, 2017: pp. 45-80.
and rodents. Eur J Neurosci. 2022;55(3):827-45. https://doi.org/10.1111/ 57. Kolk SM, Rakic P. Development of prefrontal cortex. Neuropsychophar-
ejn.15590 macology. 2022;47(1):41-57. doi: 10.1038/s41386-021-01137-9.
34. Ocklenburg S, Friedrich P, Fraenz C, Schlüter C, Beste C, Güntürkün O, 58. Matsui T, Hattori Y, Tsumura K, Aoki R, Takeda M, Nakahara K, et al.
et al. Neurite architecture of the planum temporale predicts neurophy- Executive control by fronto-parietal activity explains counterintuitive
siological processing of auditory speech. Sci Adv. 2018;4(7):eaar6830. decision behavior in complex value-based decision-making. Neu-
https://doi.org/10.1126/ sciadv.aar6830 roimage. 2022;249:118892. https://doi.org/10.1016/j.neuroima-
35. Uylings HBM, Jacobsen AM, Zilles K, Amunts K. Left-right asymme- ge.2022.118892.
try in volume and number of neurons in adult Broca’s area. Cortex. 59. Rolls ET, Wan Z, Cheng W, Feng J. Risk-taking in humans and the medial
2006;42(4):652-8. https://doi.org/10.1016/s0010-9452(08)70401-5 orbitofrontal cortex reward system. NeuroImage. 2022;249:118893. doi:
36. Schenker NM, Hopkins WD, Spocter MA, Garrison AR, Stimpson CD, 10.1016/j.neuroimage.2022.118893.
Erwin JM, et al. Broca’s area homologue in chimpanzees (Pan troglodytes): 60. Stone C, Mattingley JB, Rangelov D. On second thoughts: changes
probabilistic mapping, asymmetry, and comparison to humans. Cereb of mind in decision-making. Trends Cogn Sci. 2022;26(5):419-31. doi:
Cortex. 2010;20(3):730-42. https://doi.org/10.1093/cercor/bhp138 10.1016/j.tics.2022. 02.004.
37. Simonyan K, Horwitz B. Laryngeal motor cortex and control of 61. Amiez C, Sallet J, Hopkins WD, Meguerditchian A, Hadj-Bouziane F, Ben
speech in humans. Neuroscientist. 2011;17(2):197-208. https://doi. Hamed S, et al. Sulcal organization in the medial frontal cortex provides
org/10.1177/1073858410386727 insights into primate brain evolution. Nat Commun. 2019;10:3437. https://
38. Palomero-Gallagher N, Zilles K. Differences in cytoarchitecture of Broca’s doi.org/10.1038/ s41467-019-11347-x.
region between human, ape and macaque brains. Cortex. 2019;118:132- 62. Sherwood CC, Bauernfeind AL, Bianchi S, Raghanti MA, Hof PR. Human
53. https://doi.org/10.1016/j.cortex.2018.09.008 brain evolution writ large and small. Prog. Brain Res. 2012;195:237-54.
39. Graïc JM, Peruffo A, Corain L, Centelleghe C, Granato A, Zanellato E, doi: 10.1016/ B978-0-444-53860-4.00011-8.
et al. Asymmetry in the cytoarchitecture of the area 44 homolog of the 63. Teffer K, Buxhoeveden DP, Stimpson CD, Fobbs AJ, Schapiro SJ, Baze
brain of the chimpanzee Pan troglodytes. Front Neuroanat. 2020;14:55. WB, et al. Developmental changes in the spatial organization of neurons
https://doi.org/10.3389/fnana. 2020.00055 in the neocortex of humans and common chimpanzees. J Comp Neurol.
40. Kemmerer D. Revisiting the relation between syntax, action, and left 2013;521(18) :4249-59. doi: 10.1002/cne.23412.
BA44. Front Hum Neurosci. 2022;16:923022. https://doi.org/10.3389/ 64. Elston GN, Benavides-Piccione R, Elston A, Manger PR, Defelipe J.
fnhum.2022.923022 Pyramidal cells in prefrontal cortex of primates: marked differences in
41. Catani M, Jones DK, Hffytche D. Perisylvian language networks of the neuronal structure among species. Front Neuroanat. 2011;5:2. doi:
human brain. Ann Neurol. 2005;57(1):8-16. https://doi.org/10.1002/ 10.3389/fnana.2011.00002.
ana.20319 65. Eickhoff SB, Yeo BTT, Genon S. Imaging-based parcellations of the human
42. Vaquero L, Rodríguez-Fornells A, Reiterer SM. The left, the better: whi- brain. Nature Rev Neurosci. 2018;19:672-86. doi: 10.1038/s41583-018-
te-matter brain integrity predicts foreign language imitation ability. Cereb 0071-7.
Cortex. 2017;27(8):3906-17. https://doi.org/10.1093/cercor/bhw199 66. Wei Y, Scholtens LH, Turk E, van den Heuvel MP. Multiscale examination of
43. Ardesch DJ, Scholtens LH, Li L, Preuss TM, Rilling JK, van den Heuvel MP. cytoarchitectonic similarity and human brain connectivity. Netw Neurosci.
Evolutionary expansion of connectivity between multimodal association 2019;3(1):124-37. doi: 10.1162/netn_a_00057.

10   The uniqueness of the human brain.   Pittella JEH.


View & Review
Dement Neuropsychol 2023;17:e20230078

67. Mars RB, O’Muircheartaigh J, Folloni D, Li L, Glasser MF, Jbabdi S, et al. 72. Gotts SJ, Jo HJ, Waalace GL, Saad ZS, Cox RW, Martin A. Two distinct
Concurrent analysis of white matter bundles and grey matter networks forms of functional lateralization in the human brain. PNAS. 2013;110(36)
in the chimpanzee. Brain Struct Funct. 2019;224:1021. doi: 10.1007/ E3435-E3444. doi: 10.1073/pnas.1302581110.
s00429-018-1817-8 73. Hecht EE, Gutman DA, Bradley BA, Preuss TM, Stout D. Virtual dissec-
68. Sarubbo S, Petit L, De Benedictis A, Chioffi F, Ptito M, Dyrby TB. Uncove- tion and comparative connectivity of the superior longitudinal fasciculus
ring the inferior fronto-occipital fascicle and its topological organization in in chimpanzees and humans. Neuroimage. 2015;108:124-37. doi:
non-human primates: the missing connection for language evolution. Brain 10.1016/j.neuroimage.2014. 12.039.
Struct Funct. 2019;224(4):1553-67. doi: 10.1007/s00429-019-01856-2. 74. Pang JC, Rilling JK, Roberts JA, van den Heuvel MP, Cocchi L. Evolu-
69. Kumar V, Croxson PL, Simonyan K. Structural organization of the laryn- tionary shaping of human brain dynamics. Elife. 2022;11:e80627 doi:
geal motor cortical network and its implication for evolution of speech 10.7554/eLife.806 27.
production. J Neurosci. 2016;36(15): 4170-81. doi: 10.1523/JNEUROS- 75. Ji JL, Spronk M, Kulkarni K, Repovš G, Anticevic A, Cole MW. Mapping
CI.3914-15.2016. the human brain’s cortical-subcortical functional network organization.
70. Belyk M, Eichert N, McGettigan C. A dual larynx motor networks hypo- Neuroimage 2019;185:35-57. doi: 10.1016/j.neuroimage.2018.10.00.
thesis. Phil. Trans. R. Soc. B. 2021;376(1840):20200392. http://doi. 76. Horien C, Shen X, Scheinost D, Constable RT. The individual functional
org/10.1098/rstb.2020. 0392. connectome is unique and stable over months to years. Neuroimage
71. Brown S, Yuan Y, Belyk M. Evolution of the speech-ready brain: The 2019;189:676-87. doi: 10.1016/j.neuroimage.2019.02.002.
voice/jaw connectionin the human motor cortex. J Comp Neurol. 77. Flinn MV. The creative neurons. Front Psychol. 2021;12:765926. doi:
2021;529(5):1018-28). doi: 10.1002/cne.24997. 10.3389/ fpsyg.2021.765926.

Pittella JEH.   The uniqueness of the human brain.   11

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