Evolution of Human Brain Functions: The Functional Structure of Human Consciousness

Abstract

The functional structure of self-aware consciousness in human beings is described based on the evolution of human brain functions. Prior work on heritable temperament and character traits is extended to account for the quantum-like and holographic properties (i.e. parts elicit wholes) of self-aware consciousness. Cladistic analysis is used to identify the succession of ancestors leading to human beings. The functional capacities that emerge along this lineage of ancestors are described. The ecological context in which each cladogenesis occurred is described to illustrate the shifting balance of evolution as a complex adaptive system. Comparative neuroanatomy is reviewed to identify the brain structures and networks that emerged coincident with the emergent brain functions. Individual differences in human temperament traits were well developed in the common ancestor shared by reptiles and humans. Neocortical development in mammals proceeded in five major transitions: from early reptiles to early mammals, early primates, simians, early Homo, and modern Homo sapiens. These transitions provide the foundation for human self-awareness related to sexuality, materiality, emotionality, intellectuality, and spirituality, respectively. The functional structure of human self-aware consciousness is concerned with the regulation of five planes of being: sexuality, materiality, emotionality, intellectuality, and spirituality. Each plane elaborates neocortical functions organized around one of the five special senses. The interactions among these five planes gives rise to a 5 × 5 matrix of subplanes, which are functions that coarsely describe the focus of neocortical regulation. Each of these 25 neocortical functions regulates each of five basic motives or drives that can be measured as temperaments or basic emotions related to fear, anger, disgust, surprise, and happiness/sadness. The resulting 5 × 5 × 5 matrix of human characteristics provides a general and testable model of the functional structure of human consciousness that includes personality, physicality, emotionality, cognition, and spirituality in a unified developmental framework.

Keywords

cognition emotionality human characteristics personality thinking.

Human beings are perennially curious about their inner nature and seek to understand what motivates their desires, actions, feelings, thoughts, and values. The study of human characteristics has led to many insightful theories and useful approaches, but each suffers from serious limitations regarding its scope and the qualitative properties of its form, aetiology, and dynamics.

Regarding scope, there are many different theories that focus on sexuality, physicality, emotionality, sociality, character, cognition, or spirituality [1]. Some broad theories try to serve as a coherent theory of theories (i.e. meta-theory), as did Freud, Piaget, and Maslow [2]. Each still focused on a particular aspect of being, such as sexuality, cognition, or spirituality. Separate theories for personality, cognition, and spirituality can each be useful, but the divisions are actually artificial and impair understanding in serious ways. Health is an integrated state of physical, emotional, social, cognitive, and spiritual well-being [3,4].

Regarding qualitative properties and form, most models of human characteristics fail to recognize the unique properties of different planes of being. ‘Planes’ are defined as distinct levels of existence, thought, or development [5]. Emotions cannot be fully described or explained by sexual or material mechanisms. Symbolic communication cannot be fully explained in terms of emotional processes. Spirituality cannot be adequately explained by intellectual judgments or rules of moral conduct.

Even within the cognitive domain, there is often failure to attend to the qualitatively distinct properties of the multiple systems of learning and memory that are observed in human beings [6]. For example, associative conditioning varies quantitatively according to the strength of habits (Table 1). Aesthetic appreciation of beauty, however, is a qualitative experience. Self-aware consciousness is always subjective and holographic in form (i.e. self-aware perceptions are holistic and personal), so information about beauty cannot be specified by any amount of quantitative or objective detail [7].

Table 1.

Distinctive properties of three systems of learning and memory in human beings

System	Form of learning	Qualitative properties
Procedural	Habits and skills	Prelogical Emotion-laden Quantitative (variable strength) Not self-aware
Semantic	Facts and propositions	Logical Algorithmic Hierarchical Not self-aware
Autonoetic	Intuitions and narratives	Self-aware Holistic Biographical Creative and freely willed

No models of neurobiology or personality provide an adequate explanation of subjectivity (i.e. self-aware consciousness). There are several promising neurobiological insights for explaining different components of consciousness [8–13]. These individual components of consciousness need to be integrated in a unified general model recognizing the holographic nature of self-aware consciousness.

Personality and emotionality have other properties that must be satisfied by a general model of consciousness. Personality and emotionality have a universal structure shared by all human beings, as emphasized by Darwin and supported by cross-cultural studies of facial expression by Ekman [14]. Likewise, Chomsky suggested that there is a universal grammar for the development of language as part of the rich innate endowment of human beings [15]. He argued that without such universal structure we would not be able to communicate and respect one another as we do [16]. There may still be substantial differences among individuals in the expression of these universal functions, which provides diversity in adaptive capacities for possible ecological change [17,18].

Finally, a general model of human consciousness needs to provide a meta-theory for development, including the maturation and integration of sexual, physical, emotional, intellectual, and spiritual aspects of being [19–21]. Lifespan psychology is an effort to understand development from the perspective of multiple disciplines in an integrated fashion [22]. It recognizes biological and cultural influences on development, but lacks a coherent model of the functional structure of human beings. Development is a complex adaptive process that cannot be specified by linear stage models, such as those of Freud, Erikson, Piaget, or Kohlberg. Human consciousness is holographic, and so its development must be a quantum-like adaptive process, much like the development of fractals [7].

Unfortunately, there is no consensus at present regarding the functional structure [23] or the developmental paths [22,24] of basic human characteristics, such as personality, emotionality, or cognition. Likewise, there is no consensus regarding the structure of psychopathology and other dysfunctional human characteristics. Most psychiatrists recognize that current categorical systems of classification are seriously flawed, but do not know with what to replace them. It is impossible to build an adequate science of health and well-being without understanding how normal adaptive functions are organized [7,25]. Hence a general model of the functional structure of human consciousness is imperative for understanding well-functioning and ill-functioning human beings.

Darwin's anniversary is a propitious time for the development of a general model of the functional structure of human beings. As Darwin recognized, human evolutionary history provides a solid scientific basis for describing the functional structure of consciousness. As he asked (C Notebook, p. 166, around May 1838), ‘Why is thought being a secretion of the brain, more wonderful than gravity a property of matter? It is our arrogance…our admiration of ourselves’ [26].

Methods

Several recent scientific advances have now converged to permit the preliminary description of a general model of human consciousness that can be tested and refined by subsequent research. First, cladistic analysis is used to identify the succession of ancestors leading to human beings based on molecular phylogenetics [27,28]. A clade is a group of organisms that share a common ancestor. Recent advances in molecular phylogenetics have clarified the succession of ancestors leading to human beings from the earliest life forms [29–33].

The functional capacities that emerge along this line of ancestors are described. The ecological context in which each cladogenesis occurred is described to understand the influences on evolution, as illustrated by the co-evolution of angiosperms and the ancestors of primates [32,34,35] and the importance of hunting animals for meat for increasing body and brain size of early Homo [36]. These observations illustrate the shifting balance of evolution as a complex adaptive system [37].

Comparative neuroanatomy is reviewed to identify the brain structures and networks that emerged coincident with the emergent brain functions. Detailed neuroanatomical studies have been conducted that were guided by cladistic analysis to focus on the ancestral line leading to human beings [38,39]. Other studies identify which clades have specific brain structures and networks, such as mirror neurons [40] or von Economo neurons [8].

Results

What evolutionary transitions led to humans?

Evolution is a complex adaptive process in which multiple genetic and environmental events are constantly interacting, shifting the balance of reproductive fitness from situation to situation and time to time [37]. As a result, genetic influences on personality and other human characteristics show extensive gene–gene and gene–environmental interactions [7,41,42]. Consequently, it is important to follow the thread of evolution leading to humans as it unfolded in response to the unrepeatable ecological complexities of the past.

The timeline of major transitions in brain system structure and function in human evolution is summarized in Tables 2–4. The transitions represent the emergence of clades, usually with some living descendants of the common ancestor shared with human beings. All life forms share DNA as the mechanism of genetic inheritance, going back to the emergence of the first life forms on earth 4 billion years ago. The ancestral lineage leading to humans includes the first eukaryotes, craniates, and amniotes, thereby leading to the common ancestor shared by reptiles and mammals. Among mammals, the line continues from the earliest non-placental mammals to tree shrews and then the proto-primates called plesiadapiforms. The tree shrews were small, nocturnal, placental mammals who spent little time in maternal care. Their young developed quickly and they are free to spend most of their time having sex and eating. The pen-tailed tree shrew, Ptilocerus iowii, is found in Indonesia, Malaysia, and Thailand. It is thought to be the closest living example of the common ancestor of primates [33]. It consumes fermented nectar regularly with 3.8% alcohol without getting excessively intoxicated [59].

Table 2.

Timeline of major transitions in nervous system structure and function in human evolution: cells to reptiles

Time period (mya)	Animal clade no.	Animal group	Functional change [Reference]	Living examples
15 000	–	–	Origin of universe	Big Bang
4540	–	–	Formation of Earth	Planet Earth
4000	–	–	Prokaryotic cellular life with DNA	Archaea, Bacteria
900 Vendian	0	Choanoflagellates	Sperm-like unicellular ancestor of eukaryotes, including animals, plants, fungi [31]	Monosiga
505 Cambrian	1	Craniates	Jawless fish without vertebrae; Bilaterally symmetrical chordates with heads and neural crests [43]	Hagfish
480 Ordovician	2	Vertebrates	Vertebrae, taste buds, genome duplicated [44]	Lampreys, bony fish, amphibia
315 Carboniferous	3	Amniotes	Adapted to reproducing and living on land [45]	Reptiles

Table 3.

Timeline of major transitions in nervous system structure and function in human evolution: mammals to apes

Time period (mya)	Animal clade no.	Ancestral group	Functional change [Reference]	Living examples
220 Permian	4	Non-placental mammals	Neocortical control of sexuality, warm, milk-feeding [27]	Monotremes, marsupials
125–65 Cretaceous	5	Placental mammals	Live births, minimal maternal care, pleasure-moderating [33]	Pen-tailed tree shrew
65–55 Palaeocene	6	Plesiadapiforms	Primate-like with more maternal care and varied diet [32,35,46,47]	(fossil only)
47 Eocene	7	Prosimian primates	Solitary nocturnal foragers, agile with forward-facing eyes[48]	Lemurs, lorises, tarsiers
40 Oligocene	8	Simian primates	Diurnal and social with neocortical control of emotions [40,49,50,51]	Monkeys, gibbons
15 Miocene	9	Great apes	Neocortical control of sociality and imitative learning [51]	Orangutans, gorillas, chimps

Table 4.

Timeline of major transitions in nervous system structure and function in human evolution: early Homo to modern Homo sapiens

Time period (mya)	Animal clade no.	Animal group	Functional change [Reference]	Living examples
2.5–1.6 Pliocene–Pleistocene	9/10?	Homo habilis	‘Handy’ tool-maker, australopith-like size and proportions, brain approx. 650 cm³ [52–54]	(Fossil only)
1.8–0.3 Pleistocene (Ice Age)	10	Homo erectus	Larger body and brain, prominent parietal area for language, migrated to Eurasia, brain approx. 880 cm³ [55–57]	(Fossil only)
0.35–0.04 Palaeolithic	11	Neanderthals, ancient Homo sapiens	Larger brain volume than modern Homo, possibly interbred with other Homo [53]	(Fossil only)
0.2–present	12	Homo sapiens sapiens	Self-aware with art, science, spirituality [55,58]	Modern Homo

The primate-like mammals called Plesiadapiforms, such as Carpolestes simpsoni, are known from the late Palaeocene epoch of Wyoming. They had a grasping foot like primates, including an opposable toe and a nail rather than a claw. It could probably grasp with its hands as well. As a result, it was well-adapted to move in the terminal branches of fruit-bearing trees that flourished at that time [32,35].

Among primates, the line continues through ancestors in common with prosimians, simians, then great apes. Prosimians are typically nocturnal and solitary foragers, whereas simians (monkeys and apes) are typically diurnal and active in social groups most of the time [48,49,60]. The great apes show warm emotional expressions and affectivity, including ventral hugging, in addition to more complex imitation learning, more flexible dominance hierarchies, and communication with concrete symbols such as sign language [49,61].

Among the hominoids, the line continues through ancestors of Australopiths to early Homo. The details of the lineage are intensively debated, but the functional and structural changes are fairly clear even when the precise transitional form remains uncertain. Australopithecines had well-developed erect bipedal walking, as was shown in the fossilized footprints preserved at Laetoli in Africa,. The footprints preserve evidence of one holding hands with a younger child while a second adult followed, stepping precisely in the tracks of the first adult [55]. Homo habilis is classified as the earliest human species on the basis of an average brain volume of >600 cm³ and development of brain regions that support language functions in modern humans. Some argue, however, that it should be grouped with Australopiths, not Homo, because its body was similar to that of an Australopith [52]. It is clear that between Australopiths and Homo erectus there was a revolutionary increase in the size of the brain and body of human beings [62]. This increase required a new way of obtaining nutrients to support the greater energy consumption of a larger body and brain.

What were the circumstances of adaptive change?

Every transition in the ancestral lineage leading to modern humans involved adapting to a novel ecological challenge. Some of the major adaptive forces playing out in human evolution are summarized in Table 5. Every transition was associated with different challenges that the extant species had to adapt to or face extinction. Mass extinctions occurred often, shifting the balance of dominance from one life form to another [63,75,76]. Animals co-evolved with plants, just as both plants and animals had to adapt to the changing climate and tectonic shifts.

Table 5.

Geologic timeline of coincident events in human evolution

Time period (mya)	Emerging ancestral group	Climatic and tectonic events	Bacterial and plant events	Animal competition/extinction events [References]
650–543 Vendian	0 Choanoflagellates	Before Vendian, methane and other gases fill atmosphere, complex chemicals form in oceans.	Cyanobacteria produce oxygen as waste product, creating an oxidizing atmosphere. Plants form by symbiosis of cyanobacteria to form chloroblasts excreting oxygen, and animals cells by symbiosis with mitochondria consuming oxygen.	RNA and DNA formed in chemical soup of oceans. Increasing oxygen level retards anaerobic life and stimulates aerobic life. Bacteria, archaea, and simple soft-bodied organisms live entirely in ocean. First fossil animals appear [31,63]. Mass extinction of soft-bodied biota at end of Vendian allowed diversification of fauna with shells.
543–490 Cambrian	1 Craniates	Oxygen accumulated enough by end of Vendian and early Cambrian to form ozone layer blocking ultraviolet radiation and permitting land to be colonized. Mass extinctions may have been related to glacial cooling or oxygen depletion in the oceans.	Primitive algae and seaweeds present. Primitive plants evolve from green algae and move onto land. Fungi also may have aided colonization of land by symbiosis.	Cambrian explosion of multicellular life forms. Most major groups of animals appear in fossil records. Trilobites are the dominant animals initially, but were reduced by mass extinctions [63].
490–354 Ordovician–Devonian	2 Vertebrate	Climate is variable. Most land was in southern supercontinent Gondwana. When it shifted to South Pole, massive glaciers formed and sealevel dropped, possibly leading to mass extinctions in Late Ordovician.	True plants emerge in water and on land, and dense forests emerge during the Devonian period. There were arid periods during the early Devonian, followed by more temperate conditions allowing more plant growth.	Rapid evolution of fish in water and wingless insects on land. Ordovician and Devonian extinctions eliminate most species, leaving sharks as the top predators in oceans.
354–290 Carboniferous	3 Amniotes	Climate was mostly warm, humid and tropical initially. It then cooled with glaciations in south in Gondwana. Sealevels fell all over the world due to southern glaciation. Oxygen levels in atmosphere around 35% (compared to 21% today). The large continent Pangaea begins to form.	Great forests of fern-like seeding plants flourish and dominate land, herbivores grow large to accommodate large guts needed to digest nutrient-poor food. Extensive plant life does not decay and forms future coal deposits.	Sharks are top predators in ocean, tetrapods move to land, and first amniotes emerge. The amniote egg protects the developing fetus from desiccation on land, and reptiles thrive.
290–144 Permian–Jurassic	4 Non-placental mammals	Initially there was an ice age followed by warming. Much of land was combined in one large continent of Pangaea, much of which was arid. There were alternating warming and cooling periods.	Gymnosperm plants flourish, replacing fern forests. Conifers appear and spread inland and up mountains, and later diversify. Southern hemisphere dominated by large seeding ferns	95% of species go extinct at end of Permian, especially marine invertebrates. This allows survivors to diversify. Reptiles take over from amphibians on land. Mammal-like reptiles lose dominance, and large plant-eating dinosaurs dominate Jurassic. Mammals emerge approx. same time as dinosaurs and survive as small, prolific nocturnal animals feeding on insects and avoiding reptiles.
144–65 Cretaceous	5 Placental mammals	Pangaea is now split up in separate continents. Generally a warm climate with high sealevels. Meteorite impact in Yucatan occluded sunlight for long period at 65.5 mya, leading to extinction of dinosaurs except for ancestors of birds.	Initially angiosperm flowering plants are abundant, with pollen spread by insects. Then lack of sunlight killed much plant life and large herbivores.	Extinction event eradicates more than half of all animals, including nearly all dinosaurs [64]. Archaic mammals rapidly diversify and become dominant vertebrates.
65–55 Palaeocene epoch	6 Primate-like mammals	Initially climate was temperate, cooler and drier than the Cretaceous. Then it began to warm as Eocene approached.	Angiosperms flourish producing fruit in terminal branches of trees, stimulating agility and varied diet.	Primate-like nocturnal mammals become agile in grasping and feeding on fruits and insects in trees [34,35,46].
55–34 Eocene	7 Prosimians	Global warm and moist climate develops from pole to pole. Hothouse effect on plants and animals. Australia separates from Antarctica and current changes led to global cooling in later Eocene.	Tropical rainforests spread from pole to pole, displacing other plants. Primates appear in Asia and America.	Hothouse effect favoured smaller mammals like prosimians with relatively large surface areas [65].
34–24 Oligocene	8 Simians	Climate gets colder for 7 million years, making daytime activity desirable and competition for food greater.	Grasses evolve among the angiosperms, grasslands begin to dominate, tropical broad-leaf forests regress to equatorial belt. Primates appear in Africa for first time [63].	Monkeys have higher metabolic rates than prosimians, allowing for larger bodies and brains, stimulating shift to diurnal and social activities [66]. Diurnal elephants with trunks and raptors such as hawks also appear.
24–5.3 Miocene	9 Great apes	Climate is initially warmer than Oligocene and then becomes cooler and drier, facilitating the expansion of grasslands in continental interiors. Asia and Africa have contact and animals migrate.	Wetland forests decline, temperate grasses using C4 photosynthesis expand that assimilate CO₂ efficiently but are richer in silica	Silica-rich grasses cause worldwide extinction of most large herbivores so grasslands safer for apes [67,68].
5.3–1.8 Pliocene	9 Australopiths	Climates continue to get cooler and drier, similar to modern seasonally variable climates. Glaciation begins toward end of period.	Cooling and drying spurs spread of temperate climate grasslands and open savannas with further regression of wetland forests. Australopiths but not most other primates adapt to eating grasses or opportunistic scavenging meat of grazing animals.	Distribution of primates restricted by forests retreating. Wide expanses of open grassland provide advantage for emergent bipedal walking and opportunistically consuming grasses or meat of grazing animals [69–71].
1.8 −0.10 Pleistocene	10/11 Early Homo habilis to ancient Homo sapiens	Great Ice Age, recurrent glaciation, in 30% of world at its peak. Temperate open grasslands remain in some regions.	Glaciation caused retreat of most plant and animal life to warmer areas for food supply. Wild plants did not provide adequate energy source for large body and brains of Homo. Homo teeth and cranial structures adapted for omnivorous diet with substantial reliance on meat.	Large land mammals such as mammoths, sabre-toothed cats, bison, and birds are abundant. Human diet required meat protein, fat, and essential nutrients from hunting and fishing to support larger body and brain size [36,72,73]. Extinction of most large mammals, allowed humans and others to spread northward out of Africa if capable. By end of Pleistocene, humans have spread through most of the world.
0.10–Holocene epoch	12 Modern Homo sapiens	Ice age ended, warm habitable zones extend with fairly stable climates	Agriculture is introduced, sharply shifting available foods for diet. Plant life has not changed much during this relatively stable period until recently.	Agriculture and husbandry permitted human population expansion with more stable domesticated food sources [72,74]. Many non-domesticated species are threatened by human impact.

The adaptive challenge helps to recognize the functional shifts that occurred at each transition leading to modern human beings. Both mammals and dinosaurs emerged around the same time during the Jurassic period. The earliest mammals were small nocturnal animals that ate insects and avoided the large plant-eating dinosaurs. Then 65.5 million years ago a large asteroid struck the Yucatan and the resulting dust is thought to have occluded sunlight for so long that the herbivorous dinosaurs were extinguished, except for the ancestors of birds [63,64].

The extinction of the dinosaurs allowed mammals to diversify and they rapidly became the dominant land animals. The emergence of fruit-bearing trees provided the circumstance in which sexually prolific mammals were selected for greater agility, taste discrimination, and maternal care [34,35]. Extant prosimians are like living fossils of these Palaeocene ancestors of human beings except that they are true primates with forward-directed eyes. The prosimians thrived as nocturnal solitary foragers during most of the hothouse period of the Eocene, in which the earth was covered with tropical forest between 55 and 45 million years ago.

The global climate began to cool during the late Eocene. Vegetation changed in response to climate. As competition for resources increased, diurnal animals emerged, including elephants with trunks, diurnal raptors such as eagles and hawks, and also the first simians. Simians are typically diurnal and social, which gave them advantages in energy consumption. Simians have a higher rate of oxygen consumption than prosimians [66], so being active during the day and foraging in social groups confers an energy advantage that supported larger bodies and brains. Some prosimians did later adapt to diurnal living, but only one group of simians, the owl monkey, reverted to nocturnal existence.

When grasslands become widespread, replacing forest, most large herbivores became extinct. In contrast, Australopiths adapted well to the grasslands. They walked upright and also consumed grass or the meat of grass-grazers, giving them an advantage over apes that did not adapt for grass consumption [69–71].

Early humans developed larger bodies and brains, which required a means of richer nutrition. Hunting, fishing, tool-making, and use of fire all contributed to the supplementation of their high-fibre diets by early humans with meat for adequate nutrition during the Palaeolithic Ice Age [36,72]. They had the intelligence to migrate out of Africa and colonize areas throughout most of the world during the Pleistocene epoch. The end of the Ice Age made the development of agriculture feasible, providing a more reliable source of nutrition for modern Homo sapiens.

What brain structures emerged coincident with the functional changes?

The transitions described in Tables 2–5 can be summarized as the emergence of specific aspects of consciousness, as detailed in Table 6. The five major transitions are described more briefly in Table 7 because they are the crux of each functional development. In reptiles central regulation of brain functions is organized in the hypothalamus. Sensory information is first processed in the basal forebrain of before being relayed to the thalamus and dorsal cortex of reptiles. The dorsal cortex and thalamus of reptiles receive sensory input, but do not reciprocate with output that could modulate the hypothalamus [83]. A multi-layered neocortex first emerges in early mammals, and there is a progression of five transitions whereby the neocortex takes control of central regulatory functions from the hypothalamus. In early mammals and tree shrews, the major neocortical function is voluntary control of copulation, which is reflexive in reptiles [84]. Early mammals noted for their prolific sexuality, such as rodents and rabbits, are a sister clade of tree shrews [28]. Primary somatosensory cortex is clearly developed in early mammals and tree shrews (clades 6/7), but there is little or no differentiation of sensory neocortex from motor neocortex [38,39].

Table 6.

Evolution of major brain functions in human evolution

Clade	Emergent functions	Emergent structures
1 Craniates	Animals with skulls, all associated with emergence of the neural crest for development of central nervous system. Also all have ectodermal placodes for development of paired organs for smell, hearing, and vision in the head.	Neural crest derivatives: skull, brain with five components and cranial nerves 1–10 (except for eye muscle nerves 3,4,6, which may have been secondarily lost by hagfish). All have peripheral nervous systems, endocrine tissues, in addition to paired organs for smell, hearing and vision in head.
2 Vertebrates	Fish and amphibia show well-developed associative conditioning. Whole genome duplicated. Amphibia still reproduce in water.	Cranial nerves for eyes (3,4,6 are present typically [43].
3 Amniotes	Adaptations for tetrapods to live and reproduce on land, breathing oxygen, and amnion to protect developing fetus.	Reptile brain is centrally regulated by hypothalamus without thalamocortical feedback to or control of hypothalamus. Dorsal cortex is single layer of pyramidal neurons.
4 Non-placental mammals	All mammals are warm-blooded, have skin with hair and glands, including milk-producing glands to feed young. Early mammals are typically sexually prolific, a trait shared with rabbits and others.	Neocortex emerges with six layers and allows cortical control of sexual copulation. All special senses represented neocortically, but most of neocortex processes touch with no separate motor areas.
5 Tree shrews	Specialized genital openings and bear live young that require little maternal care. Can show restraint in sexual activity and eating, e.g. no excess leading to intoxication when consuming fermented fruits.	Somatosensory, motor, and premotor areas differentiated in neocortex. Approx. 20 distinct cortical regions compared to >200 in human beings [38].
6 Protoprimates	Enhanced physical agility to grasp food and maternal care of young. Eyes still laterally directed.	(Fossils only: functions suggest similar to prosimians except eyes not forward-directed)
7 Prosimians	Nocturnal solitary foragers with skill in finding and selecting food. Brain size varies with foraging complexity, flexibility of diet and activity patterns, not social variables. Extensive maternal care provided to young. Teeth are distinctive for highly variable diets of primates.	Taste is processed in primary gustatory cortex prior to hypothalamus and amygdala (frontal operculum and insula) [77]. Eye–hand coordination facilitated by greater topical ordering of inputs to nuclei for hand and foot and expansion of parietal association cortex. Ventromedial hypothalamus has many oxytocin receptors, allowing regulation of feeding behaviour in favour of reproductive role. Differentiation of DPIC supports awareness of the affective aspects of sensation [78].
8 Monkeys	Diurnal and social with increased metabolic rate able to support larger body and brain. Enduring social relationships, much time in social activities of large groups.	PFC (mainly orbital and medial PFC) expands and projects directly to hypothalamus, thalamus, septum, basal amygdala, and striatum. Mirror neuron system appears in monkeys, allowing mirroring of observed behaviours by neurons in speech motor area (BA 44 posterior inferior frontal gyrus), VPA, and IPL (BA 40) [40]. The VPA supports both action understanding and imitation, a precursor to language. In monkeys, affective information is also relayed to the middle insular cortex, which has extensive reciprocal connections with the amygdala and hypothalamus, so it is well-positioned for the regulation of sensuality.
9 Great apes	Highly social, warm emotional expression and affectivity, flexible dominance hierarchies, imitation learning. Australopiths developed skilled bipedal walking.	Somatosensory processing becomes serial and less parallel for greater depth of processing. Differentiation of parietal association cortex for integration of visual, auditory, and somatosensory information. Great apes and humans, and not other primates, have von Economo neurons that allow reciprocal connections of AIC and ACC. Mirror neurons are also present in great apes in Broca's area (BA 44) and IPL. Also in great apes there is differentiation of the AIC for enhanced emotional awareness, which supports the communication of social emotions in great apes [8].
10 Homo habilis	Precision grip for making stone tools, reduced size of post-canine teeth, fishing, and hunting in groups for meat. Enlarged brain size but body similar to australopiths.	Hemispheric asymmetry is observed in Homo and some Australopiths, particularly around the lateral sulcus in regions related to language [55,79]. Fossils only but enlarged frontal opercular area and IPL, suggesting emergence of language and default brain network.
11 Ancient Homo sapiens	Creation of aesthetically refined tools, language, and culture with widespread migration in social groups.	Fossils only but findings indicate language ability with prominent development of IPL (BA 39/40) and emergence of brain default network that supports daydreaming, holistic attention, and subconscious problem-solving. Default brain network includes subsystems in the ventral medial PFC, dorsal medial PFC, IPL, posterior cingulate/retrosplenial cortex, and hippocampal formation and related entorhinal and parahippocampal cortex [9,10].
12 Modern Homo sapiens sapiens	Self-aware consciousness with art, science, and spirituality	Autonoetic awareness depends on a distributed frontotemporoparietal network with encoding via hippocampus [12]. The same brain regions are most recently differentiated in evolution and are late in myelinating. The whole neocortex becomes a functional whole by linking all association areas through projections of visual system

ACC, anterior cingulate cortex; AIC anterior insular cortex; BA, Brodmann area; DPIC, dorsal posterior insular cortex; IPL parietal lobule; PFC, prefrontal cortex; VPC, ventral premotor cortex.

Table 7.

Cladistic staging of evolution of the functional components of self-aware consciousness in human beings: five basic stages

Clades	Emergent brain network	Major function (Voluntary)	Component functions†
4/5 Early mammals	Somatosensory neocortex regulating sexuality	Copulation	Sex drive Longing (Pleasure) (Eroticism) (Tenderness)
6/7 Early primates	Differentiation of sensory and motor neocortex; neocortex regulating taste	Materiality	Rhythmicity Agility Sensation (Movement) (Transformation)
8/9 Simians	Prefrontal cortex regulating limbic system [80]; von Economo neurons in AIC/ACC; mirror neuron system	Affectivity	Fulfilment Friendship Emotional awareness Romanticism (Devotion)
10/11 Early Homo	Auditory association cortex regulates cross-modal symbolism; brain default network regulates attention and daydreaming; frontoparietal perceptual–motor praxis system permits refined tool-making [81,82]	Symbolism	Taboo Allegory Empathy Discernment Aesthetics
12 Modern Homo sapiens	Autonoetic system unifying frontoparietotemporal association areas (linked by visual projection system) [6,12]	Unity	Harmony Sublimation Adoration Contemplation Universal awareness

ACC, anterior cingulate cortex; AIC, anterior insular cortex.

†Functions in parenthesis are found in human beings but not in original ancestor in which major function came under neocortical regulation.

In proto-primates and prosimians there is functional development of motor agility, better discrimination of the taste of a varied diet, more maternal care of young, and more time spent in grooming and related form of assuagement. These functions involve regulation of material things such as food and activities of daily living. Unlike rodents, in primates there is no direct path from the brainstem taste areas such as the nucleus of the solitary tract to the hypothalamus and amygdala. Information about taste in primates, in contrast, reaches the amygdala and orbitofrontal cortex from the primary taste cortex, which is in the frontal operculum and insula [77].

Prosimians have well-differentiated sensory and motor neocortical areas, in contrast to tree shrews. Detailed studies of galagos indicated several changes in brain structure that support enhanced motor agility with advanced grasping and leaping adaptations [38,39]. The findings include greater topographical ordering of sensory input for the hands and feet, premotor and supplementary motor areas, at least two motor areas in the cingulate cortex, and feedback circuits between prefrontal cortex, premotor cortex, and primary motor cortex. In addition, prosimians have an enlarged posterior parietal cortex for processing visual, auditory, and somatosensory information to form and relay instructions about hand and eye movements to premotor areas.

In simians there is emergence of affectivity with patterns of emotional expression, attachment, and friendship that are similar to human affectivity as noted by Darwin [14] and Bowlby [49,61,85]. Related brain changes include the development of prefrontal cortex for regulation of emotional functions [80], a distinctive system for interoceptive processing of sensual aspects of touch [8,78,86,87], and the emergence of the mirror neuron system on frontal and parietal cortical areas [40].

In early Homo there is emergence of symbolism, including capacities for taboo, allegory, language, empathy, and discernment [79]. Symbolism builds on the abilities needed for cooperative group foraging in simians [79]. Homo erectus showed aesthetic appreciation in the making of refined tools in their Acheulian culture [81,82]. These symbolic functions depend on processing in the inferior parietal cortex, which is a convergence area for touch, hearing, and vision, allowing cross-modal transformations important for language and other forms of symbolism [55,79,88]. The angular gyrus in particular has an important role in the comprehension of metaphor and allegory [89]. Symbolic activity enhances the capacity of the brain default network, which allows first-person perspective taking and daydreaming, as when a person is letting his or her mind freely wander about inner thoughts and feelings [9,10].

Finally, in modern human beings there is self-aware perception of a sense of unity, manifest by emergent capacities for harmony, sublimation, spiritual adoration, and contemplation [7]. These abilities give modern human beings their potential in art, science, and spirituality, sometimes leading to transcendent joy, oceanic feelings or even cosmic consciousness [7,58]. Such integrated awareness is supported by autonoetic system of learning and memory [6]. Such self-aware consciousness allows a person to travel in space and time in their recollection of episodic events. Such autobiographical thinking involves a distributed frontoparietotemporal network [12]. Essentially the visual projection system connects all tertiary association cortices so that the brain can function as a coherent whole.

Discussion

I have sketched the ancestral lineage of human beings and identified five major transitions in functional capacity: copulation, materiality, affectivity, symbolism, and self-awareness of unity. These five functions are core abilities for the regulation of what I have elsewhere called the five planes of being: sexuality, materiality, emotionality, intellectuality, and spirituality [7]. A plane can refer to a level of existence, thought, or development. The term ‘plane’ is particularly appropriate for describing these components of self-aware consciousness. It is appropriate because a plane refers to a particular level of existence, perhaps sexual, material, emotional, and so on. It also refers to particular kinds of thoughts in self-aware consciousness. Finally, it refers to components of consciousness that are inseparably connected and dynamically developing, even when its manifestation is latent.

My last statement about latent development is important, even though it may seem obscure at first. It is obscure because throughout this brief sketch of evolutionary development I have traced a specific manifest line of development. I have talked only about emergent functions, but latent processes are expected to be already under development before they are overtly manifested. Remember that evolution and development are complex adaptive systems within a whole in which everything is interconnected and interdependent. Language did not develop wholly in one abrupt step [55,79,90]. Functional precursors that are developed in response to one challenge are often co-opted for another use in different situations.

Each plane of being involves neocortical functions organized around one of the five special senses. The interactions among these five planes gives rise to a 5 × matrix of subplanes, which are functions that coarsely describe the focus of neocortical regulation (Table 8). I have deliberately focused only on the five functions in bold along the diagonal of Table 7. These diagonal components are the core functions upon which the others are built. For example, the material subplane of sexuality (satisfaction, such as assuagement by grooming) depends on the differentiation of sensory and motor functions underlying materiality. Satisfaction and enhanced maternal care (a facet of reproduction) emerge together with materiality in protoprimates and prosimians. Likewise, the emotional subplane of sexuality (sensuality) depends on emotional awareness (affectivity), and they emerge together in simians.

Table 8.

Matrix of functional components of consciousness and the animal clade in which they are first manifest†

Subplane	Sexual plane	Material plane	Emotional plane	Intellectual plane	Spiritual plane
Spiritual	Union 7	Giving of yourself 7	Exaltation 7	Philosophy 7	Unity 7
Intellect	Communion 5	Expression 5	Exhortation 5	Symbolism 5	Teaching 7
Emotional	Sensuality 4	Sensitivity 4	Affectivity 4	Symbiosis 5	Humanism 7
Material	Satisfaction 3	Materiality 3	Resurgence 4	Artistic creation 5	Incarnation 7
Sexual	Copulation 2	Reproduction 3	Intimacy 4	Suggestivity 5	Temperance 7

†Animal groups in which functional component is first manifest: 1, reptiles; 2, early mammals and tree shrews; 3, protoprimates and prosimians; 4, simians and Australopiths; 5, early Homo; 6, neanderthals and archaic Homo sapiens; 7, modern Homo sapiens sapiens.

Bolded text designates the crucial functions upon which the other functions are dependent.

Within each of the five planes of being, there are components of each plane that emerge in succession in the ancestral lineage leading to human beings. For example, in the sexual plane, copulation emerges in early mammals, satisfaction in protoprimates, sensuality in simians, and soon.

Each of these 25 neocortical functions regulates each of five basic motives or drives that can be measured as temperaments (harm avoidance, novelty seeking, reward dependence, persistence, plus coherence-seeking) or basic emotions like those described by Darwin and Ekman (fear, anger, disgust, surprise, and happiness/sadness) [14]. The resulting 5 × 5 × 5 matrix of human characteristics provides a general testable model of the functional structure of human consciousness that includes personality, physicality, emotionality, cognition, and spirituality in a unified developmental framework. Each of the components of this functional matrix can function either well or poorly, thereby providing the foundation for a positive science of well-being. I am pleased to introduce the evolutionary foundation of the science of well-being on the anniversary of Darwin's birth and his publication of The origin of species [91].

Footnotes

Acknowledgements

This work was supported by non-government funds from the Washington University Center for Psychobiology and the Anthropedia Foundation.

References

1. Hall

Lindzey

. Theories of personality. New York: John Wiley & Sons, 1978.

2. Maslow

. Higher and lower needs. J Psychol 1948; 25:433–436.

3. WHO. Mental health: new understanding, new hope. Geneva: World Health Organization, 2001.

4. Vaillant

Vaillant

. Natural history of male psychological health, XII: a 45-year study of predictors of successful aging at age 65. Am J Psychiatry 1990; 147:31–37.

5. Collins. Collins essential English dictionary. New York: Harper Collins, 2006.

6. Tulving

. Multiple memory systems and consciousness. Hum Neurobiol 1987; 6:67–80.

7. Cloninger

. Feeling good: the science of well-being. New York: Oxford University Press, 2004.

8. Craig

. How do you feel – now? The anterior insula and human awareness. Nat Rev Neurosci 2009; 10:59–70.

9. Buckner

Andrews-Hanna

Schacter

. The brain's default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci 2008; 1124:1–38.

10.

10. Raichle

MacLeod

Snyder

Powers

Gusnard

Shulman

. A default mode of brain function. Proc Natl Acad Sci USA 2001; 98:676–682.

11.

11. Gusnard

Akbudak

Shulman

Raichle

. Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proc Natl Acad Sci USA 2001; 98:4259–4264.

12.

12. Levine

. Autobiographical memory and the self in time: brain lesion effects, functional neuroanatomy, and lifespan development. Brain Cogn 2004; 55:54–68.

13.

13. Pribram

. Rethinking neural networks: quantum fields and biological data. Hillsdale, NY: Lawrence Erlbaum, 1993.

14.

14. Darwin

Ekman

Prodger

. The expression of the emotions in man and animals. London: Harpercollins Publishers, 1998.

15.

15. Chomsky

. Rules and representations. Behav Brain Sci 1980; 3:1–61.

16.

16. Chomsky

. Universals of human nature. Psychother Psychosom 2005; 74:263–268.

17.

17. Cloninger

. A systematic method for clinical description and classification of personality variants. A proposal. Arch Gen Psychiatry 1987; 44:573–588.

18.

18. Cloninger

Svrakic

Przybeck

. A psychobiological model of temperament and character. Arch Gen Psychiatry 1993; 50:975–990.

19.

19. Cloninger

. Completing the psychobiological architecture of human personality development: temperament, character, and coherence, Staudinger

Lindenberger

UER

, Understanding human development: dialogues with lifespan psychology. London: Kluwer Academic Publishers, 2003: 159–182.

20.

20. Cloninger

Svrakic

. Integrative psychobiological approach to psychiatric assessment and treatment. Psychiatry 1997; 60:120–141.

21.

21. Crain

. Theories of development: concept and applications. Englewood Cliffs, NJ: Prentice-Hall, 2000.

22.

22. Staudinger

Lindenberger

. Understanding human development: dialogues with lifespan psychology. London: Kluwer Academic Publishers, 2003.

23.

23. Cloninger

. Foreword. Lilienfeld

O’Donohue

Fowler

, Personality disorders: toward the DSM-V. Los Angeles: Sage Publications, 2007: vii–xvi.

24.

24. Bjorklund

. In search of a metatheory for cognitive development (or, Piaget is dead and I don't feel so good myself). Child Dev 1997; 68:144–148.

25.

25. Cloninger

. The science of well-being: an integrated approach to mental health and its disorders. World Psychiatry 2006; 5:71–76.

26.

26. Gruber

. Darwin on man, together with Darwin's early and unpublished notebooks. New York: EP Dutton, 1974.

27.

27. Murphy

Pringle

Crider

Springer

Miller

. Using genomic data to unravel the root of the placental mammal phylogeny. Genome Res 2007; 17:413–421.

28.

28. Murphy

Eizirik

Johnson

Zhang

Ryder

O’Brien

. Molecular phylogenetics and the origins of placental mammals. Nature 2001; 409:614–618.

29.

29. Smith

Grine

. Cladistic analysis of early Homo crania from Swartkrans and Sterkfontein, South Africa. J Hum Evol 2008; 54:684–704.

30.

30. Hammer

Karafet

Rasanayagam

. Out of Africa and back again: nested cladistic analysis of human Y chromosome variation. Mol Biol Evol 1998; 15:427–441.

31.

31. Schierwater

Eitel

Jakob

. Concatenated analysis sheds light on early metazoan evolution and fuels a modern ‘urmetazoon’ hypothesis. PLoS Biol 2009; 7:e20.

32.

32. Bloch

Silcox

Boyer

Sargis

. New Paleocene skeletons and the relationship of plesiadapiforms to crown-clade primates. Proc Natl Acad Sci USA 2007; 104:1159–1164.

33.

33. Janecka

Miller

Pringle

. Molecular and genomic data identify the closest living relative of primates. Science 2007; 318:792–794.

34.

34. Sussman

. Primate origins and the evolution of angiosperms. Am J Primatol 1991; 23:209–223.

35.

35. Sargis

. Paleontology. Primate origins nailed. Science 2002; 298:1564–1565.

36.

36. Eaton

Eaton

Konner

. Paleolithic nutrition revisited: a twelve-year retrospective on its nature and implications. Eur J Clin Nutr 1997; 51:207–216.

37.

37. Wright

. The shifting balance theory and macroevolution. Annu Rev Genet 1982; 16:1–19.

38.

38. Kaas

, The evolution of the complex sensory and motor systems of the human brain. Brain Res Bull 2008; 75:384–390.

39.

39. Kaas

. Evolution of the neocortex. Curr Biol 2006; 16:R910–R914.

40.

40. Rizzolatti

Craighero

. The mirror-neuron system. Annu Rev Neurosci 2004; 27:169–192.

41.

41. Keltikangas-Jarvinen

Raikkonen

Ekelund

Peltonen

. Nature and nurture in novelty seeking. Mol Psychiatry 2004; 9:308–311.

42.

42. Keltikangas-Jarvinen

Pulkki-Raback

Elovainio

Raitakari

Viikari

Lehtimaki

. DRD2 C32806T modifies the effect of child-rearing environment on adulthood novelty seeking. Am J Med Genet B Neuropsychiatr Genet 2009; 150B:389–394.

43.

43. Janvier

. Craniata: animals with skulls. The Tree of Life Web Project. University of Arizona College of Agriculture and Life Sciences and University of Arizona Library, 1997. Available from URL: http://tolweb.org/.

44.

44. Shubin

. Your inner fish: a journey into the 3.5-billion-year history of the human body. New York: Pantheon, 2008.

45.

45. MacLean

. Evolutionary psychiatry and the triune brain. Psychol Med 1985; 15:219–221.

46.

46. Radhakrishna

. From Purgatorius ceratops to Homo sapiens: primate evolutionary history. Resonance 2006; 11:51–60.

47.

47. Clemens

. Purgatorius, an early paromomyid primate (Mammalia). Science 1974; 184:903–905.

48.

48. Sussman

. Primate ecology and social structure, vol. 1: lorises, lemurs and tarsiers. Needham Heights, MA: Pearson Custom Publishing, 2003.

49.

49. Sussman

Chapman

. The origins and nature of sociality. New York: Aldine de Gruyter, 2004.

50.

50. Bekoff

. The emotional lives of animals. Novato, CA: New World Library, 2007.

51.

51. Goodman

. The genomic record of humankind's evolutionary roots. Am J Hum Genet 1999; 64:31–39.

52.

52. Wood

Collard

. The human genus. Science 1999; 284:65–71.

53.

53. Lee

Wolpoff

. Habiline variation: a new approach using STET. Theory Biosci 2005; 124:25–40.

54.

54. Asfaw

White

Lovejoy

Latimer

Simpson

Suwa

. Australopithecus garhi: a new species of early hominid from Ethiopia. Science 1999; 284:629–635.

55.

55. Eccles

. Evolution of the brain: creation of the self. London: Routledge, 1989.

56.

56. Hawks

Hunley

Lee

S-H

Wolpoff

. Population bottlenecks and Pleistocene human evolution. Mol Biol Evol 2000; 17:2–22.

57.

57. Lewin

. Principles of human evolution. Malden, MA: Blackwell Science, 1993.

58.

58. Mithen

. The prehistory of the mind: the cognitive origins of art, religion and science. London: Thames and Hudson, 1996.

59.

59. Wiens

Zitzmann

Lachance

. Chronic intake of fermented floral nectar by wild treeshrews. Proc Natl Acad Sci USA 2008; 105:10 426–10 431.

60.

60. Sussman

Andrianasolondraibe

Soma

Ichino

. Social behavior and aggression among ringtailed lemurs. Folia Primatol (Basel) 2003; 74:168–172.

61.

61. Preston

De Waal

. The communication of emotions and the possibility of empathy in animals. Post

, Altruism and altruistic love. New York: Oxford University Press, 2002: 284–308.

62.

62. Hawks

Hunley

Lee

Wolpoff

. Population bottlenecks and Pleistocene human evolution. Mol Biol Evol 2000; 17:2–22.

63.

63. UCMP. University of California Museum of Paleontology Geology Wing. Berkeley, CA: University of California at Berkeley, 2009.

64.

64. Bryant

Clemens

Hutchison

. Cretaceous–Tertiary dinosaur extinction. Science 1986; 234:1172–1173.

65.

65. Clemens

. Eocene and earlier deposits. Science 1982; 215:962–964.

66.

66. Armstrong

. Relative brain size in monkeys and prosimians. Am J Phys Anthropol 2005; 66:263–273.

67.

67. Badgley

Barry

Morgan

. Ecological changes in Miocene mammalian record show impact of prolonged climatic forcing. Proc Natl Acad Sci USA 2008; 105:(12) 145–149.

68.

68. Cerling

Harris

MacFadden

. Global vegetation change through the Miocene/Pliocene boundary. Nature 1997; 389:153–158.

69.

69. Lee-Thorp

Sponheimer

Luyt

. Tracking changing environments using stable carbon isotopes in fossil tooth enamel: an example from the South African hominin sites. J Hum Evol 2007; 53:595–601.

70.

70. Sponheimer

Lee-Thorp

. Isotopic evidence for the diet of an early hominid, Australopithecus africanus. Science 1999; 283:368–370.

71.

71. Sponheimer

Lee-Thorp

. Differential resource utilization by extant great apes and australopithecines: towards solving the C4 conundrum. Comp Biochem Physiol A Mol Integr Physiol 2003; 136:27–34.

72.

72. Richards

. A brief review of the archaeological evidence for Palaeolithic and Neolithic subsistence. Eur J Clin Nutr 2002; 56:16 following1262.

73.

73. Stanford

. The hunting apes: meat eating and the origins of human behavior. Princeton, NJ: Princeton University Press, 2001.

74.

74. Richards

Schulting

Hedges

. Archaeology: sharp shift in diet at onset of Neolithic. Nature 2003; 425–366.

75.

75. Raup

Sepkoski

Jr . Mass extinctions in the marine fossil record. Science 1982; 215:1501–1503.

76.

76. Raup

Sepkoski

Stigler

. Mass extinctions in the fossil record. Science 1983; 219:1240–1241.

77.

77. Verhagen

Kadohisa

Rolls

. Primate insular/opercular taste cortex: neuronal representations of the viscosity, fat texture, grittiness, temperature, and taste of foods. J Neurophysiol 2004; 92:1685–1699.

78.

78. Craig

. Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cogn Sci 2005; 9:566–571.

79.

79. Deacon

. The symbolic species: the co-evolution of language and the brain. New York: WW Norton, 1997.

80.

80. Semendeferi

Armstrong

Schleicher

Zilles

Van Hoesen

. Prefrontal cortex in humans and apes: a comparative study of area 10. Am J Phys Anthropol 2001; 114:224–241.

81.

81. Stout

Toth

Schick

Chaminade

. Neural correlates of early stone age tool-making: technology, language, and cognition in human evolution. Philos Trans R Soc London B Biol Sci 2008; 363:1939–1949.

82.

82. Stout

Toth

Schick

Stout

Hutchins

. Stone tool-making and brain activation: PET studies. J Archaeol Sci 2000; 27:1215–1223.

83.

83. Nieuwenhuys

. The neocortex. An overview of its evolutionary development, structural organization and synaptology. Anat Embryol (Berl) 1994; 190:307–337.

84.

84. Wersinger

Baum

. Sexually dimorphic processing of somatosensory and chemosensory inputs to forebrain luteinizing hormone-releasing hormone neurons in mated ferrets. Endocrinology 1997; 138:1121–1129.

85.

Bowlby

Attachment, 2nd New York: Basic Books, 1983.

86.

86. Craig

. Human feelings: why are some more aware than others? Trends Cogn Sci 2004; 8:239–241.

87.

87. Craig

. Emotional moments across time: a possible neural basis for time perception in the anterior insula. Philos Trans R Soc Lond B Biol Sci 2009; 364:1933–1942.

88.

88. McGeoch

Brang

Ramachandran

. Apraxia, metaphor and mirror neurons. Med Hypotheses 2007; 69:1165–1168.

89.

89. Ramachandran

. A brief tour of consciousness. Upper Saddle River, NJ: Pi Press, 2005.

90.

90. Hauser

Chomsky

Fitch

. The faculty of language: what is it, who has it, and how did it evolve? Science 2002; 298:1569–1579.

91.

91. Darwin

. On the origin of species by means of natural selection, 1st London: Murray, 1859.