Cortical evolution and human behaviour

Brain Research Bulletin 74 (2007) 191–205

Review

Cortical evolution and human behaviour David Neill ∗ Department of Psychiatry, School of Neurology, Neurobiology and Psychiatry, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom Received 6 March 2007; received in revised form 6 June 2007; accepted 12 June 2007 Available online 5 July 2007

Abstract All mammals have complex behaviours but these are generally stereotyped in nature and lack the flexibility of human behaviour. Can the flexibility of human behaviour be understood as an evolutionary extension of previous behaviours or is it a departure? Theories pertaining to this question have a long history including, now refuted, theories on neoteny. This paper, using an evolutionary developmental biology approach, outlines some existing theories and suggests some novel ideas. Previous trends during brain evolution are determined by outlining the phylogeny and ontogeny of the six layered mammalian isocortex with particular reference to the primate lineage. These evolutionary trends are extrapolated to hominids to postulate the effect of increasingly large brains. The palaeoanthropological literature is cited to debate the nature and time course of behavioural change during hominid evolution. In particular, when was truly flexible behaviour first evident, and did it occur gradually or suddenly? The proposed isocortical and behavioural changes during hominid evolution are then equated to determine if modern human behaviour can be seen as part of a continuum. It is concluded that a continuation of previous trends in isocortical evolution maybe inadequate to explain human behavioural flexibility. Several possible departures from previous trends that would be compatible with increased behavioural flexibility are suggested. These mainly relate to evolutionary changes in the later stages of isocortical development and in particular during the activity-dependant phase when cortico-cortical connections are refined. © 2007 Elsevier Inc. All rights reserved. Keywords: Neuroplasticity; Hominids; Neanderthals; Critical period; Bird song; Alzheimer’s disease

Contents 1. 2. 3. 4. 5. 6. 7.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Phylogeny: evolution of the isocortex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ontogeny: ventricular zone to adult behaviour . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Primate lineage—mode and process of evolutionary change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The palaeoanthropological debate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cortical connections and evolutionary change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Correspondence address: Hebburn Health Centre, Campbell Park Road, Hebburn, Tyne and Wear NE31 2SP, United Kingdom. Tel.: +44 191 451 6626; fax: +44 191 451 6651. E-mail address: [email protected]. 0361-9230/$ – see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.brainresbull.2007.06.008

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1. Introduction The evolution of nerve cells was driven by the advantages of being able to communicate and respond to the environment. As nerve cell complexes have evolved into brains the internal representation of the environment has become increasingly complex [127,167]. Behavioural patterns that enhance the chance of survival have evolved. These behaviours are involved in the procreation of food, mating, defence and communication [16]. As brains have become larger these basic behavioural patterns have been maintained although they have increased in complexity. Part of the complexity relates to internal representation by the brain, via emotions, motivations and drives. Internal representation would seem to be most complex in humans, where thought processes direct behaviour. The use of thought process enables human behaviour to be flexible, that is we can self-reflect, search for meaning and purpose to life, set individual motivation and goals. This flexibility although of obvious evolutionary advantage also enables humans to choose not to have children and to commit suicide. Whether or not other advanced species have thought process similar to humans remains a mater of debate [8,54,62,63,72,109,110,152,175]. Even if they do this would be to a lesser extent than in humans as indicated by the lack of flexibility in their behaviour. All other species on our planet, apart from humans, seem to have stereotyped and predicable behavioural patterns. Dogs behave like other dogs and cats behave like other cats. It has been possible, with selective breeding, to select for certain aspects of behaviour, for example pack behaviour in hounds, herding behaviour in sheep dogs [169]. The overall behaviour pattern however remains that of a dog. Our nearest living relative the chimpanzee, although to a lesser degree than humans, has been shown to posses many advanced human-like cognitive functions [12,59,72,150,151,152,193]. Also isolated troops of chimpanzees have been shown to posses some differences in complex behavioural patterns [12,193]. However, compared to humans, their overall behavioural pattern still remains stereotyped and predictable. In the past it has been noted that immature animals posses more flexibility in their behaviour than adults. From this observation it had been postulated that human behaviour evolved through retention of this juvenile flexibility in adults [109,133,199]. This theory has however now been generally discarded as the proposed evolutionary mechanism, paedomorphosis or ‘neoteny’ [60], does not apply overall to the human brain [122,123]. The present review outlines evolution of the mammalian isocortex from its initial formation up to the isocortex of humans. An evolutionary developmental biology approach [65,141,154,155] is used to suggest possible evolutionary changes in developmental timing or sequence that could have lead to modern human behaviour. These developmental changes can operate on individual aspects of brain development and do not necessarily have to affect the brain as a whole. In this respect paedomorphic-like changes do not need to be excluded and can be considered along with other possibilities. The compatibility

of proposed evolutionary processes with the nature and time course of behavioural change during hominid evolution is taken into account. 2. Phylogeny: evolution of the isocortex A six layered isocortex is specific to mammals. It was derived after mammals diverged from reptiles but before the split of mammals into monotremes (prototherians), marsupials (metatherians) and placentals (eutherians) (Fig. 1). The superior part of the mammalian isocortex is considered to be homologous to the dorsal cortex of reptiles and the hyperpallium (wulst) in birds (Fig. 2). All of these ‘cortical’ areas are believed to have been derived from a simple cortex present in stem amniotes. Whether part of this simple cortex also gave rise to the inferior (temporal) isocortex in mammals and at least part of the dorsal ventral ridge in sauropsids remains a matter of debate. The alternative theory suggests that the dorsal ventral ridge is a specialization in sauropsids, derived from a subcortical pallial region in stem amniotes. This same subcortical pallial region is believed to have given rise to the pallial part of the claustroamygdaloid complex in mammals [1,4,142,159]. As there is no information available on the brain of premammalian therapsids it is difficult to conclude the exact derivation of the six layered isocortex. It would seem however that a six layered cortex with primary sensory areas and thalamocortical connections was present in primitive mammals. It has been predicted to have contained in the order of 15 functionally distinct areas including two visual areas (V1, V2), a primary auditory area (A1), primary and secondary somatosenory areas (S1, S2). A large bulk of the brain would have been devoted to processing olfactory information [87,101,102,104]. Throughout mammalian evolution there has been a trend for an increase in brain size, this generally has been accompanied by a proportionate increase in body size [67,82,118]. Any deviation from this general trend can be expressed as an encephalisation quotient (EQ). An EQ above 1 indicates that the brain for that species is disproportionately large compared to body size. High EQ’s as in apes and cetaceans are associated with higher levels of intelligence [112].

Fig. 1. 180–0.05: Date of origin in million of years ago. Therapsida: includes pre-mammalian reptiles in addition to mammals. 180 Prototheria (monotremes); 175 Metatheria (marsupials); 130 Eutheria (placentals); 85 Primates; 77 Strepsirrhines (lemuriformes); 37 Anthropoidea; 33 Platyrhines; 23 Catarhines; 8 common ancestor of human and chimpanzee; 4 Australopithecines; 2 H. habilis; 0.5 H. heidelbergensis; 0.25 H. neaderthalensis; 0.1 anatomically modern humans; 0.05 behaviourally modern humans. Data derived from [3,21,92,95,129,134,136,179,187].

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Fig. 2. DCx: dorsal cortex; HYPER: hyperpallium; ICx: isocortex; MESO: mesopallium; STR: striatum; NIDO: nidopallium; DVR: dorsal ventral ridge. The cerebral hemispheres can be divided into a superior part (pallium) and an inferior region (subpallium). In mammals the pallium consists of the isocortex, hippocampal formation and part of the claustroamygdaloid complex. The basal ganglia constitute a large part of the subpallium in mammals, birds and reptiles. In mammals part of the amygdalar complex in subpallial in origin. The reptilian dorsal cortex, the superior part of the mammalian isocortex and the hyperpallium in birds are all equivalent. The dorsal ventral ridge in reptiles and birds may equate with the inferior (temporal) isocortex in mammals. The mesopallium and nidopallium equate to the dorsal ventral ridge in birds. Although the hyperpallium and the nidopallium in birds are not layered they receive thalamic input similar to layer IV of the mammalian isocortex. The hyperpallium contains a primary somatosensory area (S1) and a primary visual area (V1). The nidopallium contains a visual region called the entopallium and the primary auditory area (A1) called field L. In a similar way that expansion of the isocortex in mammals had lead to increasingly complex behaviours, expansion of the pallium in birds may have served the same function. Corvids (crows, jays, ravens and jackdaws) and parrots have forebrains relatively the same size as apes and demonstrate equivalent levels of behavioural complexity [43,79]. In addition to complex social cognition, tool manufacture has been demonstrated in corvids [44] and language abilities including subtle phonological distinctions in parrots [146]. Behavioural innovations in birds may have been particularly related to enlargement of association regions in the nidopallium and mesopallium [80,105].

With this increasing brain size there has been a disproportionate increase in isocortex as compared to other brain components [24,48]. The human brain is 21,400 times larger than the brain of the smallest shrew, the isocortex being 142,000 times larger. That is, the isocortex has increase in size by a factor of 6.6 compared to the rest of the brain [48]. The increase in cortical size is due to expansion of the surface area with little change in thickness. In evolutionary terms the cortex has been extremely adaptable or put another way it has a high level of evolvability. This evolvability has allowed mammals to specialize in specific niches and it likely to have been responsible for many speciation events. The evolvability has occurred within a framework of developmental constraints which have retained the basic primary sensory systems of vision, audition and somatosensation. For example the blind mole rat, still retains a visual cortex and the retino–geniculo-cortical pathway [87,101,102,104]. Special senses have evolved by adaptation of existing systems such as the auditory system in echolocation [25]. Evolutionary adaptations in the cortex could involve changes in the size and organization of cortical fields, generation of new cortical fields and changes in pattern of connectivity [102,103]. Primary fields can expand independently, for example the striped possum with an elongated fourth digit has representation via an expanded somatosensory cortex [101]. The generation of new cortical fields has lead to increased specialization of brain areas. In advanced mammals specialized brain areas, referred to as association cortex, increasingly outnumber primary sensory areas. For example, the primary visual area (V1) occupies 3% of isocortex in humans, 6% in chimpanzees, 12% in macaques and 19% in the mouse lemur [170].

Increasing cortical size and specialization has also necessitated redesign in connectivity through purely mechanical constraints [83]. Long cortico-cortical connections between different functional areas take up more space than short local connections and have been proportionally reduced in larger brains. The trend has been to increase the number of local cortical areas containing short connections. As a result large brains contain individual areas of increased specialization. On a gross morphological level these specializations have resulted in the brain becoming increasingly asymmetrical [87]. Complex brain functions, such as face recognition, appear to involve cooperation between several specialized areas in different part of the brain [148,164,171]. Compared to primitive mammals, early members of the phylogenic superorder leading to humans had a larger isocortex with notable expansion in the number of visual areas in the occipital and temporal cortex. A premotor area (M2) in addition to the primary motor area (M1) was also evident. Early primates, such as the Lemuriformes, continued to expand the number of visual areas as well as the number of auditory, somatosensory and motor areas. By this stage the frontal lobe contained a clear granular prefrontal region and a frontal eye field. Further expansion in the number of areas occurred through the New World monkeys (Platyrrhini), Old World monkeys and apes (Catarrhini). Old World monkeys are larger than New World monkeys and have more expansive temporal lobes, posterior parietal regions and prefrontal cortex. Common functional areas of earlier primates are present and enlarged but represent a much smaller proportion of total cortical space [87]. The morphology of the ape brain is similar to the human brain but with proportionally larger occipital lobe and smaller tempo-

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Table 1 Brain size changes during hominid evolution Species

Date (Mya)

Brain size (cm3 )

Pan troglodytes Australopithecus africanus Australopithecus boisei Homo habilis Early Homo erectus Late H. erectus Homo heidelbergensis Homo neanderthalensis Homo sapiens

– 3 2 2 1.8 0.5 0.5 0.25 –

400 450 500 600 800 950 1100 1200–1750 1200–1600

Mya: million years ago. Data derived from [88,121,161,166].

ral, frontal and parietal lobes [73]. The change to a human-like gross morphology appears to have occurred early in hominid evolution, evidence indicating its presence in the Austaralopithecines [45,73]. The brain and more specifically the isocortex continued to increase in size throughout hominid evolution (Table 1). The brain size (1100 cm3 ) in Homo heidelbergensis around 500,000 years ago was just smaller than that of modern humans. The Neanderthals had brain sizes comparable to modern humans and in some cases slightly larger. The relative brain size in Neanderthals however may have been slightly smaller due to their larger body mass. The calculation of relative brain size, expressed as EQ, is problematic in extinct hominids due to difficulties in estimating body mass and use of different formulas for EQ calculation [176]. The EQ data available is therefore much less precise and more variable than the estimates of brain size. One study [88] suggested that there was a notable increase in EQ with the appearance of the Australopithecines and Homo. Throughout the 2 million years of Homo there was little further change until a significant increase with the appearance of anatomically modern humans. Several more recent studies however suggest that the major advance in EQ was during the Homo period occurring between Homo erectus and H. heidelbergensis [161,163,166]. If these later studies are more representative then it would mean that there was only minimal advance in EQ between recent archaic Homo sapiens/Neanderthals and anatomically modern humans. Following the previous trend in primate evolution the threefold increase in brain size between Australopithecines and humans would be associated with expansion in the size of existing cortical fields and addition of new specialized cortical fields. Humans having the largest brains should have the greatest number of new specialized fields. This could explain human cognitive capabilities and behaviour. This explanation may however be inadequate as Neanderthals had similar sized brains to modern humans but may have had substantially different behavioural capabilities (see Section 5). It might be that the nature of additional specialized fields in humans differed in some respect from Neanderthals. In relation to this it has been postulated that a reduction in body size in modern humans, producing a higher EQ, resulted in modification of cortical fields [30,31]. This theory however acknowledges several points of contention. First, there is a lack of clear evidence for a specific advancement of

EQ in modern humans. Second, most body growth occurs postnatally while gross brain connectivity is completed around the perinatal period. Third, there is a lack of variation in the overall behavioural capacity of domesticated dog breeds, despite considerably variation in EQ. Brain size remains more constant than body size, hence dog breeds with small body size have higher EQ’s [30,31]. 3. Ontogeny: ventricular zone to adult behaviour Evolutionary change leading to modern human behaviour could in theory operate at any point along the developmental sequence, going from the initial designation of neural cell fate through to complex behaviour. The six layered isocortex is formed by columns of excitatory glutamatergic projection neurons with interspersed inhibitory GABAergic interneurons [111]. Glutamatergic projection neurons are formed from division of stem cells in a pseudostratified columnar epithelium in the primoridial telencephalic wall, referred to as the ventricular zone [2]. Inhibitory GABAergic neurons distend for the isocortex are born mainly in the medial ganglion eminence of the subpallium and reach the isocortex by tangential migration [202]. In recent years there have been major advances in elucidating the sequence of events from the ventricular zone to the six layered cortex [111]. The first neurons migrating from the ventricular zone form the preplate. Subsequent migrating neurons split the preplate into two layers, the marginal zone and the subplate. The marginal zone, which contains Cajal-Retzius cells, becomes layer 1 of the isocortex [143]. Further migrating neurons are deposited between these two layers to form the cortical plate. This occurs in an ‘inside-out’ pattern with younger neurons by-passing older neurons to form the more superficial layers of the cortex. Neurogenesis originates from radial glial cells in the ventricular zone, using a direct and indirect route [70,119,157]. The direct route involves an asymmetric division to produce a new radial glial cell and a neuron. The neuron moves radially from the ventricular zone to the cortical plate forming the lower layer neurons (V and VI). The indirect route involves formation of a new radial glial cell and an intermediate progenitor cell. The intermediate progenitor cells move above the ventricular zone to form the subventricular zone. Intermediate progenitor cells in the subventricular zone divide symmetrically till late in gestation and migrate radially to form the superficial layers of the cortex. Cell death by apoptosis is an integral part of this developmental period [11,33,131,177]. It is thought that as many as 50% of progenitor cells in the ventricular and subventricular zones die. The reason for such a massive cell loss is not known, one possibility is to insure control of cell numbers as the brain increases in size during the course of evolution. In addition to apoptosis cell numbers at this developmental stage can also be controlled by species-specific changes in cell cycle duration [19,99,100]. A species-specific cortical area map is predetermined in the ventricular zone [64,132,156]. This map specifies both area and layer patterning [157]. Area patterning is contributed to by three patterning centres, the anterior pole, the Hem (medial margin)

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and the Anti-Hem (lateral margin). The transcription factor Fgf8 is expressed at the anterior pole and forms a gradient in the A–P axis. Higher levels of Fgf8 in the anterior area inhibit a second transcription factor Emx2. High levels of Emx2 are associated with enlargement of the posterior cortex [157]. The Hem is involved in hippocampal determination and the Anti-Hem in determination of the limibic cortex. In terms of layer specification the transcription factors Ngn1 and Ngn2 specify layer V and VI fates whereas Tlx and Pax6 specify upper layer fates [168]. This map by differential expression of axon guidance molecules guides connectivity [149,153]. Growth cones from projecting neurons are programmed to respond to their target neurons as well as to the environment on route. Axon guidance molecules operate down stream of transcription factors and their expression varies across developmental spatial domains and with neuronal birth dates within domains [71,158]. During this initial establishment of connections there is a second apoptotic period resulting in a further massive loss of neurons, possibly as much as half of all neurons [11,29,130,144]. Survival of neurons at this stage depends on supply of neurotrophic factors, which are mainly synthesized in their target fields. This process may match the number of neurons to the size of the target field. The end result of this genetically controlled developmental process is a correctly wired brain in which all brain areas send and receive designated projections. The brain at this stage is however not refined into functional systems that will constitute the behavioural pattern of the species. To progress onto behaviour requires refinement of these circuits. The refinement occurs in the late prenatal and postnatal periods and involves a reduction in the number of connections [76,77]. This developmental period has a large ‘epigenetic component’ involving activity-dependent neuronal processes [90,185]. The initial stage, in the late prenatal and early postnatal period, is experience-independent involving spontaneously produced neuronal activity. This leads to the initial refinement of circuits and has been referred to as the ‘precritical period’ [47,93]. The following ‘critical period’ involves experience-dependant processes to refine circuits into adult behaviour [68,69]. Critical periods are windows in time in which particular neuronal circuits have heightened levels of plasticity. The length of the critical period correlates with the life span of the species and may operate for several years in long lived species. After closure of a critical period there is a constructional consolidation of selected pathways and behaviours. Findings from extensively studied birdsong may be applicable to the development of complex behaviours in general [15,38,115,186,191,204] (Fig. 3). It demonstrates the relationship between multiple brain areas, predetermined neuronal sensitivities, and sequentially connected critical periods. The first critical period is referred to as the sensory phase. During this phase certain neurons are predisposed to respond to speciesspecific birdsong. Although young birds are capable of copying heterospecific song, especially if it is the only model available, they preferentially learn conspecific songs when given a choice [114]. At the end of this period the neurons involved retain a song template. The second critical period is the sensorimotor phase in which motor circuitry is gradually shaped by performancebased feedback of the birds own song. Certain neurons, found

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Fig. 3. (→) Direct pathway; ( ) indirect pathway. Complex behaviours involve multiple brain areas. This simplified figure depicts some of the main brain areas involved in the production of birdsong. The motor pathway involves a projection from the HVC nucleus in the nidopallium to the robust nucleus of the acropallium (RA). RA then projects to the tracheosyringeal portion of the hypoglossal nucleus (nXIIts) in the brain stem. The nXIIts nucleus sends axonal fibres via the hypoglossal nerve to innervate the syrinx, which is the avian vocal organ. In addition to its direct link with RA, HVC also projects to RA indirectly via the anterior forebrain pathway. The anterior forebrain pathway is a specialised basal ganglia–thalamo-cortical loop, involving “Area X” of the medial striatum, the dorsal lateral nucleus of the medial thalamus (DLM) and the magnocellular nucleus of the anterior nidopallium (LMAN). Although not shown in this diagram there is also input from the primary auditory area (field L) in the nidopallium and from vocal and auditory regions in the mesopallium.

throughout the song circuit, develop their selectivity in parallel with production of the birds own song. Deafening during this period in addition to preventing progression also leads to deterioration of previously learned song [106,140]. After this second stage there is an extended period in which the song becomes progressively stabilized, referred to as song crystallization. Song crystallization is evident from the degree of song deterioration, after hearing loss, being much less severe in adulthood than in juveniles [13,140]. At the end of the sensorimotor stage some birds are able to produce many songs but ultimately only crystallize a few songs as adults [113,116,138,139]. Song selection at this stage is linked to social factors, for example which song stimulates the best response from females of the species. This change, referred to as the transition from ‘plastic’ song to ‘adult’ song constitutes and additional development phase occurring after the sensorimotor phase and before song crystallization. This reduction in ‘plasticity’ maybe a general developmental phase involved in defining behavioural stereotypes [113]. It has been postulated that the developmental phase of ‘plastic song’ has been retained in adults of species that are able to modify their songs on an ongoing basis [78]. This outlined complex developmental sequence leading from neural stem cells to behaviour, together with the multiple genes involved, suggests countless possibilities for random evolutionary change. Evolutionary change may not however be random and certain changes may predominate in individual evolution-

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ary lineages. It has already been stated that increasing brain size together with new cortical field formation have been dominant modes of evolution in primates. 4. Primate lineage—mode and process of evolutionary change As discussed in Section 2 the major evolutionary change in the primate lineage leading to humans has been an increase in size of the isocortex together with the formation of new cortical fields. With regards to isocortical enlargement the main evolutionary process responsible seems to have been a prolongation of developmental time. Although the intricacies of new cortical field formation are complex, some general principals have been outline. Throughout the evolution of placental mammals the size of various brain regions has generally correlated with total brain size [48,49,99]. The correlation is predicable but non-uniform with some brain regions, in particular the isocortex, showing a disproportionate increase in size. The actual slope of increase in size relates to the timing of neurogenesis, with a longer duration associated with an alar and anterior position on the prosomeric axes. As the development period is extended, more rounds of cell division are possible thus creating more precursor cells and a larger brain. Late generated structures, in particular the isocortex, accumulate a large precursor pool and hence increase more in size compared to early generated structures. The largest increase is for layer II/III neurons, which are the latest generated layers of the cortex [22,23,100]. The supragranular layers as percent of total cortical thickness are 46% primates, 36% carnivores and 19% rodents [75]. The primate order seems to have deviated from the general mammalian trend by having a larger isocortex in comparison to the limbic system than would be predicted [23]. This has been suggested to be due to a delayed onset of neurogenesis for the isocortex and advanced onset for limbic structures [49]. It could also have resulted at the level of the ventricular zone map with an increased ratio of anterior pole pattering compared to Anti-Hem pattering. Within the primate order the anthropoids have deviated from their predecessors by having an increased brain body ratio. This may represent an early developmental change allocating a greater proportion of cells towards brain as opposed to body growth [30,31]. There may have also been a further increase in brain body ratio at the advent of modern humans. This has been proposed to be due to a postnatal truncation of body growth, rather than an early embryonic effect [30,31]. The number and nature of additional cortical fields in humans has yet to be fully determined. Most will be represented by higher functional areas particularly in the prefrontal, temporal and parietal regions. Available information on new field formation however generally relates to primary sensory areas. New field formation can be influenced both by changes in the ventricular zone map and changes in peripheral receptors [89]. For example, a highly visual mammal may have resulted from any combination of increased occipital territory on the ventricular zone map and increased size of its eyes leading to increased

Table 2 Stone tool manufacture Industry

Date (Mya)

Tools

Species

Omo Oldowan

3 2

Early H. habilis H. habilis

Acheulian

1.5

Mousterian

0.25

Smashed pebbles Knapped flakes + remnant core Handaxe—bifacial flacking Levallois technique

H. erectus H. neanderthalensis

This table demonstrates a continuum of gradual increasing sophistication in stone tool manufacture over a 3 million year period of Homo evolution. The basic principal is modification of stones in order to make them more useful. It began by simply smashing stones, then to more deliberate methods of producing sharp flakes. The Levallois technique involved elaborate shaping of the core prior to striking off the flake in order to produce pre-specified types of flakes. Note: Dates ranges for the various stone tool industries may show some overlap, the above dates are only approximations.

visual input. Echolocating bats have enlargement of the ventral cochlear nucleus and auditory nerve, along with enlargement of the auditory cortex [25]. During hominid evolution new higher order cortical field formation may have been determined along the lines of the following sequence (Fig. 4). Initially, additional cortex would be added according to the proportions determined by the ventricular zone map. Position in the ventricular zone map, together with birth date of the neurons, would in turn determine gross connectivity with other areas. Refinement of this connectivity would depend on activity-dependant processes, proportional to the balance of input from existing behavioural systems. Finally, after consolidation of connections, the function of the new area would be defined. In the absence of any change in the ventricular zone map, this process would presumably lead to a gradual extension of existing behavioural repertoires along the hominid lineage. The archaeological evidence is generally compatible with this, indicating a gradual increase in the sophistication of stone tool use from early Homo habilis through to Neanderthals (Table 2) [85,184]. Whether or not modern human behaviour can be explained as part of this continuum remains a matter of debate. 5. The palaeoanthropological debate One of the most contentious and important debates in the palaeoanthropological literature is whether modern human behaviour arouse suddenly or gradually [5]. Anatomically modern humans are thought to have evolved from archaic H. sapiens/H. heidelbergensis-like ancestors in subsaharan Africa between 100,000 and 200,000 years ago [14,18,66,86,97,135,182,183,189,190,192,201]. Some of these people left Africa around 50,000 years ago [95] and populated other parts of the world, arriving in Europe at around 35,000 years ago. They brought with them a sophisticated range of behaviours creating a cultural change referred to as the Middle to Upper Palaeolithic transition. The Neanderthals and their Middle Palaeolithic or Mousterian culture had existed in Europe and Western Asia for 250,000 years, with practically no change, prior to the arrival of modern humans [85,94,96,173,184,188].

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Fig. 4. A generalised mammalian isocortex, with frontal, parietal, temporal and occipital regions. (A) During the course of evolution extension of developmental time has resulted in an increasingly large isocortex, A(i)–(ii). All else being equal, this would presumably lead to a proportional increase in all isocortical regions. Subsequent changes could however alter this situation to result in species-specific variation, for example changes in the ventricular zone map, differential rates of apoptosis, changes in cell cycle duration or body changes resulting in alterations in sensory input. (B) Represent the same isocortex as depicted in A(i) and (ii). Five individual cortical fields ( ) are represented, two in the frontal region and one in each of the other three regions. The cortico-cortical connectivity between all these fields is represented by bi-directional arrows. The evolutionary enlarged isocortex B(ii) depicts the initial anatomical connectivity of an area of new cortex () within the frontal region. This initial connectivity is developmentally determined via position within the ventricular zone map and birth date of neurons. (C) Represents the same evolutionary enlarged isocortex as shown in A(ii) and B(ii). In this case the connectivity represents neuronal activity patterns within the framework of anatomical connectivity. Each of the three diagrams (i), (ii) and (iii) depicts separate individual behaviours. Each of the behaviours utilizes different cortical fields, including the new cortical area, to varying degrees. The strength of neuronal activity in the various anatomical pathways, for each of the three behaviours, is represented as weak (· · ·), medium (↔) and strong ( ). (D) Represents the same evolutionary enlarged isocortex as in A(ii), B(ii) and C, but at a later stage of development after activity-dependant processes have refined the initial anatomical connectivity into functional connectivity. This refinement depends on the balance of neuronal activity input from all existing behaviours. Circuits with lower levels of activity will be lost and circuits with high levels of activity will be retained. The net functional connectivity of the new cortical area will therefore be defined by the balance of activity inputs from all pre-existing behaviours that are able to access it. This developmental process results in extension of existing behaviours rather than incorporation of new behaviour. Depending on its size and uniqueness of its functional connectivity pattern the new cortical area could be incorporated into pre-existing adjacent cortical fields and/or form a new cortical field. The result shown in (D) has been grossly simplified to take into account only the three behavioural circuits shown in (C). In this case the new cortical area has been utilized partly to increase the size of one of the pre-existing frontal cortical fields (a) and to form a new cortical field (b).

The Neanderthals seemed unable to adopt these new behaviours and were probably out-competed, becoming extinct in Europe 10,000 year after the arrival of modern humans [94]. It is generally accepted [94,145,188], although not by all [200], that there was little or no interbreeding between modern humans and the Neanderthals.

The marked difference between the Middle Palaeolithic and Upper Palaeolithic cultures in Europe has been well documented in books such as ‘The creative explosion’ [147] and ‘The human revolution’ [124]. Neanderthals manufactured stone flakes produced by striking a prepared core (Levallois technique). There is little evidence

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that they manufactured any other types of tools or produced art. There is also little evidence to suggest that they build shelters, stored food or use fire on a regular basis. It is still unresolved if they intentionally buried their dead [52,53,74]. Even if they did bury their dead this was on a very basic level, more like disposal of bodies, than having any meaningful significance. They probably lived in caves and mainly scavenged for an existence. The stone blades they manufactured were suitable for hafting onto spear heads, this together with evidence of severe trauma, suggests the possibility that they used short trusting spears to kill at close range. The Upper Palaeolithic culture of modern humans in Europe was markedly different [124,147]. Using various materials they manufactured a variety of different tools such as spear throwers, fish hooks, and gorges. They built shelters, stored food and used fire on a regular basis. More significantly, they produced a wealth of symbolic art forms such as sophisticated cave paintings, body ornamentations and mobility art such as ‘Venus’ figurines [107,117,195,196]. Also of great significance they buried their dead and the bodies were often associated with a complex range of items of personal adornment. This indicates ritualistic or religious meaning to these burials [10]. The European evidence suggests that the Upper Palaeolithic humans were entirely modern in their behaviour although of course they lacked the wealth of accumulated knowledge available to present day humans. The behaviour of Neanderthals however, although more advanced than their predecessors, may still have been more akin to earlier hominid ancestors than it was to modern humans [85,94,184]. In particular the evidence for little or no change in their behaviour over the time period of their existence and across their whole geographical range suggests that they lacked the characteristic flexibility of modern human behaviour. As modern human behaviour arrived in Europe rather than evolved in Europe it is not possible to address its date of origin using this data. The question of when and how sudden modern human behaviour appeared has to be addressed where it most likely originated, in sub-saharan Africa. Unlike the wealth of reasonably unambiguous data available for the Middle Palaeolithic to Upper Palaeolithic transition in Europe the data from the equivalent time period in sub-saharan Africa, called the Middle to Later Stone Age transition, is more limited and variable. A commonly held view, mainly from South African evidence, is that the culture in the Middle Stone Age and Later Stone Age equate, respectively, with that in the Middle Palaeolithic and Upper Palaeolithic [95,97,98]. This suggests that fully modern human behaviour appeared abruptly around 50,000 years ago, that is 50,000 years after the first anatomical modern humans. This sudden change in behaviour suggests a speciation event associated with a major cognitive advance and has been generally coined the ‘human revolution’. More detailed study of other sub-saharan African sites however, which may have been more permanently inhabited that the South African sites, suggests that traces of modern human type culture was evident in the Middle Stone Age [120]. These authors suggest that the Middle Stone Age does not equate with the Middle Palaeolithic and that the origin of behaviourally mod-

ern humans was less abrupt and may go back 100,000 years or more. It is further argued that these findings do not support a speciation event associated with a major cognitive advancement resulting in behaviourally modern humans. Although this disagreement presently remains unresolved [5], it would seem reasonable to suggest that even if there is evidence for the beginnings of modern human behaviour in the Middle Stone Age it does not necessarily rule out a speciation event. Support for this is evident from comparison of time scales. A 3–4 million years period from the Australopithecines up to Neanderthals would appear to represent a continuum of a gradual extension of existing stereotyped behavioural patterns (Table 2), whereas a much smaller time scale of around 50,000 years appears to have resulted in a change from non-flexible mainly stereotyped behavioural patterns to thought driven truly flexible behaviour. If a speciation event was responsible one possibility is additional cortical field formation within the prefrontal cortex. Such a change may have been evoked centrally via a change in the ventricular zone cortical map or, as previously discussed (Section 2), peripherally via a reduction in body growth [30,31]. The prefrontal cortex has extensive connections with other high order association areas. At a functional level it integrates cognitive, emotional and mnemonic processes and hence operates central executive functions [6,50,51,128]. Together with its connections it is capable of spontaneous activity in the absence of external stimulation. This relates to the conscious state, selfawareness and to self-directed autonomous behaviour [32]. As modern humans brains cannot be directly compared with those of our nearest hominid ancestors it is difficult to determine if there has been a change in size of the prefrontal cortex. Indirect studies with skull endocasts suggest a possible increase in frontal and/or temporal lobe territory in modern humans [5,108]. An alternative explanation is that there was no additional cortical field formation. Instead human specific events have resulted from changes during later developmental phases where cortico-cortical connections are refined and consolidated [125]. Alterations at these later stages rather than leading to additional cortical field formation could alter the function of existing cortical fields. If these alterations occurred in higher order association areas, including the prefrontal cortex, then they could have resulted in modern human behaviour. Postnatal body growth reduction [30,31] could have operated during this later developmental phase rather than the earlier phase of additional cortical field formation. The time period of reduced body growth would overlap with the extensive critical period in humans. If postnatal reduction in body growth had no or little effect on connectivity in higher brain centres, then a specific brain developmental change may have been responsible. To explore this possibility further requires an overview of cortico-cortical connectivity together with possible evolutionary changes that could have lead to increased flexibility of behaviour. 6. Cortical connections and evolutionary change The complexity of cortical connections is such that it is difficult to comprehend. Despite this however studies of the visual

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Fig. 5. (I–VI) Cortical layers; (→) intra-column connections; ( ) feedforward connections; ( ) feedback connections. All feedforward and feedback connections from pyramidal cells are excitatory. Ninety percent of these connections terminate on pyramidal cells and 10% terminate on GABAergic interneurons [84]. There are three subtypes of GABAergic interneurons, expressing parvalbumin, somatostatin and cholecystokinin [58,91]. The connectivity with these various GABAergic subtypes varies between cortical layers [56]. The development of GABAergic neurons, as for pyramidal neurons, is mediated through molecular cues and refined by neuronal activity [20].

cortex in cats and primates and of the somatosensory cortex in rodents have lead to recent advances in our understanding [36]. The cat visual cortex area 17 has indicated a general connectional pattern between the cortical layers within a local patch of cortex [55]. In this model thalamic input arrive in layer 4 (granular layer). Excitatory cells in layer 4 then project to layers II and III. Layers II and III pyramidal neurons project to layer 5 which in turn projects to layer 6. The loop is completed by connections from layer 6 back to layer 4 and by feedback connections from layers 5 and 6 to the thalamus (Fig. 5A). This model is based on spiny excitatory neurons and does not take into account the effect of inhibitory neurons. The model is applicable to different cortical areas and to different species [36]. A local cortical patch does not operate as a discrete unit but is connected laterally to between 10 and 30 other patches in the same processing area. These other patches are regularly spaced as a circle around the activated patch. The connections between different cortical areas are referred to by the terms feedforward and feedback [162] (Fig. 5B). Feedforward connections originate mainly in the superficial layers (II and III) and, as for thalamic input, connect to layer 4 of a different area. Feedback connections originate mainly in layers 5 and 6 of one area and terminate outside layer 4 of the recipient area. Individual cortical areas can be related to each other on a hierarchical basis according to their feedforward–feedback relationship [46]. Feedforward connections are sent generally from a lower cortical processing area to a higher area whereas feedback connections connect a higher area to a lower area. The hierarchy can also be expressed in terms of percentage of supragranular layer projections (%SG) between areas. Lower processing areas have between 76–96%SG, equivalent areas 39–69%SG and higher

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Fig. 6. (I–VI) Cortical layers; (A) lower processing area; (B) intermediate pro) feedforward connections; ( cessing area; (C) higher processing area; ( ) feedback connections; (→) local intra-column connections; (夽) feedback connections from superficial cortical layers are massively pruned during the activity-dependant phase of development [9]. There is much less effect on feedforward and GABAergic connections [9,126]. Feedback connections from and to the intermediate processing area (B) are omitted to prevent over complicating the diagram.

areas 0–33%SG [61]. Connections between equivalent areas are referred to as lateral connections. Inputs into layer 4, whether from the thalamus or from feedforward cortical connections, are considered ‘driving’ in nature [28,174]. Driving inputs are strong inputs that are able to produce firing of a postsynaptic neuron. The driving network applies to information received from the external environment (Fig. 6). Information is initially passed from sensory receptors to the thalamus then to layer 4 of a lower processing area of the cortex and through feedforward layers II and III projections to progressively higher processing cortical areas. Feedback connections, acting in the opposite direction, from the higher processing areas to lower processing area are considered to be ‘modulatory’ rather than ‘driving’. Modulatory inputs are generally weaker than driving inputs and by themselves are unlikely to fire postsynaptic neurons. Their action is to exert a modifying influence on driving inputs. The feedforward driving and feedback modulatory roles hold best for early sensory areas. With local and long distance cortico-cortical connections between higher association areas the distinction still applies but is more diffuse in terms of laminar termination [7,160]. Feedforward projections originate in the upper layers (II, III) and terminate in the deep layers (IV, V, VI). Feedback projections originate in deep layers (V, VI) and terminate mostly in upper layers (I, II, III). Eulaminate (granular) association cortical areas with six well-defined layers generally have feedforward connections when connecting to

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agranular limbic cortical areas. In the opposite direction limbic cortical areas generally connect to eulaminate association cortical areas via feedback connections. Eulaminate association cortical areas connect to each other via relatively equal proportions of feedforward and feedback connections. In functional terms the driving nature of feedforward connections suggests a bottom-up control of behaviour (Fig. 6). That is the environment exerting a dominant influence on behaviour. This would be especially true for primitive animals with small brains. With increasing brain size and complexity top-down influence will become more influential. Their influence however is most likely modulatory or predominately modulatory, it may therefore determine the choice between several different environmentally evoked responses, rather than evoke behaviour independently of the environment. This system would appear to be in keeping with the predominately stereotyped behavioural patterns of all non-human mammals. An evolutionary change that could have produced increased flexibility in human behaviour is a change in mode of function of feedback connections from higher brain centres. Instead of being predominately modulatory they could have evolved a driving influence on behaviour. The result could be that thoughts, acting independent of input from the external environment, could direct behaviour. This is not to say that self-motivated behaviour does not occur in other higher mammals, but the extent would be considerable less than in humans. An increased driving nature of feedback connections could have resulted from an alteration of the pattern and/or extent of connectivity. In relation to this, distinct changes in the pattern and extent of feedback connectivity occur as normal events during the activity-dependent developmental period. They could therefore be subject to evolutionary change by a simple, possibly one step change in developmental sequence. The driving and modulatory effects of feedforward and feedback connections respectively are thought to relate to the balance and timing of neuronal excitation and inhibition [17,34,35,172]. Feedforward circuits generate excitement followed by strong inhibition, whereas feedback circuits generate excitement followed by weak inhibition. As both feedforward and feedback connections are excitatory their inhibition occurs indirectly via connections with GABAergic interneurons. Stronger feedforward inhibition results from connections to thick proximal GABAergic dendrites and weaker feedback inhibition results from connections with thinner distal GABAergic dendrites [57,197,198,203]. Interestingly, this feedback connectivity results during the critical period, via a retraction of synapses from thick proximal dendrites and retreat to thinner distal processes [203]. Evolutionary change in feedback connections, from a modulatory to a driving action, could therefore in theory result from retention of an earlier developmental phase. That is, retention of connections to thick proximal GABAergic dendrites. In addition to, or in direct relation to, this pattern change in feedback connections to GABAergic interneurons, there is extensive pruning of feedback connections from supragranular layer neurons during the activity-dependant developmental period [9] (Fig. 6). Feedforward connections develop prena-

tally and do not seem to be remodelled to any significant extent by activity-dependant processes. In contrast there is a 28–84% reduction in feedback connections from supragranular layer neurons in the activity-dependant developmental period. An evolutionary induced reduction of this developmental phase could hence contribute to a driving nature of feedback connections, possibly via retained synapses onto thick GABAergic dendrites. In addition to the above, excitatory-inhibitory balance and its link to GABA transmission, seem to have major roles throughout the critical period [68]. Cortical GABA transmission has been shown to be involved in the initiation and closure of critical periods [68]. Procedures that artificially delay the critical period also delay the anatomical maturation of GABAergic inhibition [68,165]. During birdsong development GABA transmission increases during the motor rehearsal stage and may aid matching of sub-song with the template song. A second theory, that would be compatible with increased flexibility of human behaviour, is a partial rather than complete closure of critical periods in higher brain centres. Unlike birdsong that becomes crystallized and unchangeable in the adult, humans still retain some capacity to learn new languages as adults [26,37,81,194]. Children learn languages much easier than adults but the fact that adults retain some potential indicates that the critical period may only be partially closed. More speculatively, a possible third theory may relate to the developmental phase leading from ‘plastic’ to ‘adult’ birdsong [113]. Retention of the earlier developmental phase associated with ‘plastic’ song could result in more flexible behaviour. It is not clear however if this developmental step applies to all behaviours and to all species. The complexity of higher order association connections, together with a lack of information relating to humans [27,178], makes it difficult to obtain evidence to support or refute human specific evolutionary change in cortico-cortical connections. In addition to excitatory pyramidal connections there are three subtypes of GABA interneurons [58,91] that could have independent effects during the critical period [17]. The only report of a possible cortico-cortical connectivity change in humans relates to the detection of extensively branched and spinous layer III pyramidal neurons in the granular prefrontal cortex [39,40,41,42]. The presence of these branched and spinous granular prefrontal cortical neurons may relate to an increase/change in connectivity. This connectivity change could represent a human specific speciation event, however there is some evidence indicating that an increase in dendritic spines had been a gradual trend during the course of primate evolution. If this is true it follows that it maybe entirely a consequence of cortical enlargement rather than the result of a speciation event. Whatever scenario applies, these spinous neurons have greater neuroplastic potential [180,181] and hence may allow greater behavioural flexibility. 7. Conclusion Whether or not modern human behaviour represents a departure form previous trends during hominid evolution remains a matter of debate. Comparative behaviour does however suggest

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