Article

Exceptional Evolutionary Expansion of Prefrontal Cortex in Great Apes and Humans

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Abstract

One of the enduring questions that has driven neuroscientific enquiry in the last century has been the nature of differences in the prefrontal cortex of humans versus other animals [1]. The prefrontal cortex has drawn particular interest due to its role in a range of evolutionarily specialized cognitive capacities such as language [2], imagination [3], and complex decision making [4]. Both cytoarchitectonic [5] and comparative neuroimaging [6] studies have converged on the conclusion that the proportion of prefrontal cortex in the human brain is greatly increased relative to that of other primates. However, considering the tremendous overall expansion of the neocortex in human evolution, it has proven difficult to ascertain whether this extent of prefrontal enlargement follows general allometric growth patterns, or whether it is exceptional [1]. Species' adherence to a common allometric relationship suggests conservation through phenotypic integration, while species' deviations point toward the occurrence of shifts in genetic and/or developmental mechanisms. Here we investigate prefrontal cortex scaling across anthropoid primates and find that great ape and human prefrontal cortex expansion are non-allometrically derived features of cortical organization. This result aligns with evidence for a developmental heterochronic shift in human prefrontal growth [7, 8], suggesting an association between neurodevelopmental changes and cortical organization on a macroevolutionary scale. The evolutionary origin of non-allometric prefrontal enlargement is estimated to lie at the root of great apes (∼19-15 mya), indicating that selection for changes in executive cognitive functions characterized both great ape and human cortical organization.

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... Sur le plan anatomique, un faisceau de fibres relie le gyrus fusiforme au sillon intrapariétal (Jitsuishi & Yamaguchi, 2020). Ce dernier est également impliqué dans l'évaluation d'un statut social (Chiao et al., 2009 (Smaers et al., 2017). Il a été suggéré que les exigences computationnelles de la vie dans des sociétés à l'organisation complexe auraient joué un rôle crucial dans le développement exceptionnel du cortex préfrontal (Dunbar & Shultz, 2007). ...
... D'autre part, les régions cérébrales impliquées dans la perception des visages sont aussi mobilisées, de même que des régions frontales appartenant au « cerveau social ». A cet égard, il a été remarqué que le cortex préfrontal était particulièrement développé chez les grands singes et encore plus chez Homo sapiens (Smaers et al., 2017). Cette région joue également un rôle important dans la capacité de manipuler des symboles (Nieder, 2009). ...
Thesis
Les découvertes archéologiques décrivant les premières gravures paléolithiques abstraites et l’ornementation du corps, à travers les objets de parure et l’utilisation de pigments, suggèrent que l’utilisation de signes et/ou de symboles n’est pas circonscrite à Homo sapiens mais pourrait concerner des Hominines beaucoup plus anciens. Nous plaçant dans une perspective neuroarchélologique, nos études visent à inférer les bases neurales nécessaires à l’apparition de ces premiers comportements attestant d’une pensée symbolique. Nous avons utilisé l’Imagerie par Résonance Magnétique fonctionnelle (IRMf), qui permet d’enregistrer l’activité cérébrale de participants, lorsque nous leur présentions des stimuli issus d’innovations culturelles potentiellement symboliques. Il s’agissait de versions schématiques et de photographies des premières gravures paléolithiques, puis de visages culturellement ornementés avec des perles en bois et des traits de peinture rouge, inspirés d’ornementations préhistoriques.Les résultats de la première étude montrent que la perception visuelle des premières gravures paléolithiques abstraites mobilise des aires cérébrales visuelles associatives, situées dans la partie antérieure de la voie occipito-temporale. Ces régions, impliquées dans la reconnaissance et l’identification de percepts visuels, indiquent que les premières gravures paléolithiques abstraites sont perçues comme des stimuli auxquels on peut attribuer une signification. A cet égard, cette observation est compatible avec l’hypothèse proposant que ces premières gravures auraient pu constituer des signes voire des symboles.Dans une deuxième étude, afin de mimer les effets de familiarité des gravures que nos ancêtres possédaient sans doute, nous avons comparé les réponses cérébrales d’experts archéologues et de participants novices dans une tâche de discrimination de gravures intentionnellement produites par des Hominines et de marques issues de processus naturels. Les résultats montrent un effet de familiarité avec ce type de matériel. En effet, lorsque des archéologues catégorisaient les motifs, ils mobilisaient davantage la partie ventrale du cortex occipital latéral, ainsi que le thalamus médiodorsal. Ces activations refléteraient l’analyse fine perceptive réalisée, en lien avec des connaissances stockées à long terme. Par ailleurs, la catégorisation des motifs abstraits en fonction de leur origine humaine ou naturelle a révélé l’engagement des structures sous-corticales comme la tête du noyau caudé et le thalamus, et de régions corticales dont l’insula antérieure et ce, quel que soit le niveau d’expertise des participants. Ces régions appartiennent au réseau de la saillance, qui joue un rôle dans la détection d’éléments pertinents de l’environnement pour effectuer la tâche.Enfin, la troisième étude montre que l’attribution d’un statut social à partir de visages culturalisés mobilise des régions visuelles de la voie occipito-temporale, manifestant le traitement approfondi d’informations visuelles, jusqu’au pôle temporal dont il a été suggéré un rôle d’association entre la perception de visages et l’identité d’informations à propos d’une personne, des régions impliquées dans la détection d’éléments saillants de l’environnement et des régions frontales appartenant au « cerveau social ».Le travail de ma thèse suggère qu’au Paléolithique et Stone Age, les bases neurales étaient déjà fonctionnelles pour sélectionner les éléments pertinents de l’environnement afin de reconnaitre des productions intentionnelles d’autrui, puis d’être capable d’y attacher une signification, probablement culturellement déterminée, ceci dans le contexte d’une organisation sociale toujours plus complexe.
... Brain allometry describes the quantitative scaling relationship between changes in the size of one structure relative to another structure, often the whole brain or cerebral cortex (Mars et al., 2017;Smaers et al., 2017). Previous allometric studies suggested that the association cortex (prefrontal, temporal, and parietal regions) scales with positive allometry (i.e., increases in size disproportionally, or more rapidly) across primates (Passingham and Smaers, 2014;Mars et al., 2017). ...
... Previous allometric studies suggested that the association cortex (prefrontal, temporal, and parietal regions) scales with positive allometry (i.e., increases in size disproportionally, or more rapidly) across primates (Passingham and Smaers, 2014;Mars et al., 2017). Utilizing parcellation-based delineations, a recent study provided evidence that human brains have a greater proportion of prefrontal cortex gray matter volume than other primates (Donahue et al., 2018), and other studies demonstrate that human prefrontal expansion is greater than would be expected from allometric scaling in nonhuman primates (Passingham and Smaers, 2014;Smaers et al., 2017), although some conflicting analyses remain (Gabi et al., 2016). In the present study, we used macroanatomical boundaries to identify the boundaries of the IPL and a connectivity-based parcellation approach to subdivide the IPL, which helped to reveal its internal organization. ...
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The inferior parietal lobule (IPL) is one of the most expanded cortical regions in humans relative to other primates. It is also among the most structurally and functionally asymmetric regions in the human cerebral cortex. Whether the structural and connectional asymmetries of IPL subdivisions differ across primate species and how this relates to functional asymmetries remain unclear. We identified IPL subregions that exhibited positive allometric in both hemispheres, scaling across rhesus macaque monkeys, chimpanzees, and humans. The patterns of IPL subregions asymmetry were similar in chimpanzees and humans, but no IPL asymmetries were evident in macaques. Among the comparative sample of primates, humans showed the most widespread asymmetric connections in the frontal, parietal, and temporal cortices, constituting leftward asymmetric networks that may provide an anatomical basis for language and tool use. Unique human asymmetric connectivity between the IPL and primary motor cortex might be related to handedness. These findings suggest that structural and connectional asymmetries may underlie hemispheric specialization of the human brain.
... In addition, genetic and developmental heterochronic shifts of the human striatum (Sousa et al., 2017) have brought changes in the direction of trait variation on a macro-evolutionary scale, such as a significantly smaller volume than predicted based on primate scaling trends (Barger et al., 2014). Interspecies volumetric abnormal changes also exist in some brain regions that are strongly connected to the ventral striatum, including the evolutionary expansions of the human prefrontal cortex, amygdala (Amyg), and the hippocampus (Hipp) (Somel et al., 2011;Barger et al., 2014;Carlén, 2017;Smaers et al., 2017). All of these volumetric abnormal changes may be accompanied by unique modifications of their connectivities with the ventral striatal components. ...
... In subsequent connection analyses, dissimilar interspecies RCS fingerprints, i.e., the macroscopic white matter tracts layout, of the ventral striatum-like division were also found. This result aligns with disproportionate volumetric differences in the regions associated with the ventral striatum, including both the disproportionate growth of the human prefrontal cortex (Carlén, 2017;Smaers et al., 2017), prefrontal white matter (Schoenemann et al., 2005), Hipp and Amyg (Barger et al., 2014) during primate evolution, and the significantly smaller human striatum (which may influence the ventral striatum) than those predicted based on primate scaling trends (Barger et al., 2014). More importantly, this interspecies connectivity difference may suggest a functional modification of the ventral striatum, which was inferred and is summarized as follows. ...
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Although the evolutionarily conserved functions of the ventral striatal components have been used as a priori knowledge for further study, whether these functions are conserved between species remains unclear. In particular, whether macroscopic connectivity supports this given the disproportionate volumetric differences between species in the brain regions that project to the ventral striatum, including the prefrontal and limbic areas, has not been established In this study, the human and macaque striatum was first tractographically parcellated to define the ventral striatum and its two subregions, the nucleus accumbens (Acb)-like and the neurochemically unique domains of the Acb and putamen (NUDAPs)-like divisions. Our results revealed a similar topographical distribution of the connectivity-based ventral striatal components in the two primate brains. Successively, a set of targets was extracted to construct a connectivity fingerprint to characterize these parcellation results, enabling cross-species comparisons. Our results indicated that the connectivity fingerprints of the ventral striatum-like divisions were dissimilar in the two species. We localized this difference to specific targets to analyze possible interspecies functional modifications. Our results also revealed interspecies-convergent connectivity ratio fingerprints of the target group to these two ventral striatum-like subregions. This convergence may suggest synchronous connectional changes of these ventral striatal components during primate evolution.
... Alternatively, the lack of an association between noradrenergic stimulation and working memory performance in the present study and inconsistent findings in earlier studies (Chamberlain et al. 2006;Chamberlain and Robbins 2013) may be due to differences between species. Although brains of humans and non-human primates are thought to be similar in structure and function, there is evidence for important differences between species that concern mainly the prefrontal cortex (Smaers et al. 2017;Teffer and Semendeferi 2012). Beyond changes in the distribution of different cell types, and the addition of novel cortical areas that do not have an analogue in the non-human brain, it is suggested that a phylogenetically recent reorganization of the human frontal cortex resulted in a distributed neural brain network with a dominant role of the prefrontal cortex (Smaers et al. 2017), thus causing differential processing of information in the human and nonhuman brain. ...
... Although brains of humans and non-human primates are thought to be similar in structure and function, there is evidence for important differences between species that concern mainly the prefrontal cortex (Smaers et al. 2017;Teffer and Semendeferi 2012). Beyond changes in the distribution of different cell types, and the addition of novel cortical areas that do not have an analogue in the non-human brain, it is suggested that a phylogenetically recent reorganization of the human frontal cortex resulted in a distributed neural brain network with a dominant role of the prefrontal cortex (Smaers et al. 2017), thus causing differential processing of information in the human and nonhuman brain. Another potential explanation for the inconsistent findings regarding the relationship between noradrenaline and working memory in humans may include the variety of (noradrenergic) receptors and potential pharmacological mechanisms. ...
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RationaleWorking memory depends on prefrontal cortex functioning, which is particularly sensitive to levels of noradrenaline. Studies in non-human primates have shown that modest levels of noradrenaline improve working memory, and that higher levels of noradrenaline impair working memory performance. However, research in humans provided inconsistent findings concerning noradrenergic effects on working memory.Objective The present study aimed at assessing dose-dependent effects of yohimbine, an alpha-2 adrenoceptor antagonist, on working memory performance in healthy humans. We further aimed to explore a potential interactive effect between noradrenergic arousal and lack of control over aversive events on working memory performance.Methods We used a double-blind, fully crossed, placebo-controlled, between-subject design. Participants (N = 121) performed an adaptive n-back task before and after oral administration of either a placebo, 20 mg, or 40 mg yohimbine and a manipulation of controllability, during which participants could either learn to avoid electric shocks (controllability groups), had no instrumental control over shock administration (uncontrollability groups), or did not receive any shocks (no-shock control group).ResultsWhile no significant results of noradrenergic stimulation through yohimbine were obtained using conventional frequentist analyses, additional Bayesian analyses provided strong evidence for the absence of an association between pharmacological treatment and working memory performance. We further observed no effect of controllability and no interaction between noradrenergic stimulation and the manipulation of controllability.Conclusions Our results suggest that noradrenergic stimulation through yohimbine does not affect (non-spatial) working memory in healthy human participants.
... In the human brain, the numbers of streamlines reaching lateral orbital, ventrolateral, insular, and opercular areas were higher than the corresponding numbers in the macaque brain, suggesting a more widespread pattern of connectivity in human prefrontal cortex ( Figure 4B). This may reflect prefrontal cortical expansion in humans compared to that in other Old World primates (Smaers et al., 2017). As discussed above, in the most anterior part of the prefrontal cortex, AmF and UF tend to intermingle, and it is therefore not surprising to see that both reached the frontal pole (area 10 m), including the human lateral frontal pole (area 10 l) for which the homology in the macaque monkey brain is debated (Neubert et al., 2015). ...
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The interactions of anterior temporal structures, and especially the amygdala, with the prefrontal cortex are pivotal to learning, decision-making, and socio-emotional regulation. A clear anatomical description of the organization and dissociation of fiber bundles linking anterior temporal cortex/amygdala and prefrontal cortex in humans is still lacking. Using diffusion imaging techniques, we reconstructed fiber bundles between these anatomical regions in human and macaque brains. First, by studying macaques, we assessed which aspects of connectivity known from tracer studies could be identified with diffusion imaging. Second, by comparing diffusion imaging results in humans and macaques, we estimated the patterns of fibers coursing between human amygdala and prefrontal cortex and compared them with those in the monkey. In posterior prefrontal cortex, we observed a prominent and well-preserved bifurcation of bundles into primarily two fiber systems—an amygdalofugal path and an uncinate path—in both species. This dissociation fades away in more rostral prefrontal regions.
... Peneliti otak menjelaskan bahwa PFC hanya ada pada otak manusia, yg membedakan otak manusia dengan otak binatang. PFC ini berfungsi berfungsi menggabungkan informasi dari semua indera dan membentuk kepribadian dan perilaku social manusia, sehingga manusia berbahasa, berimajinasi, melakukan penilaian (baik dan buruk atau benar dan salah), mengambilan keputusan seperti apa ia harus bersikap atau bertindak, serta merancang masa depan (Sherwood & Smaers, 2013;Smaers et al., 2017;Tim Sejiwa, 2018). Saat melihat konten porno pertama kali, biasanya anak akan merasa jijik dan tidak pantas karena aktifnya sistem limbik di otak. ...
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... Shape change is amplified anteriorly in hominoids, but laterally and posteriorly in cercopithecoids (figure 2b). The highly developed temporal lobes in this latter taxon are associated with increased visual acuity and geographic, individual and object recognition [32], whereas fronto-parietal reorganization in hominoids is associated with the emergence of increased cognitive capacities, tool use and language [33][34][35][36]. ...
Article
Large brains are a defining feature of primates, as is a clear allometric trend between body mass and brain size. However, important questions on the macroevolution of brain shape in primates remain unanswered. Here we address two: (i), does the relationship between the brain size and its shape follow allometric trends and (ii), is this relationship consistent over evolutionary time? We employ three-dimensional geometric morphometrics and phylogenetic comparative methods to answer these questions, based on a large sample representing 151 species and most primate families. We found two distinct trends regarding the relationship between brain shape and brain size. Hominoidea and Cercopithecinae showed significant evolutionary allometry, whereas no allometric trends were discernible for Strepsirrhini, Colobinae or Platyrrhini. Furthermore, we found that in the taxa characterized by significant allometry, brain shape evolution accelerated, whereas for taxa in which such allometry was absent, the evolution of brain shape decelerated. We conclude that although primates in general are typically described as large-brained, strong allometric effects on brain shape are largely confined to the order's representatives that display more complex behavioural repertoires.
... Association cortex volume scales differently in monkeys and apes [31][32][33], which can be taken to indicate a grade change with respect to this aspect of brain organization because a grade designates a group of species based on similar morphological traits. Here, we investigate how these differences in volume are accompanied by differences in long-range connectivity. ...
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The temporal association cortex is considered a primate specialization and is involved in complex behaviors, with some, such as language, particularly characteristic of humans. The emergence of these behaviors has been linked to major differences in temporal lobe white matter in humans compared with monkeys. It is unknown, however, how the organization of the temporal lobe differs across several anthropoid primates. Therefore, we systematically compared the organization of the major temporal lobe white matter tracts in the human, gorilla, and chimpanzee great apes and in the macaque monkey. We show that humans and great apes, in particular the chimpanzee, exhibit an expanded and more complex occipital–temporal white matter system; additionally, in humans, the invasion of dorsal tracts into the temporal lobe provides a further specialization. We demonstrate the reorganization of different tracts along the primate evolutionary tree, including distinctive connectivity of human temporal gray matter.
... Moreover, in the primate lineage, the size of a key structure implicated in mental construction-the vmPFC-co-varies with foraging complexity (Louail et al., 2019). This is consistent with accumulating evidence that a number of additional features of the prefrontal and medial cortex, which are implicated in a broad range of higher-order cognitive processes, are shared by humans with the other great apes, but less so with monkeys and lesser apes (e.g., Smaers et al., 2017;Amiez et al., 2019). This extends beyond measurements that target the size of relevant neural structures, to also include patterns of cortical serotonergic, dopaminergic and cholinergic innervation. ...
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... Indeed, such processes involve some regions of the prefrontal cortex (e.g. frontal pole, dorsal prefrontal cortex) that are characterized by an exceptional expansion in both human and great apes, with the origin of this enlargement being estimated at the root of great apes [105]. ...
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... In particular, a series of reports have considered the question of the exceptionality of the size of the human prefrontal cortex relative to other primate species (Smaers et al., 2011, Barton & Venditti, 2013a. Some of these reports suggest an exceptionally large and significantly more asymmetric prefrontal cortex (Smaers et al., 2011(Smaers et al., , 2017Smaers, 2013), whereas others find it to be as large as expected (Barton & Venditti, 2013a, b;Miller et al., 2019). The problem does not appear to be settled, but the availability of published data on prefrontal grey and white matter volume has allowed researchers to contrast their different methodological approaches using the same data. ...
... The brains of humans and other primates or rodents differ in a number of neuroanatomical patterns such as wrinkles, size, morphology, and connectivity; cell biological differences such as cell ratios and population distribution; and molecular differences such as gene expression (Hill and Walsh, 2005;Sherwood et al., 2008;Defelipe, 2011;Preuss, 2011Preuss, , 2017Gabi et al., 2016;Smaers et al., 2017;Li et al., 2018;Rilling and van den Heuvel, 2018). Structurally, the enlarged human brain is unique in the layered structure of the human cerebral cortex. ...
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The hippocampal complex (HC) is central to long‐term memory storage and retrieval as well as spatial navigation across many species. Notably, humans appear to have greatly enhanced or possibly unique HC‐mediated capacities such as constructive episodic simulation. Key studies have shown that the human HC is disproportionately large amongst hominoids, but much remains unknown at the levels of evolutionary substructural reorganization and ecological selection. Here, we calculated relative sizes of 12 HC subregions in a diverse sample of 44 primate species. We then used a Bayesian phylogenetic method, selective regime analysis, to identify 27 separate evolutionary shifts in HC organization across 65 million years of primate evolution. Additionally, a series of multi‐variate phylogenetic regressions using HC‐related ecological variables as predictors (Diet Breadth, Population Density, Group Size, Home Range Size, and Residual Home Range) revealed that relative fascia dentata and CA1 size were both significantly predicted by species' home range size (after correcting for body size). However, perhaps the most notable finding of this study was that the shifts in HC size and subregional organization in the human lineage were the largest seen in all of primate evolution, rendering modern humans with a HC that is a clear outlier amongst all non‐human primates investigated here. Given the extensive literature confirming the relationship between HC organization and function, these selective shifts are likely to have played a significant role in the emergence of human‐specific capacities, such as constructive episodic simulation. This article is protected by copyright. All rights reserved. Timeline of hippocampal complex (HC) reorganization events in primate evolution leading to the human lineage. The six key stages of this deep evolutionary history marked by violet circles over their respective nodes on the phylogenetic tree, and described in the boxes below.
Thesis
Für die meisten Säugetiere ist Navigation eine essentielle kognitive Fähigkeit. Im Bereich der Neurowissenschaften gab es immense Fortschritte im Verständnis neuronaler Grundlagen von Navigation. Diese Dissertation beschäftigt sich mit der neuronalen Grundlage von Navigation im Hinblick auf Hirnstruktur (d.h. Parasubikulum) und ethologisch relevante Verhaltensweisen (d.h. Heimkehr und Spielverhalten). Im ersten Kapitel konzentriere ich mich auf das Verhältnis von Struktur und Funktion im Parasubikulum. Wir postulieren, dass das Parasubikulum durch seine selektive Vernetzung mit dem entorhinalen Kortex, durch seine starke interne Konnektivität, sowie wegen dem hohen Grad räumlich selektiver Aktivitätsmuster seiner Neurone im Bezug auf die Kontrolle von Gitterzellaktivität und räumlicher Navigation eine herausragende Stellung einnimmt. Im zweiten Kapitel untersuche ich die neuronale Grundlage von Heimkehr. Wir nutzen die starke Verbundenheit von Laborratten zu ihrem Zuhause. Wir zeigen, dass das Parasubikulum und der entorhinale Kortex keinen expliziten Heimvektor besitzen und dass die Präsenz des Zuhauses keine globale Veränderung der neuralen Repräsentation des Raums hervorruft. Allerdings führte die Präsenz des Zuhauses oder anderer geometrischer Objekte zu einer Verzerrung von Gitterzellen. Im dritten Kapitel unteruche ich Navigation im Hinblick auf Spielverhalten. Ratten erlernen das Versteckspiel schnell und verhalten sich erstaunlich regelkonform. Zeigen Ratten spielspezifische Vokalisationen. Gleichzeitige Ableitungen neuronaler Aktivität im medialen präfrontalen Kortex offenbarten starke und spezifische Antworten der meisten Nervenzellen auf verschiedene Phasen des Spiels des spezifischen Spielkontextes wiederspiegeln. Diese Arbeit liefert durch ihren ethologischen Ansatz und durch Verhaltensanalysen von sich frei verhaltenden Tieren einen wichtigen Beitrag zum besseren Verständnis neuronaler Grundlagen von Navigation im Säugetiergehirn.
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The frontal lobe is central to distinctive aspects of human cognition and behavior. Some comparative studies link this to a larger frontal cortex and even larger frontal white matter in humans compared with other primates, yet others dispute these findings. The discrepancies between studies could be explained by limitations of the methods used to quantify volume differences across species, especially when applied to white matter connections. In this study, we used a novel tractography approach to demonstrate that frontal lobe networks, extending within and beyond the frontal lobes, occupy 66% of total brain white matter in humans and 48% in three monkey species, Chlorocebus aethiops, Macaca mulatta and Macaca fascicularis, all male. The simian-human differences in proportional frontal tract volume were significant for projection, commissural and both intra- and interlobar association tracts. Among the long association tracts the greatest difference was found for tracts involved in motor planning, auditory memory, top-down control of sensory information, and visuospatial attention, with no significant differences in frontal limbic tracts important for emotional processing. In addition we found that a non-frontal tract, the anterior commissure, had a smaller volume fraction in humans, suggesting that the disproportionally large volume of human frontal lobe connections is accompanied by a reduction in the proportion of some non-frontal connections. These findings support a hypothesis of an overall rearrangement of brain connections during human evolution.
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There has been a recent increase in the use of Cannabis-based products containing high levels of Δ⁹-tetrahydrocannabinol (THC) by adolescents. We now know this impacts adolescent cognitive function during this critical period of brain development that results in affecting select brain functions in adulthood. In this chapter, we discuss the relationship between adolescent exposure to cannabinoids, brain development, and adulthood behavioral outcomes, with a focus on mesocorticolimbic function and behaviors. After reviewing how endocannabinoids (eCB) signaling is involved in brain development, we summarize evidence gathered in human adolescents focusing on how THC exposure changes brain anatomy, connectivity, and dopaminergic function in human adults. This evidence is placed in the context of the cognitive aptitude and behaviors of adolescents and their access to high THC products and novel delivery devices. We then summarize evidence in pre-clinical rodent models, including evidence gathered at the molecular and cellular levels showing how THC/cannabinoid exposure impacts the mesocorticolimbic system and reward/addiction-like behaviors in adulthood. These results are discussed in the context of our current understanding of cannabinoid pharmacokinetics (PK) and pharmacodynamics (PD), and the role of eCB signaling in adolescent brain development. Finally, we review novel experimental approaches to study adolescence self-administration of THC in rodents and results suggesting that cannabidiol (CBD) might alleviate the impact of THC on adolescent brains. Together, this chapter emphasizes the urgent need to address the increased use of high THC products by adolescents and study the mechanism by which THC impacts adolescent brain development to help discover viable therapeutic approaches.
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Attention is fundamental to all cognition. In the primate brain, it is implemented by a large-scale network that consists of areas spanning across all major lobes, also including subcortical regions. Classical attention accounts assume that control over the selection process in this network is exerted by ‘top-down’ mechanisms in the fronto-parietal cortex that influence sensory representations via feedback signals. More recent studies have expanded this view of attentional control. In this review, we will start from a traditional top-down account of attention control, and then discuss more recent findings on feature-based attention, thalamic influences, temporal network dynamics, and behavioral dynamics that collectively lead to substantial modifications. We outline how the different emerging accounts can be reconciled and integrated into a unified theory.
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Crocodylomorpha, which includes living crocodylians and their extinct relatives, has a rich fossil record, extending back for more than 200 million years. Unlike modern semi‐aquatic crocodylians, extinct crocodylomorphs exhibited more varied lifestyles, ranging from marine to fully terrestrial forms. This ecological diversity was mirrored by a remarkable morphological disparity, particularly in terms of cranial morphology, which seems to be closely associated with ecological roles in the group. Here, I use geometric morphometrics to comprehensively investigate cranial shape variation and disparity in Crocodylomorpha. I quantitatively assess the relationship between cranial shape and ecology (i.e. terrestrial, aquatic, and semi‐aquatic lifestyles), as well as possible allometric shape changes. I also characterize patterns of cranial shape evolution and identify regime shifts. I found a strong link between shape and size, and a significant influence of ecology on the observed shape variation. Terrestrial taxa, particularly notosuchians, have significantly higher disparity, and shifts to more longirostrine regimes are associated with large‐bodied aquatic or semi‐aquatic species. This demonstrates an intricate relationship between cranial shape, body size and lifestyle in crocodylomorph evolutionary history. Additionally, disparity‐through‐time analyses were highly sensitive to different phylogenetic hypotheses, suggesting the description of overall patterns among distinct trees. For crocodylomorphs, most results agree in an early peak during the Early Jurassic and another in the middle of the Cretaceous, followed by nearly continuous decline until today. Since only crown‐group members survived through the Cenozoic, this decrease in disparity was likely the result of habitat loss, which narrowed down the range of crocodylomorph lifestyles.
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The selection of model species tends to involve two typically unstated assumptions, namely: (1) that the similarity between species decreases steadily with phylogenetic distance, and (2) that similarities are greater at lower levels of biological organization. The first assumption holds on average, but species similarities tend to decrease with the square root of divergence time, rather than linearly, and lineages with short generation times (which includes most model species) tend to diverge faster than average, making the decrease in similarity non-monotonic. The second assumption is more difficult to test. Comparative molecular research has traditionally emphasized species similarities over differences, whereas comparative research at higher levels of organization frequently highlights the species differences. However, advances in comparative genomics have brought to light a great variety of species differences, not just in gene regulation but also in protein coding genes. Particularly relevant are cases in which homologous high-level characters are based on non-homologous genes. This phenomenon of non-orthologous gene displacement, or “deep non-homology,” indicates that species differences at the molecular level can be surprisingly large. Given these observations, it is not surprising that some findings obtained in model species do not generalize across species as well as researchers had hoped, even if the research is molecular.
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The dramatic evolutionary expansion of the neocortex, together with a proliferation of specialized cortical areas, is believed to underlie the emergence of human cognitive abilities. In a broader phylogenetic context, however, neocortex evolution in mammals, including humans, is remarkably conservative, characterized largely by size variations on a shared six-layered neuronal architecture. By contrast, the telencephalon in non-mammalian vertebrates, including reptiles, amphibians, bony and cartilaginous fishes, and cyclostomes, features a great variety of very different tissue structures. Our understanding of the evolutionary relationships of these telencephalic structures, especially those of basally branching vertebrates and invertebrate chordates, remains fragmentary and is impeded by conceptual obstacles. To make sense of highly divergent anatomies requires a hierarchical view of biological organization, one that permits the recognition of homologies at multiple levels beyond neuroanatomical structure. Here we review the origin and diversification of the telencephalon with a focus on key evolutionary innovations shaping the neocortex at multiple levels of organization.
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Human cognitive abilities are generally thought to arise from cortical expansion over the course of human brain evolution. In addition to increased neuron numbers, this cortical expansion might be driven by adaptations in the properties of single neurons and their local circuits. We review recent findings on the distinct structural, functional, and transcriptomic features of human cortical neurons and their organization in cortical microstructure. We focus on the supragranular cortical layers, which showed the most prominent expansion during human brain evolution, and the properties of their principal cells: pyramidal neurons. We argue that the evolutionary adaptations in neuronal features that accompany the expansion of the human cortex partially underlie interindividual variability in human cognitive abilities.
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Comparative variation in brain size is arguably one of the most dominant features of primate evolution. Enduring questions in this context comprise whether evolutionary changes in certain brain regions outpace changes in other regions, and to what extent such regional variation between species explains comparative variation in overall brain size. To answer this question, we investigate the tempo and mode of evolution of brain organization using the largest combination of brain regions and species analyzed to date (36 brain regions, together representing over 90% of overall brain size, across 17 anthropoid primates, including humans). Following studies suggesting that the expansion of the major constituent regions of the cortico-cerebellar system (CCS) predominantly explain human brain size expansion, we test whether the link between variation in the CCS and brain size is consistent across primates. Results indicate that the constituent brain regions of the CCS show the highest rates of evolution, demonstrate a significant modular pattern of evolution, and closely align with changes in overall brain size. This phenotypic structure is consistent across different taxonomic scales, suggesting that the evolution of anthropoid brain organization is underpinned by a stable genetic structure and is characterized by a conserved evolutionary trajectory towards the CCS. Results hereby suggest that the expansion of the CCS is the primary driver of brain expansion in anthropoid primates. These findings have fundamental implications for our understanding of the nature of primate and human cognition, and the genetic and developmental structure that underpins brain evolution.
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Because of the central role of the hippocampus in representing spatial and temporal details of experience, comparative studies of its volume and structure are relevant to understanding the evolution of representational memory across species. The hippocampal formation, however, is organized into separate anatomical subregions with distinct functions, and little is known about the evolutionary diversification of these subregions. We investigate relative volumetric changes in hippocampal subregions across a large sample of primate species. We then compare the evolution of the hippocampal formation to the neocortex. Results across hippocampal subregions indicate that, compared to strepsirrhines, the anthropoid lineage displays a decrease in relative CA3, fascia dentata, subiculum, and rhinal cortex volume in tandem with an increase in relative neocortical volume. These findings indicate that hippocampal function in anthropoids might be substantially augmented by the executive decision-making functions of the neocortex. Humans are found to have a unique cerebral organization combining increased relative CA3, subiculum, and rhinal cortex with increased relative neocortical volumes, suggesting that these regions may play a role in behaviors that are uniquely specialized in humans.
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While research in previous decades demonstrated a link between the pulvinar nucleus of the thalamus and visual selective attention, the pulvinar's specific functional role has remained elusive. However, methodological advances in electrophysiological recordings in non-human primates, including simultaneous recordings in multiple brain regions, have recently begun to reveal the pulvinar's functional contributions to selective attention. These new findings suggest that the pulvinar is critical for the efficient transmission of sensory information within and between cortical regions, both synchronizing cortical activity across brain regions and controlling cortical excitability. These new findings further suggest that the pulvinar's influence on cortical processing is embedded in a dynamic selection process that balances sensory and motor functions within the large-scale network that directs selective attention.
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The development of executive functions (EF) during ascending ontogeny is addressed on the basis of current theoretical concepts of their neurobiological bases. Behavioral methods for evaluating EF in preschool children (3–6 years of age) are analyzed, as is the link between these methods and various theoretical approaches. Among existing methods of evaluating EF, methods of assessing the formation and maintenance of activity aims and plans realizing these aims are underrepresented or completely missing. Behavioral tasks which can be used to evaluate goal-setting and planning with the objective of combining behavioral, neuroimaging, and electrophysiological methods are discussed.
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Subdivisions of the prefrontal cortex (PFC) evolved at different times. Agranular parts of the PFC emerged in early mammals, and rodents, primates, and other modern mammals share them by inheritance. These are limbic areas and include the agranular orbital cortex and agranular medial frontal cortex (areas 24, 32, and 25). Rodent research provides valuable insights into the structure, functions, and development of these shared areas, but it contributes less to parts of the PFC that are specific to primates, namely, the granular, isocortical PFC that dominates the frontal lobe in humans. The first granular PFC areas evolved either in early primates or in the last common ancestor of primates and tree shrews. Additional granular PFC areas emerged in the primate stem lineage, as represented by modern strepsirrhines. Other granular PFC areas evolved in simians, the group that includes apes, humans, and monkeys. In general, PFC accreted new areas along a roughly posterior to anterior trajectory during primate evolution. A major expansion of the granular PFC occurred in humans in concert with other association areas, with modifications of corticocortical connectivity and gene expression, although current evidence does not support the addition of a large number of new, human-specific PFC areas.
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Human brains are exceptionally large, support distinctive cognitive processes, and evolved by natural selection to mediate adaptive behavior. Comparative biology situates the human brain within an evolutionary context to illuminate how it has been shaped by selection and how its structure relates to evolutionary function, while identifying the developmental and molecular changes that were involved. Recent applications of powerful phylogenetic methods have uncovered new findings, some of which overturn conventional wisdom about how and why brains evolve. Here, we focus on four long-standing claims about brain evolution and discuss how new work has either contradicted these claims or shown the relevant phenomena to be more complicated than previously appreciated. Throughout, we emphasize studies of non-human primates and hominins, our close relatives and recent ancestors.
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A crucial design feature of language useful for determining when grammatical language evolved in the human lineage is our ability to combine meaningless units to form a new unit with meaning (combinatoriality) and to further combine these meaningful units into a larger unit with a novel meaning (compositionality). There is overlap between neural bases that underlie hierarchical cognitive functions required for compositionality in both linguistic and nonlinguistic contexts (e.g., tool use). Therefore, evidence of compositional tool use in the archaeological record should signify, at the very least, the cognitive capacity for grammatical language by that point in time. We devise a novel system to evaluate the level of hierarchical nesting of tool components in single tool use activities. In the application of this system, we demonstrate that nonhuman primates, and by extension, the last common ancestor shared by Pan and Homo, are capable of basic combinatoriality; however, their technology does not approach the compositionality observable in modern human tool use. The prehistoric archaeological record supports a continuous evolution of combinatorial tool use into compositional tool use, with evidence for human-like levels of by 0.93 million years ago (Ma), or possibly as early as 1.7 Ma. While compositional language could have lagged behind compositional tool use, if language and technology coevolved according to the Technological Origin for Language hypothesis, which proposes a feedback system between the two, then evidence for hierarchical tool use structures implies a similar level of complexity in linguistic structures.
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In this article we review publications relevant to addressing widely reported claims in both the academic and popular press that chimpanzees working memory (WM) is comparable to, if not exceeding, that of humans. WM is a complex multidimensional construct with strong parallels in humans to prefrontal cortex and cognitive development. These parallels occur in chimpanzees, but to a lesser degree. We review empirical evidence and conclude that the size of WM in chimpanzees is 2 ± 1 versus Miller’s famous 7 ± 2 in humans. Comparable differences occur in experiments on chimpanzees relating to strategic and attentional WM subsystems. Regardless of the domain, chimpanzee WM performance is comparable to that of humans around the age of 4 or 5. Next, we review evidence showing parallels among the evolution of WM capacity in hominins ancestral to Homo sapiens, the phylogenetic evolution of hominins leading to Homo sapiens, and evolution in the complexity of stone tool technology over this time period.
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Transposable elements (TEs) significantly contribute to shaping the diversity of the human genome, and lines of evidence suggest TEs as one of driving forces of human brain evolution. Existing computational approaches, including cross-species comparative genomics and population genetic modeling, can be adapted for the study of the role of TEs in evolution. In particular, diverse ancient and archaic human genome sequences are increasingly available, allowing reconstruction of past human migration events and holding the promise of identifying and tracking TEs among other evolutionarily important genetic variants at an unprecedented spatiotemporal resolution. However, highly degraded short DNA templates and other unique challenges presented by ancient human DNA call for major changes in current experimental and computational procedures to enable the identification of evolutionarily important TEs. Ancient human genomes are valuable resources for investigating TEs in the evolutionary context, and efforts to explore ancient human genomes will potentially provide a novel perspective on the genetic mechanism of human brain evolution and inspire a variety of technological and methodological advances. In this review, we summarize computational and experimental approaches that can be adapted to identify and validate evolutionarily important TEs, especially for human brain evolution. We also highlight strategies that leverage ancient genomic data and discuss unique challenges in ancient transposon genomics.
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Extraversion is a consistent predictor of informal leader emergence, however little is known about extraversion’s causal effect in terms of predicting the transition to formal leadership. Using two large household samples from Germany (Study 1, n1 = 6,709) and Australia (Study 2, n2 = 6,056), we test whether trait extraversion predicts the transition of employed persons into formal leadership positions. Using survival analysis with Cox proportional hazards regression within a non‐linear generalised additive modelling (GAM) framework, we modelled the relationship between extraversion and the ‘hazard’ of transitioning into a formal leadership role. After controlling for sex, height, age, education and the other big five traits, we found that extraversion consistently predicted the hazard of transitioning into a formal leadership role over time. Given the importance of leadership to life outcomes, being more likely to transition into a formal leadership role may afford extraverts with considerable cumulative benefits over their career.
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Cognitive flexibility is a core component of executive function, a suite of cognitive capacities that enables individuals to update their behavior in dynamic environments. Human executive functions are proposed to be enhanced compared to other species, but this inference is based primarily on neuroanatomical studies. To address this, we examined the nature and origins of a core component of executive function—cognitive flexibility—in chimpanzees, our closest living relatives. Across three studies, we examined different components of cognitive flexibility using reversal learning tasks where individuals first learned one contingency and then had to shift responses when contingencies flipped. In Study 1, we tested n = 82 chimpanzees ranging from juvenility to adulthood on a spatial reversal task, to characterize the development of basic shifting skills. In Study 2, we tested how n = 24 chimpanzees use spatial versus arbitrary perceptual information to shift, a proposed difference between human and nonhuman cognition. In Study 3, we tested n = 40 chimpanzees on a probabilistic reversal task. We found an extended developmental trajectory for basic shifting and shifting in response to probabilistic feedback—chimpanzees did not reach mature performance until late in ontogeny. Additionally, females were faster to shift than males were. We also found that chimpanzees were much more successful when using spatial versus perceptual cues, and highly perseverative when faced with probabilistic versus consistent outcomes. These results identify both core features of chimpanzee cognitive flexibility that are shared with humans, as well as constraints on chimpanzee cognitive flexibility that may represent evolutionary changes in human cognitive development. This article is protected by copyright. All rights reserved
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How does the organization of neural information processing enable humans’ sophisticated cognition? Here we decompose functional interactions between brain regions into synergistic and redundant components, revealing their distinct information-processing roles. Combining functional and structural neuroimaging with meta-analytic results, we demonstrate that redundant interactions are predominantly associated with structurally coupled, modular sensorimotor processing. Synergistic interactions instead support integrative processes and complex cognition across higher-order brain networks. The human brain leverages synergistic information to a greater extent than nonhuman primates, with high-synergy association cortices exhibiting the highest degree of evolutionary cortical expansion. Synaptic density mapping from positron emission tomography and convergent molecular and metabolic evidence demonstrate that synergistic interactions are supported by receptor diversity and human-accelerated genes underpinning synaptic function. This information-resolved approach provides analytic tools to disentangle information integration from coupling, enabling richer, more accurate interpretations of functional connectivity, and illuminating how the human neurocognitive architecture navigates the trade-off between robustness and integration. Decomposing neural information into synergistic and redundant components, Luppi et al. show how core brain regions support higher cognition in virtue of their synergy, revealing that human brains leverage synergistic information more than macaques.
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The neurocircuitry that contributes to the pathophysiology of posttraumatic stress disorder (PTSD) and major depressive disorder (MDD), psychiatric conditions that exhibit a high degree of comorbidity, likely involves both overlapping and unique structural and functional changes within multiple limbic brain regions. In this review, we discuss neurobiological alterations that are associated with PTSD and MDD, and highlight both similarities and differences that may exist between these disorders to argue for the existence of a shared neurobiology. We highlight the key contributions based on preclinical studies, emerging from the late Professor Ronald Duman’s research, that have shaped our understanding of the neurocircuitry that contributes to both the etiopathology and treatment of MDD and PTSD.
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Birds share an array of unique characteristics among extant land vertebrates. Among these, external and microstructural characteristics of extant bird eggs have been linked to changes in reproductive strategy that arose among non‐avian theropod dinosaurs. More recently, differences in egg proportions recovered in crown birds relative to other dinosaurs were suggested as possibly linked to avian flight, but dense sampling close to its proposed origin was lacking. Here we assess the evolution of eggshell thickness in a targeted sample of 114 dinosaurs including birds, and test the relationship of eggshell thickness with potential life history correlates and locomotor mode using phylogenetic comparative methods. Only egg mass and flight are identified as significant predictors of eggshell thickness. While a high correlation between egg mass and eggshell thickness is expected, that relationship is much stronger in flying taxa, which show a significantly higher slope and lower residual variance than flightless species. This suggests stabilizing selection of eggshell thickness among theropods, as recovered for other traits in extant birds (e.g. genome size, metabolic rate). Within living birds, Eufalconimorphae present an apomorphic increase in relative eggshell thickness which remains unexplained, as few morphological synapomorphies of this clade have been identified. This article is protected by copyright. All rights reserved
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Relative brain size has long been considered a reflection of cognitive capacities and has played a fundamental role in developing core theories in the life sciences. Yet, the notion that relative brain size validly represents selection on brain size relies on the untested assumptions that brain-body allometry is restrained to a stable scaling relationship across species and that any deviation from this slope is due to selection on brain size. Using the largest fossil and extant dataset yet assembled, we find that shifts in allometric slope underpin major transitions in mam-malian evolution and are often primarily characterized by marked changes in body size. Our results reveal that the largest-brained mammals achieved large relative brain sizes by highly divergent paths. These findings prompt a reevaluation of the traditional paradigm of relative brain size and open new opportunities to improve our understanding of the genetic and developmental mechanisms that influence brain size.
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Among the many lines of research that have been exploring how embodiment contributes to cognition, one focuses on how the neural substrates of language may be shared, or at least closely coupled, with those of action. This paper revisits a particular proposal that has received considerable attention—namely, that the forms of hierarchical sequencing that characterize both linguistic syntax and goal-directed action are underpinned partly by common mechanisms in left Brodmann area (BA) 44, a cortical region that is not only classically regarded as part of Broca's area, but is also a core component of the human Mirror Neuron System. First, a recent multi-participant, multi-round debate about this proposal is summarized together with some other relevant findings. This review reveals that while the proposal is supported by a variety of theoretical arguments and empirical results, it still faces several challenges. Next, a narrower application of the proposal is discussed, specifically involving the basic word order of subject (S), object (O), and verb (V) in simple transitive clauses. Most languages are either SOV or SVO, and, building on prior work, it is argued that these strong syntactic tendencies derive from how left BA44 represents the sequential-hierarchical structure of goal-directed actions. Finally, with the aim of clarifying what it might mean for syntax and action to have "common" neural mechanisms in left BA44, two different versions of the main proposal are distinguished. Hypothesis 1 states that the very same neural mechanisms in left BA44 subserve some aspects of hierarchical sequencing for syntax and action, whereas Hypothesis 2 states that anatomically distinct but functionally parallel neural mechanisms in left BA44 subserve some aspects of hierarchical sequencing for syntax and action. Although these two hypotheses make different predictions, at this point neither one has significantly more explanatory power than the other, and further research is needed to elaborate and test them.
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Many aspects of cognition and behaviour are regulated by noradrenergic projections to the forebrain originating from the locus coeruleus, acting through alpha and beta adrenoreceptors. Loss of these projections is common in neurodegenerative diseases and contributes to their cognitive and behavioural deficits. We review the evidence for a noradrenergic modulation of cognition in its contribution to Alzheimer's disease, Parkinson's disease and other cognitive disorders. We discuss the advances in human imaging and computational methods that quantify the locus coeruleus and its function in humans, and highlight the potential for new noradrenergic treatment strategies.
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We generated induced excitatory neurons (iNeurons, iNs) from chimpanzee, bonobo and human stem cells by expressing the transcription factor neurogenin‑2 (NGN2). Single cell RNA sequencing (scRNAseq) showed that genes involved in dendrite and synapse development are expressed earlier during iNs maturation in the chimpanzee and bonobo than the human cells. In accordance, during the first two weeks of differentiation, chimpanzee and bonobo iNs showed repetitive action potentials and more spontaneous excitatory activity than human iNs, and extended neurites of higher total length. However, the axons of human iNs were slightly longer at 5 weeks of differentiation. The timing of the establishment of neuronal polarity did not differ between the species. Chimpanzee, bonobo and human neurites eventually reached the same level of structural complexity. Thus, human iNs develop slower than chimpanzee and bonobo iNs and this difference in timing likely depends on functions downstream of NGN2.
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In classical neuroscience experiments, neural activity is measured across many identical trials of animals performing simple tasks and is then analyzed, associating neural responses to pre-defined experimental parameters. This type of analysis is not suitable for patterns of behavior that unfold freely, such as play behavior. Here, we attempt an alternative approach for exploratory data analysis on a single-trial level, applicable in more complex and naturalistic behavioral settings in which no two trials are identical. We analyze neural population activity in the prefrontal cortex (PFC) of rats playing hide-and-seek and show that it is possible to discover what aspects of the task are reflected in the recorded activity with a limited number of simultaneously recorded cells (≤ 31). Using hidden Markov models, we cluster population activity in the PFC into a set of neural states, each associated with a pattern of neural activity. Despite high variability in behavior, relating the inferred states to the events of the hide-and-seek game reveals neural states that consistently appear at the same phases of the game. Furthermore, we show that by applying the segmentation inferred from neural data to the animals’ behavior, we can explore and discover novel correlations between neural activity and behavior. Finally, we replicate the results in a second dataset and show that population activity in the PFC displays distinct sets of states during playing hide-and-seek and observing others play the game. Overall, our results reveal robust, state-like representations in the rat PFC during unrestrained playful behavior and showcase the applicability of population analyses in naturalistic neuroscience.
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A wide homology between human and macaque striatum is often assumed as in both the striatum is involved in cognition, emotion and executive functions. However, differences in functional and structural organization between human and macaque striatum may reveal evolutionary divergence and shed light on human vulnerability to neuropsychiatric diseases. For instance, dopaminergic dysfunction of the human striatum is considered to be a pathophysiological underpinning of different disorders, such as Parkinson's disease (PD) and schizophrenia (SCZ). Previous investigations have found a wide similarity in structural connectivity of the striatum between human and macaque, leaving the cross-species comparison of its functional organization unknown. In this study, resting-state functional connectivity (RSFC) derived striatal parcels were compared based on their homologous cortico-striatal connectivity. The goal here was to identify striatal parcels whose connectivity is human-specific compared to macaque parcels. Functional parcellation revealed that the human striatum was split into dorsal, dorsomedial, and rostral caudate and ventral, central, and caudal putamen, while the macaque striatum was divided into dorsal, and rostral caudate and rostral, and caudal putamen. Cross-species comparison indicated dissimilar cortico-striatal RSFC of the topographically similar dorsal caudate. We probed clinical relevance of the striatal clusters by examining differences in their cortico-striatal RSFC and gray matter (GM) volume between patients (with PD and SCZ) and healthy controls. We found abnormal RSFC not only between dorsal caudate, but also between rostral caudate, ventral, central and caudal putamen and widespread cortical regions for both PD and SCZ patients. Also, we observed significant structural atrophy in rostral caudate, ventral and central putamen for both PD and SCZ while atrophy in the dorsal caudate was specific to PD. Taken together, our cross-species comparative results revealed shared and human-specific RSFC of different striatal clusters reinforcing the complex organization and function of the striatum. In addition, we provided a testable hypothesis that abnormalities in a region with human-specific connectivity, i.e., dorsal caudate, might be associated with neuropsychiatric disorders.
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The first few months after birth, when a child begins to interact with the environment, are critical to human brain development. The human frontal lobe is important for social behavior and executive function; it has increased in size and complexity relative to other species, but the processes that have contributed to this expansion are unknown. Our studies of postmortem infant human brains revealed a collection of neurons that migrate and integrate widely into the frontal lobe during infancy. Chains of young neurons move tangentially close to the walls of the lateral ventricles and along blood vessels. These cells then individually disperse long distances to reach cortical tissue, where they differentiate and contribute to inhibitory circuits. Late-arriving interneurons could contribute to developmental plasticity, and the disruption of their postnatal migration or differentiation may underlie neurodevelopmental disorders. © 2016, American Association for the Advancement of Science. All rights reserved.
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Phylogenetic generalized least squares (PGLS) has become one of the most commonly used phylogenetic comparative methods. Despite its common use, descriptions and applications of methods to test for species' deviations from allometric predictions using phylogenetic regression have been piecemeal. We simplify previous computational descriptions of PGLS standard errors in a manner that can be easily generalized towards more complex general linear models. We focus on the implementation of phylogenetic analysis of covariance, which provides a direct test for the equality of intercepts and slopes. Our computational descriptions allow testing whether individual species, or a group of species, deviate significantly from allometric predictions. The use of PGLS confidence and prediction intervals and phylogenetic analysis of covariance is exemplified in an analysis of brain structure volumes in primates. This article is protected by copyright. All rights reserved.
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Phylogenetic comparative analysis is an approach to inferring evolutionary process from a combination of phylogenetic and phenotypic data. The last few years have seen increasingly sophisticated models employed in the evaluation of more and more detailed evolutionary hypotheses, including adaptive hypotheses with multiple selective optima and hypotheses with rate variation within and across lineages. The statistical performance of these sophisticated models has received relatively little systematic attention, however. We conducted an extensive simulation study to quantify the statistical properties of a class of models toward the simpler end of the spectrum that model phenotypic evolution using Ornstein-Uhlenbeck processes. We focused on identifying where, how, and why these methods break down so that users can apply them with greater understanding of their strengths and weaknesses. Our analysis identifies three key determinants of performance: a discriminability ratio, a signal-to-noise ratio, and the number of taxa sampled. Interestingly, we find that model-selection power can be high even in regions that were previously thought to be difficult, such as when tree size is small. On the other hand, we find that model parameters are in many circumstances difficult to estimate accurately, indicating a relative paucity of information in the data relative to these parameters. Nevertheless, we note that accurate model selection is often possible when parameters are only weakly identified. Our results have implications for more sophisticated methods inasmuch as the latter are generalizations of the case we study. © The Author(s) 2015. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For Permissions, please email: journals.permissions@oup.com.
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Phenotypic integration is a pervasive characteristic of organisms. Numerous analyses have demonstrated that patterns of phenotypic integration are conserved across large clades, but that significant variation also exists. For example, heterochronic shifts related to different mammalian reproductive strategies are reflected in postcranial skeletal integration and in coordination of bone ossification. Phenotypic integration and modularity have been hypothesized to shape morphological evolution, and we extended simulations to confirm that trait integration can influence both the trajectory and magnitude of response to selection. We further demonstrate that phenotypic integration can produce both more and less disparate organisms than would be expected under random walk models by repartitioning variance in preferred directions. This effect can also be expected to favour homoplasy and convergent evolution. New empirical analyses of the carnivoran cranium show that rates of evolution, in contrast, are not strongly influenced by phenotypic integration and show little relationship to morphological disparity, suggesting that phenotypic integration may shape the direction of evolutionary change, but not necessarily the speed of it. Nonetheless, phenotypic integration is problematic for morphological clocks and should be incorporated more widely into models that seek to accurately reconstruct both trait and organismal evolution.
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A general model of neural development is derived to fit 18 mammalian species, including humans, macaques, several rodent species, and six metatherian (marsupial) mammals. The goal of this work is to describe heterochronic changes in brain evolution within its basic developmental allometry, and provide an empirical basis to recognize equivalent maturational states across animals. The empirical data generating the model comprises 271 developmental events, including measures of initial neurogenesis, axon extension, establishment, and refinement of connectivity, as well as later events such as myelin formation, growth of brain volume, and early behavioral milestones, to the third year of human postnatal life. The progress of neural events across species is sufficiently predictable that a single model can be used to predict the timing of all events in all species, with a correlation of modeled values to empirical data of 0.9929. Each species' rate of progress through the event scale, described by a regression equation predicting duration of development in days, is highly correlated with adult brain size. Neural heterochrony can be seen in selective delay of retinogenesis in the cat, associated with greater numbers of rods in its retina, and delay of corticogenesis in all species but rodents and the rabbit, associated with relatively larger cortices in species with delay. Unexpectedly, precocial mammals (those unusually mature at birth) delay the onset of first neurogenesis but then progress rapidly through remaining developmental events.
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"In vivo Brodmann mapping" or non-invasive cortical parcellation using MRI, especially by measuring cortical myelination, has recently become a popular research topic, though myeloarchitectonic cortical parcellation in humans previously languished in favor of cytoarchitecture. We review recent in vivo myelin mapping studies and discuss some of the different methods for estimating myelin content. We discuss some ways in which myelin maps may improve surface registration and be useful for cross-modal and cross-species comparisons, including some preliminary cross-species results. Next, we consider neurobiological aspects of why some parts of cortex are more myelinated than others. Myelin content is inversely correlated with intracortical circuit complexity-in general, more myelin content means simpler and perhaps less dynamic intracortical circuits. Using existing PET data and functional network parcellations, we examine metabolic differences in the differently myelinated cortical functional networks. Lightly myelinated cognitive association networks tend to have higher aerobic glycolysis than heavily myelinated early sensory-motor ones, perhaps reflecting greater ongoing dynamic anabolic cortical processes. This finding is consistent with the hypothesis that intracortical myelination may stabilize intracortical circuits and inhibit synaptic plasticity. Finally, we discuss the future of the in vivo myeloarchitectural field and cortical parcellation--"in vivo Brodmann mapping"--in general.
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Nerve myelination facilitates saltatory action potential conduction and exhibits spatiotemporal variation during development associated with the acquisition of behavioral and cognitive maturity. Although human cognitive development is unique, it is not known whether the ontogenetic progression of myelination in the human neocortex is evolutionarily exceptional. In this study, we quantified myelinated axon fiber length density and the expression of myelin-related proteins throughout postnatal life in the somatosensory (areas 3b/3a/1/2), motor (area 4), frontopolar (prefrontal area 10), and visual (areas 17/18) neocortex of chimpanzees (N = 20) and humans (N = 33). Our examination revealed that neocortical myelination is developmentally protracted in humans compared with chimpanzees. In chimpanzees, the density of myelinated axons increased steadily until adult-like levels were achieved at approximately the time of sexual maturity. In contrast, humans displayed slower myelination during childhood, characterized by a delayed period of maturation that extended beyond late adolescence. This comparative research contributes evidence crucial to understanding the evolution of human cognition and behavior, which arises from the unfolding of nervous system development within the context of an enriched cultural environment. Perturbations of normal developmental processes and the decreased expression of myelin-related molecules have been related to psychiatric disorders such as schizophrenia. Thus, these species differences suggest that the human-specific shift in the timing of cortical maturation during adolescence may have implications for vulnerability to certain psychiatric disorders.
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The primate cerebral cortex is characterized by regional variation in the structure of pyramidal neurons, with more complex dendritic arbors and greater spine density observed in prefrontal compared with sensory and motor cortices. Although there are several investigations in humans and other primates, virtually nothing is known about regional variation in the morphology of pyramidal neurons in the cerebral cortex of great apes, humans' closest living relatives. The current study uses the rapid Golgi stain to quantify the dendritic structure of layer III pyramidal neurons in 4 areas of the chimpanzee cerebral cortex: Primary somatosensory (area 3b), primary motor (area 4), prestriate visual (area 18), and prefrontal (area 10) cortex. Consistent with previous studies in humans and macaque monkeys, pyramidal neurons in the prefrontal cortex of chimpanzees exhibit greater dendritic complexity than those in other cortical regions, suggesting that prefrontal cortical evolution in primates is characterized by increased potential for integrative connectivity. Compared with chimpanzees, the pyramidal neurons of humans had significantly longer and more branched dendritic arbors in all cortical regions.
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Increased connectivity of high-order association regions in the neocortex has been proposed as a defining feature of human brain evolution. At present, however, there are limited comparative data to examine this claim fully. We tested the hypothesis that the distribution of neuropil across areas of the neocortex of humans differs from that of one of our closest living relatives, the common chimpanzee. The neuropil provides a proxy measure of total connectivity within a local region because it is composed mostly of dendrites, axons, and synapses. Using image analysis techniques, we quantified the neuropil fraction from both hemispheres in six cytoarchitectonically defined regions including frontopolar cortex (area 10), Broca's area (area 45), frontoinsular cortex (area FI), primary motor cortex (area 4), primary auditory cortex (area 41/42), and the planum temporale (area 22). Our results demonstrate that humans exhibit a unique distribution of neuropil in the neocortex compared to chimpanzees. In particular, the human frontopolar cortex and the frontoinsular cortex had a significantly higher neuropil fraction than the other areas. In chimpanzees these prefrontal regions did not display significantly more neuropil, but the primary auditory cortex had a lower neuropil fraction than other areas. Our results support the conclusion that enhanced connectivity in the prefrontal cortex accompanied the evolution of the human brain. These species differences in neuropil distribution may offer insight into the neural basis of human cognition, reflecting enhancement of the integrative capacity of the prefrontal cortex.
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Over the course of ontogenesis, the human brain and human cognitive abilities develop in parallel, resulting in a phenotype strikingly distinct from that of other primates. Here, we used microarrays and RNA-sequencing to examine human-specific gene expression changes taking place during postnatal brain development in the prefrontal cortex and cerebellum of humans, chimpanzees, and rhesus macaques. We show that the most prominent human-specific expression change affects genes associated with synaptic functions and represents an extreme shift in the timing of synaptic development in the prefrontal cortex, but not the cerebellum. Consequently, peak expression of synaptic genes in the prefrontal cortex is shifted from <1 yr in chimpanzees and macaques to 5 yr in humans. This result was supported by protein expression profiles of synaptic density markers and by direct observation of synaptic density by electron microscopy. Mechanistically, the human-specific change in timing of synaptic development involves the MEF2A-mediated activity-dependent regulatory pathway. Evolutionarily, this change may have taken place after the split of the human and the Neanderthal lineages.
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While multiple studies have reported the accelerated evolution of brain gene expression in the human lineage, the mechanisms underlying such changes are unknown. Here, we address this issue from a developmental perspective, by analyzing mRNA and microRNA (miRNA) expression in two brain regions within macaques, chimpanzees, and humans throughout their lifespan. We find that constitutive gene expression divergence (species differences independent of age) is comparable between humans and chimpanzees. However, humans display a 3-5 times faster evolutionary rate in divergence of developmental patterns, compared to chimpanzees. Such accelerated evolution of human brain developmental patterns (i) cannot be explained by life-history changes among species, (ii) is twice as pronounced in the prefrontal cortex than the cerebellum, (iii) preferentially affects neuron-related genes, and (iv) unlike constitutive divergence does not depend on cis-regulatory changes, but might be driven by human-specific changes in expression of trans-acting regulators. We show that developmental profiles of miRNAs, as well as their target genes, show the fastest rates of human-specific evolutionary change, and using a combination of computational and experimental methods, we identify miR-92a, miR-454, and miR-320b as possible regulators of human-specific neural development. Our results suggest that different mechanisms underlie adaptive and neutral transcriptome divergence, and that changes in the expression of a few key regulators may have been a major driving force behind rapid evolution of the human brain.
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Detailed cytoarchitectonic studies of the human cerebral cortex appeared during the first quarter of the 20th century. The incorporation of the cytoarchitectonic map by Brodmann (1909) in the Talairach proportional stereotaxic space (Talairach and Tournoux, 1988) has established the Brodmann numerical nomenclature as the basis for describing the cortical location of structural and functional findings obtained with modern neuroimaging. In experimental anatomical and physiological investigations of the macaque monkey performed during the last 50 years, the numerical architectonic nomenclature used to describe findings in the prefrontal cortex has been largely based on the map by Walker (1940). Unfortunately, the map by Walker was not based on a comparative investigation of the cytoarchitecture of the human and macaque monkey prefrontal cortex and, as a result, the nomenclature and the criteria for demarcating areas in the two primate species are not always consistent. These discrepancies are a major obstacle in the ability to compare experimental findings from nonhuman primates with results obtained in functional and structural neuroimaging of the human brain. The present article outlines these discrepancies in the classical maps and describes comparative investigations of the cytoarchitecture of the prefrontal cortex of the macaque monkey and human (Petrides and Pandya, 1994, 1999, 2002a) in order to resolve these discrepancies and enable easy translation of experimental research in the monkey to findings in the human brain obtained with modern neuroimaging.
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The prefrontal cortex is commonly associated with cognitive capacities related to human uniqueness: purposeful actions towards higher-level goals, complex social information processing, introspection, and language. Comparative investigations of the prefrontal cortex may thus shed more light on the neural underpinnings of what makes us human. Using histological data from 19 anthropoid primate species (6 apes including humans and 13 monkeys), we investigate cross-species relative size changes along the anterior (prefrontal) and posterior (motor) axes of the cytoarchitectonically defined frontal lobe in both hemispheres. Results reveal different scaling coefficients in the left versus right prefrontal hemisphere, suggest that the primary factor underlying the evolution of primate brain architecture is left hemispheric prefrontal hyperscaling, and indicate that humans are the extreme of a left prefrontal ape specialization in relative white to grey matter volume. These results demonstrate a neural adaptive shift distinguishing the ape from the monkey radiation possibly related to a cognitive grade shift between (great) apes and other primates.
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In development, timing is of the utmost importance, and the timing of developmental processes often changes as organisms evolve. In human evolution, developmental retardation, or neoteny, has been proposed as a possible mechanism that contributed to the rise of many human-specific features, including an increase in brain size and the emergence of human-specific cognitive traits. We analyzed mRNA expression in the prefrontal cortex of humans, chimpanzees, and rhesus macaques to determine whether human-specific neotenic changes are present at the gene expression level. We show that the brain transcriptome is dramatically remodeled during postnatal development and that developmental changes in the human brain are indeed delayed relative to other primates. This delay is not uniform across the human transcriptome but affects a specific subset of genes that play a potential role in neural development.
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Analysis of data collected on 131 species of primates, bats, and insectivores showed that the sizes of brain components, from medulla to forebrain, are highly predictable from absolute brain size by a nonlinear function. The order of neurogenesis was found to be highly conserved across a wide range of mammals and to correlate with the relative enlargement of structures as brain size increases, with disproportionately large growth occurring in late-generated structures. Because the order of neurogenesis is conserved, the most likely brain alteration resulting from selection for any behavioral ability may be a coordinated enlargement of the entire nonolfactory brain.
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This article reviews attempts to characterize the mental operations mediated by left inferior prefrontal cortex, especially the anterior and inferior portion of the gyrus, with the functional neuroimaging techniques of positron emission tomography and functional magnetic resonance imaging. Activations in this region occur during semantic, relative to nonsemantic, tasks for the generation of words to semantic cues or the classification of words or pictures into semantic categories. This activation appears in the right prefrontal cortex of people known to be atypically right-hemisphere dominant for language. In this region, activations are associated with meaningful encoding that leads to superior explicit memory for stimuli and deactivations with implicit semantic memory (repetition priming) for words and pictures. New findings are reported showing that patients with global amnesia show deactivations in the same region associated with repetition priming, that activation in this region reflects selection of a response from among numerous relative to few alternatives, and that activations in a portion of this region are associated specifically with semantic relative to phonological processing. It is hypothesized that activations in left inferior prefrontal cortex reflect a domain-specific semantic working memory capacity that is invoked more for semantic than nonsemantic analyses regardless of stimulus modality, more for initial than for repeated semantic analysis of a word or picture, more when a response must be selected from among many than few legitimate alternatives, and that yields superior later explicit memory for experiences.
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The prefrontal cortex has long been suspected to play an important role in cognitive control, in the ability to orchestrate thought and action in accordance with internal goals. Its neural basis, however, has remained a mystery. Here, we propose that cognitive control stems from the active maintenance of patterns of activity in the prefrontal cortex that represent goals and the means to achieve them. They provide bias signals to other brain structures whose net effect is to guide the flow of activity along neural pathways that establish the proper mappings between inputs, internal states, and outputs needed to perform a given task. We review neurophysiological, neurobiological, neuroimaging, and computational studies that support this theory and discuss its implications as well as further issues to be addressed
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Geographic variation in some aspects of chimpanzee behavior has been interpreted as evidence for culture. Here we document similar geographic variation in orangutan behaviors. Moreover, as expected under a cultural interpretation, we find a correlation between geographic distance and cultural difference, a correlation between the abundance of opportunities for social learning and the size of the local cultural repertoire, and no effect of habitat on the content of culture. Hence, great-ape cultures exist, and may have done so for at least 14 million years.
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The cortical circuits subserving neural processing of human language are localized to the inferior frontal operculum and the posterior perisylvian region. Functional language dominance has been related to anatomical asymmetry of Broca's area and the planum temporale. The evolutionary history of these asymmetric patterns, however, remains obscure. Although testing of hypotheses about the evolution of language areas requires comparison to homologous regions in the brains of our closest living relatives, the great apes, to date little is known about normal interindividual variation of these regions in this group. Here we focus on Brodmann's area 44 in African great apes (Pan troglodytes and Gorilla gorilla). This area corresponds to the pars opercularis of the inferior frontal gyrus (IFG), and has been shown to exhibit both gross and cytoarchitectural asymmetries in humans. We calculated frequencies of sulcal variations and mapped the distribution of cytoarchitectural area 44 to determine whether its boundaries occurred at consistent macrostructural landmarks. A considerable amount of variation was found in the distribution of the inferior frontal sulci among great ape brains. The inferior precentral sulcus in particular was often bifurcated, which made it impossible to determine the posterior boundary of the pars opercularis. In addition, the distribution of Brodmann's area 44 showed very little correspondence to surface anatomy. We conclude that gross morphologic patterns do not offer substantive landmarks for the measurement of Brodmann's area 44 in great apes. Whether or not Broca's area homologue of great apes exhibits humanlike asymmetry can only be resolved through further analyses of microstructural components.
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A rapidly growing number of recent studies show that imagining the future depends on much of the same neural machinery that is needed for remembering the past. These findings have led to the concept of the prospective brain; an idea that a crucial function of the brain is to use stored information to imagine, simulate and predict possible future events. We suggest that processes such as memory can be productively re-conceptualized in light of this idea.
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The arcuate fasciculus is a white-matter fiber tract that is involved in human language. Here we compared cortical connectivity in humans, chimpanzees and macaques (Macaca mulatta) and found a prominent temporal lobe projection of the human arcuate fasciculus that is much smaller or absent in nonhuman primates. This human specialization may be relevant to the evolution of language.
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Planning for future needs has traditionally been considered to be restricted to human cognition. Although recent studies on great ape and corvid cognition challenge this belief, the phylogenesis of human planning remains largely unknown. The complex skill for future planning has not yet been satisfactorily established in any other extant primate species than our own. In humans, planning for future needs rely heavily on two overarching capacities, both of which lie at the heart of our cognition: self-control, often defined as the suppression of immediate drives in favor of delayed rewards, and mental time travel, which could be described as a detached mental experience of a past or future event. Future planning is linked to additional high complexity cognition such as metacognition and a consciousness usually not attributed to animals. In a series of four experiments based on tool use, we demonstrate that chimpanzees (Pan troglodytes) and orangutans (Pongo abelii) override immediate drives in favor of future needs, and they do not merely rely on associative learning or semantic prospection when confronted with a planning task. These results suggest that great apes engage in planning for the future by out competing current drives and mentally pre-experiencing an upcoming event. This suggests that the advanced mental capacities utilized in human future planning are shared by phylogenetically more ancient species than previously believed.
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Human evolution is widely thought to have involved a particular expansion of prefrontal cortex. This popular notion has recently been challenged, although controversies remain. Here we show that the prefrontal region of both human and nonhuman primates holds about 8% of cortical neurons, with no clear difference across humans and other primates in the distribution of cortical neurons or white matter cells along the anteroposterior axis. Further, we find that the volumes of human prefrontal gray and white matter match the expected volumes for the number of neurons in the gray matter and for the number of other cells in the white matter compared with other primate species. These results indicate that prefrontal cortical expansion in human evolution happened along the same allometric trajectory as for other primate species, without modification of the distribution of neurons across its surface or of the volume of the underlying white matter. We thus propose that the most distinctive feature of the human prefrontal cortex is its absolute number of neurons, not its relative volume.
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The detection of evolutionary shifts in trait evolution from extant taxa is motivated by the study of convergent evolution, or to correlate shifts in traits with habitat changes or with changes in other phenotypes. We propose here a phylogenetic lasso method to study trait evolution from comparative data and detect past changes in the expected mean trait values. We use the Ornstein-Uhlenbeck process, which can model a changing adaptive landscape over time and over lineages. Our method is very fast, running in minutes for hundreds of species, and can handle multiple traits. We also propose a phylogenetic Bayesian information criterion (pBIC) that accounts for the phylogenetic correlation between species, as well as for the complexity of estimating an unknown number of shifts at unknown locations in the phylogeny. This criterion does not suffer model overfitting and has high precision, so it offers a conservative alternative to other information criteria. Our re-analysis of Anolis lizard data suggests a more conservative scenario of morphological adaptation and convergence than previously proposed. Software is available on GitHub. This article is protected by copyright. All rights reserved.
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1.For the study of macroevolution, phenotypic data are analyzed across species on a dated phylogeny using phylogenetic comparative methods. In this context, the Ornstein-Uhlenbeck (OU) process is now being used extensively to model selectively-driven trait evolution, whereby a trait is attracted to a selection optimum μ.2.We report here theoretical properties of the maximum likelihood (ML) estimators for these parameters, including their non-uniqueness and inaccuracy, and show that theoretical expectations indeed apply to real trees. We provide necessary conditions for ML estimators to be well-defined and practical implications for model parametrization.3.We then show how these limitations carry over to difficulties in detecting shifts in selection regimes along a phylogeny. When the phylogenetic placement of these shifts is unknown, we identify a “large p - small n” problem where traditional model selection criteria fail and favor overly complex scenarios. Instead, we propose a modified criterion that is better adapted to change-point models.4.The challenges we identify here are inherent to trait evolution models on phylogenetic trees when observations are limited to present-day taxa, and require the addition of fossil taxa to be alleviated. We conclude with recommendations for empiricists.This article is protected by copyright. All rights reserved.
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There has been no agreement as to whether the prefrontal cortex is especially enlarged in the human brain. To answer this question, we analyzed the only two datasets that provide information on total prefrontal cortex volume based on cytoarchitectonic criteria. One delineated the prefrontal cortex proper on the basis of cytoarchitectonic criteria; the other used a proxy of the prefrontal cortex based on a cytoarchitectonic delineation of the frontal lobe. To investigate whether all cortical association areas, including the prefrontal cortex, are enlarged in the human brain, we scaled the different areas to a common reference, the primary visual cortex. To investigate whether the prefrontal cortex is more enlarged than other association areas, we scaled it relative to its inputs from and outputs to other nonprimary areas. We carried out separate regression analyses using different data samples as a predictive baseline group: data for monkeys alone informs us on whether great apes are different from monkeys; data for all non-human anthropoids, including great apes, informs us on whether humans are different from all other primates. The analyses show that the value for the human prefrontal cortex is greater than expected, and that this is true even when data for the great apes are included in the analysis. They also show that the chimpanzee prefrontal cortex is greater than expected for a monkey with a similar sized cortex. We discuss possible functional consequences. © 2014 S. Karger AG, Basel.
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Increased relative brain size characterizes the evolution of primates, suggesting that enhanced cognition plays an important part in the behavioral adaptations of this mammalian order. In addition to changes in brain anatomy, cognition can also be regulated by molecular changes that alter synaptic function, but little is known about modifications of synapses in primate brain evolution. The aim of the current study was to investigate the expression patterns and evolution of 20 synaptic genes from the prefrontal cortex of 12 primate species. The genes investigated included glutamate receptors, scaffolding proteins, synaptic vesicle components, as well as factors involved in synaptic vesicle release and structural components of the nervous system. Our analyses revealed that there have been significant changes during primate brain evolution in the components of the glutamatergic signaling pathway in terms of gene expression, protein expression, and promoter sequence changes. These results could entail functional modifications in the regulation of specific genes related to processes underlying learning and memory.
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Comparative neuroanatomy shows that new prefrontal areas emerged during the evolution of anthropoid primates to augment prefrontal, parietal, and temporal areas that had evolved in earlier primates. We recently proposed that the new anthropoid areas reduce foraging errors by generating goals from current contexts and learning to do so rapidly, sometimes based on single events. Among the contexts used to generate these goals, the posterior parietal cortex provides the new prefrontal areas with information about relational metrics such as order, number, duration, length, distance and proportion, which play a crucial role in foraging choices. Here we propose that this specialized network later became adapted to support the human capacity for reasoning and general problem-solving.
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Evolutionary neuroscientists seek to understand what makes the human neocortex special aside from its extraordinary expansion. New analyses find that the frontal lobes of humans are not relatively enlarged given our species' brain size. But are statistical cut-offs masking biologically meaningful changes in the size of the human prefrontal cortex?
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One of the most pervasive assumptions about human brain evolution is that it involved relative enlargement of the frontal lobes. We show that this assumption is without foundation. Analysis of five independent data sets using correctly scaled measures and phylogenetic methods reveals that the size of human frontal lobes, and of specific frontal regions, is as expected relative to the size of other brain structures. Recent claims for relative enlargement of human frontal white matter volume, and for relative enlargement shared by all great apes, seem to be mistaken. Furthermore, using a recently developed method for detecting shifts in evolutionary rates, we find that the rate of change in relative frontal cortex volume along the phylogenetic branch leading to humans was unremarkable and that other branches showed significantly faster rates of change. Although absolute and proportional frontal region size increased rapidly in humans, this change was tightly correlated with corresponding size increases in other areas and whole brain size, and with decreases in frontal neuron densities. The search for the neural basis of human cognitive uniqueness should therefore focus less on the frontal lobes in isolation and more on distributed neural networks.
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Comparative analyses of primate brain evolution have highlighted changes in size and internal organization as key factors underlying species diversity. It remains, however, unclear (i) how much variation in mosaic brain reorganization versus variation in relative brain size contributes to explaining the structural neural diversity observed across species, (ii) which mosaic changes contribute most to explaining diversity, and (iii) what the temporal origin, rates and processes are that underlie evolutionary shifts in mosaic reorganization for individual branches of the primate tree of life. We address these questions by combining novel comparative methods that allow assessing the temporal origin, rate and process of evolutionary changes on individual branches of the tree of life, with newly available data on volumes of key brain structures (prefrontal cortex, frontal motor areas and cerebrocerebellum) for a sample of 17 species (including humans). We identify patterns of mosaic change in brain evolution that mirror brain systems previously identified by electrophysiological and anatomical tract-tracing studies in non-human primates and functional connectivity MRI studies in humans. Across more than 40 Myr of anthropoid primate evolution, mosaic changes contribute more to explaining neural diversity than changes in relative brain size, and different mosaic patterns are differentially selected for when brains increase or decrease in size. We identify lineage-specific evolutionary specializations for all branches of the tree of life covered by our sample and demonstrate deep evolutionary roots for mosaic patterns associated with motor control and learning.
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Understanding human-specific patterns of brain gene expression and regulation can provide key insights into human brain evolution and speciation. Here, we use next-generation sequencing, and Illumina and Affymetrix microarray platforms, to compare the transcriptome of human, chimpanzee, and macaque telencephalon. Our analysis reveals a predominance of genes differentially expressed within human frontal lobe and a striking increase in transcriptional complexity specific to the human lineage in the frontal lobe. In contrast, caudate nucleus gene expression is highly conserved. We also identify gene coexpression signatures related to either neuronal processes or neuropsychiatric diseases, including a human-specific module with CLOCK as its hub gene and another module enriched for neuronal morphological processes and genes coexpressed with FOXP2, a gene important for language evolution. These data demonstrate that transcriptional networks have undergone evolutionary remodeling even within a given brain region, providing a window through which to view the foundation of uniquely human cognitive capacities.
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This paper posits that the brain evolved for the control of action rather than for the development of cognition per se. We note that the terms commonly used to describe brain-behavior relationships define, and in many ways limit, how we conceptualize and investigate them and may therefore constrain the questions we ask and the utility of the "answers" we generate. Many constructs are so nonspecific and over-inclusive as to be scientifically meaningless. "Executive function" is one such term in common usage. As the construct is increasingly focal in neuroscience research, defining it clearly is critical. We propose a definition that places executive function within a model of continuous sensorimotor interaction with the environment. We posit that control of behavior is the essence of "executive function," and we explore the evolutionary advantage conferred by being able to anticipate and control behavior with both implicit and explicit mechanisms. We focus on the cerebellum's critical role in these control processes. We then hypothesize about the ways in which procedural (skill) learning contributes to the acquisition of declarative (semantic) knowledge. We hypothesize how these systems might interact in the process of grounding knowledge in sensorimotor anticipation, thereby directly linking movement to thought and "embodied cognition." We close with a discussion of ways in which the cerebellum instructs frontal systems how to think ahead by providing anticipatory control mechanisms, and we briefly review this model's potential applications.
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It has been suggested that interconnected brain areas evolve in tandem because evolutionary pressures act on complete functional systems rather than on individual brain areas. The cerebellar cortex has reciprocal connections with both the prefrontal cortex and motor cortex, forming independent loops with each. Specifically, in capuchin monkeys cerebellar cortical lobules Crus I and Crus II connect with prefrontal cortex, whereas the primary motor cortex connects with cerebellar lobules V, VI, VIIb, and VIIIa. Comparisons of extant primate species suggest that the prefrontal cortex has expanded more than cortical motor areas in human evolution. Given the enlargement of the prefrontal cortex relative to motor cortex in humans, our hypothesis would predict corresponding volumetric increases in the parts of the cerebellum connected to the prefrontal cortex, relative to cerebellar lobules connected to the motor cortex. We tested the hypothesis by comparing the volumes of cerebellar lobules in structural MRI scans in capuchins, chimpanzees and humans. The fractions of cerebellar volume occupied by Crus I and Crus II were significantly larger in humans compared to chimpanzees and capuchins. Our results therefore support the hypothesis that in the cortico-cerebellar system, functionally related structures evolve in concert with each other. The evolutionary expansion of these prefrontal-projecting cerebellar territories might contribute to the evolution of the higher cognitive functions of humans.