Brain reorganization, not relative brain size, primarily characterizes anthropoid brain evolution

In the paper

“The origin of the great ape grade shift in prefrontal white matter evolution is inferred to date back to the dawn of the ape radiation (at least 20 Ma).”

In the paper

“We further find that, across more than 40 Myr of anthropoid evolution, different neocortical and cerebellar areas varied in their contributions to different mosaic patterns.”

In the paper

“The principal component that we find to contribute most to explaining evolutionary changes in primate brain reorganization indicates high loadings for prefrontal white matter (table 1).”

In the paper

“and different mosaic patterns are differentially selected for when brains increase or decrease in size.”

In the paper

“PC3 (14.7%) involves the hippocampal formation (hippocampus and entorhinal cortex)”

In the paper

“and demonstrate deep evolutionary roots for mosaic patterns associated with motor control and learning.”

In the paper

“PC2 (18.7%) is predominantly associated with prefrontal white matter”

In the paper

“PC6 (6%) structures involved in the execution of motor plans (spinocerebellum, mesencephalon and medulla)”

In the paper

“Across more than 40 Myr of anthropoid primate evolution, mosaic changes contribute more to explaining neural diversity than changes in relative brain size”

• Also stated in: § 3. Discussion · plain

  “The finding that mosaic changes contribute more to explaining neural system diversity across species than changes in relative brain size”

In the paper

“We identify lineage-specific evolutionary specializations for all branches of the tree of life covered by our sample”

In the paper

“The dissociation of the hippocampus–entorhinal (PC3) and prefronto-striatal (PC4) formations in different principal components (table 1)”

In the paper

“Other brain formations (prefrontal white matter, hippocampal–entorhinal and descending motor pathway) display significantly increased variation in lineages where brain size decreases compared with those where brain size increases (figure 2; PC2: F = 0.0037, p < 0.0001; PC3: F = 0.0066, p < 0.0002; PC6: F = 0.0395, p = 0.0067).”

In the paper

“In monkeys, investment in prefrontal white matter is mainly displayed in species that have decreased absolute brain size in their lineage (Cebus, Alouatta, Miopithecus; electronic supplementary material, S1)”

In the paper

“PC7 (4.6%) structures associated with motor learning (cerebrocerebellum and frontal motor areas)”

In the paper

“Subsequent PCs indicate low loadings for relative brain size”

In the paper

“PC1 indicates high inverse loadings of relative brain size and the relative volume of olfactory bulb and medulla.”

In the paper

“PC4 (12.7%) the prefronto-striatal formation”

In the paper

“Phylogenetic principal components analysis of relative brain size and the relative size of 20 brain structures/areas reveals that seven principal components explain up to 90.4 per cent of neural structure variation observed across 17 primate species (spanning more than 40 Myr of evolution [26]).”

What the sources say

• Not checked yetcites [26] Wilkinson RD, Steiper ME, Soligo C, Martin RD, Yang Z, Tavare S. 2011. Dating primate divergences through an integrated analysis of palaeontological and molecular data. Syst. Biol. 60, 16–31 10.1093/sysbio/syq054 (doi:10.1093/sysbio/syq054) [DOI] [PMC free article] [PubMed] [Google Scholar] source

In the paper

“Evolutionary investment in these brain systems is shown to originate in the ape ancestral lineage (approx. 30–20 Ma).”

In the paper

“Results indicate that three mosaic patterns differentiate great apes (and humans) from other primates when considered in conjunction with an overall increase in brain size: prefrontal white matter, prefronto-striatal and cortico-cerebellar (figure 1).”

In the paper

“that some organizational changes have deep evolutionary roots dating back at least to the divergence of apes and Old World monkeys (between 30 and 20 Ma).”

In the paper

“while PC7 loads on structures associated with cortico-cerebellar connectivity (cerebrocerebellum and frontal motor areas) [33,61,62] (table 1).”

What the sources say

• Not checked yetcites [33] Krienen FM, Buckner RL. 2009. Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb. Cortex 19, 2485–2497 10.1093/cercor/bhp135 (doi:10.1093/cercor/bhp135) [DOI] [PMC free article] [PubMed] [Google Scholar] source
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In the paper

“Results indicate a high evolvability of mosaic brain reorganization in primates”

In the paper

“We also show that different neocortical and cerebellar areas contribute differently to explaining different mosaic patterns in different lineages”

In the paper

“Phylogenetic mapping of these two PCs suggests differential evolutionary investment across different species.”

In the paper

“In monkeys, Cebus has the highest score for PC7 (see electronic supplementary material, S1)”

In the paper

“our method estimates the value for the great ape last common ancestor (LCA) at 385cc”

In the paper

“our method predicts the value for the ape LCA at 348cc and the LCA of Old World monkeys and apes at 225cc”

In the paper

“Other brain formations (prefrontal white matter, hippocampal–entorhinal, paleocortex and descending motor pathway) display increased variation in lineages where brain size decreases, suggesting asymmetry in brain reorganization depending on whether the brain increases or decreases in absolute size (see figure 2 and electronic supplementary material, S2).”

In the paper

“the LCA of apes at 348cc”

In the paper

“These trends are further extended in humans with an additional investment in absolute brain size (see figure 1c and electronic supplementary material, S2) [63].”

What the sources say

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In the paper

“PC6 indicates high loadings of structures involved in descending motor pathways (spinocerebellum, mesencephalon and medulla) [60]”

What the sources say

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In the paper

“our method estimates this value to be 385cc”

In the paper

“PC6 further indicates increased variation when brain size decreases (similar to PC3)”

In the paper

“and confound the different evolutionary scenarios (in terms of patterns of increase/decrease between two traits) that underlie allometric residuals [7].”

What the sources say

• Not checked yetcites [7] Smaers JB, Dechmann DKN, Goswami A, Soligo C, Safi K. 2012. Comparative analyses of evolutionary rates reveal different pathways to encephalization in bats, carnivorans, and primates. Proc. Natl Acad. Sci. USA 109, 18 006–18 011 10.1073/pnas.1212181109 (doi:10.1073/pnas.1212181109) [DOI] [PMC free article] [PubMed] [Google Scholar] source

In the paper

“Allometric approaches further fail to reveal the temporal origin and rate of evolutionary changes taking place on individual branches of the tree of life covered by the sample”

What the sources say

• Not checked yetcites [7] Smaers JB, Dechmann DKN, Goswami A, Soligo C, Safi K. 2012. Comparative analyses of evolutionary rates reveal different pathways to encephalization in bats, carnivorans, and primates. Proc. Natl Acad. Sci. USA 109, 18 006–18 011 10.1073/pnas.1212181109 (doi:10.1073/pnas.1212181109) [DOI] [PMC free article] [PubMed] [Google Scholar] source

In the paper

“Mosaic studies have mainly focused on allometric scaling trends of particular brain structures [4,17].”

What the sources say

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In the paper

“the systemic interaction between different brain structures, in which individual brain structures contribute to different information processing loops to various extents, is better reflected in approaches that allow assessing the extent to which particular variables differentially contribute to explaining different patterns of covariation between all variables in the model (e.g. principal compon”

What the sources say

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In the paper

“The relative size of individual brain structures indicates variation beyond purely size-related allometric scaling [3,4].”

What the sources say

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In the paper

“suggesting that, once evolved, patterns of connectivity and modularity associated with larger brains may be maintained when brains undergo secondary reductions in size.”

In the paper

“The finding that mosaic changes contribute more to explaining neural system diversity across species than changes in relative brain size confirms that the traditional focus on relative brain size [2,41–43] significantly underestimates the contribution of different neural pathways to primate neural system diversity.”

What the sources say

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In the paper

“comparative data on brain structures that are fundamental to neural processing (prefrontal cortex, frontal motor areas and cerebellar lobules) have not been available until very recently [11,17,19–21], hampering more in-depth insights on the systemic nature of mosaic brain evolution.”

What the sources say

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In the paper

“representing patterns of size-independent mosaic changes”

In the paper

“and can roughly be associated with social reasoning, motor control, learning and memory [36–40].”

What the sources say

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In the paper

“The identification of prefrontal white matter as a distinct contribution to explaining neural system diversity confirms this view.”

In the paper

“Because of its combined multimodal and modular nature, the prefrontal cortex is thus likely to be under particular pressure to change the space attributed to its white matter as the size of the brain changes over millions of years of evolution.”

In the paper

“Overall, our results indicate that neural adaptation in anthropoid primates primarily involves differential selection on multiple size-independent organizational patterns across different taxonomic groups”

In the paper

“The derived pattern of prefrontal white matter evolution in humans aligns with recent work on prefrontal neuropil distribution supporting the conclusion that enhanced connectivity in the prefrontal cortex accompanied the evolution of the human brain [52].”

What the sources say

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In the paper

“The argument is that as particular mosaic patterns increase or decrease over evolutionary time, the absolute size attributed to each mosaic pattern (and thus its number of cells) will contribute to its computational power.”

In the paper

“Because brain (structure) size scales approximately isometrically as a function of cell number (and therefore computational power) in primates [24,25]”

What the sources say

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In the paper

“This result is in line with the view that changes in prefrontal white matter are, at least in part, owing to the geometric constraints of size on multimodal connectivity.”

In the paper

“As brains change in size over evolutionary time, multimodal connectivity may be under particular pressure as interacting areas change in distance to each other, affecting the length and thickness (to maintain optimal conduction times) of axons [5,50].”

What the sources say

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In the paper

“These patterns of size-independently co-evolving brain structures correspond to brain systems that have been described in electrophysiological and anatomical tract-tracing studies in non-human primates [27–31] and MRI studies in humans [32–35]”

What the sources say

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In the paper

“The novel comparative approach we employ allows inferring the temporal origin, rate and process of evolutionary changes for all individual lineages of the tree of life covering the sample [7].”

What the sources say

• Not checked yetcites [7] Smaers JB, Dechmann DKN, Goswami A, Soligo C, Safi K. 2012. Comparative analyses of evolutionary rates reveal different pathways to encephalization in bats, carnivorans, and primates. Proc. Natl Acad. Sci. USA 109, 18 006–18 011 10.1073/pnas.1212181109 (doi:10.1073/pnas.1212181109) [DOI] [PMC free article] [PubMed] [Google Scholar] source

In the paper

“that patterns of brain reorganization may indicate different evolutionary pathways across different species depending on whether brain size increases or decreases”

In the paper

“suggesting asymmetry in brain reorganization depending on whether the brain increases or decreases in absolute size”

In the paper

“this level of accuracy far exceeds what can be attained with alternative methods and demonstrates the accuracy of our model estimates.”

In the paper

“Our primate results also point in this direction.”

In the paper

“In conclusion, our results contribute to explaining primate neural system diversity by quantifying the extent to which variation in anthropoid brain adaptation is principally explained by differential selection on multiple size-independent organizational patterns across different taxonomic groups rather than changes in overall brain size.”

• Also stated in: § 3. Discussion · boosted

  “Overall, our results demonstrate that anthropoid primate brain evolution is primarily characterized by selection on multiple size-independent patterns of brain structure covariation.”

In the paper

“suggests they have evolved as mosaic patterns”

In the paper

“congruent with their increased sensorimotor capacities [64].”

What the sources say

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