Comparison of bonobo and chimpanzee brain microstructure reveals differences in socio-emotional circuits

Issa, Habon; Staes, Nicky; Diggs-Galligan, Sophia; Stimpson, Cheryl D.; Gendron‐Fitzpatrick, Annette; Taglialatela, Jared P.; Hof, Patrick R.; Hopkins, William D.; Sherwood, Chet C.

doi:10.1007/s00429-018-1751-9

Cited by 18 publications

(13 citation statements)

References 139 publications

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“…After Nimchinsky's works, research on spindle-shaped cells in the cerebral cortex greatly expanded with comparative studies between different species (Table 1; Hof and van der Gucht, 2007;Butti et al, 2009Butti et al, , 2014Hakeem et al, 2009;Allman et al, 2010Allman et al, , 2011bButti and Hof, 2010;Evrard et al, 2012;Raghanti et al, 2015Raghanti et al, , 2019García-Cabezas et al, 2016;Evrard, 2019;Issa et al, 2019;Cabeen et al, 2020), studies on spindle-shaped cells in neuropathology or neurodivergent states (Table 2; Allman et al, 2005;Kaufman et al, 2008;Nitrini, 2008;Seeley, 2008;Simms et al, 2009;Brüne et al, 2010Brüne et al, , 2011Santos et al, 2011;Kim et al, 2012;Santillo et al, 2013;Santillo and Englund, 2014;Uppal et al, 2014;Gefen et al, 2015Gefen et al, , 2018Senatorov et al, 2015;Liu et al, 2016;Krause et al, 2017;Yang et al, 2017;Braak and Del Tredici, 2018;Fathy et al, 2018;Gami-Patel et al, 2019;Lin et al, 2019;Nana et al, 2019;Tan et al, 2019;...…”

Section: Historical Context Of Ven Research Classical Studies Described Vens Only In Primatesmentioning

confidence: 99%

“…Great apes ACC (Nissl) Rose, 1928a,b;Nimchinsky et al, 1999;Allman et al, 2010;Issa et al, 2019;Evrard, 2019;Cabeen et al, 2020 Macaque monkey ACC (Nissl) and FI (Nissl and Golgi) Nimchinsky et al, 1999;Allman et al, 2010;Evrard et al, 2012;García-Cabezas et al, 2016;Evrard, 2019 Elephants ACC and FI (Nissl) Hakeem et al, 2009 Cetaceans ACC, AI, and FP (Nissl) Hof and van der Gucht, 2007;Butti et al, 2009;Raghanti et al, 2019 Manatee ACC and insula (Nissl) Butti and Hof, 2010 Pygmy hippopotamus Frontal and temporal neo-cortex, primary visual and primary motor areas (Golgi and Nissl) Butti and Hof, 2010;Butti et al, 2014 Artiodactyls and perissodactyls frontal pole, ACC, anterior insula, occipital pole (Nissl) Raghanti et al, 2015 (Dijkstra et al, 2018). The aforementioned demonstrates that the molecular characterization of VENs is still not completed and it is likely that only a combination of molecular markers and morphological descriptors will provide means for reliable detection of these cells.…”

Section: Speciesmentioning

confidence: 99%

“…After Nimchinsky’s works, research on spindle-shaped cells in the cerebral cortex greatly expanded with comparative studies between different species ( Table 1 ; Hof and van der Gucht, 2007 ; Butti et al, 2009 , 2014 ; Hakeem et al, 2009 ; Allman et al, 2010 , 2011b ; Butti and Hof, 2010 ; Evrard et al, 2012 ; Raghanti et al, 2015 , 2019 ; García-Cabezas et al, 2016 ; Evrard, 2019 ; Issa et al, 2019 ; Cabeen et al, 2020 ), studies on spindle-shaped cells in neuropathology or neurodivergent states ( Table 2 ; Allman et al, 2005 ; Kaufman et al, 2008 ; Nitrini, 2008 ; Seeley, 2008 ; Simms et al, 2009 ; Brüne et al, 2010 , 2011 ; Santos et al, 2011 ; Kim et al, 2012 ; Santillo et al, 2013 ; Santillo and Englund, 2014 ; Uppal et al, 2014 ; Gefen et al, 2015 , 2018 ; Senatorov et al, 2015 ; Liu et al, 2016 ; Krause et al, 2017 ; Yang et al, 2017 ; Braak and Del Tredici, 2018 ; Fathy et al, 2018 ; Gami-Patel et al, 2019 ; Lin et al, 2019 ; Nana et al, 2019 ; Tan et al, 2019 ; Jacot-Descombes et al, 2020 ; Pasquini et al, 2020 ) and molecular studies (including immunohistochemical characterization and transcriptomics) ( Fajardo et al, 2008 ; Stimpson et al, 2011 ; Cobos and Seeley, 2015 ; Dijkstra et al, 2018 ; Yang et al, 2019 ; Hodge et al, 2020 ). However, the amount of detailed morphological studies using Golgi staining ( Watson et al, 2006 ; Banovac et al, 2019 ; Correa-Júnior et al, 2020 ), especially in non-human species ( ...…”

Section: Historical Context Of Ven Researchmentioning

confidence: 99%

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Von Economo Neurons – Primate-Specific or Commonplace in the Mammalian Brain?

Banovac

Sedmak

Judaš

et al. 2021

Front. Neural Circuits

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The pioneering work by von Economo in 1925 on the cytoarchitectonics of the cerebral cortex revealed a specialized and unique cell type in the adult human fronto-insular (FI) and anterior cingulate cortex (ACC). In modern studies, these neurons are termed von Economo neurons (VENs). In his work, von Economo described them as stick, rod or corkscrew cells because of their extremely elongated and relatively thin cell body clearly distinguishable from common oval or spindle-shaped infragranular principal neurons. Before von Economo, in 1899 Cajal depicted the unique somato-dendritic morphology of such cells with extremely elongated soma in the FI. However, although VENs are increasingly investigated, Cajal’s observation is still mainly being neglected. On Golgi staining in humans, VENs have a thick and long basal trunk with horizontally oriented terminal branching (basilar skirt) from where the axon arises. They are clearly distinguishable from a spectrum of modified pyramidal neurons found in infragranular layers, including oval or spindle-shaped principal neurons. Spindle-shaped cells with highly elongated cell body were also observed in the ACC of great apes, but despite similarities in soma shape, their dendritic and axonal morphology has still not been described in sufficient detail. Studies identifying VENs in non-human species are predominantly done on Nissl or anti-NeuN staining. In most of these studies, the dendritic and axonal morphology of the analyzed cells was not demonstrated and many of the cells found on Nissl or anti-NeuN staining had a cell body shape characteristic for common oval or spindle-shaped cells. Here we present an extensive literature overview on VENs, which demonstrates that human VENs are specialized elongated principal cells with unique somato-dendritic morphology found abundantly in the FI and ACC of the human brain. More research is needed to properly evaluate the presence of such specialized cells in other primates and non-primate species.

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Section: Historical Context Of Ven Research Classical Studies Described Vens Only In Primatesmentioning

confidence: 99%

Section: Speciesmentioning

confidence: 99%

Section: Historical Context Of Ven Researchmentioning

confidence: 99%

See 1 more Smart Citation

Von Economo Neurons – Primate-Specific or Commonplace in the Mammalian Brain?

Banovac

Sedmak

Judaš

et al. 2021

Front. Neural Circuits

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“…If bonobos show age-related increases in DHEA/S similar to those clearly documented for wild chimpanzees by Sabbi et al (4), together the two species would represent a common pattern useful as a single comparison for humans. On other hand, if patterns of adrenarche are different, it is possible that DHEAS may have some role in reported differences between chimpanzee and bonobo brains (83)(84)(85). This is a topic worthy of investigation in its own right.…”

Section: Adrenarche In Chimpanzees and Bonobosmentioning

confidence: 99%

“…Based on the first three sections I end with suggestions for future research directions in the comparative study of adrenarche and middle childhood among both the great apes and humans. Current evidence for adrenarche and its relationship to differences in hormonal (81), cranial (82), and brain (83)(84)(85) traits in these two related species (86) is quite limited. A simple direct comparison of adrenarcheal timing in the two species would add immensely to our understanding.…”

Section: Introductionmentioning

confidence: 99%

DHEAS and Human Development: An Evolutionary Perspective

Campbell

2020

Front. Endocrinol.

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Adrenarche, the post-natal rise of DHEA and DHEAS, is unique to humans and the African Apes. Recent findings have linked DHEA in humans to the development of the left dorsolateral prefrontal cortex (LDPFC) between the ages of 4-8 years and the right temporoparietal junction (rTPJ) from 7 to 12 years of age. Given the association of the LDLPFC with the 5-to-8 transition and the rTPJ with mentalizing during middle childhood DHEA may have played an important role in the evolution of the human brain. I argue that increasing protein in the diet over the course of human evolution not only increased levels of DHEAS, but linked meat consumption with brain development during the important 5-to-8 transition. Consumption of animal protein has been associated with IGF-1, implicated in the development of the adrenal zona reticularis (ZR), the site of DHEAS production. In humans and chimps, the zona reticularis emerges at 3-4 years, along with the onset of DHEA/S production. For chimps this coincides with weaning and peak synaptogenesis. Among humans, weaning is completed around 2 ½ years, while synaptogenesis peaks around 5 years. Thus, in chimpanzees, early cortical maturation is tied to the mother; in humans it may be associated with post-weaning provisioning by others. I call for further research on adrenarche among the African apes as a critical comparison to humans. I also suggest research in subsistence populations to establish the role of nutrition and energetics in the timing of adrenarche and the onset of middle childhood.

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Sociobiological Interactions

Colombo

2022

Dominance Behavior

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Comparison of bonobo and chimpanzee brain microstructure reveals differences in socio-emotional circuits

Cited by 18 publications

References 139 publications

Von Economo Neurons – Primate-Specific or Commonplace in the Mammalian Brain?

Von Economo Neurons – Primate-Specific or Commonplace in the Mammalian Brain?

DHEAS and Human Development: An Evolutionary Perspective

Sociobiological Interactions

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