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

  • Habon A. Issa
  • Nicky Staes
  • Sophia Diggs-Galligan
  • Cheryl D. Stimpson
  • Annette Gendron-Fitzpatrick
  • Jared P. Taglialatela
  • Patrick R. Hof
  • William D. Hopkins
  • Chet C. Sherwood
Original Article

Abstract

Despite being closely related, bonobos and chimpanzees exhibit several behavioral differences. For instance, studies indicate that chimpanzees are more aggressive, territorial, and risk-taking, while bonobos exhibit greater social tolerance and higher rates of socio-sexual interactions. To elucidate the potential neuroanatomical variation that accompanies these differences, we examined the microstructure of selected brain areas by quantifying the neuropil fraction, a measure of the relative tissue area occupied by structural elements of connectivity (e.g., dendrites, axons, and synapses) versus cell bodies. In bonobos and chimpanzees, we compared neuropil fractions in the nucleus accumbens (NAc; core and shell), amygdala (whole, accessory basal, basal, central and lateral nuclei), anterior cingulate cortex (ACC; dorsal and subgenual), anterior insular cortex (AIC), and primary motor cortex (M1). In the dorsal ACC and frontoinsular cortex (FI) we also quantified numbers of von Economo neurons (VENs), a unique subset of neurons thought to be involved in rapid information processing during social interactions. We predicted that the neuropil fraction and number of VENs in brain regions associated with socio-emotional processing would be higher in bonobos. In support of this hypothesis, we found that bonobos had significantly greater neuropil in the central and accessory basal nuclei of the amygdala, as well as layers V–VI of the subgenual ACC. However, we did not find a difference in the numbers of VENs between the two species. These findings support the conclusion that bonobo and chimpanzee brains differ in the anatomical organization of socio-emotional systems that may reflect species-specific variation in behavior.

Keywords

Microstructure Neuropil Amygdala Social cognition Bonobo Chimpanzee Von Economo neurons 

Notes

Acknowledgements

The authors would like to thank Yerkes National Primate Research Center (supported by National Institutes for Health Grant ORIP/OD P51 OD011132), the National Chimpanzee Brain Resource (supported by National Institutes for Health Grant R24 NS092988-02), Milwaukee County Zoo, Jacksonville Zoo, and veterinary technicians for the donation of specimens. We would also like to thank Dr. Amy Bauernfeind for helpful discussion and Dr. John Allman for providing bonobo samples. This work was supported by the National Science Foundation (SMA-1542848) and the James S. McDonnell Foundation (220020293).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

429_2018_1751_MOESM1_ESM.docx (42 kb)
Supplementary material 1 (DOCX 41 KB)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Anthropology, Center for the Advanced Study of Human PaleobiologyThe George Washington UniversityWashingtonUSA
  2. 2.Comparative Pathology Lab-RARCUniversity of WisconsinMadisonUSA
  3. 3.Department of Ecology, Evolution, and Organismal BiologyKennesaw State UniversityKennesawUSA
  4. 4.Ape Cognition and Conservation InitiativeDes MoinesUSA
  5. 5.Fishberg Department of Neuroscience and Friedman Brain InstituteIcahn School of Medicine at Mount SinaiNew YorkUSA
  6. 6.Neuroscience Institute and Language Research CenterGeorgia State UniversityAtlantaUSA

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