Evolution of White Matter Connectivity and Cortical Myelination in Hominoids: Wild Chimpanzee Pilot

Poster No:

T090 

Submission Type:

Abstract Submission 

Authors:

Cornelius Eichner1, Evgeniya Kirilina2,3, Michael Paquette1, Toralf Mildner4, Torsten Schlumm4, Kerrin Pine2, Christa Müller-Axt4, Ilona Lipp2, Harald Möller4, Guillermo Gallardo4, Roman Wittig5, Catherine Crockford5, Nikolaus Weiskopf2, Angela Friederici1, Alfred Anwander1

Institutions:

1Department of Neuropsychology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany, 2Department of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany, 3Neurocomputation and Neuroimaging Unit, Department of Education and Psychology, Free University Berlin, Berlin, Germany, 4Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany, 5Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany

E-Poster

Introduction:

The correspondence between white matter connections and cortical myelination of humans and non-human primates, such as great apes, remains largely unknown. Comparative studies of brain connectivity and cortical organization provide important insights into the ontogeny of human cognitive functions, such as language and social cognition [1,2]. However, prior comparative research is exclusively based on data acquired from captive animals, resulting in limited generalisability of findings. Captive apes may not show the rich vocal communication and similar social cognition observed in wild-living chimpanzees [3,4]. Natural habitats are likely to facilitate diverse behavior through flexible and adaptive brain changes, which might be less pronounced in animals held in captivity. Therefore, cross-species brain-behavior comparisons will greatly benefit from data acquired from wild animals.
Adopting a fully sustainable approach, we here aim to characterize the evolution of cortical- and white matter microstructure in relation to the behavior of wild living apes. Quantitative MRI and histology data are collected from ex vivo brains of wild chimpanzees, which died of natural causes in sub-Saharan Africa. In addition to the brain data, the chimpanzee populations in focus are very well characterized behaviorally. In this study, we show initial MRI data from the world's first wild chimpanzee brain.

Methods:

Data were acquired from the brain of a 6-year-old juvenile wild female chimpanzee from Taï National Forest (Ivory Coast). The animal died from a natural cause without human interference. The brain was extracted on site four hours after death and immersion-fixed with 4% paraformaldehyde. Diffusion (dMRI) data were acquired on a 3T Connectom System [5] (Siemens Healthineers) with max gradient strength of 300mT/m and a 23-channel surface coil, using segmented EPI: 1mm isotropic resolution, 72 sagittal slices, TR=10s, TE=44ms, b=3000s/mm2, 12 segments, 60 directions, 4 averages. MP-PCA denoising [6] was employed to increase SNR. Deterministic tracking and visualization of the processed dataset were performed using brainGL. Quantitative MRI data were acquired through Multiparametric maps (MPM) [7] using a 7T System (Siemens Healthcare) and a 32-channel head coil. FLASH data with 0.4 mm isotropic resolution were acquired using three different flip angels (12°, 45°, and 60°) and an off-resonance saturation pulse [8]. MPMs of three quantitative myelin markers (R1, R2*, MVF) [9] were calculated based on these data and reference calibration scans.

Results:

The short postmortem time before tissue fixation ensured high tissue quality for MRI investigation. The fiber tracking results are displayed in Fig. 1. Ex vivo fiber tracking could resolve tracts which show some correspondence with the language system in humans. Please note, that Chimpanzees do not express their full adult vocal repertoire until they reach at least an age of 12 yrs. Thus, it might be possible that the corresponding white matter pathways of a juvenile chimpanzee are not as extensive of those of an adult chimpanzee. Results from quantitative MRI are displayed in Fig. 2. The maps suggest weaker myelination in the frontal lobe compared to the motor, somatosensory, primary auditory and primary visual cortices.

Conclusions:

In this work, we acquired high-quality ex vivo dMRI and quantitative MRI data of the first wild chimpanzee brain. The proposed sustainable approach allows getting unique insights into brain organization in great apes without disturbing their natural life. First results indicate the feasibility of comparing white matter tracts of the language system and cortical myelination to the human developmental trajectory [1,10]. In the future, we expect to collect a substantial number of brains from apes of different ages, alongside extensive individual behavioral records, allowing us to gather important information on the evolution of the hominoid connectome.
Supporting Image: OHBM_Fig1.png
Supporting Image: OHBM_Fig2.png
 

Imaging Methods:

Anatomical MRI 1
Diffusion MRI

Language:

Language Other 2

Neuroanatomy:

Cortical Cyto- and Myeloarchitecture
White Matter Anatomy, Fiber Pathways and Connectivity

Keywords:

HIGH FIELD MR
Language
Myelin
Tractography
WHITE MATTER IMAGING - DTI, HARDI, DSI, ETC
Other - Monkey

1|2Indicates the priority used for review

My abstract is being submitted as a Software Demonstration.

No

Please indicate below if your study was a "resting state" or "task-activation” study.

Other

Healthy subjects only or patients (note that patient studies may also involve healthy subjects):

Healthy subjects

Was any human subjects research approved by the relevant Institutional Review Board or ethics panel? NOTE: Any human subjects studies without IRB approval will be automatically rejected.

Not applicable

Was any animal research approved by the relevant IACUC or other animal research panel? NOTE: Any animal studies without IACUC approval will be automatically rejected.

Yes

Please indicate which methods were used in your research:

Structural MRI
Diffusion MRI

For human MRI, what field strength scanner do you use?

3.0T
7T

Which processing packages did you use for your study?

FSL
Other, Please list  -   BrainGL, MRTRIX
SPM

Provide references using author date format

[1] Donahue C.J. et al. (2018), ‘Quantitative assessment of prefrontal cortex in humans relative to nonhuman primates’, Proceedings of the National Academy of Sciences, vol. 115 (22) E5183-E5192.
[2] Rilling J.R. et al. (2008), ‘The evolution of the arcuate fasciculus revealed with comparative DTI’, Nature Neuroscience, vol.11, pp. 426–428.
[3] Crockford C. et al. (2017), ‘Vocalizing in chimpanzees is influenced by social-cognitive processes’, Science Advances, vol. 3, no. 11, e1701742.
[4] Crockford C. In press. Why Does the Chimpanzee Vocal Repertoire Remain Poorly Understood? And What Can Be Done About It. In: The Tai Chimpanzees: 40 years of Research. Oxford University Press.
[5] Setsompop K. et al. (2013), ‘Pushing the limits of in vivo diffusion MRI for the Human Connectome Project’, Neuroimage, vol. 80, pp. 220-233.
[6] Veraart J. et. al (2016), ‘Diffusion MRI noise mapping using random matrix theory’, Magnetic Resonance in Medicine, vol. 76, no. 5, pp. 1582-1593.
[7] Weiskopf N. et al. (2013), ‘Quantitative multi-parameter mapping of R1, PD*, MT, and R2* at 3T: a multi-center validation’. Frontiers in Neuroscience, vol 7, no. 95.
[8] Trampel R. et al. (2017), ‘In-vivo magnetic resonance imaging (MRI) of laminae in the human cortex’. NeuroImage. https://doi.org/10.1016/j.neuroimage.2017.09.037
[9] Stüber C. et al. (2014), ‘Myelin and iron concentration in the human brain: a quantitative study of MRI contrast’, Neuroimage, volume 93, no. 1, pp. 95-106.
[10] Perani, D. et al. (2011), ‘Neural language networks at birth.’ Proceedings of the National Academy of Sciences vol. 108 no. 38, pp. 16056–16061.