Evolution and ontogeny of cortical microstructure facilitating hand movements

2140 

Abstract Submission 

Maëlig Chauvel¹, Evgeniya Kirilina¹, Ilona Lipp¹, Sonja Ebel^2,3, Kathrin Kopp^2,3, Carsten Jaeger^1,4, Saskia Helbling^1,5, Peter McColgan⁶, Kerrin Pine¹, Luke J. Edwards¹, Tobias Graessle^7,8, Denis Chaimow¹, Catherine Crockford^9,10,11, Roman Wittig^9,10,11, Nikolaus Weiskopf^1,12,13

¹Department of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany, ²Department of Comparative Cultural Psychology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany, ³Human Biology & Primate Cognition Group, Institute of Biology at Leipzig University, Leipzig, Germany, ⁴Paul Flechsig Institute - Center of Neuropathology and Brain Research, Faculty of Medicine, Universität Leipzig, Leipzig, Germany, ⁵Ernst Strüngmann Institute for Neuroscience in Cooperation with Max Planck Society, Frankfurt am Main, Germany, ⁶University College London, London, United Kingdom, ⁷Ecology and Emergence of Zoonotic Diseases, Helmholtz Institute for One Health, Greifswald, Germany, ⁸Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute, Berlin, Germany, ⁹Department of Human Behavior, Ecology and Culture, Max Planck Institute for Evolutionary Anthropolog, Leipzig, Germany, ¹⁰Ape Social Mind Lab, Institute of Cognitive Science Marc Jeannerod, UMR 5229, CNRS, Lyon, France, ¹¹Taï Chimpanzee Project, Centre Suisse de Recherches Scientifiques, Abidjan, Cote D'Ivoire, ¹²Felix Bloch Institute for Solid State Physics, Faculty of Physics and Earth Sciences, Leipzig University, Leipzig, Germany, ¹³Wellcome Centre for Human Neuroimaging, Institute of Neurology, University College London, London, United Kingdom

Maëlig Chauvel  
Department of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences
Leipzig, Germany

Evgeniya Kirilina  
Department of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences
Leipzig, Germany

Ilona Lipp  
Department of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences
Leipzig, Germany

Sonja Ebel  
Department of Comparative Cultural Psychology, Max Planck Institute for Evolutionary Anthropology|Human Biology & Primate Cognition Group, Institute of Biology at Leipzig University
Leipzig, Germany|Leipzig, Germany

Kathrin Kopp  
Department of Comparative Cultural Psychology, Max Planck Institute for Evolutionary Anthropology|Human Biology & Primate Cognition Group, Institute of Biology at Leipzig University
Leipzig, Germany|Leipzig, Germany

Carsten Jaeger  
Department of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences|Paul Flechsig Institute - Center of Neuropathology and Brain Research, Faculty of Medicine, Universität Leipzig
Leipzig, Germany|Leipzig, Germany

Saskia Helbling  
Department of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences|Ernst Strüngmann Institute for Neuroscience in Cooperation with Max Planck Society
Leipzig, Germany|Frankfurt am Main, Germany

Peter McColgan, PhD  
University College London
London, United Kingdom

Kerrin Pine  
Department of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences
Leipzig, Germany

Luke J. Edwards  
Department of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences
Leipzig, Germany

Tobias Graessle  
Ecology and Emergence of Zoonotic Diseases, Helmholtz Institute for One Health|Epidemiology of Highly Pathogenic Microorganisms, Robert Koch Institute
Greifswald, Germany|Berlin, Germany

Denis Chaimow  
Department of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences
Leipzig, Germany

Catherine Crockford  
Department of Human Behavior, Ecology and Culture, Max Planck Institute for Evolutionary Anthropolog|Ape Social Mind Lab, Institute of Cognitive Science Marc Jeannerod, UMR 5229, CNRS|Taï Chimpanzee Project, Centre Suisse de Recherches Scientifiques
Leipzig, Germany|Lyon, France|Abidjan, Cote D'Ivoire

Roman Wittig  
Department of Human Behavior, Ecology and Culture, Max Planck Institute for Evolutionary Anthropolog|Ape Social Mind Lab, Institute of Cognitive Science Marc Jeannerod, UMR 5229, CNRS|Taï Chimpanzee Project, Centre Suisse de Recherches Scientifiques
Leipzig, Germany|Lyon, France|Abidjan, Cote D'Ivoire

Nikolaus Weiskopf  
Department of Neurophysics, Max Planck Institute for Human Cognitive and Brain Sciences|Felix Bloch Institute for Solid State Physics, Faculty of Physics and Earth Sciences, Leipzig University|Wellcome Centre for Human Neuroimaging, Institute of Neurology, University College London
Leipzig, Germany|Leipzig, Germany|London, United Kingdom

The remarkable efficiency and precision in coordination of human hand movements surpass those of other species, including our closest living relatives, the great apes. The evolution of the human hand function was paralleled by the expansion of its functional representation in humans and great apes' motor and somatosensory cortices(1). Fine motor skills of the human hand, enabling complex tool manipulation tasks, require fast and precise neuronal control facilitated by myelinated intracortical and projection fibers within the motor cortex. In humans, the hand-controlling area in the motor cortex has higher levels of myelin as compared to the face-controlling area as shown by quantitative MRI (qMRI)(2) but it is not known whether this is a human-specific phenomenon, or if it is already observed in great apes. Herein, we compared the microstructure of the functional subdivisions within primary motor cortex in humans and chimpanzees using high resolution qMRI and characterized the lifespan trajectory of different cortical motor regions.

Sixteen post mortem chimpanzee brains (8 f, age 1.1-52y) were collected in field sites, sanctuaries and zoos using an ethical pipeline(3) and studied with ultra-high resolution qMRI. In vivo qMRI data of ten human participants (6 f, 28 ± 3.6 y) from a previously published study were analyzed(4). QMRI were acquired at 7T using multi-parametric mapping(5,6) with 500μm and 300μm resolutions for humans and chimpanzees, respectively. Magnetization transfer saturation (MTsat) served as a myelin marker(7), the effective transverse relaxation rate (R2*) as a marker for iron content(8). Cortical surfaces for both species were reconstructed using the Freesurfer recon-all pipeline. Areas within the primary motor cortex controlling the hand, face, and foot movements were manually delineated based on sulcal anatomy (Fig. 1.A). Median R2* and MTsat values were extracted for the hand, face and foot regions and compared in paired t-tests. An exponential saturation model(9) for age-related increase of iron and myelin was fitted to R2* and MTsat values to characterize the lifespan trajectories in each cortical area. A time constant indicating the age at which around 63.2% of all age-related changes were completed was determined for each area within the motor cortex (Fig. 1.B right).

Differences in microstructure of the foot, hand and face regions of the motor cortex were observed in both species (Fig. 1.B) with significantly higher R2* in hand areas as compared to the foot and face areas, implying higher levels of cortical iron and myelin in the former. A non-significant tendency towards higher MTsat values in the hand area in humans was observed. In chimpanzees, significantly higher MTsat values for hand compared to face and foot areas were found. Developmental myelination and age-related iron accumulation of R2* and MTsat in chimpanzees are shown in Fig 1.B right. Age-related iron accumulation (measured with R2*) was described by a time constant of 30y±22 for all three regions. This is slower than values reported in the human motor cortex, which found iron accumulated with a time constant of 20 years(9). The developmental myelination in chimpanzees measured with MTsat was characterized by time constants 2.1y±0.5, 2.4y±0.5 and 2.4y±0.6 for face, hand and foot areas, respectively.

For the first time we showed that microstructure of the hand knob area in the chimpanzee motor cortex is different from the subdivisions controlling other movements and thus that the evolution of hand motor skills is not only manifested in alterations to sulcal anatomy but also in pronounced changes of cortical microstructure. We found elevated myelin and iron content in the hand knob area in both species and characterized developmental myelination and iron accumulation within the chimpanzee motor cortex. These findings may enhance our understanding of the anatomical basis for distinct behaviors like remarkable tool use seen in hominids.

Motor Planning and Execution

Cortical Anatomy and Brain Mapping

Cortical Cyto- and Myeloarchitecture ¹

Anatomical MRI ²

Imaging Methods Other

ANIMAL STUDIES

Cross-Species Homologues

HIGH FIELD MR

Motor

STRUCTURAL MRI

Other - Chimpanzee Brain ; Hand