The human premotor cortex: cytoarchitectonic 3D maps and structure-function relationships

Poster No:

1698 

Submission Type:

Abstract Submission 

Authors:

Sabine Ruland1, Benjamin Sigl2, Jeanette Stangier2, Svenja Caspers2, Sebastian Bludau3, Hartmut Mohlberg1, Peter Pieperhoff1, Katrin Amunts1

Institutions:

1Forschungszentrum Juelich GmbH, Juelich, North Rhine-Westphalia, 2Heinrich Heine University Duesseldorf, Duesseldorf, North Rhine-Westphalia, 3Forschungszentrum Julich GmbH, Juelich, NRW

First Author:

Sabine Ruland  
Forschungszentrum Juelich GmbH
Juelich, North Rhine-Westphalia

Co-Author(s):

Benjamin Sigl  
Heinrich Heine University Duesseldorf
Duesseldorf, North Rhine-Westphalia
Jeanette Stangier  
Heinrich Heine University Duesseldorf
Duesseldorf, North Rhine-Westphalia
Svenja Caspers  
Heinrich Heine University Duesseldorf
Duesseldorf, North Rhine-Westphalia
Sebastian Bludau  
Forschungszentrum Julich GmbH
Juelich, NRW
Hartmut Mohlberg  
Forschungszentrum Juelich GmbH
Juelich, North Rhine-Westphalia
Peter Pieperhoff  
Forschungszentrum Juelich GmbH
Juelich, North Rhine-Westphalia
Katrin Amunts  
Forschungszentrum Juelich GmbH
Juelich, North Rhine-Westphalia

Introduction:

The human premotor cortex (PM) is involved in action preparation and execution but also in various cognitive functions like space perception, action understanding, imitation, cognitive manipulation and attention (Abe & Hanakawa, 2009; Rizzolatti et al., 2002; Schubotz & von Cramon, 2003). In this context, the frontal eye field (FEF) is of particular interest. Its microstructural correlate has long been disputed and linked to the prefrontal cortex and/or the premotor cortex (Vernet et al., 2014). However, a detailed microstructural map of the PM which goes beyond the single Brodmann area 6 to advance the analysis of structure-function relationships is still missing. Therefore, the aim of the study was to map the PM based on cytoarchitectonic differences, compute 3D probabilistic maps and to carry out an initial comparison with results from functional studies.

Methods:

Ten human brains were paraffin-embedded, cut into 20 m thick sections and stained for cell bodies. Cytoarchitecture was characterised by the Grey Level Index (GLI), a measure of cell packing density, that was obtained from digitised histological images of the sections. GLI profiles running over the cortical ribbon allowed to detect borders between cytoarchitectonic areas based on image analysis and multivariate statistical tests and to describe the areas in quantitative terms (Schleicher et al., 2009). A multidimensional scaling was performed to identify groupings of areas based on cytoarchitectonic similarities. The 3D reconstructed areas were registered to the MNI Colin27 and ICBM152 brains (Evans, et a., 2012). Probabilistic maps were generated to quantify the interindividual variability in extent and localization of the areas (Amunts et al., 2020). Finally, the maps were spatially compared with results from functional studies from the literature on the FEF and inferior FEF (iFEF) (Amiez & Petrides, 2009; Bedini & Baldauf, 2021; Petit & Pouget, 2019; Vernet et al., 2014), body movement and attention (Schubotz & von Cramon, 2001).

Results:

Seven new areas, 6d1-6d3, 6v1-6v3 and 6r1, were mapped within the PM based on cytoarchitectonic differences. Whereas 6d1-6d3 and 6v1-6v3 were agranular, area 6r1 showed a discontinuous, thin layer IV. The PM areas were arranged in a rostro-caudal and dorso-ventral order on the precentral, superior frontal and middle frontal gyri and sulci (Fig. 1). Especially, the rostral extension of areas 6v1 and 6v2 on the middle frontal gyrus showed a high interindividual variability. The location of their rostral borders to areas of the dorsolateral prefrontal cortex was associated with a posterior segment of the middle fontal sulcus. The multidimensional scaling revealed two groups of PM areas: the dorsally located areas, 6d1-6d3 and the ventrally located areas 6v1-6v3, 6r1. The superior frontal sulcus served as the anatomical landmark of this subdivision. A spatial comparison of the new maps with results from functional studies (Fig. 2), showed a high overlap of the frontal eye field and inferior frontal eye field with the maps of areas 6v1 and 6v2. Activations related to foot, leg movement and reaching were located mainly within the areas 6d1 and 6d2, those of mouth movement and grasping in 6v3. Areas 6d1, 6v2, and 6r1 seem to be involved in tasks related to spatial, object and temporal attention.
Supporting Image: Figure1.png
   ·Maximum probabilistic map of cytoarchitectonic premotor areas
Supporting Image: Figure2.png
   ·Spatial comparison of the PM map and coordinates reported for the FEF and iFEF
 

Conclusions:

Our work uncovers a fundamental organisational principle of the human PM and provides anatomical maps that go beyond previous parcellations with respect to their degree of precision and accuracy, reproducibility, information on interindividual variability and usability.
The openly accessible 3D maps provide the neuroanatomical framework to clearly localise and spatially anchor results of studies addressing structure-function relationships and connectivity. In addition, the maps and especially their interindividual information will inform neurosurgery to better navigate and improve preoperative planning.

Motor Behavior:

Motor Planning and Execution 1
Visuo-Motor Functions

Neuroanatomy, Physiology, Metabolism and Neurotransmission:

Cortical Anatomy and Brain Mapping 2
Cortical Cyto- and Myeloarchitecture

Perception, Attention and Motor Behavior:

Attention: Visual

Keywords:

Atlasing
Cortex
Cortical Layers
Motor
Open Data
Other - Cytoarchitecture, Probabilistic Maps, Frontal Eye Field

1|2Indicates the priority used for review

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Provide references using APA citation style.

1. Abe, M., & Hanakawa, T. (2009). Functional coupling underlying motor and cognitive functions of the dorsal premotor cortex. Behavioural brain research, 198(1), 13-23.
2. Amunts, K., Mohlberg, H., Bludau, S., & Zilles, K. (2020). Julich-Brain: A 3D probabilistic atlas of the human brain's cytoarchitecture. Science, 369(6506), 988-992.
3. Amiez, C., & Petrides, M. (2009). Anatomical organization of the eye fields in the human and non-human primate frontal cortex. Progress in neurobiology, 89(2), 220-230.
4. Bedini, M., & Baldauf, D. (2021). Structure, function and connectivity fingerprints of the frontal eye field versus the inferior frontal junction: A comprehensive comparison. The European journal of neuroscience, 54(4), 5462-5506.
5. Petit, L., & Pouget, P. (2019). The comparative anatomy of frontal eye fields in primates. Cortex, 118, 51-64.
6. Rizzolatti, G., Fogassi, L., & Gallese, V. (2002). Motor and cognitive functions of the ventral premotor cortex. Current opinion in neurobiology, 12(2), 149-54.
7. Schleicher, A., Morosan, P., Amunts, K., & Zilles, K. (2009). Quantitative architectural analysis: a new approach to cortical mapping. Journal of autism and developmental disorders, 39(11), 1568-1581.
8. Schubotz, R.I., & von Cramon, D.Y. (2003) Functional-anatomical concepts of human premotor cortex: evidence from fMRI and PET studies. Neuroimage, 20 Suppl 1, S120–S131.
9. Schubotz, R.I., & von Cramon, D.Y. (2001). Functional organization of the lateral premotor cortex: fMRI reveals different regions activated by anticipation of object properties, location and speed. Brain research. Cognitive brain research, 11(1), 97-112.
10. Vernet, M., Quentin, R., Chanes, L., Mitsumasu, A., Valero-Cabre, A. (2014). Frontal eye field, where art thou? Anatomy, function, and non-invasive manipulation of frontal regions involved in eye movements and associated cognitive operations. Frontiers in integrative neuroscience, 8, 66.

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