Journal Article

Sub-millimeter fMRI reveals multiple topographical digit representations that form action maps in human motor cortex

Bönstrup, Marlene, Glen, Daniel R., Ivanov, Dimo, Huber, Laurentius, Kashyap, Sriranga, Goense, Jozien, Poser, Benedikt A., Bandettini, Peter A., Marrett, Sean, Finn, Emily S., Handwerker, Daniel A., Petridou, Natalia

2020

Overview

The human brain coordinates a wide variety of motor activities. On a large scale, the cortical motor system is topographically organized such that neighboring body parts are represented by neighboring brain areas. This homunculus-like somatotopic organization along the central sulcus has been observed using neuroimaging for large body parts such as the face, hands and feet. However, on a finer scale, invasive electrical stimulation studies show deviations from this somatotopic organization that suggest an organizing principle based on motor actions rather than body part moved. It has not been clear how the action-map organization principle of the motor cortex in the mesoscopic (sub-millimeter) regime integrates into a body map organization principle on a macroscopic scale (cm). Here we developed and applied advanced mesoscopic (sub-millimeter) fMRI and analysis methodology to non-invasively investigate the functional organization topography across columnar and laminar structures in humans. Compared to previous methods, in this study, we could capture locally specific blood volume changes across entire brain regions along the cortical curvature. We find that individual fingers have multiple mirrored representations in the primary motor cortex depending on the movements they are involved in. We find that individual digits have cortical representations up to 3 ​mm apart from each other arranged in a column-like fashion. These representations are differentially engaged depending on whether the digits’ muscles are used for different motor actions such as flexion movements, like grasping a ball or retraction movements like releasing a ball. This research provides a starting point for non-invasive investigation of mesoscale topography across layers and columns of the human cortex and bridges the gap between invasive electrophysiological investigations and large coverage non-invasive neuroimaging. [Display omitted] •A sub-millimeter fMRI method is developed to image neural microcircuitry in humans.•The method can capture large FOVs with thin slices for ‛columnar’ and ‛laminar’ mapping.•An analysis pipeline is developed to investigate topographical representations that have only been visible in animals so far.•Novel findings include a mirrored finger representation in the human motor cortex.

• Publisher: Elsevier Inc,Elsevier Limited,Elsevier
• Subject: Adult / Brain Mapping / Cortex (motor) / Cortical columns / Cortical layers / Electrical stimuli / Fingers & toes / Fingers - physiology / fMRI / Functional magnetic resonance imaging / Functional morphology / Homunculus / Humans / Investigations / Magnetic Resonance Imaging / Medical imaging / Motor Activity - physiology / Motor cortex / Motor Cortex - anatomy & histology / Motor Cortex - diagnostic imaging / Motor Cortex - physiology / Muscles / Neuroimaging / Topography / VASO