The laminar pattern of proprioceptive activation in human primary motor cortex

TY - JOUR

T1 - The laminar pattern of proprioceptive activation in human primary motor cortex

AU - Knudsen, Lasse

AU - Guo, Fanhua

AU - Sharoh, Daniel

AU - Huang, Jiepin

AU - Blicher, Jakob U

AU - Lund, Torben E

AU - Zhou, Yan

AU - Zhang, Peng

AU - Yang, Yan

N1 - © The Author(s) 2025. Published by Oxford University Press.

PY - 2025/4/1

Y1 - 2025/4/1

N2 - The primary motor cortex (M1) is increasingly being recognized for its vital role in proprioceptive somatosensation. However, our current understanding of proprioceptive processing at the laminar scale is limited. Empirical findings in primates and rodents suggest a pronounced role of superficial cortical layers, but the involvement of deep layers has yet to be examined in humans. Submillimeter resolution functional magnetic resonance imaging (fMRI) has emerged in recent years, paving the way for studying layer-dependent activity in humans (laminar fMRI). In the present study, laminar fMRI was employed to investigate the influence of proprioceptive somatosensation on M1 deep layer activation using passive finger movements. Significant M1 deep layer activation was observed in response to proprioceptive stimulation across 10 healthy subjects using a vascular space occupancy (VASO)-sequence at 7 T. For further validation, two additional datasets were included which were obtained using a balanced steady-state free precession sequence with ultrahigh (0.3 mm) in-plane resolution, yielding converging results. These results were interpreted in the light of previous laminar fMRI studies and the active inference account of motor control. We propose that a considerable proportion of M1 deep layer activation is due to proprioceptive influence and that deep layers of M1 constitute a key component in proprioceptive circuits.

AB - The primary motor cortex (M1) is increasingly being recognized for its vital role in proprioceptive somatosensation. However, our current understanding of proprioceptive processing at the laminar scale is limited. Empirical findings in primates and rodents suggest a pronounced role of superficial cortical layers, but the involvement of deep layers has yet to be examined in humans. Submillimeter resolution functional magnetic resonance imaging (fMRI) has emerged in recent years, paving the way for studying layer-dependent activity in humans (laminar fMRI). In the present study, laminar fMRI was employed to investigate the influence of proprioceptive somatosensation on M1 deep layer activation using passive finger movements. Significant M1 deep layer activation was observed in response to proprioceptive stimulation across 10 healthy subjects using a vascular space occupancy (VASO)-sequence at 7 T. For further validation, two additional datasets were included which were obtained using a balanced steady-state free precession sequence with ultrahigh (0.3 mm) in-plane resolution, yielding converging results. These results were interpreted in the light of previous laminar fMRI studies and the active inference account of motor control. We propose that a considerable proportion of M1 deep layer activation is due to proprioceptive influence and that deep layers of M1 constitute a key component in proprioceptive circuits.

KW - Adult

KW - Brain Mapping

KW - Female

KW - Fingers/physiology

KW - Humans

KW - Image Processing, Computer-Assisted

KW - Magnetic Resonance Imaging

KW - Male

KW - Motor Cortex/physiology

KW - Movement/physiology

KW - Proprioception/physiology

KW - Young Adult

KW - VASO

KW - cortical layers

KW - balanced-SSFP

KW - laminar fMRI

KW - primary motor cortex

UR - http://www.scopus.com/inward/record.url?scp=105002809365&partnerID=8YFLogxK

U2 - 10.1093/cercor/bhaf076

DO - 10.1093/cercor/bhaf076

M3 - Journal article

C2 - 40233153

SN - 1047-3211

VL - 35

JO - Cerebral cortex (New York, N.Y. : 1991)

JF - Cerebral cortex (New York, N.Y. : 1991)

IS - 4

M1 - bhaf076

ER -