Coordinated multilaminar dynamics underlie multiplexed computation in macaque motor cortex

Abstract

Functional multiplexing is a signature of higher-order brain regions, supported by single-unit mixed selectivity and the recurrent circuitry of the six-layered cortical microcircuit, which allows columns to retain incoming information and integrate it into stable latent representations. It remains unclear whether multiplexing arises from specialized processing within individual layers or from the collective coordination of multiple layers. Here, we analyzed laminar recordings from macaque motor cortex during a delayed match-to-sample task. We identified laminarly distributed, behaviorally specific subspaces that encoded distinct task variables. When the behavioral meaning of a variable was preserved, the same coding subspace was reused across time; when sample information was transformed into a match, the sample subspace was recycled to instead encode stimulus validity. In contrast, identical sensory variables -such as target direction-engaged distinct subspaces when their computational role differed, e.g. during visual encoding versus motor preparation. Subtle variations in laminar weights gave rise to multiple coexistent subspaces, enabling multiplexed representations at the columnar scale. Beyond their coexistence, we tracked the temporal evolution of individual coding subspaces. Task timing paced their geometric reorganization, with task-relevant information propagating along structured trajectories as the laminar center of mass shifted between superficial and deep layers. These laminar trajectories were consistent across sites, though propagation patterns varied, while overall population activity lacked structured dynamics, leaving coherent laminar information to emerge atop a background of unspecific fluctuations. HighlightsO_LICoordinated multilaminar activity encodes task-relevant information in motor cortex C_LIO_LIDifferent layer combinations span multiplexed coding spaces C_LIO_LICoding spaces for task condition, cue and direction are flexibly repurposed over time C_LIO_LITask timing paces the geometric reorganization of coding spaces C_LI Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=200 SRC="FIGDIR/small/690660v2_ufig1.gif" ALT="Figure 1"> View larger version (52K): org.highwire.dtl.DTLVardef@12158d4org.highwire.dtl.DTLVardef@4ee7b3org.highwire.dtl.DTLVardef@4dd46corg.highwire.dtl.DTLVardef@1b533f3_HPS_FORMAT_FIGEXP M_FIG C_FIG