Area- and Layer-Specific Organization of Multimodal Timescales in Macaque Motor Cortex

Abstract

Hierarchy in the brain emerges across spatial and temporal scales, enabling transformations from rapid sensory encoding to sustained cognitive control, and this organization is well established in sensory systems. In contrast, the hierarchical organization of the primate motor cortex remains debated, partly due to its agranular architecture and the absence of clear layer-constrained input-output projections. In particular, the relative hierarchical position of the dorsal premotor cortex (PMd) and the primary motor cortex (M1) cannot be resolved from anatomy alone. To investigate their relative organization, we adopted a unique multimodal approach using timescales derived from both single-unit spiking activity (SUA) and local field potentials (LFPs) in macaques performing a delayed-match-to-sample reaching task. We found convergent evidence for inter-areal temporal organization, with longer SUA timescales and smaller LFP aperiodic spectral exponents in M1. Across cortical depth, however, temporal dynamics depended on signal modality. LFP autocorrelation timescales were systematically longer in deep layers of M1, and this was accompanied by smaller LFP spectral exponents in deep layers in both areas. In contrast, SUA did not show significant laminar differences in timescales. Functionally, neurons with longer timescales exhibited more stable representations of the movement direction during movement preparation in PMd and broader temporal generalization during execution in both areas. Our results place M1 above PMd in the temporal hierarchy, and provide the first laminar characterization of SUA timescales in any cortical area. The divergence in laminar temporal organization between SUA and LFP possibly reflects their different physiological origins. Extracellular spikes capture neuronal output near the cell body, whereas LFPs primarily reflect synaptic population activity, potentially exhibiting layer differences in integration of apical and basal dendritic inputs. HighlightsSUA and LFP-derived temporal dynamics place M1 above PMd in the cortical hierarchy SUA shows no laminar differences in temporal dynamics LFP exhibits significant layer-dependent temporal differences Longer SUA timescales link to slower movement encoding dynamics