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

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The paper studied intrinsic timescales across cortical area (dorsal premotor cortex versus primary motor cortex) and cortical depth in macaques performing a delayed-match-to-sample reaching task, using both single-unit spiking activity and local field potentials. It found convergent multimodal evidence for an inter-areal temporal hierarchy, with M1 showing longer spiking timescales and smaller LFP aperiodic spectral exponents than PMd, while laminar effects depended on signal modality: LFP spectral exponents were smaller in deep layers in both areas and LFP-autocorrelation timescales were longer in deep layers in M1, whereas spiking intrinsic timescales showed no significant laminar differences. Functionally, neurons with longer timescales maintained more stable planned movement direction representations during preparation and showed slower temporal evolution of movement encoding during execution. The paper does not explicitly discuss endometriosis or adenomyosis; it was included in the corpus via a keyword match in the upstream search index.

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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. Highlights SUA 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
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Abstract Hierarchy in the brain emerges across spatial and temporal scales, enabling transformations from rapid sensory encoding to sustained cognitive control. Hierarchical gradients are 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 laminar input-output projections, that obscures the distinction between feedforward and feedback pathways. 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 here adopted a multimodal approach using intrinsic 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 hierarchy, with longer spiking timescales and smaller LFP aperiodic spectral exponents in M1. Across cortical depth, however, temporal organization depended on signal modality. LFP spectral exponents were significantly smaller in deep than superficial layers in both areas, and LFP-autocorrelation timescales were longer in deep layers in M1. In contrast, spiking activity did not show significant laminar differences in intrinsic timescales. Functionally, neurons with longer timescales exhibited more stable representations of the planned movement direction during motor preparation in PMd and slower temporal evolution of movement encoding during execution in both areas. In conclusion, multimodal temporal measures converge on the same hierarchical organization across these two motor areas, with M1 placed higher than PMd. Our study provides the first characterization of intrinsic spiking timescales across cortical layers in any cortical area and shows that laminar temporal organization depends on the neural signal analyzed. This divergence likely reflects their distinct physiological origins. Spikes capture neuronal output, whereas LFPs primarily reflect synaptic and dendritic population activity, potentially integrating differential contributions from apical and basal dendritic inputs. Competing Interest Statement The authors have declared no competing interest.

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