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Kilavik, B. E.

Publications and source records attributed to Kilavik, B. E..

5 recordsLinked to original sources

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

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

neuroscience↗

Coordinated multilaminar dynamics underlie multiplexed computation in motor cortex

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

neuroscience↗

Spontaneous spiking statistics form unique area-specific fingerprints and reflect the hierarchy of cerebral cortex

The cerebral cortex is hierarchically organised from sensory to higher cognitive areas1-4. Several dynamical5-8 and anatomical1-4,8 measures, such as timescales and neurotransmitter receptor expression, have independently been linked to the cortical hierarchy. However, a systematic and quantitative characterisation of the relationship between spontaneous spiking activity and the cortical hierarchy remains elusive. Here, we test the hypothesis that single-neuron spontaneous spiking statistics uniquely characterise each cortical area, and that they quantitatively correlate with the cortical hierarchy. We study the spontaneous activity of neurons in seven macaque cortical areas (V1, V4, DP, 7A, M1, PMd, PFC)9-12 in the eyes-open and eyes-closed conditions recorded in a dim-lit room. First, we uncover that the firing rate, inter-spike interval variation, and cross-correlation form a unique fingerprint of the cortical areas, but only when considering them in combination. Second, we show that the differences between the spiking statistics correlate with multiple anatomical markers1,2,4,13-17 of the cortical hierarchy. This effect is much stronger in the eyes-closed condition, suggesting that visual input or the expectation thereof modulates the hierarchical organisation of spontaneous activity. We also observe an increase in timescales up the hierarchy, in agreement with previous findings5,18,19. In conclusion, we demonstrate that spontaneous single-neuron spiking activity reflects the hierarchical organisation of the cerebral cortex: distinct spiking statistics for hierarchically distant areas; similar statistics for nearby areas. Our results thus add a new dynamical dimension to the concept of the cortical hierarchy.

neuroscience↗

Distinct sources and behavioral correlates of macaque motor cortical low and high beta

HIGHLIGHTSO_LIThe low beta rhythm is dominant in M1 and the high beta rhythm in PMd C_LIO_LIThe beta rhythms correlate with task-instructed and uninstructed behavior C_LIO_LILow beta reflects movement preparation and spontaneous postural dynamics C_LIO_LIHigh beta reflects temporal task prediction and dynamical visuospatial attention C_LI Low and high beta frequency rhythms were observed in the motor cortex, but their respective sources and behavioral correlates remain unknown. We studied local field potentials during pre-cued reaching behavior in macaques. They contained a low beta band (<20Hz) dominant in primary motor cortex and a high beta band (>20Hz) dominant in dorsal premotor cortex. Low beta correlated positively with reaction time from visual cue onset, and negatively with uninstructed hand postural micro-movements throughout the trial. High beta reflected temporal task prediction, with selective modulations before and during cues, which were enhanced in moments of increased focal attention when the gaze was on the work area. This double-dissociation in sources and behavioral correlates of motor cortical low and high beta, with respect to both task-instructed and spontaneous behavior, reconciles the largely disparate roles proposed for the beta rhythm, by suggesting band-specific roles in both movement control and spatio-temporal attention. O_FIG O_LINKSMALLFIG WIDTH=179 HEIGHT=200 SRC="FIGDIR/small/534535v2_ufig1.gif" ALT="Figure 1"> View larger version (48K): org.highwire.dtl.DTLVardef@fdd46aorg.highwire.dtl.DTLVardef@84b620org.highwire.dtl.DTLVardef@d12baaorg.highwire.dtl.DTLVardef@89a757_HPS_FORMAT_FIGEXP M_FIG C_FIG

neuroscience↗

On the relationship between LFP beta oscillation amplitude and firing rate of individual neurons in monkey motor cortex

It is a long-standing controversial issue whether an intrinsic relationship between the local field potential (LFP) beta oscillation amplitude and the spike rate of individual neurons in the motor cortex exists. Beta oscillations are prominent in motor cortical LFPs, and their relationship to the local neuronal spiking activity has been extensively studied. Many studies demonstrated that the spikes of individual neurons lock to the phase of LFP beta oscillations. However, the results concerning whether there is also an intrinsic relationship between the amplitude of LFP beta oscillations and the firing rate of individual neurons are contradictory. Some studies suggest a systematic mapping of spike rates onto LFP beta amplitude, and others find no systematic relationship. To resolve this controversy, we correlated the amplitude of LFP beta oscillations recorded in motor cortex of two male macaque monkeys with spike counts of individual neurons during visuomotor behavior, in two different manners. First, in an analysis termed task-related correlation, data obtained across all behavioral task epochs was included. These task-related correlations were frequently significant, and in majority of negative sign. Second, in an analysis termed trial-by-trial correlation, only data from a fixed pre-cue task epoch was included, and correlations were calculated across trials. Such trial-by-trial correlations were weak and rarely significant. We conclude that there is no intrinsic relationship between the firing rate of individual neurons and LFP beta oscillation amplitude in macaque motor cortex, beyond each of these signals being modulated by external factors such as the behavioral task.\n\nSIGNIFICANCE STATEMENTWe addressed the long-standing controversial issue of whether there is an intrinsic relationship between the local field potential (LFP) beta oscillation amplitude and the spike rate of individual neurons in the motor cortex. In two complementary analyses of data from macaque monkeys, we first demonstrate that the unfolding behavioral task strongly affects both the LFP beta amplitude and the neuronal spike rate, creating task-related correlations between the two signals. However, when limiting the influence of the task, by restricting our analysis to a fixed task epoch, correlations between the two signals were largely eliminated. We conclude that there is no intrinsic relationship between the firing rate of individual neurons and LFP beta oscillation amplitude in motor cortex.

neuroscience↗