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

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Abstract

The cerebral cortex, from sensory to higher cognitive areas, is hierarchically organised 1–4 . Several dynamical 5–7 and anatomical 1–4 measures, such as timescales and neurotransmitter receptor expression, have independently been linked to the cortical hierarchy. However, a systematic quantitative link between anatomical markers of the cortical hierarchy and single-neuron dynamics has not yet been established. Here, we hypothesise that the single-neuron spontaneous spiking statistics uniquely characterise each cortical area, and that they quantitatively correlate with the cortical hierarchy. We consider the spontaneous activity of neurons in seven cortical areas (V1, V4, DP, 7A, M1, PMd, PFC) in macaques 8–11 in the eyes-open and eyes-closed conditions. First, we show 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 find that the differences between the spiking statistics strongly correlate with multiple anatomical markers 1,2,4,12–16 of the cortical hierarchy, especially in the eyes-closed condition. We also observe a correlation between autocorrelation timescales and the anatomical hierarchy, consistent with previous findings 5,17,18 . 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.

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