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 areas 1–4 . Several dynamical 5–8 and anatomical 1–4,8 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 markers 1,2,4,13–17 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 findings 5,18,19 . 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.