A hierarchy of intrinsic timescales across primate cortex

Abstract

Specialization and hierarchy are organizing principles for primate cortex, yet there is little direct evidence for how cortical areas are specialized in the temporal domain. We measured timescales of intrinsic fluctuations in spiking activity across areas and found a hierarchical ordering, with sensory and prefrontal areas exhibiting shorter and longer timescales, respectively. On the basis of our findings, we suggest that intrinsic timescales reflect areal specialization for task-relevant computations over multiple temporal ranges.

Figure 1

Spike-count autocorrelation reveals a hierarchical ordering of intrinsic timescales. (a) Datasets span seven cortical areas in the macaque monkey: MT, LIP, LPFC, OFC, ACC, S1, and S2. (b) Anatomical hierarchy of the areas, based on long-range projection patterns^,. (c) Spike-count autocorrelation was computed for neuronal spiking activity during the foreperiod of cognitive tasks. Each panel shows the dataset for one of six research groups. The decay of autocorrelation was fit by an exponential decay with an offset. Some areas in datasets show refractory adaptation at short time lags, which were excluded from the fit (Online Methods). Solid lines show the exponential fit. Intrinsic timescale extracted from the fit is shown for each area. Autocorrelation was computed with 50-ms time bins. (d) Intrinsic timescales across the visual–prefrontal hierarchy in five datasets (left), and the somatosensory hierarchy (right). Error bars mark s.e.

Figure 2

Links between intrinsic timescale and longer functional timescales. (a) Autocorrelation offset (B) reflects the strength of contributions with long timescales, which do not decay substantially within the fixation epoch. (b) Autocorrelation offset increases with intrinsic timescale. Colored lines show trends for individual datasets. The arrow shows the slope of dependence from a regression analysis (slope m = 0.8 ± 0.2 kHz). (c) In the Lee dataset, we previously measured timescales characterizing the decay of modulation of single-neuron firing rates by reward events, while monkeys performed a competitive decision-making task. The ordering of areas by reward timescale aligns with the ordering by intrinsic timescale. Error bars mark s.e.