Reciprocal feature encoding by cortical excitatory and inhibitory neurons

Abstract

In the cortex, the interplay between excitation and inhibition determines the fidelity of neuronal representations ^1–8. However, while the receptive fields of excitatory neurons are often fine-tuned to the encoded features ^9–12, the principles governing the tuning of inhibitory neurons are still elusive ^13–21. We addressed this problem by recording populations of neurons in the postsubiculum (PoSub), a cortical area where the receptive fields of most excitatory neurons correspond to a specific head-direction (HD) ^12,22–25. In contrast to PoSub-HD cells, the tuning of fast-spiking (FS) cells, the largest class of cortical inhibitory neurons ^26–28, was broad and heterogeneous. However, we found that PoSub-FS cell tuning curves were often fine-tuned in the spatial frequency domain, which resulted in various radial symmetries in their HD tuning. In addition, the average frequency spectrum of PoSub-FS cell populations was virtually indistinguishable from that of PoSub-HD cells but different from that of the upstream thalamic HD cells, suggesting that this population co-tuning in the frequency domain has a local origin. Two observations corroborated this hypothesis. First, PoSub-FS cell tuning was independent of upstream thalamic inputs. Second, PoSub-FS cell tuning was tightly coupled to PoSub-HD cell activity even during sleep. Together, these findings provide evidence that the resolution of neuronal tuning is an intrinsic property of local cortical networks, shared by both excitatory and inhibitory cell populations. We hypothesize that this reciprocal feature encoding supports two parallel streams of information processing in thalamocortical networks.