Reciprocal representation of encoded features by cortical excitatory and inhibitory neuronal populations.

Abstract

In the cortex, the interplay between excitation and inhibition determines the fidelity of neuronal representations. However, while the receptive fields of excitatory neurons are often fine-tuned to the encoded features, the principles governing the tuning of inhibitory neurons are still elusive. 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). In contrast to PoSub-HD cells, the tuning of fast-spiking (FS) cells, the largest class of cortical inhibitory neurons, 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, recordings and specific optogenetic manipulations of the upstream thalamic populations as well as computational models suggest that this population co-tuning in the frequency domain has a local origin. 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.