Excitatory and inhibitory intracortical circuits for orientation and direction selectivity

The computations performed by a neuron arise from the functional properties of the circuits providing its synaptic inputs. A prime example of these computations is the selectivity of primary visual cortex (V1) for orientation and motion direction. V1 neurons in layer 2/3 (L2/3) receive input mostly from intracortical circuits1, which involve excitation2-9 and inhibition10-12. To understand how an L2/3 neuron achieves its selectivity, therefore, one must characterize the functional organization of both its excitatory and inhibitory presynaptic ensembles. Here we establish this organization, and show how it predicts orientation selectivity and reveals a new cortical circuit for direction selectivity. We identified the presynaptic partners of pyramidal neurons in mouse V1 through rabies monosynaptic tracing1,13, and imaged the functional properties of the postsynaptic neuron and of its presynaptic ensemble. Excitatory presynaptic neurons were predominantly tuned to the postsynaptic neurons preferred orientation. Excitation and inhibition described an inverted Mexican hat, with inhibitory presynaptic neurons densest near the postsynaptic neuron and excitatory ones distributed more distally. Excitation and inhibition also differed in laminar origin: inhibitory presynaptic neurons concentrated in L2/3 while excitatory ones dominated in L4. The distribution of excitatory neurons in visual space was coaxial with the postsynaptic neurons preferred orientation and lay upstream of the neurons preferred direction. Inhibitory presynaptic neurons, instead, clustered more symmetrically around the postsynaptic neuron and favoured locations downstream of its preferred direction. These results demonstrate that L2/3 neurons obtain orientation selectivity from co-tuned neurons in L4 and beyond, and enhance it by contrasting an elongated excitatory input with a concentric inhibitory input. Moreover, L2/3 neurons can obtain direction selectivity through visually offset14 excitation and inhibition. These circuit motifs resemble those seen in the thalamocortical pathway15-20 and in direction selective cells in the retina21,22, suggesting that they are canonical across brain regions.