Spatial connectivity matches direction selectivity in visual cortex.

Abstract

The selectivity of neuronal responses arises from the architecture of excitatory and inhibitory connections. In primary visual cortex, the selectivity of layer 2/3 neurons for stimulus orientation and direction is thought to arise from similarly-selective intracortical inputs1–7. A neuron’s excitatory inputs, however, can have diverse stimulus preferences1–4,6–8, and inhibitory inputs can be promiscuous9 and unselective10. Here we show that excitatory and inhibitory intracortical connections to a layer 2/3 neuron accord with its selectivity by obeying precise spatial patterns. We used rabies tracing1,11 to label and functionally image the excitatory and inhibitory inputs to individual pyramidal neurons of mouse visual cortical layer 2/3. Presynaptic excitatory neurons spanned layers 2/3 and 4 and were distributed coaxial to the postsynaptic neuron’s preferred orientation, favouring the region opposite to its preferred direction. By contrast, presynaptic inhibitory neurons resided within layer 2/3 and favoured locations near the postsynaptic neuron and ahead of its preferred direction. The direction selectivity of a postsynaptic neuron was unrelated to the selectivity of presynaptic neurons but correlated with the spatial displacement between excitatory and inhibitory presynaptic ensembles. Similar asymmetric connectivity establishes direction selectivity in the retina12–16, suggesting that this circuit motif might be canonical in sensory processing.