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 inputs 1 – 7 . A neuron’s excitatory inputs, however, can have diverse stimulus preferences 1 – 4 , 6 – 8 , and inhibitory inputs can be promiscuous 9 and unselective 10 . 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 tracing 1 , 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 retina 12 – 16 , suggesting that this circuit motif might be canonical in sensory processing.

Local Connectivity and Synaptic Dynamics in Mouse and Human Neocortex

“…These data were well fit by the Gaussian model (Fig 2A, solid red line) and indicated low peak connectivity among excitatory cells (~5%), moderate connectivity rates among inhibitory cells (~11%), and higher connectivity across E-I cell classes (E→I 12%, I→E 15%). In a rabies tracing study of primary visual cortex L2/3, E→E connections were found to have a wider lateral extent compared to I→E (28) . We confirm this result and additionally find that E→E and I→I connections have a similar spatial extent that is larger than both E→I and I→E connections.…”

How Cortical Circuits Implement Cortical Computations: Mouse Visual Cortex as a Model

“…Similarly, the spatial position (in terms of retinotopic coordinates) of inhibitory neurons that are presynaptic to a direction-selective neuron is offset relative to that of its presynaptic excitatory neurons. This spatial offset predicts the preferred direction of the direction-selective neuron (Rossi et al 2020).…”

“…This applies to both feedforward connectivity from L4 to L2/3 and recurrent connectivity within L2/3. Panel a adapted from Ko et al (2011), Lee et al (2016), Lien & Scanziani (2013), Morgenstern et al (2016), Rossi et al (2020), Wertz et al (2015), and Yoshimura et al (2005). (b) The spatial organization of connectivity is coaxial, whereby a neuron (red) tends to receive input from neurons (green) with similar orientation preference and whose location, in retinotopic coordinates, is along the axis of their preferred orientation.…”

The physiological basis for the computation of direction selectivity in theDrosophilaOFF pathway

“…64 Recent evidence shows a V1 neuron receives spatially offset inputs from excitatory and inhibitory neuron populations in agreement with its direction selectivity. 65 In carnivores and primates, the simple cell subunits also have a push-pull structure. 27–29 Similarly, T5 neurons show a contrast-opponent organization ( Fig.…”