Spatial connectivity matches direction selectivity in visual cortex

• Published in: Nature (London) 2020-12, Vol.588 (7839), p.648-652
• Main Authors: Rossi, L. Federico, Harris, Kenneth D., Carandini, Matteo
• Format: Article
• Language: English
• Subjects: 13; 13/1; 13/109; 13/51; 14; 14/1; 14/35; 14/69; 631/378/2613/1875; 631/378/3920; 64; 64/60; 9/10; Animals; Circuits; Excitatory Postsynaptic Potentials; Female; Humanities and Social Sciences; Information processing; Inhibitory Postsynaptic Potentials; Male; Mice; multidisciplinary; Neural circuitry; Neural Inhibition; Neural networks; Neural Pathways; Neuroanatomical Tract-Tracing Techniques; Neurons; Observations; Orientation behavior; Physiological aspects; Preferences; Preferred orientation; Presynaptic Terminals - physiology; Pyramidal cells; Pyramidal Cells - physiology; Rabies; Rabies virus - metabolism; Receptors, Virus - metabolism; Retina - cytology; Retina - physiology; Science; Science (multidisciplinary); Selectivity; Sensory integration; Somatosensory cortex; Viral Envelope Proteins - genetics; Viral Envelope Proteins - metabolism; Visual cortex; Visual Cortex - cytology; Visual Cortex - physiology
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/s41586-020-2894-4

The selectivity of neuronal responses arises from the architecture of excitatory and inhibitory connections. In the primary visual cortex, the selectivity of a neuron in layer 2/3 for stimulus orientation and direction is thought to arise from intracortical inputs that are similarly selective 1 – 8 . However, the excitatory inputs of a neuron can have diverse stimulus preferences 1 – 4 , 6 , 7 , 9 , and inhibitory inputs can be promiscuous 10 and unselective 11 . Here we show that the 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 , 12 to label and functionally image the excitatory and inhibitory inputs to individual pyramidal neurons of layer 2/3 of the mouse visual cortex. Presynaptic excitatory neurons spanned layers 2/3 and 4 and were distributed coaxial to the preferred orientation of the postsynaptic neuron, 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 13 – 17 . This suggests that this circuit motif might be canonical in sensory processing. In the mouse visual cortex, the excitatory and inhibitory presynaptic neurons of individual layer 2/3 pyramidal neurons are spatially offset to generate direction-selective responses.