Bridging the Functional and Wiring Properties of V1 Neurons Through Sparse Coding

The functional properties of neurons in the primary visual cortex (V1) are thought to be closely related to the structural properties of this network, but the specific relationships remain unclear. Previous theoretical studies have suggested that sparse coding, an energy-efficient coding method, might underlie the orientation selectivity of V1 neurons. We thus aimed to delineate how the neurons are wired to produce this feature. We constructed a model and endowed it with a simple Hebbian learning rule to encode images of natural scenes. The excitatory neurons fired sparsely in response to images and developed strong orientation selectivity. After learning, the connectivity between excitatory neuron pairs, inhibitory neuron pairs, and excitatory-inhibitory neuron pairs depended on firing pattern and receptive field similarity between the neurons. The receptive fields (RFs) of excitatory neurons and inhibitory neurons were well predicted by the RFs of presynaptic excitatory neurons and inhibitory neurons, respectively. The excitatory neurons formed a small-world network, in which certain local connection patterns were significantly overrepresented. Bidirectionally manipulating the firing rates of inhibitory neurons caused linear transformations of the firing rates of excitatory neurons, and vice versa. These wiring properties and modulatory effects were congruent with a wide variety of data measured in V1, suggesting that the sparse coding principle might underlie both the functional and wiring properties of V1 neurons.