Model-Based Approach Shows ON Pathway Afferents Elicit a Transient Decrease of V1 Responses

Neurons in the primary visual cortex (V1) receive excitation and inhibition from distinct parallel pathways processing light-ness (ON) and darkness (OFF). V1 neurons overall respond more strongly to dark than light stimuli, consistent with a pre-ponderance of darker regions in natural images, as well as human psychophysics. However, it has been unclear whether this dark-dominance is because of more excitation from the OFF pathway or more inhibition from the ON pathway. To under-stand the mechanisms behind dark-dominance, we record electrophysiological responses of individual simple-type V1 neurons to natural image stimuli and then train biologically inspired convolutional neural networks to predict the neurons' responses. Analyzing a sample of 71 neurons (in anesthetized, paralyzed cats of either sex) has revealed their responses to be more driven by dark than light stimuli, consistent with previous investigations. We show that this asymmetry is predominantly because of slower inhibition to dark stimuli rather than to stronger excitation from the thalamocortical OFF pathway. Consistent with dark-dominant neurons having faster responses than light-dominant neurons, we find dark-dominance to solely occur in the early latencies of neurons' responses. Neurons that are strongly dark-dominated also tend to be less orien-tation-selective. This novel approach gives us new insight into the dark-dominance phenomenon and provides an avenue to address new questions about excitatory and inhibitory integration in cortical neurons.

Automated summary

Neurons in the primary visual cortex (V1) respond more strongly to dark stimuli due to slower inhibition to dark stimuli rather than stronger excitation from the OFF pathway. This dark-dominance occurs in the early latencies of neurons' responses and is associated with less orientation selectivity. This novel approach provides new insight into the dark-dominance phenomenon and opens up avenues for further exploration of excitatory and inhibitory integration in cortical neurons.