Ian K Christie, Paul Miller, Stephen D Van Hooser

The development of direction-selective cortical columns requires visual experience, but the neural circuits and plasticity mechanisms that are responsible for this developmental transition are unknown. To gain insight into the mechanisms that could underlie experience-dependent increases in selectivity, we explored families of cortical amplifier models that enhance weakly biased feed-forward signals. Here, we focused exclusively on possible contributions of cortico-cortical connections and took feed-forward input to be constant. We modeled pairs of interconnected columns that received equal and oppositely biased inputs. In a single-element model of cortical columns, we found 2 ways that cortical columns could receive biased feed-forward input and exhibit strong but unselective responses to stimuli: 1) within-column recurrent excitatory connections could be strong enough to amplify both strong or weak feed-forward input, or 2) columns that received differently-biased inputs could have strong excitatory cross-connections that destroy selectivity. A Hebbian plasticity rule combined with simulated experience with stimuli weakened these strong cross-connections across cortical columns, allowing the individual columns to respond selectively to their biased inputs. In a model that included both excitatory and inhibitory neurons in each column, an additional means of obtaining selectivity through the cortical circuit was uncovered: cross-column suppression of inhibition-stabilized networks. When each column operated as an inhibition-stabilized network, cross-column excitation onto inhibitory neurons forced competition between the columns, but in a manner that did not involve strong null direction inhibition, consistent with experimental measurements of direction selectivity in visual cortex. Experimental predictions of these possible contributions of cortical circuits are discussed.