Cortical amplification models of experience-dependent development of selective columns and response sparsification

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 feedforward signals. Here we focused exclusively on possible contributions of cortico-cortical connections and took feedforward 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 two ways that cortical columns could receive biased feedforward input and exhibit strong but unselective responses to stimuli: 1) within-column recurrent excitatory connections could be strong enough to amplify both strong and weak feedforward 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.NEW & NOTEWORTHY Sensory circuits are initially constructed via mechanisms that are independent of sensory experience, but later refinement requires experience. We constructed models of how circuits that receive biased feedforward inputs can be initially unselective and then be modified by experience and plasticity so that the resulting circuit exhibits increased selectivity. We propose that neighboring cortical columns may initially exhibit coupling that is too strong for selectivity. Experience-dependent mechanisms decrease this coupling so individual columns can exhibit selectivity.