Coexistence of Lateral and Co-Tuned Inhibitory Configurations in Cortical Networks

The responses of neurons in sensory cortex depend on the summation of excitatory and inhibitory synaptic inputs. How the excitatory and inhibitory inputs scale with stimulus depends on the network architecture, which ranges from the lateral inhibitory configuration where excitatory inputs are more narrowly tuned than inhibitory inputs, to the co-tuned configuration where both are tuned equally. The underlying circuitry that gives rise to lateral inhibition and co-tuning is yet unclear. Using large-scale network simulations with experimentally determined connectivity patterns and simulations with rate models, we show that the spatial extent of the input determined the configuration: there was a smooth transition from lateral inhibition with narrow input to co-tuning with broad input. The transition from lateral inhibition to co-tuning was accompanied by shifts in overall gain (reduced), output firing pattern (from tonic to phasic) and rate-level functions (from non-monotonic to monotonically increasing). The results suggest that a single cortical network architecture could account for the extended range of experimentally observed response types between the extremes of lateral inhibitory versus co-tuned configurations. Author Summary: The cerebral cortex contains a network of electrically active cells (neurons) interconnected by synapses, which may be excitatory (tending to increase activity) or inhibitory. Network activity, i.e., the ensemble of activity patterns of the individual cells, is driven by input from the sense organs, and creates an internal representation of features of the outside world. In auditory cortex, sound frequency (pitch) is encoded by the physical location of activity in the network. Thus, connections among cells at various distances may blur or sharpen the frequency representation. Recent work in living animals has yielded conflicting results: sharpening of responses via lateral inhibition in some cases, versus balanced excitation and inhibition (co-tuning) in others. It was previously unknown whether a single cortical network architecture could account for this spectrum of findings. Here, computer simulations based on experimental data reveal that this is indeed the case. Varying input to the network causes smooth transitions between lateral inhibition and co-tuning, accompanied by changes in the strength and timing of the responses. Diverse input-dependent response patterns in a single network may be a general mechanism enabling the brain to process a wide range of sensory information under various conditions.