The Role of Thalamic Population Synchrony in the Emergence of Cortical Feature Selectivity

In a wide range of studies, the emergence of orientation selectivity in primary visual cortex has been attributed to a complex interaction between feed-forward thalamic input and inhibitory mechanisms at the level of cortex. Although it is well known that layer 4 cortical neurons are highly sensitive to the timing of thalamic inputs, the role of the stimulus-driven timing of thalamic inputs in cortical orientation selectivity is not well understood. Here we show that the synchronization of thalamic firing contributes directly to the orientation tuned responses of primary visual cortex in a way that optimizes the stimulus information per cortical spike. From the recorded responses of geniculate X-cells in the anesthetized cat, we synthesized thalamic sub-populations that would likely serve as the synaptic input to a common layer 4 cortical neuron based on anatomical constraints. We used this synchronized input as the driving input to an integrate-and-fire model of cortical responses and demonstrated that the tuning properties match closely to those measured in primary visual cortex. By modulating the overall level of synchronization at the preferred orientation, we show that efficiency of information transmission in the cortex is maximized for levels of synchronization which match those reported in thalamic recordings in response to naturalistic stimuli, a property which is relatively invariant to the orientation tuning width. These findings indicate evidence for a more prominent role of the feed-forward thalamic input in cortical feature selectivity based on thalamic synchronization.Author Summary: While the visual system is selective for a wide range of different inputs, orientation selectivity has been considered the preeminent property of the mammalian visual cortex. Existing models of this selectivity rely on varying relative importance of feedforward thalamic input and intracortical influence. Recently, we have shown that pairwise timing relationships between single thalamic neurons can be predictive of a high degree of orientation selectivity. Here we have constructed a computational model that predicts cortical orientation tuning from thalamic populations. We show that this arrangement, relying on precise timing differences between thalamic responses, accurately predicts tuning properties as well as demonstrates that certain timing relationships are optimal for transmitting information about the stimulus to cortex.