A geniculocortical circuit model predicts functional organization underlying efficient spatial frequency coding in...

Neural encoding of sensory information becomes more efficient when distinct stimuli evoke uncorrelated activity patterns. Spatial frequency (SF) information becomes decorrelated early in visual processing in a manner that involves both temporal differentiation in the dorsal lateral geniculate nucleus (dLGN) and firing rate differentiation in the primary visual cortex (V1). However, the specific functional circuit configurations that enable this synergy are not fully understood. To address this gap, we developed a geniculocortical subunit model to identify functional circuit configurations capable of producing a decorrelated V1 population response. We found that decorrelation could be explained by the combined activity of two complementary circuit configurations with distinct functional organization. The first circuit was characterized by temporally organized, late-onset dLGN inputs coupled to weak and delayed intracortical inhibition, whereas the second was characterized by less temporally constrained, early-onset dLGN inputs coupled to strong and early intracortical inhibition. Eliminating SF selectivity in upstream dLGN subunits did not affect SF decorrelation in the modeled V1 population response, indicating that decorrelation tolerates weak SF selectivity and is primarily driven by temporal organization. Together, these results suggest that biologically plausible circuit configurations are likely to produce SF decorrelation in the cortex through the temporal organization of feedforward inputs and intracortical inhibition.

When visual information enters the early stages of the visual system, it elicits patterns of neuronal activity that encode stimulus features. These codes are more efficient and support better feature discrimination when different stimuli elicit distinct and uncorrelated activity patterns. Population activity patterns depend on how neurons with different functional properties are organized within circuits. We wanted to understand how the functional configuration of circuits connecting the dorsal lateral geniculate nucleus and primary visual cortex enable the decorrelation of spatial frequency-evoked activity patterns. We explored these configurations in a simple computational model that simulates joint geniculate and cortical activity via connected subunits. The model predicted two complementary circuit configurations that recreated the most important underlying dynamics for differentiating SF-evoked activity. These configurations were primarily constrained by the temporal characteristics of geniculate responses and cortical inhibition rather than how strongly individual thalamic units responded to specific spatial frequencies. These findings provide testable predictions about the organization of visual circuits and highlight the importance of temporal organization in efficient coding.