Laminar-specific control of response gain and orientation-tuning by parvalbumin-expressing inhibitory interneurons in primate visual cortex

Understanding the role of different inhibitory interneuron subtypes in cortical computations is essential for explaining sensory processing in the neocortex. Orientation tuning in primate primary visual cortex (V1) provides a canonical model for studying how cortical sensory circuits and inhibitory interneurons compute relevant stimulus features. The selective feedforward convergence of non–orientation-selective thalamic afferents establishes initial orientation tuning in the granular V1 input layer. As signals propagate through the cortical microcircuit, orientation tuning sharpens in extra-granular layers, yet the underlying mechanisms and the contribution of specific inhibitory neuron subtypes remain unresolved. To study the role of the largest cortical inhibitory neuron subclass, parvalbumin-expressing (PV⁺) interneurons, in this V1 computation, we combined laminar extracellular recordings with bidirectional optogenetic manipulations of PV⁺ cells in marmoset V1. We find striking laminar specificity: in the granular layer, PV⁺ cells implement divisive/ multiplicative linear gain control, whereas in extra-granular layers they exert tuned nonlinear suppression that enhances orientation tuning. Computational modeling suggests that PV+ neurons control gain by modulating a neuron’s spiking threshold, and orientation tuning by modulating a neuron’s input noise, which regulates the neuron’s input–output function. Our findings reconcile discrepancies in previous rodent studies, reveal important species differences, and establish a framework for understanding layer-dependent inhibitory computations in the primate cortex.