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Understanding how cortical inhibition shapes circuit function requires identifying the connectivity rules relating the response properties of inhibitory interneurons and their postsynaptic targets. Here we explore the orientation tuning of layer 2/3 inhibitory inputs in the ferret visual cortex using a combination of in vivo axon imaging, functional input mapping, and physiology. Inhibitory boutons exhibit robust orientation-tuned responses with preferences that can differ significantly from the cortical column in which they reside. Inhibitory input fields measured with patterned optogenetic stimulation and intracellular recordings revealed that these inputs originate from a wide range of orientation domains, inconsistent with a model of co-tuned inhibition and excitation. Intracellular synaptic conductance measurements confirm that individual neurons can depart from a co-tuned regime. Our results argue against a simple rule for the arrangement of inhibitory inputs supplied by layer 2/3 circuits and suggest that heterogeneity in presynaptic inhibitory networks contributes to neural response properties. • GABAergic boutons have diverse orientation preferences within orientation domains • Single-neuron inhibitory input fields originate from diverse orientation domains • Conductance measurements show inhibition and excitation are not strictly co-tuned Scholl et al. examine the functional connectivity of layer 2/3 inhibitory inputs onto single neurons in the ferret visual cortex. This study argues against a simple rule describing the arrangement of inhibitory inputs supplied by layer 2/3 circuits. [ABSTRACT FROM AUTHOR]