A transthalamic pathway is crucial for stimulus feature selectivity in higher order cortex.

Sensory perception arises from activity between cortical areas, first primary cortex and then higher order cortices. This communication is served at least in part by transthalamic (cortico-thalamo-cortical) pathways, which ubiquitously parallel direct corticocortical pathways, yet their role in sensory processing has largely been ignored. Here, we show that the transthalamic pathway from S1 to S2 propagates task-relevant information required for correct sensory decisions. Using optogenetics, we specifically inhibited the pathway at its synapse in higher order somatosensory thalamus of mice performing a texture-based discrimination task. At the same time, the cellular effects of inhibition were monitored in primary or secondary cortex using two-photon calcium imaging. Inhibition severely impaired performance in a delayed discrimination task, despite intact direct corticocortical projections, thus challenging the purely corticocentric map of perception. Interestingly, the inhibition did not reduce overall cell responsiveness to texture stimulation in somatosensory cortex, but rather disrupted the texture selectivity of cells, a discriminability that develops over task learning. This discriminability was more disrupted in the secondary than primary somatosensory cortex, emphasizing the feedforward influence of the transthalamic route. Transthalamic pathways thus appear critical in delivering performance-relevant information to higher order cortex and are critical hierarchical pathways in perceptual decision-making.