Sensory information can only be used meaningfully in the brain when integrated with and compared with internally generated top-down signals. However, we know little about the brainwide afferents that convey such top-down signals, their information content, and learning-related plasticity. Pardi et al. identified the higher-order thalamus as a major source of top-down input to mouse auditory cortex and investigated a circuit in cortical layer 1 that facilitates plastic changes and flexible responses. These results demonstrate how top-down feedback information can reach cortical areas through a noncortical structure that has received little attention despite its widespread connections with the cortex. Science , this issue p. [844][1] The sensory neocortex is a critical substrate for memory. Despite its strong connection with the thalamus, the role of direct thalamocortical communication in memory remains elusive. We performed chronic in vivo two-photon calcium imaging of thalamic synapses in mouse auditory cortex layer 1, a major locus of cortical associations. Combined with optogenetics, viral tracing, whole-cell recording, and computational modeling, we find that the higher-order thalamus is required for associative learning and transmits memory-related information that closely correlates with acquired behavioral relevance. In turn, these signals are tightly and dynamically controlled by local presynaptic inhibition. Our results not only identify the higher-order thalamus as a highly plastic source of cortical top-down information but also reveal a level of computational flexibility in layer 1 that goes far beyond hard-wired connectivity. [1]: /lookup/doi/10.1126/science.abc2399