Subcortical coding of predictable and unsupervised sound-context associations

Our environment is made of a myriad of stimuli present in combinations often patterned in predictable ways. For example, there is a strong association between where we are and the sounds we hear. Like so many environmental patterns, sound-context associations are learned implicitly, in an unsupervised manner, and are highly informative and predictive of normality. Yet, we know little about where and how unsupervised sound-context associations are coded in the brain. Here we measured plasticity in the auditory midbrain of mice living over days in a naturalistic environment designed to present sound-context associations with different degrees of predictability. Plasticity in the auditory midbrain, a hub of auditory input and multimodal feedback, developed over days and reflected learning of contextual information in a manner that depended on the predictability of the sound-context association and not on reinforcement. Plasticity took the form of broad frequency shifts in tuning in auditory midbrain neurons. These shifts were paralleled by an increase in response gain and correlated with an increase in neuronal frequency discrimination. Thus, the auditory midbrain codes for unsupervised predictable sound-context associations, revealing a subcortical engagement in the detection of contextual sounds. This detection might facilitate the processing of behaviorally relevant foreground information described to occur in cortical auditory structures.