Reinforcement Learning Recruits Somata and Apical Dendrites across Layers of Primary Sensory Cortex

The mammalian brain can form associations between behaviorally relevant stimuli in an animal’s environment. While such learning is thought to primarily involve high-order association cortex, even primary sensory areas receive long-range connections carrying information that could contribute to high-level representations. Here, we imaged layer 1 apical dendrites in the barrel cortex of mice performing a whisker-based operant behavior. In addition to sensory-motor events, calcium signals in apical dendrites of layers 2/3 and 5 neurons and in layer 2/3 somata track the delivery of rewards, both choice related and randomly administered. Reward-related tuft-wide dendritic spikes emerge gradually with training and are task specific. Learning recruits cells whose intrinsic activity coincides with the time of reinforcement. Layer 4 largely lacked reward-related signals, suggesting a source other than the primary thalamus. Our results demonstrate that a sensory cortex can acquire a set of associations outside its immediate sensory modality and linked to salient behavioral events. [Display omitted] •Events outside a cortical area’s modality can trigger tuft-wide dendritic spikes•Rewards modulate dendritic and somatic activity in layers 1, 2/3, and 5, but not 4•Reward-related activity emerges gradually with training and is task specific•Both expected and unexpected rewards can modulate primary sensory cortex Previously, the only known triggers of apical dendritic spikes were “bottom-up” events, such as appropriate sensory stimuli or an animal’s location in space. Lacefield et al. show that reinforced associations are powerful triggers of apical dendrite activity and that reward can manipulate perceptions at their earliest stages of cortical processing.