Learning from unexpected events in the neocortical microcircuit

Scientists have long conjectured that the neocortex learns the structure of the environment in a predictive, hierarchical manner. To do so, expected, predictable features are differentiated from unexpected ones by comparing bottom-up and top-down streams of data. It is theorized that the neocortex then changes the representation of incoming stimuli, guided by differences in the responses to expected and unexpected events. Such differences in cortical responses have been observed; however, it remains unknown whether these unexpected event signals govern subsequent changes in the brain’s stimulus representations, and, thus, govern learning. Here, we show that unexpected event signals predict subsequent changes in responses to expected and unexpected stimuli in individual neurons and distal apical dendrites that are tracked over a period of days. These findings were obtained by observing layer 2/3 and layer 5 pyramidal neurons in primary visual cortex of awake, behaving mice using two-photon calcium imaging. We found that many neurons in both layers 2/3 and 5 showed large differences between their responses to expected and unexpected events. These unexpected event signals also determined how the responses evolved over subsequent days, in a manner that was different between the somata and distal apical dendrites. This difference between the somata and distal apical dendrites may be important for hierarchical computation, given that these two compartments tend to receive bottom-up and top-down information, respectively. Together, our results provide novel evidence that the neocortex indeed instantiates a predictive hierarchical model in which unexpected events drive learning.