Updating Contextual Sensory Expectations for Adaptive Behavior

The brain has the extraordinary capacity to construct predictive models of the environment by internalizing statistical regularities in the sensory inputs. The resulting sensory expectations shape how we perceive and react to the world; at the neural level, this relates to decreased neural responses to expected than unexpected stimuli (“expectation suppression”). Crucially, expectations may need revision as context changes. However, existing research has often neglected this issue. Further, it is unclear whether contextual revisions apply selectively to expectations relevant to the task at hand, hence serving adaptive behavior. The present fMRI study examined how contextual visual expectations spread throughout the cortical hierarchy as we update our beliefs. We created a volatile environment: two alternating contexts contained different sequences of object images, thereby producing context-dependent expectations that needed revision when the context changed. Human participants of both sexes attended a training session before scanning to learn the contextual sequences. The fMRI experiment then tested for the emergence of contextual expectation suppression in two separate tasks, respectively, with task-relevant and task-irrelevant expectations. Effects of contextual expectation emerged progressively across the cortical hierarchy as participants attuned themselves to the context: expectation suppression appeared first in the insula, inferior frontal gyrus, and posterior parietal cortex, followed by the ventral visual stream, up to early visual cortex. This applied selectively to task-relevant expectations. Together, the present results suggest that an insular and frontoparietal executive control network may guide the flexible deployment of contextual sensory expectations for adaptive behavior in our complex and dynamic world.