Context-dependent odor learning requires the anterior olfactory nucleus

Learning to associate the context in which a stimulus occurs is an important aspect of animal learning. We propose that the association of an olfactory stimulus with its multisensory context is mediated by projections from ventral hippocampal networks (vHC) to the anterior olfactory nucleus (AON). Using a contextually-cued olfactory discrimination task, rats were trained to associate two olfactory stimuli with different responses depending on visuo-spatial context. Temporary lesions of the AON or vHC impaired performance on this task. In contrast, such lesions did not impair performance on a non-contextual olfactory discrimination task. Moreover, vHC lesions also impaired performance on an analogous contextually-cued texture discrimination task, whereas AON lesions affected only olfactory contextual associations. We describe a distinct role for the AON in olfactory processing, and conclude that early olfactory networks such as the olfactory bulb and AON function as multimodal integration networks rather than processing olfactory signals exclusively. Significance statement Contextual information has long been known to play a key role in cognitive functions such as memory and decision making. We here show the contextual modulation of neural information in early primary sensory networks and its effects on contextually conditional learned behavior. We propose that projections from ventral hippocampus to anterior olfactory nucleus convey contextual information to the early olfactory system, modulating sensory representations and olfactory perception. Using behavioral pharmacology and computational modeling, we show how established network structures can mediate multimodal information and use context to make olfactory decisions.