Acquisition of non-olfactory encoding improves odour discrimination in olfactory cortex

Abstract

Primary sensory cortices, initially considered elementary encoders of physicochemical attributes of environmental stimuli, are now known to be modulated by other aspects of experience, such as attentional state and internal expectations 1-3, movement-related signals 4-7 and spatial information 2, 8, 9. However, the specific role of these signals in cortical sensory processing is not fully understood 10. Here we reveal multiple and diverse non-olfactory responses in the primary olfactory (piriform) cortex (PCx), which dynamically enhance PCx odour discrimination according to behavioural demands. We designed a behavioural task using a virtual reality environment and performed recordings in PCx neurons. In this task, mice were trained to associate specific odours with visual contexts in order to receive a reward. We found that learning shifts PCx activity from encoding solely odour identity to a more complex regime. In this regime, positional, contextual, and associative responses emerge on odour-responsive neurons that thus become mixed-selective. Contextual information is sustained in PCx activity of expert animals, specifically when visual context identity is needed to solve the task. After learning, odours are better decoded from PCx activity when mice are engaged in the task and when odours are presented within a rewarded context. This enhancement of PCx olfactory processing is reliant on the acquired mixed-selectivity. Thus, the integration of extra-sensory inputs within primary sensory cortices can encode the behavioural relevance of encountered stimuli while improving sensory processing.