Flavour refers to the sensory experience of food, which is a combination of sensory inputs sourced from multiple modalities during consumption, including taste and odour. Previous work has demonstrated that orally‐sourced taste and odour cues interact to determine perceptual judgements of flavour stimuli, although the underlying cellular‐ and circuit‐level neural mechanisms remain unknown. We recently identified a region of the piriform olfactory cortex in rats that responds to both taste and odour stimuli. Here, we investigated how converging taste and odour inputs to this area interact to affect single neuron responsiveness ensemble coding of flavour identity. To accomplish this, we recorded spiking activity from ensembles of single neurons in the posterior piriform cortex (pPC) in awake, tasting rats while delivering taste solutions, odour solutions and taste + odour mixtures directly into the oral cavity. Our results show that taste and odour inputs evoke highly selective, temporally‐overlapping responses in multisensory pPC neurons. Comparing responses to mixtures and their unisensory components revealed that taste and odour inputs interact in a non‐linear manner to produce unique response patterns. Taste input enhances trial‐by‐trial decoding of odour identity from small ensembles of simultaneously recorded neurons. Together, these results demonstrate that taste and odour inputs to pPC interact in complex, non‐linear ways to form amodal flavour representations that enhance identity coding. Key points Experience of food involves taste and smell, although how information from these different senses is combined by the brain to create our sense of flavour remains unknown. We recorded from small groups of neurons in the olfactory cortex of awake rats while they consumed taste solutions, odour solutions and taste + odour mixtures. Taste and smell solutions evoke highly selective responses. When presented in a mixture, taste and smell inputs interacted to alter responses, resulting in activation of unique sets of neurons that could not be predicted by the component responses. Synergistic interactions increase discriminability of odour representations. The olfactory cortex uses taste and smell to create new information representing multisensory flavour identity.
How an odor is perceived is to a large extent dependent on the context in which that odor is (or has been) experienced. For example, experiencing an odor in mixture with taste during consumption can instill taste qualities in the percept of that odor (e.g., vanilla—an odor—has a gustatory quality: sweet). How associative features of odors are encoded in the brain remains unknown, but previous work suggests an important role for ongoing interactions between piriform cortex and extra-olfactory systems. Here we tested the hypothesis that piriform cortex dynamically encodes taste associations of odors. Rats were trained to associate one of two odors with saccharin; the other odor remained neutral. Before and after training, we tested preferences for the saccharin-associated odor versus the neutral odor, and recorded spiking responses from ensembles of neurons in posterior piriform cortex (pPC) to intra-oral delivery of small drops of the same odor solutions. The results show that animals successfully learned taste-odor associations. At the neural level, single pPC neuron responses to the saccharin-paired odor were selectively altered following conditioning. Altered response patterns appeared after 1 second following stimulus delivery, and successfully discriminated between the two odors. However, firing rate patterns in the late epoch appeared different from firing rates early in the early epoch (<1 second following stimulus delivery). That is, in different response epoch, neurons used different codes to represent the difference between the two odors. The same dynamic coding scheme was observed at the ensemble level.Significance StatementOdors carry important meaning beyond their chemical identity. One particularly salient example of this are food odors, which play an important role in determining flavor preferences and food choice behavior. How these extra-olfactory aspects of odor are represented is unknown. Using extracellular recordings in awake rats in the context of a flavor preference learning task, we show that learned taste associations of odor stimuli are represented in the dynamic firing patterns of posterior piriform cortex neurons. The results suggest that associative odor coding results from ongoing interactions between olfactory and extra-olfactory systems.
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