Retronasal Odor Perception Requires Taste Cortex, but Orthonasal Does Not

Abstract

Smells can arise from a source external to the body and stimulate the olfactory epithelium upon inhalation through the nares (orthonasal olfaction). Alternatively, smells may arise from inside the mouth during consumption, stimulating the epithelium upon exhalation (retronasal olfaction). Both ortho- and retronasal olfaction produce highly salient percepts, but the two percepts have very different behavioral implications. Here, we use optogenetic manipulation in the context of a flavor preference learning paradigm to investigate differences in the neural circuits that process information in these two submodalities of olfaction. Our findings support a view in which retronasal, but not orthonasal, odors share processing circuitry commonly associated with taste. First, our behavioral results reveal that retronasal odors induce rapid preference learning and have a potentiating effect on orthonasal preference learning. Second, we demonstrate that inactivation of the insular gustatory cortex selectively impairs expression of retronasal preferences. Thus, orally sourced (retronasal) olfactory input is processed by a brain region responsible for taste processing, whereas externally sourced (orthonasal) olfactory input is not.

Keywords: flavor; gustatory cortex; learning; multisensory; odor; orthonasal; preference; retronasal; smell; taste.

Figure 1.. Conceptual and experimental design.

(A) Odors enter the nasal cavity via the external nares (orthonasal) or through the internal nares via the back of the throat when food is consumed (retronasal). (B) Odor preference was assessed before and after training sessions consisting of alternating days with exposure to sweet-paired odor A and plain water-paired odor B. Exact duration of training varied between the different conditions (2, 4 or 6-day training), as indicated in the text and Figures.

Figure 2.. Learning and expression of ortho and retronasal odor preferences.

(A-D) Mean (±SEM) preference for odor A (the odor paired with sweet taste during training) before and after training in the Retro (A), Ortho (B), Retro/Ortho (C) and Cmbd/Ortho (D) conditions. (E) Mean (±SEM) change in preference (post–pre) for all conditions.

Figure 3.. Effect of GCx on the expression of ortho- and retronasal preferences.

(A-B) Mean (±SEM) preference for the odor A before and after training in the Retro GCx, Ortho GCx (A), and Cmbd/Ortho GCx and GC intact conditions (B). Note: Retro, 4-day GCx data are from [17] and included here for new analysis. See also Figure S1.