Retronasal Odor Perception Requires Taste Cortex, but Orthonasal Does Not

Abstract

Summary 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 sub-modalities 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.

Multisensory interactions underlying flavor consumption in rats: the role of experience and unisensory component liking

“…However, it is possible that the training paradigm used in the present study was not effective in establishing taste–smell congruency. Rats were exposed to specific taste–smell combinations from weaning to early adulthood, covering an extensive period during which animals are known to learn about the sensory qualities of food (Fanselow and Birk 1982; Sclafani and Ackroff 1994; Stevenson 2001; Gautam and Verhagen 2010; Maier et al 2014; Blankenship et al 2019). Nonetheless, the establishment of flavor correspondences may occur during a critical period outside of the training period used here, or require more extensive exposure.…”

“…Our finding that experience does not affect instantaneous decisions about taste–smell mixtures relative to their components does not imply that experience has no effect on perception of the components. Although we did not compare component consumption before and after training, it is possible, and perhaps even likely, that our training procedure changed the palatability of components through associative learning (Holman 1975; Rescorla and Cunningham 1978; Rescorla 1980; Fanselow and Birk 1982; Holder 1991; Capaldi et al 1994; Yeomans et al 2006; Blankenship et al 2019). It is also possible that mere exposure to the individual components (regardless of the exact pairings) is necessary for their integration during subsequent testing.…”

Chemospecific deficits in taste sensitivity following bilateral or right hemispheric gustatory cortex lesions in rats

“…This suggests that GC may be critical in more complex processes that includes integration of taste signals with those from other modalities so as to optimize adaptive taste‐related behavior such as what occurs during associative learning (Vincis & Fontanini, 2016). Moreover, GC may be involved with the integration of chemosensory signals leading to flavor perception, as suggested by the identification of single neurons in this brain site that respond to both taste and olfactory stimuli (Samuelsen & Fontanini, 2017; Maier, 2016) and recently complemented by the finding that retronasally, but not orthonasally, learned preferences requires the GC (Blankenship, Grigorova, Katz, & Maier, 2019). Nevertheless, our findings demonstrate that the detection of different classes of taste compounds is not uniformly processed in gustatory brain regions.…”

Flavor education and training in olfactory dysfunction: a pilot study

“…Recent findings suggest OT to be driven "top-down", hence coming from central processes [35]. Furthermore, same odors were found to activate different central structures when applied retronasally versus orthonasally and retronasal odor perception stimulates many brain regions including gustatory circuits [36,37]. It hence seems appealing to also use the retronasal route for conscious stimulation and structured training.…”