For many years, the prevailing views for the organization and function of the taste system at the periphery centered around the concept of taste coding via broadly tuned taste receptor cells (38
). Hence, individual taste receptor cells were proposed to express receptors for various taste qualities and thus respond to multiple taste stimuli. Now, however, we know that each of the five basic tastes is mediated by its own class of taste receptor cells, each tuned to a single taste quality (i.e. sweet-cells, bitter-cells, etc), thus defining a “one-cell one-taste” coding logic (9
). Notably, existing models of taste coding in insula included proposals of broadly tuned neurons across taste qualities [with no spatial segregation (15
)], as well as others suggesting a certain degree of topographic organization, but with no region dedicated to the processing of only one taste quality (20
). While we cannot rule out the existence of sparse numbers of broadly tuned cells (24
) distributed throughout the taste cortex (i.e. non-clustered), our results demonstrate that the individual basic tastes are represented in the insula by finely tuned cells organized in a precise and spatially ordered gustotopic map, where each taste quality is encoded in its own (segregated) stereotypical cortical field.
The organization of the primary taste cortex appears, at first glance, reminiscent of the somatosensory, auditory, and visual system, which exhibit spatially organized somatotopic, tonotopic and retinotopic cortical maps (17
). However, unlike these three sensory modalities where their cortical maps reflect smooth transitions across features of sensory space, this is not the case in the taste system. Furthermore, in the somatosensory, auditory and visual systems the peripheral receptors display exacting spatial order, while in taste, a distributed ensemble of peripheral receptor cells in the tongue, without any spatial organization (but with defined identities), nonetheless converge into a fixed cortical map where neurons with similar response profiles are clustered. Why should taste be represented in a spatial map? We speculate this organization has an ancient evolutionary, possibly developmental rather than a strictly functional origin. Indeed, the perceptual space to be represented by the taste system is limited to just a handful of qualities, thus having each basic taste represented in individually segregated fields provides a simple and elegant architectural solution to pattern, wire, and interconnect the ensembles of neurons representing each taste quality.
Our studies suggest that the cortical fields representing the individual basic tastes cover only a small fraction of the insula. What does the rest of the insula do? In our systematic exploration of insula we found that outside the hot spots, only small numbers of sparsely distributed neurons exhibited significant fluorescent changes during the window of tastant presentation, (Fig. S6; see also Fig. S4
). Importantly, the same results were observed in animals lacking taste receptor function (e.g. in knockouts of receptor proteins; see Fig. S6
), and irrespective of the quality of the taste stimulus (including to artificial saliva alone), implying these do not represent responses to the individual basic tastes. Hence, the inter hot-spot regions might be involved in other aspects of taste coding, like in the representation of taste mixes and thus help code the perception of “flavor” [e.g. responding to several rather than a single taste (24
)]. In addition, insular cortex responds to more than just taste, and it is often thought of as a site for multisensory integration (15
). Thus, these areas may participate in the integration of taste with the other senses.
The discovery of a gustotopic map in the mammalian cortex, together with the advent of sophisticated genetic and optical tools (43
) should now make it possible to experimentally manipulate taste cortex with exquisite finesse. In future studies, it will also be important to elucidate how taste intensity is encoded in the insular cortex, and to determine whether taste qualities with similar valence project to common targets. Likewise, tracing the connectivity of each of the basic taste qualities to higher brain stations will help decipher how these integrate with other modalities, and combine with the internal and emotional states to ultimately choreograph taste behaviors (44