The Biology of Taste
The taste system is in charge of evaluating the nutritious content of food sources, and preventing the ingestion of toxic substances. Sweet taste permits the identification of energy-rich nutrients, umami allows the recognition of amino acids, salt taste ensures the proper dietary electrolyte balance, and sour and bitter warn against the intake of potentially noxious and/or poisonous chemicals. Surprisingly, although we can taste a large repertoire of chemical entities, it is now generally accepted that qualitatively they evoke very few distinct taste sensations: sweet, bitter, sour, salty and savory (or umami). While this repertoire may appear modest, it has accommodated the evolutionary need for an effective and reliable platform to help recognize and distinguish key components of the animals’ diet.
In humans, taste has the additional value of contributing to the overall pleasure and enjoyment of a meal. Notably, taste behaviors are exquisitely modulated by the internal state (for example hunger, satiety, emotion and expectation), thus providing a powerful experimental model for the study of brain circuits mediating innate rewarding and aversive behaviors, and their modulation by our physiological and emotional state.
In rodents, taste information travels from taste receptor cells (TRC) in the oral cavity to the primary gustatory cortex (insular cortex) via four neural stations: TRCs to taste ganglia (e.g. geniculate or petrosal), then to nucleus of the solitary tract, the parabrachial nucleus, the thalamus, and finally, to the taste cortex (1,2).
Over the past 20 years, we have identified the cells and receptors for every one of the five basic taste qualities (3,4,5)(6,7), and demonstrated that each taste is mediated by its own receptor expressed in distinct classes of taste receptor cells (sweet cells, bitter cells, sour cells, etc.). This work defined the identity of the sensory detectors that allow us to recognize and respond to food sources, and elucidated the fundamental logic of taste coding at the periphery: one taste-one cell, each hardwired via labeled lines to trigger predetermined behaviors (8,9,10,11).
At the periphery, the five basic classes of taste cells signal to a matching set of ganglion neurons (e.g. sweet TRC-> sweet ganglion neuron, bitter TRC->bitter ganglion neuron)(12). How do ganglion processes identify their proper TRC partners? We combined single-cell functional imaging and mouse genetics to demonstrate that sweet and bitter TRCs use distinct signaling molecules to guide wiring of the peripheral taste system. Indeed, we engineered animals with mis-wired taste systems, whereby bitter neurons now respond to sweet tastants, or sweet neurons that respond to bitter (13). Together, these results uncovered the wiring of the taste system at the periphery, and proved the labeled line organization of the taste system
Studying the coding and organization of the taste system in the brain showed that different taste modalities are represented in taste cortex as a map (14). By manipulating the cortical fields representing the two most salient taste qualities, sweet and bitter, we demonstrated that it is possible to directly control an animal’s internal representation, sensory perception, and most notably their behavioral actions, in the absence of any sensory input (15).
The ability of the taste system to identify a tastant (what does it taste like?) enables animals to recognize and discriminate between the different basic taste qualities. The valence of a tastant (is it appetitive or aversive?) specifies its hedonic value, and the execution of selective behaviors. Recently, we showed that the amygdala -one of the key brain centers involved in the coding of emotions – is necessary and sufficient to drive valence-specific behaviors to taste stimuli (16). By manipulating selective taste inputs to the amygdala, we demonstrated that it is possible to impose a positive or negative valence to a neutral water stimulus, and even to reverse the hedonic value of a sweet or bitter tastant. Remarkably, animals with silenced amygdala no longer exhibit behavior that reflects the valence associated with delivery of sweet and bitter stimuli. Nonetheless, these animals can still identify and discriminate between tastants. These results help explain how the taste system generates stereotypic and predetermined attractive and aversive taste behaviors, and substantiate distinct neural substrates for the discrimination of taste identity and the assignment of valence.