Recognizing Taste: Coding Patterns Along the Neural Axis in Mammals

Abstract

The gustatory system encodes information about chemical identity, nutritional value, and concentration of sensory stimuli before transmitting the signal from taste buds to central neurons that process and transform the signal. Deciphering the coding logic for taste quality requires examining responses at each level along the neural axis-from peripheral sensory organs to gustatory cortex. From the earliest single-fiber recordings, it was clear that some afferent neurons respond uniquely and others to stimuli of multiple qualities. There is frequently a "best stimulus" for a given neuron, leading to the suggestion that taste exhibits "labeled line coding." In the extreme, a strict "labeled line" requires neurons and pathways dedicated to single qualities (e.g., sweet, bitter, etc.). At the other end of the spectrum, "across-fiber," "combinatorial," or "ensemble" coding requires minimal specific information to be imparted by a single neuron. Instead, taste quality information is encoded by simultaneous activity in ensembles of afferent fibers. Further, "temporal coding" models have proposed that certain features of taste quality may be embedded in the cadence of impulse activity. Taste receptor proteins are often expressed in nonoverlapping sets of cells in taste buds apparently supporting "labeled lines." Yet, taste buds include both narrowly and broadly tuned cells. As gustatory signals proceed to the hindbrain and on to higher centers, coding becomes more distributed and temporal patterns of activity become important. Here, we present the conundrum of taste coding in the light of current electrophysiological and imaging techniques at several levels of the gustatory processing pathway.

Keywords: geniculate ganglion; gustatory coding; gustatory cortex; nucleus of solitary tract; taste bud; taste quality.

Figure 1.

Schematics of the (A) rodent and (B) human gustatory pathways with a focus on peripheral and thalamo-cortical relays. In both species, information is conveyed via cranial nerves VII, IX, and X from the tongue to the brainstem. NST, nucleus of the solitary tract; PbN, parabrachial nucleus; VPMpc, parvicellular portion of the ventroposteromedial nucleus of the thalamus; IC, insular cortex; OFC, orbitofrontal cortex.