Parallel processing in mammalian taste buds?

Abstract

ROPER, S.D. Parallel processing in mammalian taste buds? Physiol Behav XXX(Y) 000-000, 2009. There is emerging evidence that two parallel lines of gustatory information are generated in taste buds. One pathway leads to higher cortical centers and is involved in discriminating basic taste qualities (sweet, bitter, sour, salty, umami) and perceiving flavors. The other pathway may conduct information involved in physiological reflexes such as swallowing, salivation, and cephalic phase digestion. If this notion is true, the existence of two populations of taste bud cells that have different functional characteristics may lie at the origins of the two pathways. This speculative concept is explored in this review of taste signal processing in mammalian taste buds.

Fig. 1

Parallel neuronal pathways for information from taste buds to higher brain centers. In rodents, neurons in the parabrachial nucleus project to thalamocortical and ventral forebrain structures. (In primates, however, signals from the nucleus of the solitary tract travel directly to the thalamus). Discrimination of the basic taste qualities is believed to be take place in the primary gustatory cortex, at least in primates [3]. Neurons that project to the reticular formation (blue) initiate physiological reflexes, including those involved in cephalic phase digestion, triggered by taste stimulation. Central pathways for these cephalic phase reflexes are not known in great detail. Modified from [1,2].

Fig. 2

CHO cells stably expressing high affinity receptors for neurotransmitters constitute effective biosensors for identifying taste transmitters. This micrograph shows a biosensor cell, held on the tip of a glass micropipette and apposed to a Presynaptic Cell isolated from a mouse vallate papilla. Presynaptic taste cells isolated from transgenic mice that express GFP on the GAD67 promoter fluoresce green [24], allowing confident identification of this cell type, as shown here. Presynaptic cells, when depolarized by KCl, secrete serotonin, and in some cases (~33%) co-secrete noradrenalin with serotonin. (No cells were found with depolarization-evoked noradrenalin alone). Modified from [25].

Fig. 3

Ca²⁺ imaging of a serotonin biosensor cell closely apposed to an isolated Presynaptic Cell (such as in Fig. 2). The Presynaptic Cell (Pre) and the biosensor cell (5HT-Bio) were both loaded with the Ca²⁺-sensitive dye, Fura 2. Depolarizing the Presynaptic Cell with 50 mM KCl (bar below traces) generated a robust signal in the Presynaptic Cell due to Ca²⁺ influx. This was followed after a brief latency by a 5-HT biosensor cell response, indicating depolarization-evoked release of 5-HT from the Presynaptic Cell. KCl had no direct effect on the biosensor cell. Signals were only observed when the biosensor cell was pressed against the Presynaptic Cell. Modified from [29].

Fig. 4

Schematic diagram of hypothesized signal processing in mammalian taste buds. At left is shown a postulated taste bud processing unit, consisting of a cluster of Receptor (Type II) Cells, a Presynaptic (Type III) Cell, and their nerve innervation. For simplicity, only 1 Presynaptic Cell is illustrated. Type I ensheathing glial-like cells that may surround the cluster and limit ATP diffusion have also been omitted for clarity. At the right is shown the same cluster, but expanded to illustrate cell-to-cell communication mediated by taste-evoked ATP. Taste excitation by sweet, bitter or umami compounds stimulate Receptor cells to secrete ATP and activate 1° gustatory afferent fibers. Taste-evoked ATP also excites Presynaptic Cells which form synapses with as-yet unidentified fibers (shown by “?”). Sour and salty stimuli act directly on Presynaptic Cells [27]. Presynaptic Cells release serotonin and noradrenalin, perhaps as neurocrine transmitters at their synapses, or as paracrine transmitters acting within the confines of the taste bud, or both.