Bradley K. Formaker

Responses of the hamster chorda tympani nerve to binary component taste stimuli: evidence for peripheral gustatory mixture interactions.

Studies of taste mixtures suggest that stimuli which elicit different perceptual taste qualities physiologically interact in the gustatory system and thus, are not independently processed. The present study addressed the role of the peripheral gustatory system in these physiological interactions by measuring the effects of three heterogeneous taste mixtures on responses of the chorda tympani (CT) nerve in the hamster (Mesocricetus auratus). Binary taste stimuli were presented to the anterior tongue and multi-fiber neural responses were recorded from the whole CT. Stimuli consisted of a concentration series of quinine.HCl (QHCl: 1-30 mM), sodium chloride (NaCl: 10-250 mM), sucrose (50-500 mM) and binary combinations of the three different chemicals. Each mixture produced a unique pattern of results on CT response magnitudes measured 10 s into the response. Sucrose responses were inhibited by quinine in QHCl-sucrose mixtures. Neural activity did not increase when quinine was added to 50-250 mM NaCl in QHCl-NaCl mixtures. However, the neural activity elicited by sucrose-NaCl mixtures was greater than the activity elicited by either component stimulus presented alone. The results demonstrate that gustatory mixture interactions are initiated at the level of the taste bud or peripheral nerve. Mechanisms for these interactions are unknown. The results are consistent with one component stimulus modifying the interaction of the other component stimulus with its respective transduction mechanism. Alternatively, peripheral inhibitory mechanisms may come into play when appetitive and aversive stimuli are simultaneously presented to the taste receptors.

Taste responses to mixtures: analytic processing of quality.

The tastes of 100 mM sodium chloride (NaCl), 100 mM sucrose, and 1 mM quinine hydrochloride in mixtures were investigated in golden hamsters (Mesocricetus auratus) with a conditioned taste aversion (CTA) paradigm. CTAs, established in golden hamsters by injection of lithium chloride, were quantified as percent suppression of control 1-hr stimulus intake. CTAs for 10 of 15 stimulus pairs with common components symmetrically cross-generalized, suggesting that component qualities were recognized in binary and ternary mixtures. However, CTAs to quinine were hardly learned and were weakly expressed when quinine was mixed with NaCl, and generalizations from multiple to single stimuli were stronger than vice versa (i.e., asymmetric). The behaviors reflect peripheral inhibition and/or central mixture suppression. Nonetheless, components retain their distinct qualities in mixtures, suggesting that taste processing is analytic.

Opponent effects of quinine and sucrose on single fiber taste responses of the chorda tympani nerve.

Responses of single chorda tympani fibers to mixtures of taste stimuli were studied in the golden hamster (Mesocricetus auratus). Sucrose-best neurons showed significant suppression to quinine-sucrose mixtures compared to sucrose alone. Quinine may exert its effect as an opponent stimulus in the receptor cells at the second messenger level. This suppression may make bitter quinine more readily detected when embedded in mixtures with sweeteners.

Peripheral gustatory processing of sweet stimuli by golden hamsters.

Behaviors and taste-nerve responses to bitter stimuli are linked to compounds that bind T2 receptors expressed in one subset of taste-bud receptor cells (TRCs); and behavioral and neural responses to sweet stimuli are linked to chemical compounds that bind a T1 receptor expressed in a different TRC subset. Neural and behavioral responses to bitter-sweet mixtures, however, complicate the ostensible bitter and sweet labeled lines. In the golden hamster, Mesocricetus auratus, quinine hydrochloride, the bitter prototype, suppresses chorda tympani (CT) nerve responses to the sweet prototype: sucrose. This bitter-sweet inhibition was tested with concentration series of sucrose and dulcin, a hydrophobic synthetic sweetener that hamsters behaviorally cross-generalize with sucrose. Dulcin, sucrose and other sweeteners activate one subset of CT fibers: S neurons; whereas, quinine activates a separate subset of CT fibers: E neurons. Whole-nerve and S-neuron CT responses to a sweetener concentration series, mixed with 0, 1, 3 and 10 mM quinine, were measured for 0-2.5 s transient and/or 2.6-10 s steady-state response periods. Ten-sec total single-fiber records, aligned at response onset, were averaged for 100 ms bins to identify response oscillations. Quinine inhibition of dulcin and sucrose responses was identical. Each log molar increment in quinine resulted in equivalent declines in response to either sweetener. Furthermore, sucrose response decrements paralleled response increments in quinine-sensitive CT neurons to the same quinine increases. A 1.43 Hz bursting rhythm to the sweeteners was unchanged by quinine inhibition or decreases in sweetener concentration. Taste-bud processing, possibly between-cell inhibition and within-cell negative feedback, must modify signals initiated by T1 receptors before they are transmitted to the brain.

Responses of the Hamster Chorda Tympani Nerve to Sucrose+Acid and Sucrose+Citrate Taste Mixtures

Studies of taste receptor cells, chorda tympani (CT) neurons, and brainstem neurons show stimulus interactions in the form of inhibition or enhancement of the effectiveness of sucrose when mixed with acids or citrate salts, respectively. To investigate further the effects of acids and the trivalent citrate anion on sucrose responses in hamsters (Mesocricetus auratus), we recorded multifiber CT responses to 100 mM sucrose; a concentration series of HCl, citric acid, acetic acid, sodium citrate (with and without amiloride added), potassium citrate, and all binary combinations of acids and salts with 100 mM sucrose. Compared with response additivity, sucrose responses were increasingly suppressed in acid + sucrose mixtures with increases in titratable acidity, but HCl and citric acid were more effective suppressors than acetic acid. Citrate salts suppressed sucrose responses and baseline CT neural activity to a similar degree. Citrate salts also elicited prolonged, concentration-dependent, water-rinse responses. The specific loss in sucrose effectiveness as a CT stimulus with increasing titratable acidity was confirmed; however, no increase in sucrose effectiveness was found with the addition of citrate. Further study is needed to define the chemical basis for effects of acids and salts in taste mixtures.

Amiloride-Sensitive and Amiloride-Insensitive Responses to NaCl + Acid Mixtures in Hamster Chorda Tympani Nerve

Component signaling in taste mixtures containing both beneficial and dangerous chemicals depends on peripheral processing. Unidirectional mixture suppression of chorda tympani (CT) nerve responses to sucrose by quinine and acid is documented for golden hamsters (Mesocricetus auratus). To investigate mixtures of NaCl and acids, we recorded multifiber responses to 50 mM NaCl, 1 and 3 mM citric acid and acetic acid, 250 μM citric acid, 20 mM acetic acid, and all binary combinations of each acid with NaCl (with and without 30 μM amiloride added). By blocking epithelial Na(+) channels, amiloride treatment separated amiloride-sensitive NaCl-specific responses from amiloride-insensitive electrolyte-generalist responses, which encompass all of the CT response to the acids as well as responses to NaCl. Like CT sucrose responses, the amiloride-sensitive NaCl responses were suppressed by as much as 50% by citric acid (P = 0.001). The amiloride-insensitive electrolyte-generalist responses to NaCl + acid mixtures approximated the sum of NaCl and acid component responses. Thus, although NaCl-specific responses to NaCl were weakened in NaCl-acid mixtures, electrolyte-generalist responses to acid and NaCl, which tastes KCl-like, were transmitted undiminished in intensity to the central nervous system. The 2 distinct CT pathways are consistent with known rodent behavioral discriminations.