Peripheral gustatory processing of sweet stimuli by golden hamsters
Introduction
S neurons, a subset of chorda tympani (CT) neurons well-defined in the golden hamster (Mesocricetus auratus), are quite specific for stimuli that are sweet and respond with a characteristic rhythmic bursting pattern [4], [13], [14], [45], [47]. The CT innervates taste buds within fungiform papillae in the epithelium of the anterior two-thirds of the tongue. Taste-nerve and behavioral responses of transgenic mice, and the distribution of candidate sweet and bitter G-protein coupled receptors (GPCR) among taste receptor cells (TRCs) are consistent with labeled-line codes for the sweet and bitter tastes. A labeled line transmits information about one taste quality from TRCs to brain [34], [50], [66]. Bitter and sweet GPCR determine chemical selectivity and are expressed in separate TRC subsets that initiate, respectively, behavioral aversion or preference [28], [38], [63], [65]. However, transmission of information about sweet stimuli to the brain by S neurons [17] occurs after initial processing among TRCs in taste buds [24], [35]. Studies of taste-nerve responses to stimulus mixtures suggest possible functions of the taste-bud processing.
Candidate peripheral labeled-line codes are based on studies using single-compound, uni-quality stimuli. However, the gustatory system most often deals with heterogeneous mixtures composed of stimuli with different taste qualities. In mixtures, quinine hydrochloride, a prototype bitter stimulus, inhibits CT afferent signals elicited by a prototype sweet stimulus: sucrose. Primary evidence for this interaction comes from the hamster CT, which shows response suppression exclusively in S neurons. In the CT there is no reciprocal suppression of quinine responses by sucrose [9], [10], a reciprocity observed in third order taste neurons of the parabrachial nucleus [59], [60]. How across-quality inhibition relates to proposed peripheral labeled-line codes has not been addressed.
Hamsters behaviorally prefer and cross-generalize with sucrose many, but by no means all, stimuli that are sweet to humans [4], [52]. Such stimuli include the synthetic sweetener, dulcin (p-ethoxyphenyl urea), and the amino acid, d-phenylalanine [30], [40]. Hamsters do not behaviorally cross-generalize the sweeteners with quinine. Besides inhibiting sucrose responses in CT S neurons, quinine, along with other ionic stimuli that hamsters cross-generalize with quinine, activates electrolyte-sensitive E neurons [15], [18], [39]. E neurons are generalists that are also activated by non-bitter stimuli [14], and, thus, are unlikely bitter-labeled lines.
To determine whether quinine inhibition is specific for disaccharides like sucrose or may be as broad as the stimulus set activating S neurons, quinine–dulcin mixtures were studied. Dulcin, an aryl urea, is structurally similar to the sweet amino acid d-phenylalanine. Importantly, like sucrose, dulcin specifically activates CT S neurons [4], [12], [47]; and both sucrose and dulcin are ligands for the rat candidate T1 sweet receptor, heterodimeric GPCR, T1R2/T1R3 [28]. Analysis of CT whole-nerve and single-unit data on quinine–dulcin and quinine–sucrose mixtures is straightforward because quinine and sweeteners activate distinct subsets CT neurons.
Section snippets
Subjects
Electrophysiological responses were recorded from the right chorda tympani nerve (CT) of 12 adult, male, 110–180 g, golden hamsters (Mesocricetus auratus).
Surgical procedure
Hamsters were anesthetized by intraperitoneal injection of sodium pentobarbital (Abbot Labs, N. Chicago, IL, USA; initial dose: 80 mg/kg, subsequent doses: 40 mg/kg) to maintain a surgical level of anesthesia, and terminated at the end of the experiment. Body temperature was regulated at ∼37 °C with a Deltaphase® isothermal pad. A tracheal
Quinine–dulcin binary mixtures, whole CT nerve responses
Fig. 3 presents the average results for concentration series of quinine alone and quinine mixed with 3 or 10 mM dulcin. The 1 mM dulcin did not elicit reliable CT responses and when mixed with the series of quinine concentrations, elicited response levels indistinguishable from responses to quinine. It was thus omitted from further analysis.
To see if quinine inhibited responses to dulcin as hypothesized, data from six nerves for 3 and 10 mM dulcin mixed with 0, 1, 3 and 10 mM quinine (two upper
Discussion
Inhibitory effects of aversive compounds on neural taste responses to palatable compounds appear in species as diverse invertebrate flies: Phormia regina [5] and leeches: Hirudo medicinalis [27] and vertebrate rodents: Mesocricetus auratus [9], [10]. The inhibition is present in the gustatory periphery and not generated by circuitry in the central nervous system (CNS). Multiple aversive compounds with little structural similarity inhibit effects of palatable sugars in blowflies and palatable
Conclusion
We demonstrate “bitter-sweet” inhibition and a “sweet” rhythm in hamster chorda tympani responses that are indicative of the kinds of processing of gustatory information that occur in taste buds, and demonstrate that signaling of sweet taste by GPCRs is not transmitted unchanged via CT afferents to the brainstem.
Acknowledgements
This work was supported by a grant from the National Institutes of Health (USA), National Institute on Deafness and other Communicative Disorders: DC 004099.
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3.37 - A Perspective on Chemosensory Quality Coding
2020, The Senses: A Comprehensive Reference: Volume 1-7, Second EditionSalt taste inhibition by cathodal current
2009, Brain Research BulletinCitation Excerpt :Also, −10-μA imposed on 1 mM saccharin elicits bursting activity in hamster single CT nerve fibers specific to sugar and saccharin [45]. Bursting CT responses are associated with sweet stimuli in hamsters [12]. We saw no increment in intensity or sweet identity of supra-threshold Na-saccharin or Na-benzoate during weak cathodal current in humans.
Cracking taste codes by tapping into sensory neuron impulse traffic
2008, Progress in NeurobiologyCitation Excerpt :CT neurons with similar sucrose-best response profiles have been described for other species (cf., Section 4). They burst with a 1.4 Hz “sweet rhythm” to sweeteners as well as mixtures containing sweeteners (Frank et al., 2005). CT S neurons are rare in the lab rat CT (Frank et al., 1983); but despite their 6–11% frequency, rat S specialist CT neurons, recorded by microelectrode from the geniculate ganglion (GG), respond robustly and selectively (Lundy and Contreras, 1999; Breza et al., 2006, 2007).
The taste of sugars
2008, Neuroscience and Biobehavioral ReviewsCitation Excerpt :Responses can also be described in terms of their rhythms or patterns. For example, it has been common to observe rhythmic “swells” or “bursts” of firing in response to sucrose and other sweeteners in a subset of neurons in the CT (Ogawa et al., 1969, 1973, 1974; Sato et al., 1969; Mistretta, 1972; Nagai and Ueda, 1981; Frank et al., 2005) and, to a lesser extent, in the PBN (Perrotto and Scott, 1976) and gustatory thalamus (Scott and Erickson, 1971). In contrast, reports of these patterns are rare for non-sweet stimuli.
A Perspective on Chemosensory Quality Coding
2008, The Senses: A Comprehensive ReferenceCycloheximide: No ordinary bitter stimulus
2007, Behavioural Brain ResearchCitation Excerpt :Chlorhexidine is a bitter-tasting bis-biguanide antiseptic with taste-altering properties in humans [14,34]. Binary mixtures of equally aversive 30 μM CyX or 0.2 mM chlorhexidine with the highly preferred 5 mM dulcin (Sigma, St. Louis MO, USA), a sweetener with properties quite similar to sucrose in hamsters [33], were also tested to see if adding a sweetener decreases negative reactions to CyX and chlorhexidine as it does other aversive stimuli [87]. Finally, NaOH-treated CyX (for description of treatment, see Section 2.4, below) was tested to determine any effect of a fragrant ketone breakdown product: 2,4-dimethylcyclohexanone (Fig. 1) on intake behavior.