Constructing quality profiles for taste compounds in rats: A novel paradigm
Introduction
The systematic examination of the critical stimulus features and the underlying neurobiological processes that lead to the perception of quality is central to an understanding of sensory function. In the study of the gustatory system, this has been challenging because the qualitative features of taste stimuli do not vary along any simple continuous physical dimension that is analogous to wavelength for color vision or frequency of sound pressure for auditory pitch. Instead, taste quality appears to be limited to a few categories. The exact number of qualitative categories is debated and likely varies across species. In most, but not all mammals that have been examined, there is evidence that sugars, salts, acids, and plant alkaloids generally lead to discriminable taste sensations that humans describe as sweet, salty, sour, and bitter, respectively. Some synthetic compounds also fall into these categories. Additional taste qualities have been proposed as well, such as umami [1], [2], fat (e.g., [3], [4]), and polysaccharide taste (e.g., [5]), but there is a general agreement that sweet, sour, salty, and bitter and their analogous perceptions in non-human mammals, including the rat, represent core qualitative components of compounds that stimulate the gustatory system, notwithstanding important species exceptions (e.g., [6], [7]).
Animal models have proven to be indispensable in the neurobiological analysis of taste function owing largely to the fact that the gustatory system can be manipulated anatomically, genetically, and pharmacologically in controlled ways. Ultimately, the effects of such manipulations on the taste-related behavior of the animal must be assessed. In this regard, rodents have proven their utility. Nevertheless, it remains a challenge to characterize the taste quality of compounds perceived by non-verbal subjects such as rats.
With some exceptions, the most common method used to assess taste quality in rodent models is the conditioned taste aversion (CTA) generalization paradigm. In this procedure an animal is presented with a taste solution, which serves as the conditioned stimulus (CS), followed by induction of visceral malaise. After such a conditioning trial, animals will avoid ingesting the CS as well as compounds that are thought to possess a similar taste quality. In a seminal experiment, Nowlis, Frank and Pfaffmann [8] built on the prior use of the CTA generalization paradigm by Nachman [9] and Tapper and Halpern [10], by using various taste compounds as CSs in different groups of hamsters and rats and then testing each group for their intake suppression of 0.1 M sucrose, 0.1 M NaCl, 0.01 mM HCl, and 0.0001 mM quinine hydrochloride. Accordingly, taste quality profiles for each compound were derived based on the inferred similarity of the CS with each of the prototypical test stimuli.
Although this procedure has provided valuable information to researchers interested in taste processing, like all behavioral techniques, it possesses some interpretive and methodological limitations. One constraint is that a novel CS must be used with each group. Thus, a large number of animals are required to comprehensively assess taste quality generalization. Another limitation is that some stimuli (e.g., quinine or HCl) are inherently avoided by rats, consequently making it difficult to differentiate conditioned from unconditioned suppression of intake (i.e., a “floor effect”). Additionally, stimulus intensity dynamism (see [11]) presents a caveat for data interpretation that must be considered. This refers to the documented tendency of animals to display increased responses to stimuli that have higher intensity than the training stimulus and decreased responses to stimuli that have a lower intensity. Interactions between intensity of the CS and the test stimulus (TS) have been reported to influence the magnitude of avoidance displayed after taste aversion conditioning [11], [12], [13]. Finally, given that testing occurs in extinction, the number of test stimuli and test sessions possible is restricted. For the reasons outlined above, a major objective of this experiment was to develop a procedure that circumvents the interpretive and methodological limitations associated with the CTA approach, yet still provide a measure of generalization that could provide insight regarding the taste quality of test compounds. Here we present a new operant taste generalization procedure modeled after work conducted by Morrison [14] that permits inferences to be formed regarding the degree to which test compounds taste similar to sucrose, NaCl, citric acid, and quinine hydrochloride providing a qualitative profile for a given taste stimulus in a manner similar to that derived from CTA paradigms but without some of the limitations of the latter technique.
Section snippets
Experiment 1
It was necessary to select concentrations of tastants that were relatively matched for intensity so that discriminations would be based on quality. Although it is virtually impossible to exactly match intensity across compounds in animals, a range of concentrations can be chosen that produce overlapping degrees of responsiveness in a given behavioral task. For this purpose, we assessed concentration–response functions using a brief-access taste test and then chose concentrations from the
Experiment 2
The curves obtained in Experiment 1 show the unconditioned licking responses to each taste compound tested. As expected, licking of NaCl, quinine, and citric acid decreased as a monotonic function of concentration. Conversely, as the sucrose concentration was increased, the unconditioned licking response increased in a monotonic fashion. The range of concentration-dependent licking observed allowed us to select concentrations for the discrimination task described below that produced overlapping
Experiment 3
In Experiment 2 rats competently performed a task in which they were required to discriminate one prototypical taste compound, thought to be representative of one of the putative four basic taste qualities, from the other three prototypical taste compounds. Furthermore, an analysis of the untrained responses of the animals to novel concentrations or mixtures of some of the training compounds led to generalization profiles that could be considered as indicators of how NaCl-like, sucrose-like,
General discussion
The results of these experiments demonstrate that rats are quite competent at discriminating between sucrose, NaCl, citric acid, and quinine supporting the view that these compounds are representative of independent perceptual taste qualities that humans refer to as — salty, sweet, sour, and bitter. Importantly, rats behaviorally generalized novel concentrations of these 4 compounds to their respective standards. This latter outcome shows that the rats were not learning specific responses to
Acknowledgements
This research was supported by Grants R01-DC01628 [ACS] and F31-DC007301 [CLG] from the National Institute on Deafness and Other Communication Disorders. Portions of this work were presented at the annual meeting of the Association for Chemoreception Sciences in Sarasota, Florida, April 2006, and the Society for the Study of Ingestive Behavior, Steamboat Springs, CO, July 2007, and were in partial fulfillment of the requirements of Doctor of Philosophy at the University of Florida. We wish to
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Now at the Department of Psychology, University of Iowa, Iowa City, IA 52242, USA.
- 2
Now at the Department of Psychology and Program in Neuroscience, The Florida State University, Tallahassee, FL, 32306, USA.