Linking peripheral taste processes to behavior
Introduction
Our understanding of peripheral gustatory mechanisms continues to advance at a rapid pace. Ultimately, these neurobiological processes must be linked to behavioral outcomes. At times, such efforts have produced seemingly paradoxical results; for example, knocking out a taste receptor caused severe impairments in one behavioral task but not in another. To explain these apparent disparities, it is important to realize that there are at least three categories of taste processing [1]. Stimulus identification is the detection or discrimination of sensory signals arising from taste cell activation. Ingestive motivation involves processes that promote or discourage ingestion. Digestive preparation refers to feed-forward physiological reflexes that protect oral tissues, aid digestion, and facilitate homeostasis. It must also be recognized that behavioral responses to taste stimuli can be influenced by nongustatory factors, including olfactory, somatosensory, and visceral signals. We propose that integrating these perspectives into studies of taste function will help establish more logical links between neural processes and taste-related behavior.
Section snippets
Stimulus identification
Stimulus identification refers to the ability of animals to discriminate between the gustatory signals generated by different taste stimuli. Such processes allow animals to learn about foods by associating particular tastes with other stimuli and/or outcomes, ultimately facilitating survival. In humans, stimulus identification can be assessed through verbal qualitative descriptors such as ‘sweet,’ ‘sour,’ ‘salty,’ ‘bitter’ and ‘umami.’ In nonverbal animals, more objective approaches, such as
Ingestive motivation
The motivational function of taste has been referred to as affect, hedonics, palatability, and reward. All of these processes share the same fundamental property of facilitating or inhibiting ingestion. It is important to recognize that two taste compounds can be equally preferred or avoided but have distinct taste qualities. For instance, even though rats avoid high concentrations of quinine and NaCl, they can nevertheless discriminate the tastes of these stimuli.
Digestive preparation
A third function of gustatory input is the activation of physiological reflexes that produce effects like delaying gastric emptying, protecting the oral cavity, facilitating digestion, and maintaining homeostasis. These are commonly referred to as cephalic-phase reflexes because they are triggered by the stimulation of head receptors. For instance, a recent study documented that bitter taste alone can delay gastric emptying in human subjects [54•]. This could have adaptive value in that it
Conclusion
The three categories of taste function discussed here must have dissociable neural substrates at some level in the gustatory neuraxis (Figure 1) [61]. Although these substrates have yet to be clearly delineated, there are hints in the literature. For example, in rats, stimulus identification relies on input from the gustatory branches of the facial nerve, whereas taste signals carried by the glossopharyngeal nerve appear unnecessary to support this function [see [62, 63]]. Neurons in the
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
We would like to thank Clare Mathes and Yada Treesukosol for providing feedback on the article. ACS would also like to acknowledge research support from the National Institute on Deafness and Other Communication Disorders (R01-DC-004574).
References (68)
Linking gustatory neurobiology to behavior in vertebrates
Neurosci Biobehav Rev
(2000)- et al.
Inhibition by amiloride of chorda tympani responses evoked by monovalent salts
Brain Res
(1985) - et al.
Amiloride-sensitive sodium channels in taste
Curr Top Membr
(1999) - et al.
Amiloride-sensitive NaCl taste responses are associated with genetic variation of ENaC alpha-subunit in mice
Am J Physiol Regul Integr Comp Physiol
(2008) - et al.
Specificity of amiloride inhibition of hamster taste responses
Brain Res
(1990) - et al.
Anion size does not compromise sodium recognition by rats after acute sodium depletion
Behav Neurosci
(2004) - et al.
Sucrose and monosodium glutamate taste thresholds and discrimination ability of T1R3 knockout mice
Chem Senses
(2006) - et al.
Human receptors for sweet and umami taste
Proc Natl Acad Sci U S A
(2002) - et al.
The receptors and coding logic for bitter taste
Nature
(2005) - et al.
Rats fail to discriminate quinine from denatonium: implications for the neural coding of bitter-tasting compounds
J Neurosci
(2002)
CD36 gene deletion reduces fat preference and intake but not post-oral fat conditioning in mice
Am J Physiol Regul Integr Comp Physiol
T1R3 taste receptor is critical for sucrose but not Polycose taste
Am J Physiol Regul Integr Comp Physiol
Contribution of orosensory stimulation to strain differences in oil intake by mice
Physiol Behav
Fat and carbohydrate preferences in mice: the contribution of alpha-gustducin and Trpm5 taste-signaling proteins
Am J Physiol Regul Integr Comp Physiol
Brief oral stimulation, but especially oral fat exposure, elevates serum triglycerides in humans
Am J Physiol Gastrointest Liver Physiol
Tasting fat: cephalic phase hormonal responses and food intake in restrained and unrestrained eaters
Physiol Behav
Salt taste transduction occurs through an amiloride-sensitive sodium transport pathway
Science
Amiloride-sensitive channels in type I fungiform taste cells in mouse
BMC Neurosci
NaCl responsive taste cells in the mouse fungiform taste buds
Neuroscience
Amiloride inhibition of responses of rat single chorda tympani fibers to chemical and electrical tongue stimulations
Brain Res
Gustatory neuron types in rat geniculate ganglion
J Neurophysiol
Amiloride disrupts NaCl versus KCl discrimination performance: implications for salt taste coding in rats
J Neurosci
Amiloride-sensitive sodium channels and expression of sodium appetite in rats
Am J Physiol Regul Integr Comp Physiol
The representation of taste quality in the mammalian nervous system
Behav Cogn Neurosci Rev
The mammalian amiloride-insensitive non-specific salt taste receptor is a vanilloid receptor-1 variant
J Physiol
A psychophysical and electrophysiological analysis of salt taste in Trpv1 null mice
Am J Physiol Regul Integr Comp Physiol
Detection of NaCl and KCl in TRPV1 knockout mice
Chem Senses
The receptors for mammalian sweet and umami taste
Cell
Detection of sweet and umami taste in the absence of taste receptor T1r3
Science
The receptors and cells for mammalian taste
Nature
Distinct contributions of T1R2 and T1R3 taste receptor subunits to the detection of sweet stimuli
Curr Biol
Multiple sweet receptors and transduction pathways revealed in knockout mice by temperature dependence and gurmarin sensitivity
Am J Physiol Regul Integr Comp Physiol
Behavioral discrimination between sucrose and other natural sweeteners in mice: implications for the neural coding of T1R ligands
J Neurosci
Mammalian sweet taste receptors
Cell
Cited by (84)
Oral glucose sensing in cephalic phase insulin release
2023, AppetiteEarly-life influences of low-calorie sweetener consumption on sugar taste
2023, Physiology and BehaviorY1 receptors modulate taste-related behavioral responsiveness in male mice to prototypical gustatory stimuli
2021, Hormones and BehaviorCitation Excerpt :For example, the experiments suggesting that Y1R activation leads to TRC hyperpolarization was done using CV taste buds. The response properties of TRCs from different papillae often differ substantially (e.g., Dana and McCaughey, 2015; Kim et al., 2003; Shingai and Beidler, 1985) and may contribute differentially to the functional aspects of taste (e.g., sensory discriminative vs. affective functioning; Spector, 2003 for a review; Spector and Glendinning, 2009). Consequently, the influence of a given molecular manipulation on taste-related behavior, which results from the processing of sensory input by the entirety of the gustatory system, may not be easily predicted by observing the output of individual TRCs.
The fungiform papilla is a complex, multimodal, oral sensory organ
2021, Current Opinion in Physiology3.09 - Microphysiology of Taste Buds
2020, The Senses: A Comprehensive Reference: Volume 1-7, Second Edition