Linking peripheral taste processes to behavior

https://doi.org/10.1016/j.conb.2009.07.014Get rights and content

The act of eating and drinking brings food-related chemicals into contact with taste cells. Activation of these taste cells, in turn, engages neural circuits in the central nervous system that help animals identify foods and fluids, determine what and how much to eat, and prepare the body for digestion and assimilation. Analytically speaking, these neural processes can be divided into at least three categories: stimulus identification, ingestive motivation, and digestive preparation. This review will discuss recent advances in peripheral gustatory mechanisms, primarily from rodent models, in the context of these three major categories of taste function.

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)

  • A. Sclafani et al.

    CD36 gene deletion reduces fat preference and intake but not post-oral fat conditioning in mice

    Am J Physiol Regul Integr Comp Physiol

    (2007)
  • S. Zukerman et al.

    T1R3 taste receptor is critical for sucrose but not Polycose taste

    Am J Physiol Regul Integr Comp Physiol

    (2009)
  • J.I. Glendinning et al.

    Contribution of orosensory stimulation to strain differences in oil intake by mice

    Physiol Behav

    (2008)
  • A. Sclafani et al.

    Fat and carbohydrate preferences in mice: the contribution of alpha-gustducin and Trpm5 taste-signaling proteins

    Am J Physiol Regul Integr Comp Physiol

    (2007)
  • R.D. Mattes

    Brief oral stimulation, but especially oral fat exposure, elevates serum triglycerides in humans

    Am J Physiol Gastrointest Liver Physiol

    (2009)
  • S.R. Crystal et al.

    Tasting fat: cephalic phase hormonal responses and food intake in restrained and unrestrained eaters

    Physiol Behav

    (2006)
  • G.I. Heck et al.

    Salt taste transduction occurs through an amiloride-sensitive sodium transport pathway

    Science

    (1984)
  • A. Vandenbeuch et al.

    Amiloride-sensitive channels in type I fungiform taste cells in mouse

    BMC Neurosci

    (2008)
  • R. Yoshida et al.

    NaCl responsive taste cells in the mouse fungiform taste buds

    Neuroscience

    (2009)
  • Y. Ninomiya et al.

    Amiloride inhibition of responses of rat single chorda tympani fibers to chemical and electrical tongue stimulations

    Brain Res

    (1988)
  • R.F. Lundy et al.

    Gustatory neuron types in rat geniculate ganglion

    J Neurophysiol

    (1999)
  • A.C. Spector et al.

    Amiloride disrupts NaCl versus KCl discrimination performance: implications for salt taste coding in rats

    J Neurosci

    (1996)
  • I.L. Bernstein et al.

    Amiloride-sensitive sodium channels and expression of sodium appetite in rats

    Am J Physiol Regul Integr Comp Physiol

    (1987)
  • A.C. Spector et al.

    The representation of taste quality in the mammalian nervous system

    Behav Cogn Neurosci Rev

    (2005)
  • V. Lyall et al.

    The mammalian amiloride-insensitive non-specific salt taste receptor is a vanilloid receptor-1 variant

    J Physiol

    (2004)
  • Y. Treesukosol et al.

    A psychophysical and electrophysiological analysis of salt taste in Trpv1 null mice

    Am J Physiol Regul Integr Comp Physiol

    (2007)
  • C. Ruiz et al.

    Detection of NaCl and KCl in TRPV1 knockout mice

    Chem Senses

    (2006)
  • G.Q. Zhao et al.

    The receptors for mammalian sweet and umami taste

    Cell

    (2003)
  • S. Damak et al.

    Detection of sweet and umami taste in the absence of taste receptor T1r3

    Science

    (2003)
  • J. Chandrashekar et al.

    The receptors and cells for mammalian taste

    Nature

    (2006)
  • Y. Nie et al.

    Distinct contributions of T1R2 and T1R3 taste receptor subunits to the detection of sweet stimuli

    Curr Biol

    (2005)
  • T. Ohkuri et al.

    Multiple sweet receptors and transduction pathways revealed in knockout mice by temperature dependence and gurmarin sensitivity

    Am J Physiol Regul Integr Comp Physiol

    (2009)
  • C.D. Dotson et al.

    Behavioral discrimination between sucrose and other natural sweeteners in mice: implications for the neural coding of T1R ligands

    J Neurosci

    (2007)
  • G. Nelson et al.

    Mammalian sweet taste receptors

    Cell

    (2001)
  • Cited by (84)

    • Y1 receptors modulate taste-related behavioral responsiveness in male mice to prototypical gustatory stimuli

      2021, Hormones and Behavior
      Citation 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.

    • 3.09 - Microphysiology of Taste Buds

      2020, The Senses: A Comprehensive Reference: Volume 1-7, Second Edition
    View all citing articles on Scopus
    View full text