Coding in the mammalian gustatory system

Trends in Neurosciences

Volumn 33, Issue 7, 2010, Pages 326-334

  Carleton, Alan ^a   Accolla, Riccardo ^b   Simon, Sidney A ^c  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b Analysis and Perception Department   (Switzerland)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN STEM; FRONTAL CORTEX; GUSTATORY SYSTEM; NONHUMAN; PRIORITY JOURNAL; REVIEW; STATE DEPENDENT LEARNING; TASTE; TASTE BUD; ANATOMY AND HISTOLOGY; ANIMAL; BRAIN CORTEX; CYTOLOGY; INNERVATION; NERVE CELL; PHYSIOLOGY; SOLITARY TRACT NUCLEUS; STIMULATION; THALAMUS; TONGUE;

ANIMALS; BRAIN STEM; CEREBRAL CORTEX; NEURONS; SOLITARY NUCLEUS; STIMULATION, CHEMICAL; TASTE; TASTE BUDS; TASTE PERCEPTION; THALAMUS; TONGUE;

EID: 77954385728     PISSN: 01662236     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tins.2010.04.002     Document Type: Review

References (98)

1. Dalton P., et al. The merging of the senses: integration of subthreshold taste and smell. Nat. Neurosci. 2000, 3:431-432.
2. Gottfried J.A., Dolan R.J. The nose smells what the eye sees: crossmodal visual facilitation of human olfactory perception. Neuron 2003, 39:375-386.
3. Zaidi F.N., et al. Types of taste circuits synaptically linked to a few geniculate ganglion neurons. J. Comp. Neurol. 2008, 511:753-772.
4. Spector A.C., Travers S.P. The representation of taste quality in the mammalian nervous system. Behav. Cogn. Neurosci. Rev. 2005, 4:143-191.
5. Tokita K., et al. Afferent connections of the parabrachial nucleus in C57BL/6J mice. Neuroscience 2009, 161:475-488.
6. Ongur D., Price J.L. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb. Cortex 2000, 10:206-219.
7. Smith D.V., St John S.J. Neural coding of gustatory information. Curr. Opin. Neurobiol. 1999, 9:427-435.
8. Kinnamon J.C., Yang R. Ultrastructure of taste buds. The Senses: A Comprehensive Reference 2008, 135-156. Academic Press. S. Firestein, G.K. Beauchamp (Eds.).
9. Finger T.E. Cell types and lineages in taste buds. Chem. Senses 2005, 30(Suppl 1):i54-55.
10. Okubo T., et al. Cell lineage mapping of taste bud cells and keratinocytes in the mouse tongue and soft palate. Stem Cells 2009, 27:442-450.
11. Shigemura N., 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, 294:R66-75.
12. Vandenbeuch A., et al. Amiloride-sensitive channels in type I fungiform taste cells in mouse. BMC Neurosci. 2008, 9:1.
13. Chandrashekar J., et al. The cells and peripheral representation of sodium taste in mice. Nature 2010, 464:297-301.
14. Chandrashekar J., et al. The receptors and cells for mammalian taste. Nature 2006, 444:288-294.
15. Perez C.A., et al. A transient receptor potential channel expressed in taste receptor cells. Nat. Neurosci. 2002, 5:1169-1176.
16. Huang A.L., et al. The cells and logic for mammalian sour taste detection. Nature 2006, 442:934-938.
17. Chandrashekar J., et al. The taste of carbonation. Science 2009, 326:443-445.
18. Lyall V., et al. Decrease in rat taste receptor cell intracellular pH is the proximate stimulus in sour taste transduction. Am. J. Physiol. Cell Physiol. 2001, 281:C1005-1013.
19. Chen X., et al. Capsaicin and carbon dioxide act by distinct mechanisms on sensory nerve terminals in the cat cornea. Pain 1997, 70:23-29.
20. Yarmolinsky D.A., et al. Common sense about taste: from mammals to insects. Cell 2009, 139:234-244.
21. Mueller K.L., et al. The receptors and coding logic for bitter taste. Nature 2005, 434:225-229.
22. Zhao G.Q., et al. The receptors for mammalian sweet and umami taste. Cell 2003, 115:255-266.
23. Gilbertson T.A., et al. Distribution of gustatory sensitivities in rat taste cells: whole-cell responses to apical chemical stimulation. J. Neurosci. 2001, 21:4931-4941.
24. Riera C.E., et al. Sensory attributes of complex tasting divalent salts are mediated by TRPM5 and TRPV1 channels. J. Neurosci. 2009, 29:2654-2662.
25. Watson K.J., et al. Expression of aquaporin water channels in rat taste buds. Chem. Senses 2007, 32:411-421.
26. Cameron P., et al. The molecular basis for water taste in Drosophila. Nature 2010, 465:91-95.
27. Gaillard D., et al. The gustatory pathway is involved in CD36-mediated orosensory perception of long-chain fatty acids in the mouse. FASEB J. 2008, 22:1458-1468.
28. Oliveira-Maia A.J., et al. Nicotine activates TRPM5-dependent and independent taste pathways. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:1596-1601.
29. Lyall V., et al. The mammalian amiloride-insensitive non-specific salt taste receptor is a vanilloid receptor-1 variant. J. Physiol. 2004, 558:147-159.
30. Clapp T.R., et al. Mouse taste cells with G protein-coupled taste receptors lack voltage-gated calcium channels and SNAP-25. BMC Biol. 2006, 4:7.
31. Roper S.D. Parallel processing in mammalian taste buds?. Physiol. Behav. 2009, 97:604-608.
32. Huang Y.J., et al. The role of pannexin 1 hemichannels in ATP release and cell-cell communication in mouse taste buds. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:6436-6441.
33. Romanov R.A., et al. Voltage dependence of ATP secretion in mammalian taste cells. J. Gen. Physiol. 2008, 132:731-744.
34. Finger T.E., et al. ATP signaling is crucial for communication from taste buds to gustatory nerves. Science 2005, 310:1495-1499.
35. Huang Y.J., et al. Mouse taste buds use serotonin as a neurotransmitter. J. Neurosci. 2005, 25:843-847.
36. Ohtubo Y., et al. Optical recordings of taste responses from fungiform papillae of mouse in situ. J. Physiol. 2001, 530:287-293.
37. Tomchik S.M., et al. Breadth of tuning and taste coding in mammalian taste buds. J. Neurosci. 2007, 27:10840-10848.
38. Huang Y.A., et al. Presynaptic (type III) cells in mouse taste buds sense sour (acid) taste. J. Physiol. 2008, 586:2903-2912.
39. Kawai K., et al. Leptin as a modulator of sweet taste sensitivities in mice. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:11044-11049.
40. Yoshida R., et al. Endocannabinoids selectively enhance sweet taste. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:935-939.
41. Seta Y., et al. Expression of galanin and the galanin receptor in rat taste buds. Arch. Histol. Cytol. 2006, 69:273-280.
42. Shin Y.K., et al. Modulation of taste sensitivity by GLP-1 signaling. J. Neurochem. 2008, 106:455-463.
43. Zhao F.L., et al. Expression, physiological action, and coexpression patterns of neuropeptide Y in rat taste-bud cells. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:11100-11105.
44. Berthoud H.R., Morrison C. The brain, appetite, and obesity. Annu. Rev. Psychol. 2008, 59:55-92.
45. Cao Y., et al. GABA expression in the mammalian taste bud functions as a route of inhibitory cell-to-cell communication. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:4006-4011.
46. Tsurugizawa T., et al. Effects of isoflurane and alpha-chloralose anesthesia on BOLD fMRI responses to ingested L-glutamate in rats. Neuroscience 2010, 165:244-251.
47. Bender G., et al. Neural correlates of evaluative compared with passive tasting. Eur. J. Neurosci. 2009, 30:327-338.
48. Fairhall S.L., Macaluso E. Spatial attention can modulate audiovisual integration at multiple cortical and subcortical sites. Eur. J. Neurosci. 2009, 29:1247-1257.
49. Krupa D.J., et al. Layer-specific somatosensory cortical activation during active tactile discrimination. Science 2004, 304:1989-1992.
50. Lemon C.H., Smith D.V. Neural representation of bitter taste in the nucleus of the solitary tract. J. Neurophysiol. 2005, 94:3719-3729.
51. Geran L.C., Travers S.P. Single neurons in the nucleus of the solitary tract respond selectively to bitter taste stimuli. J. Neurophysiol. 2006, 96:2513-2527.
52. Geran L.C., Travers S.P. Bitter-responsive gustatory neurons in the rat parabrachial nucleus. J. Neurophysiol. 2009, 101:1598-1612.
53. Travers S.P., Geran L.C. Bitter-responsive brainstem neurons: characteristics and functions. Physiol. Behav. 2009, 97:592-603.
54. Verhagen J.V., et al. Responses to taste stimulation in the ventroposteromedial nucleus of the thalamus in rats. J. Neurophysiol. 2003, 89:265-275.
55. Boucher Y., et al. Trigeminal modulation of gustatory neurons in the nucleus of the solitary tract. Brain Res. 2003, 973:265-274.
56. Di Lorenzo P.M. The neural code for taste in the brain stem: response profiles. Physiol. Behav. 2000, 69:87-96.
57. Smith D.V., et al. Medullary taste responses are modulated by the bed nucleus of the stria terminalis. Chem. Senses 2005, 30:421-434.
58. Zhu M., et al. Activation of delta-opioid receptors reduces excitatory input to putative gustatory cells within the nucleus of the solitary tract. J. Neurophysiol. 2009, 101:258-268.
59. Di Lorenzo P.M., et al. Temporal coding of sensation: mimicking taste quality with electrical stimulation of the brain. Behav. Neurosci. 2003, 117:1423-1433.
60. Di Lorenzo P.M., et al. Dynamic coding of taste stimuli in the brainstem: effects of brief pulses of taste stimuli on subsequent taste responses. J. Neurosci. 2003, 23:8893-8902.
61. Di Lorenzo P.M., et al. Quality time: representation of a multidimensional sensory domain through temporal coding. J. Neurosci. 2009, 29:9227-9238.
62. Gutierrez R., et al. Spike timing precision of licking-synchronized neurons in the taste-reward circuit is enhanced upon lerning. J. Neurosci. 2010, 30:287-303.
63. Hallock R.M., Di Lorenzo P.M. Temporal coding in the gustatory system. Neurosci. Biobehav. Rev. 2006, 30:1145-1160.
64. Roussin A.T., et al. Variability in responses and temporal coding of tastants of similar quality in the nucleus of the solitary tract of the rat. J. Neurophysiol. 2008, 99:644-655.
65. Hanamori T., et al. Responses of neurons in the insular cortex to gustatory, visceral, and nociceptive stimuli in rats. J. Neurophysiol. 1998, 79:2535-2545.
66. Kadohisa M., et al. Neuronal representations of stimuli in the mouth: the primate insular taste cortex, orbitofrontal cortex and amygdala. Chem. Senses 2005, 30:401-419.
67. Yamamoto T., et al. Gustatory responses of cortical neurons in rats. I. Response characteristics. J. Neurophysiol. 1984, 51:616-635.
68. Katz D.B., et al. Dynamic and multimodal responses of gustatory cortical neurons in awake rats. J. Neurosci. 2001, 21:4478-4489.
69. Miller P., Katz D.B. Stochastic transitions between neural states in taste processing and decision-making. J. Neurosci. 2010, 30:2559-2570.
70. Halpern B.P. Constraints imposed on taste physiology by human taste reaction time data. Neurosci. Biobehav. Rev. 1986, 10:135-151.
71. Jones L.M., et al. Natural stimuli evoke dynamic sequences of states in sensory cortical ensembles. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:18772-18777.
72. Stapleton J.R., et al. Ensembles of gustatory cortical neurons anticipate and discriminate between tastants in a single lick. Front. Neurosci. 2007, 1:161-174.
73. Stapleton J.R., et al. Rapid taste responses in the gustatory cortex during licking. J. Neurosci. 2006, 26:4126-4138.
74. Accolla R., et al. Differential spatial representation of taste modalities in the rat gustatory cortex. J. Neurosci. 2007, 27:1396-1404.
75. Accolla R., Carleton A. Internal body state influences topographical plasticity of sensory representations in the rat gustatory cortex. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:4010-4015.
76. Schoenfeld M.A., et al. Functional magnetic resonance tomography correlates of taste perception in the human primary taste cortex. Neuroscience 2004, 127:347-353.
77. Katz D.B., et al. Gustatory processing is dynamic and distributed. Curr. Opin. Neurobiol. 2002, 12:448-454.
78. Nitschke J.B., et al. Altering expectancy dampens neural response to aversive taste in primary taste cortex. Nat. Neurosci. 2006, 9:435-442.
79. Small D.M., et al. Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron 2003, 39:701-711.
80. Grinvald A., Hildesheim R. VSDI: a new era in functional imaging of cortical dynamics. Nat. Rev. Neurosci. 2004, 5:874-885.
81. Grossman S.E., et al. Learning-related plasticity of temporal coding in simultaneously recorded amygdala-cortical ensembles. J. Neurosci. 2008, 28:2864-2873.
82. Yasoshima Y., Yamamoto T. Short-term and long-term excitability changes of the insular cortical neurons after the acquisition of taste aversion learning in behaving rats. Neuroscience 1998, 84:1-5.
83. Lara A.H., et al. Encoding of gustatory working memory by orbitofrontal neurons. J. Neurosci. 2009, 29:765-774.
84. Rolls E.T., Grabenhorst F. The orbitofrontal cortex and beyond: from affect to decision-making. Prog. Neurobiol. 2008, 86:216-244.
85. Rolls E.T., et al. Sensory-specific and motivation-specific satiety for the sight and taste of food and water in man. Physiol. Behav. 1983, 30:185-192.
86. Rolls E.T., et al. Hunger modulates the responses to gustatory stimuli of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. Eur. J. Neurosci. 1989, 1:53-60.
87. de Araujo I.E., et al. Human cortical responses to water in the mouth, and the effects of thirst. J. Neurophysiol. 2003, 90:1865-1876.
88. Wan S., et al. Presynaptic melanocortin-4 receptors on vagal afferent fibers modulate the excitability of rat nucleus tractus Solitarius neurons. J. Neurosci. 2008, 28:4957-4966.
89. de Araujo I.E., et al. Neural ensemble coding of satiety states. Neuron 2006, 51:483-494.
90. Watanabe M., et al. Behavioral reactions reflecting differential reward expectations in monkeys. Exp. Brain Res. 2001, 140:511-518.
91. Ogawa H., et al. Multiple sensitivity of chordat typani fibres of the rat and hamster to gustatory and thermal stimuli. J. Physiol. 1968, 199:223-240.
92. Harada S., Smith D.V. Gustatory sensitivities of the hamster's soft palate. Chem. Senses 1992, 17:37-51.
93. Garcia J., et al. Conditioned aversion to saccharin resulting from exposure to gamma radiation. Science 1955, 122:157-158.
94. Bathellier B., et al. Dynamic ensemble odor coding in the mammalian olfactory bulb: sensory information at different timescales. Neuron 2008, 57:586-598.
95. Erickson R.P. The evolution of neural coding ideas in the chemical senses. Physiol. Behav. 2000, 69:3-13.
96. Grinvald A., et al. In vivo optical imaging cortical architecture and dynamics. Modern Techniques in Neuroscience Research 1999, 893-969. Springer Verlag. U. Windhorst, H. Johansson (Eds.).
97. Frostig R.D., et al. Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:6082-6086.
98. Bathellier B., et al. Wavelet-based multi-resolution statistics for optical imaging signals: application to automated detection of odour activated glomeruli in the mouse olfactory bulb. Neuroimage 2007, 34:1020-1035.