Neural coding of gustatory information

Current Opinion in Neurobiology

Volumn 9, Issue 4, 1999, Pages 427-435

  Smith, David V ^a   St John, Steven J ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMILORIDE;

BRAIN; GUSTATORY NERVOUS SYSTEM; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SENSORY NERVE CONDUCTION; SENSORY RECEPTOR; SIGNAL TRANSDUCTION; STIMULUS; TASTE; TEMPERATURE; TOUCH;

EID: 0033178521     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(99)80064-6     Document Type: Article

References (70)

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27. 27. Gilbertson TA, Fontenot DT: Distribution of amiloride-sensitive sodium channels in the oral cavity of the hamster. Chem Senses 1998, 23:495-499. Patch-clamp recording of isolated taste buds from different regions of the hamster oral cavity demonstrated that cells from fungiform, foliate and vallate papillae, and the soft palate all contain functional amiloride-sensitive sodium channels.
28. 28. Kretz O, Barbry P, Bock R, Lindemann B: Differential expression of RNA and protein of the three pore-forming subunits of the amiloride-sensitive epithelial sodium channel in taste buds of the rat. J Histochem Cytochem 1999, 47:51-64. Using both immunohistochemistry and in situ hybridization, these investigators demonstrated that the α-subunit of the amiloride-sensitive epithelial sodium channel (ENaC) is present in taste buds of both the anterior and posterior tongue of the rat, but that the β- and γ-subunits are much less prevalent. Given that all three subunits are necessary for channel function, these data support the electrophysiological findings that the posterior tongue of the rat does not have an amiloride-blockable sodium response [30•,31].
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30. +.
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45. 45. Danilova V, Hellekant G, Tinti JM, Nofre C: Gustatory responses of the hamster mesocricetus auratus to various compounds considered sweet by humans. J Neurophysiol 1998, 80:2102-2112. This paper describes the results of electrophysiological recordings from single hamster CT nerve fibers to a wide range of sweet-tasting stimuli and compares these responses to the results of two-bottle preference tests and conditioned taste aversion generalization tests for the same stimuli. Many stimuli that are sweet to humans (11 out of 26) appear to be tasteless to hamsters or to taste different than sucrose. The authors argue that activity in sucrose-best fibers elicits 'liking' and activity in quinine-or HCl-best fibers elicits 'rejection'.
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48. 48. Giza BK, Scott TR: Intravenous insulin infusions in rats decrease gustatory-evoked responses to sugars. Am J Physiol 1987, 252:R994-R1002.
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50. 50. Bradley RM, Grabauskas G: Neural circuits for taste: excitation, inhibition, and synaptic plasticity in the rostral gustatory zone of the nucleus of the solitary tract. In Olfaction and Taste XII: An International Symposium. Edited by Murphy C. New York: New York Academy of Sciences; 1998:467-474. This paper summarizes the results of several studies on in vitro brain slices through the NST of the rat. These studies show that the neurotransmitter between peripheral fibers and NST cells is glutamate (mediated by ionotropic receptors), that the cells are inhibited by GABA, and that the activity in NST cells is a complex sum of excitatory and inhibitory postsynaptic potentials. Further, if inhibitory postsynaptic potentials are initiated by tetanic stimulation, they undergo both short- and long-term changes, demonstrating synaptic plasticity at the first central gustatory relay.
51. 51. Smith DV, Li C-S, Davis BJ: Excitatory and inhibitory modulation of taste responses in the hamster brainstem. In Olfaction and Taste XII: An International Symposium. Edited by Murphy C. New York: New York Academy of Sciences; 1998:450-456. Extracellular recording from neurons in the hamster NST shows that taste-evoked activity in these cells is blocked by glutamate antagonists, inhibited by GABA, and excited by substance P. NST cells are maintained under tonic GABAergic inhibition and are further inhibited via descending connections from gustatory cortex. These in vivo experiments confirm that taste-elicited activity is modulated by these neurotransmitter systems, all of which have been shown to operate in vitro [50•] in the gustatory portion of the NST.
52. A antagonist, bicuculline, in a dose-dependent manner. One of the roles of GABA in the gustatory system is to sharpen the breadth of tuning of cells to taste stimulation. Microinjection of bicuculline resulted in a significant increase in the breadth of responsiveness of cells sensitive to GABAergic modulation.
53. 53. Kobashi M, Bradley RM: Effects of GABA on neurons of the gustatory and visceral zones of the parabrachial nucleus in rats. Brain Res 1998, 799:323-328. Patch recordings from cells in slices through the rat parabrachial nuclei (PbN) demonstrated that about two thirds of the cells in both the gustatory and visceral portions of this nuclear complex are inhibited by GABA. These data show that the modulatory effects of GABA, which were evident in the medulla [50•,51•,52••], also operate at the next synaptic relay in this system.
54. 54. Ogawa H, Hasegawa K, Otawa S, Ikeda I: GABAergic inhibition and modifications of taste responses in the cortical taste area in rats. Neurosci Res 1998, 32:85-95. In vivo recording from the cortical taste area of rats demonstrated that these cells, like those at lower relay nuclei in the gustatory system [50•,51•,52••,53•], are modulated by GABA. Further, GABA inhibited the responses of 58% of taste-responsive cells, and bicuculline increased the discharge in about 69% of these cells. The response profiles and receptive fields of these cortical neurons were altered by GABAergic modulation.
55. 55. Yanagisawa K, Bartoshuk LM, Catalanotto FA, Karrer TA, Kveton JF: Anesthesia of the chorda tympani nerve and taste phantoms. Physiol Behav 1998, 63:329-335. Anesthesia of the chorda tympani nerves in humans results in an increase in the perceived intensity of quinine applied to the back of the tongue. Forty percent of subjects reported taste phantoms located on the posterior tongue as well. The authors suggest that these effects could be mediated by a release of inhibition between the VIIth and IXth cranial nerves.
56. 56. St John SJ, Garcea M, Spector AC: Combined, but not single, gustatory nerve transection substantially alters taste-guided behavior to quinine in rats. Behav Neurosci 1994, 108:131-140.
57. 57. St John SJ, Spector AC: Combined glossopharyngeal and chorda tympani nerve transection elevates quinine detection thresholds in rats (Rattus norvegicus). Behav Neurosci 1996, 110:1456-1468.
58. 58. St John SJ, Spector AC: Behavioral discrimination between quinine and KCl is dependent on input from the seventh cranial nerve: implications for the functional roles of the gustatory nerves in rats. J Neurosci 1998, 18:4353-4362. The ability of rats to behaviorally discriminate quinine from KCl (at various concentrations) was tested before and after gustatory nerve cuts. Total impairment was seen only after combined transection of the glossopharyngeal, chorda tympani, and greater superficial petrosal nerves, but combined greater superficial petrosal and chorda tympani transection caused near total impairments. Glossopharyngeal transection alone was without effect, whereas chorda tympani transection alone caused significant deficits. On the basis of this and other nerve cut studies, the authors concluded that the IXth nerve does not play a substantial role in allowing rats to make qualitative discriminations, an ability that appears to rely heavily on input from the VIIth nerve.
59. 59. Dinkens ME, Travers SP: Effects of chorda tympani nerve anesthesia on taste responses in the NST. Chem Senses 1998, 23:661-673. Unlike psychophysical reports in humans [55•], anesthesia of the chorda tympani nerve did not result in increased responsiveness to taste stimuli applied to the posterior tongue of the rat when cells in the NST were recorded. However, a subset of cells responsive to palatal stimulation did increase responsiveness during chorda tympani anesthesia. These results corroborate and extend earlier findings in rats of convergence in the brainstem of anterior tongue and palatal taste inputs.
60. 60. Frank ME: Taste-responsive neurons of the glossopharyngeal nerve of the rat. J Neurophysiol 1991, 65:1452-1463.
61. 61. Spector AC, St John SJ: Role of taste in the microstructure of quinine ingestion by rats. Am J Physiol 1998, 274:R1687-R1703. The authors examined the role of taste in ingestion of quinine by water-deprived rats. Quinine (relative to water) caused a decrease in 45 min, single-bottle intake by virtue of reducing the size of 'bursts' of licking and the volume of fluid ingested per lick. Surprisingly, the number of bursts increased when quinine was the stimulus. Transection of the chorda tympani and glossopharyngeal nerves (and to a lesser but significant extent, transection of the glossopharyngeal nerve alone) opposed the effects of quinine. The authors concluded that the aversive taste of quinine acts on processes that control the termination of a burst of licking, whereas taste appeared to contribute less to processes involved in the initiation of licking.
62. 62. Markison S, St John SJ, Spector AC: Glossopharyngeal nerve transection reduces quinine avoidance in rats not given presurgical stimulus exposure. Physiol Behav 1999, 65:773-778. The concentration-dependent unconditioned avoidance of quinine was assessed in rats with and without bilateral glossopharyngeal nerve transection using brief access trials. In contrast to a previous study that used a within-subjects design [56], IXth nerve transection produced a small but significant decrease in quinine avoidance. Thus, the IXth nerve appears to play some role in quinine avoidance, but the authors argue that pre-exposure to quinine (as in a before-after, within-subjects design) may mask effects of nerve transection in this task.
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65. 65. 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. Taste-responsive neurons of the rat gustatory cortex were examined before, during, and after the formation of a LiCl-induced taste aversion to saccharin. Of 14 taste-responsive neurons, all showed an enhanced response to saccharin after conditioned taste aversion. Of these, the enhancement persisted for the duration of the experiment in six neurons (i.e. 4-6 h after LiCl injection). Enhancement was lost 30-60 min after conditioning in the other eight neurons.
66. 66. Nishijo H, Uwano T, Tamura R, Ono T: Gustatory and multimodal neuronal responses in the amygdala during licking and discrimination of sensory stimuli in awake rats. J Neurophysiol 1998, 79:21-36. Detailed analyses of 84 oral sensory neurons in the amygdala of awake rats are presented. Taste stimuli were infused intraorally during positive and negative reinforcement conditioning paradigms. In contrast to recordings in other parts of the gustatory system, quinine evoked greater responses than NaCl, citric acid, or sucrose at commonly used stimulus intensities. The data suggested that the amygdala represents stimuli along payability lines, rather than on the basis of taste quality.
67. 67. Reilly S: The role of the gustatory thalamus in taste-guided behavior. Neurosci Biobehav Rev 1998, 22:883-901. In this review, the author notes that the literature on the gustatory thalamus is replete with contradictions: whereas some studies find that lesions of the thalamus disrupt salt appetite, preferences and aversions, and conditioned taste aversions, others conclude that thalamic lesions have no effect. These disparities could result, in part, from the locations of the lesions: electrolytic lesions of thalamus not only destroy this nucleus but also damage fibers that carry gustatory information to ventral forebrain nuclei such as amygdala and hypothalamus. The author argues convincingly that the thalamus is not necessary for the expression of innate preferences and aversions, conditioned taste aversions, or salt appetite. Recent studies appear to implicate the thalamus in more complex gustatory processing related to foraging (food seeking) behavior.
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69. 69. Karimnamazi H, Travers JB: Differential projections from gustatory responsive regions of the parabrachial nucleus to the medulla and forebrain. Brain Res 1998, 813:283-302. An anatomical study of the projections to and from the parabrachial nuclei (PbN) of the rat was conducted using electrophysiologically guided injections of anterograde and retrograde tracers. A principal aim of the study was to compare afferent and efferents from the 'waist' region of the PbN (central medial and ventrolateral subdivisions) with those of the external region (external medial and external lateral subdivisions). Descending projections to the medullary parvocellular reticular formation were almost exclusively from the waist area. Ascending connections to amygdala from the external region of PbN terminated in the capsular region of the central nucleus, whereas waist area projections terminated in the central medial and lateral subnuclei of the central nucleus of the amygdala.
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