Temporal Characteristics of Gustatory Responses in Rat Parabrachial Neurons Vary by Stimulus and Chemosensitive Neuron Type

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Geran, Laura ^a   Travers, Susan ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CITRIC ACID; CYCLOHEXIMIDE; QUININE; SODIUM CHLORIDE; SUCROSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BITTER TASTE; CELL TYPE; CHEMOSENSITIVITY; CONTROLLED STUDY; MALE; NERVE CELL; NERVE CELL STIMULATION; NERVE POTENTIAL; NONHUMAN; ORGANOLEPTIC PROPERTY; PARABRACHIAL NUCLEUS; RAT; SALTINESS; SOUR TASTE; STIMULUS RESPONSE; SWEETNESS; TASTE DISCRIMINATION; TIME;

ACTION POTENTIALS; ANIMALS; MALE; NEURONS; RATS; REACTION TIME; TASTE PERCEPTION;

EID: 84885081495     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0076828     Document Type: Article

References (60)

1. Fishman IY, (1957) Single fiber gustatory impulses in rat and hamster. J Cell Physiol 49: 319-334. doi:10.1002/jcp.1030490213. PubMed: 13481071.
2. Beidler LM, (1953) Properties of chemoreceptors of tongue of rat. J Neurophysiol 16: 595-607. PubMed: 13109546.
3. Pfaffmann C, (1941) Gustatory afferent impulses. J Cell Physiol 17: 243-258. doi:10.1002/jcp.1030170209.
4. Katz DB, Simon SA, Nicolelis MA, (2001) Dynamic and multimodal responses of gustatory cortical neurons in awake rats. J Neurosci 21: 4478-4489. PubMed: 11404435.
5. Di Lorenzo PM, Victor JD, (2003) Taste response variability and temporal coding in the nucleus of the solitary tract of the rat. J Neurophysiol 90: 1418-1431. doi:10.1152/jn.00177.2003. PubMed: 12966173.
6. Roussin AT, Victor JD, Chen JY, Di Lorenzo PM, (2008) Variability in responses and temporal coding of tastants of similar quality in the nucleus of the solitary tract of the rat. J Neurophysiol 99: 644-655. doi:10.1152/jn.00920.2007. PubMed: 17913985.
7. Chen JY, Di Lorenzo PM, (2008) Responses to binary taste mixtures in the nucleus of the solitary tract: neural coding with firing rate. J Neurophysiol 99: 2144-2157. doi:10.1152/jn.01020.2007. PubMed: 18287552.
8. Di Lorenzo PM, Chen JY, Victor JD, (2009) Quality time: representation of a multidimensional sensory domain through temporal coding. J Neurosci 29: 9227-9238. doi:10.1523/JNEUROSCI.5995-08.2009. PubMed: 19625513.
9. Rosen AM, Victor JD, Di Lorenzo PM, (2011) Temporal coding of taste in the parabrachial nucleus of the pons of the rat. J Neurophysiol 105: 1889-1896. doi:10.1152/jn.00836.2010. PubMed: 21307316.
10. Norgren R, Leonard CM, (1973) Ascending central gustatory pathways. J Comp Neurol 150: 217-237. doi:10.1002/cne.901500208. PubMed: 4723066.
11. Geran LC, Travers SP, (2009) Bitter-responsive gustatory neurons in the rat parabrachial nucleus. J Neurophysiol 101: 1598-1612. doi:10.1152/jn.91168.2008. PubMed: 19129294.
12. Herbert H, Moga MM, Saper CB, (1990) Connections of the parabrachial nucleus with the nucleus of the solitary tract and the medullary reticular formation in the rat. J Comp Neurol 293: 540-580. doi:10.1002/cne.902930404. PubMed: 1691748.
13. Geran LC, Travers SP, (2006) Single neurons in the nucleus of the solitary tract respond selectively to bitter taste stimuli. J Neurophysiol 96: 2513-2527. doi:10.1152/jn.00607.2006. PubMed: 16899635.
14. Smith DV, Travers JB, (1979) A metric for breadth of tuning of gustatory neurons. Chem Sens 4: 215-229. doi:10.1093/chemse/4.3.215.
15. Spector AC, Travers SP, (2005) The representation of taste quality in the mammalian nervous system. Behav Cogn Neurosci Rev 4: 143-191. doi:10.1177/1534582305280031. PubMed: 16510892.
16. Victor JD, Purpura KP, (1996) Nature and precision of temporal coding in visual cortex: a metric-space analysis. J Neurophysiol 76: 1310-1326. PubMed: 8871238.
17. Legéndy CR, Salcman M, (1985) Bursts and recurrences of bursts in the spike trains of spontaneously active striate cortex neurons. J Neurophysiol 53: 926-939. PubMed: 3998798.
18. Lestienne R, Tuckwell HC, (1998) The significance of precisely replicating patterns in mammalian CNS spike trains. Neuroscience 82: 315-336. PubMed: 9466445.
19. Sachdev RN, Gilman S, Aldridge JW, (1991) Bursting properties of units in cat globus pallidus and entopeduncular nucleus: the effect of excitotoxic striatal lesions. Brain Res 549: 194-204. doi:10.1016/0006-8993(91)90458-8. PubMed: 1884215.
20. Sheinberg DL, Logothetis NK, (2001) Noticing familiar objects in real world scenes: the role of temporal cortical neurons in natural vision. J Neurosci 21: 1340-1350. PubMed: 11160405.
21. Softky WR, Koch C, (1993) The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci 13: 334-350. PubMed: 8423479.
22. Fulwiler CE, Saper CB, (1984) Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Res 319: 229-259. PubMed: 6478256.
23. Scott K, (2004) The sweet and the bitter of mammalian taste. Curr Opin Neurobiol 14: 423-427. doi:10.1016/j.conb.2004.06.003. PubMed: 15321062.
24. Danilova V, Hellekant G, (2003) Comparison of the responses of the chorda tympani and glossopharyngeal nerves to taste stimuli in C57BL/6J mice. BMC Neurosci 4: 5. doi:10.1186/1471-2202-4-5. PubMed: 12617752.
25. Boudreau JC, Do LT, Sivakumar L, Oravec J, Rodriguez CA, (1987) Taste systems of the petrosal ganglion of the rat glossopharyngeal nerve. Chem Sens 12: 437-458. doi:10.1093/chemse/12.3.437.
26. Lundy RF Jr., Contreras RJ, (1999) Gustatory neuron types in rat geniculate ganglion. J Neurophysiol 82: 2970-2988. PubMed: 10601433.
27. Breza JM, Nikonov AA, Contreras RJ, (2010) Response latency to lingual taste stimulation distinguishes neuron types within the geniculate ganglion. J Neurophysiol 103: 1771-1784. doi:10.1152/jn.00785.2009. PubMed: 20107132.
28. Ogawa H, Hayama T, Ito S, (1987) Response properties of the parabrachio-thalamic taste and mechanoreceptive neurons in rats. Exp Brain Res 68: 449-457. PubMed: 3691718.
29. Halsell CB, Travers SP, (1997) Anterior and posterior oral cavity responsive neurons are differentially distributed among parabrachial subnuclei in rat. J Neurophysiol 78: 920-938. PubMed: 9307125.
30. Lundy RF Jr., Norgren R, (2004) Activity in the hypothalamus, amygdala, and cortex generates bilateral and convergent modulation of pontine gustatory neurons. J Neurophysiol 91: 1143-1157. PubMed: 14627662.
31. Chen JY, Victor JD, Di Lorenzo PM, (2010) Temporal coding of intensity of NaCl and HCl in the nucleus of the solitary tract of the rat. J Neurophysiol 105: 697-711. PubMed: 21106899.
32. Fontanini A, Katz DB, (2006) State-dependent modulation of time-varying gustatory responses. J Neurophysiol 96: 3183-3193. doi:10.1152/jn.00804.2006. PubMed: 16928791.
33. Stapleton JR, Lavine ML, Wolpert RL, Nicolelis MA, Simon SA, (2006) Rapid taste responses in the gustatory cortex during licking. J Neurosci 26: 4126-4138. doi:10.1523/JNEUROSCI.0092-06.2006. PubMed: 16611830.
34. Roussin AT, D'Agostino AE, Fooden AM, Victor JD, Di Lorenzo PM, (2012) Taste coding in the nucleus of the solitary tract of the awake, freely licking rat. J Neurosci 32: 10494-10506. doi:10.1523/JNEUROSCI.1856-12.2012. PubMed: 22855799.
35. Halpern BP, Tapper DN, (1971) Taste stimuli: quality coding time. Science 171: 1256-1258. doi:10.1126/science.171.3977.1256. PubMed: 5545205.
36. Scott TR, (1974) Behavioral support for a neural taste theory. Physiol Behav 12: 413-417. doi:10.1016/0031-9384(74)90118-8. PubMed: 4820137.
37. Gutierrez R, Simon SA, Nicolelis MA, (2010) Licking-induced synchrony in the taste-reward circuit improves cue discrimination during learning. J Neurosci 30: 287-303. doi:10.1523/JNEUROSCI.0855-09.2010. PubMed: 20053910.
38. Weiss MS, Di Lorenzo PM, (2012) Not so fast: taste stimulus coding time in the rat revisited. Front. J Integr Neurosci 6: 27.
39. Nishijo H, Norgren R, (1991) Parabrachial gustatory neural activity during licking by rats. J Neurophysiol 66: 974-985. PubMed: 1753297.
40. Cross BA, Dyer RG, (1970) Effect of hypophysectomy on firing rates of hypothalamic neurones in diencephalic islands. J Endocrinol 48: 475-476. doi:10.1677/joe.0.0480475. PubMed: 5529683.
41. Villars PS, Kanusky JT, Dougherty TB, (2004) Stunning the neural nexus: mechanisms of general anesthesia. AANA J 72: 197-205. PubMed: 15208967.
42. Larson-Powers N, Pangborn RM, (1978) Paired comparison and time-intensity measurements of the sensory properties of beverages and gelatins containing sucrose or synthetic sweeteners. J Food Sci 43: 41-46. doi:10.1111/j.1365-2621.1978.tb09732.x.
43. Cubero-Castillo E, Noble AC, (2001) Effect of compound sequence on bitterness enhancement. Chem Sens 26: 419-424. doi:10.1093/chemse/26.4.419. PubMed: 11369676.
44. Pangborn RM, Lewis MJ, Yamashita JF, (1983) Comparison of time-intensity with category scaling of bitterness of iso-a-acids in model systems and in beer. J Inst Brew 89.
45. Kobayakawa T, Ogawa H, Kaneda H, Ayabe-Kanamura S, Endo H, et al. (1999) Spatio-temporal analysis of cortical activity evoked by gustatory stimulation in humans. Chem Sens 24: 201-209. doi:10.1093/chemse/24.2.201. PubMed: 10321821.
46. Saito S, Endo H, Kobayakawa T, Ayabe-Kanamura S, Kikuchi Y, et al. (1998) Temporal process from receptors to higher brain in taste detection studied by gustatory-evoked magnetic fields and reaction times. Ann N Y Acad Sci 855: 493-497. doi:10.1111/j.1749-6632.1998.tb10612.x. PubMed: 9929645.
47. Bujas Z, Szabo S, Ajduković D, Mayer D, (1989) Individual gustatory reaction times to various groups of chemicals that provoke basic taste qualities. Percept Psychophys 45: 385-390. doi:10.3758/BF03210710. PubMed: 2726399.
48. Travers JB, Travers SP, Norgren R, (1987) Gustatory neural processing in the hindbrain. Annu Rev Neurosci 10: 595-632. doi:10.1146/annurev.ne.10.030187.003115. PubMed: 3551765.
49. Kay LM, Beshel J, Brea J, Martin C, Rojas-Líbano D, et al. (2009) Olfactory oscillations: the what, how and what for. Trends Neurosci 32: 207-214. doi:10.1016/j.tins.2008.11.008. PubMed: 19243843.
50. Frank ME, Formaker BK, Hettinger TP, (2005) Peripheral gustatory processing of sweet stimuli by golden hamsters. Brain. Res Bull 66: 70-84. doi:10.1016/j.brainresbull.2005.04.004.
51. Mistretta CM, (1972) A quantitative analysis of rat chorda tympani fiber discharge patterns. In: Schneider D, eds. Olfaction & TasteIV. Stuttgart: Wissenschaftliche. pp. pp. 294-300.
52. Ogawa H, Sato M, Yamashita S, (1969) Gustatory impulse discharges in response to saccharin in rats and hamsters. J Physiol 204: 311-329. PubMed: 5824641.
53. Di Lorenzo PM, Hallock RM, Kennedy DP, (2003) Temporal coding of sensation: mimicking taste quality with electrical stimulation of the brain. Behav Neurosci 117: 1423-1433. doi:10.1037/0735-7044.117.6.1423. PubMed: 14674860.
54. Travers SP, Norgren R, (1989) The time course of solitary nucleus gustatory responses: influence of stimulus and site of application. Chem Sens 14: 55-74. doi:10.1093/chemse/14.1.55.
55. Frank ME, (1991) Taste-responsive neurons of the glossopharyngeal nerve of the rat. J Neurophysiol 65: 1452-1463. PubMed: 1875254.
56. Kim MJ, Mizumori SJ, Bernstein IL, (2010) Neuronal representation of conditioned taste in the basolateral amygdala of rats. Neurobiol Learn Mem 93: 406-414. doi:10.1016/j.nlm.2009.12.007. PubMed: 20026412.
57. Laviolette SR, Lipski WJ, Grace AA, (2005) A subpopulation of neurons in the medial prefrontal cortex encodes emotional learning with burst and frequency codes through a dopamine D4 receptor-dependent basolateral amygdala input. J Neurosci 25: 6066-6075. doi:10.1523/JNEUROSCI.1168-05.2005. PubMed: 15987936.
58. Lisman JE, (1997) Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20: 38-43. doi:10.1016/S0166-2236(96)10070-9. PubMed: 9004418.
59. Khosravi-Hashemi N, Chacron MJ, (2012) Bursts and isolated spikes code for opposite movement directions in midbrain electrosensory neurons. PLOS ONE 7: e40339. doi:10.1371/journal.pone.0040339. PubMed: 22768279.
60. Khosravi-Hashemi N, Fortune ES, Chacron MJ, (2011) Coding movement direction by burst firing in electrosensory neurons. J Neurophysiol 106: 1954-1968. doi:10.1152/jn.00116.2011. PubMed: 21775723.