Lateral hypothalamus contains two types of palatability- related taste responses with distinct dynamics

Journal of Neuroscience

Volumn 33, Issue 22, 2013, Pages 9462-9473

  Li, Jennifer X ^a   Yoshida, Takashi ^b,c   Monk, Kevin J ^a   Katz, Donald B ^a  

^a BRANDEIS UNIVERSITY   (United States)

^b KYUSHU UNIVERSITY   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; FEMALE; LATERAL HYPOTHALAMUS; NERVE POTENTIAL; NONHUMAN; PALATABILITY; PRIORITY JOURNAL; RAT; TASK PERFORMANCE; TASTE PREFERENCE;

ANALYSIS OF VARIANCE; ANIMALS; FEMALE; FOOD; FOOD PREFERENCES; HYPOTHALAMIC AREA, LATERAL; NEURAL PATHWAYS; OXYGEN; RATS; RATS, LONG-EVANS; TASTE;

EID: 84878280528     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3935-12.2013     Document Type: Article

References (98)

1. Aleksanyan ZA, Buresová O, Bures J (1976) Modification of unit responses to gustatory stimuli by conditioned taste aversion in rats. Physiol Behav 17:173-179. CrossRef Medline
2. Anand BK, Brobeck JR (1951) Localization of a "feeding center" in the hypothalamus of the rat. Proc Soc Exp Biol Med 77:323-324. Medline
3. Anderson AK, Christoff K, Stappen I, Panitz D, Ghahremani DG, Glover G, Gabrieli JD, SobelN (2003) Dissociated neural representations of intensity and valence in human olfaction. Nat Neurosci 6:196-202. CrossRef Medline
4. Berk ML, Finkelstein JA (1982) Efferent connections of the lateral hypothalamic area of the rat: an autoradiographic investigation. Brain Res Bull 8:511-526. CrossRef Medline
5. Berridge KC (1996) Food reward: brain substrates of wanting and liking. Neurosci Biobehav Rev 20:1-25. CrossRef Medline
6. Berridge KC, Robinson TE (2003) Parsing reward. Trends Neurosci 26:507-513. CrossRef Medline
7. Berridge KC, Valenstein ES (1991) What psychological process mediates feeding evoked by electrical stimulation of the lateral hypothalamus? Behav Neurosci 105:3-14. CrossRef Medline
8. Berridge K, Grill HJ, Norgren R (1981) Relation of consummatory responses and preabsorptive insulin release to palatability and learned taste aversions. J Comp Physiol Psychol 95:363-382. CrossRef Medline
9. Berthoud HR, Münzberg H (2011) The lateral hypothalamus as integrator of metabolic and environmental needs: from electrical self-stimulation to opto-genetics. Physiol Behav 104:29-39. CrossRef Medline
10. Blood AJ, Zatorre RJ, Bermudez P, EvansAC (1999) Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions. Nat Neurosci 2:382-387. CrossRef Medline
11. Breslin PA, Spector AC, Grill HJ (1992) A quantitative comparison of taste reactivity behaviors to sucrose before and after lithium chloride pairings: a unidimensional account of palatability. Behav Neurosci 106:820-836. CrossRef Medline
12. Broberger C, De Lecea L, Sutcliffe JG, Hökfelt T (1998) Hypocretin/orexinand melanin-concentrating hormone-expressing cells form distinct populations in the rodent lateral hypothalamus: relationship to the neuropeptide Y and agouti gene-related protein systems. J Comp Neurol 402:460-474. CrossRef Medline
13. Bueter M, Miras AD, Chichger H, Fenske W, Ghatei MA, Bloom SR, Unwin RJ, Lutz TA, Spector AC, le Roux CW (2011) Alterations of sucrose preference after Roux-en-Y gastric bypass. Physiol Behav 104:709-721. CrossRef Medline
14. Burton MJ, Rolls ET, Mora F (1976) Effects of hunger on the responses of neurons in the lateral hypothalamus to the sight and taste of food. Exp Neurol 51:668-677. CrossRef Medline
15. Caulliez R, Meile MJ, Nicolaidis S (1996) A lateral hypothalamic D1 dopaminergic mechanism in conditioned taste aversion. Brain Res 729:234-245. CrossRef Medline
16. Chen X, Gabitto M, Peng Y, Ryba NJ, Zuker CS (2011) A gustotopic map of taste qualities in the mammalian brain. Science 333:1262-1266. CrossRef Medline
17. Clarke SN, Ossenkopp KP (1998) Taste reactivity responses in rats: influence of sex and the estrous cycle. Am J Physiol 274:R718-R724. Medline
18. Csicsvari J, Hirase H, Czurkó A, Mamiya A, Buzsáki G (1999) Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J Neurosci 19:274-287. Medline de
19. Araujo IE, Gutierrez R, Oliveira-Maia AJ, Pereira A Jr, Nicolelis MA, Simon SA (2006) Neural ensemble coding of satiety states. Neuron 51: 483-494. CrossRef Medline
20. Dess NK (2000) Responses to basic taste qualities in rats selectively bred for high versus low saccharin intake. Physiol Behav 69:247-257. CrossRef Medline
21. Di Lorenzo PM, Lemon CH, Reich CG (2003) Dynamic coding of taste stimuli in the brainstem: effects of brief pulses of taste stimuli on subsequent taste responses. J Neurosci 23:8893-8902. Medline
22. Ferssiwi A, Cardo B, Velley L (1987) Gustatory preference-aversion thresholds are increased by ibotenic acid lesion of the lateral hypothalamus in the rat. Brain Res 437:142-150. CrossRef Medline
23. Fontanini A, Katz DB (2006) State-dependent modulation of time-varying gustatory responses. J Neurophysiol 96:3183-3193. CrossRef Medline
24. Fontanini A, Grossman SE, Figueroa JA, Katz DB (2009) Distinct subtypes of basolateral amygdala taste neurons reflect palatability and reward. J Neurosci 29:2486-2495. CrossRef Medline
25. Forestell CA, LoLordo VM (2003) Palatability shifts in taste and flavour preference conditioning. Q J Exp Psychol B 56:140-160. CrossRef Medline
26. Formaker BK, Frank ME (1996) Responses of the hamster chorda tympani nerve to binary component taste stimuli: evidence for peripheral gustatory mixture interactions. Brain Res 727:79-90. CrossRef Medline
27. Frank ME (2000) Neuron types, receptors, behavior, and taste quality. Physiol Behav 69:53-62. CrossRef Medline
28. Frank ME, Formaker BK, Hettinger TP (2003) Taste responses to mixtures: analytic processing of quality. Behav Neurosci 117:228-235. CrossRef Medline
29. Fukuda M, Ono T, Nishino H, Nakamura K (1986) Neuronal responses in monkey lateral hypothalamus during operant feeding behavior. Brain Res Bull 17:879-883. CrossRef Medline
30. Fukuda M, Ono T, Nakamura K, Tamura R (1990) Dopamine and ACh involvement in plastic learning by hypothalamic neurons in rats. Brain Res Bull 25:109-114. CrossRef Medline
31. Galaverna OG, Seeley RJ, Berridge KC, Grill HJ, Epstein AN, Schulkin J (1993) Lesions of the central nucleus of the amygdala. I: Effects on taste reactivity, taste aversion learning and sodium appetite. Behav Brain Res 59:11-17. CrossRef Medline
32. Gentet LJ, Avermann M, Matyas F, Staiger JF, Petersen CC (2010) Membrane potential dynamics of GABAergic neurons in the barrel cortex of behaving mice. Neuron 65:422-435. CrossRef Medline
33. Geran LC, Travers SP (2009) Bitter-responsive gustatory neurons in the rat parabrachial nucleus. J Neurophysiol 101:1598-1612. CrossRef Medline
34. Goto M, Canteras NS, Burns G, Swanson LW (2005) Projections from the subfornical region of the lateral hypothalamic area. J Comp Neurol 493: 412-438. CrossRef Medline
35. Grabenhorst F, Rolls ET, Parris BA, d'Souza AA (2010) How the brain represents the reward value of fat in the mouth. Cereb Cortex 20:1082-1091. CrossRef Medline
36. Grill HJ, Norgren R (1978) The taste reactivity test. I. Mimetic responses to gustatory stimuli in neurologically normal rats. Brain Res 143:263-279. CrossRef Medline
37. Grossman SE, Fontanini A, Wieskopf JS, Katz DB (2008) Learning-related plasticity of temporal coding in simultaneously recorded amygdalacortical ensembles. J Neurosci 28:2864-2873. CrossRef Medline
38. Grossman SP, Dacey D, Halaris AE, Collier T, Routtenberg A (1978) Aphagia and adipsia after preferential destruction of nerve cell bodies in hypothalamus. Science 202:537-539. CrossRef Medline
39. Haddad R, Weiss T, Khan R, Nadler B, Mandairon N, Bensafi M, Schneidman E, Sobel N (2010) Global features of neural activity in the olfactory system form a parallel code that predicts olfactory behavior and perception. J Neurosci 30:9017-9026. CrossRef Medline
40. Hagan JJ, Leslie RA, Patel S, Evans ML, Wattam TA, Holmes S, Benham CD, Taylor SG, Routledge C, Hemmati P, Munton RP, Ashmeade TE, Shah AS, Hatcher JP, Hatcher PD, Jones DN, Smith MI, Piper DC, Hunter AJ, Porter RA, et al (1999) Orexin A activates locus coeruleus cell firing and increases arousal in the rat. Proc Natl Acad Sci U S A 96:10911-10916. CrossRef Medline
41. Hahn JD, Swanson LW (2010) Distinct patterns of neuronal inputs and outputs of the juxtaparaventricular and suprafornical regions of the lateral hypothalamic area in the male rat. Brain Res Rev 64:14-103. CrossRef Medline
42. Hassani OK, Lee MG, Jones BE (2009) Melanin-concentrating hormone neurons discharge in a reciprocal manner to orexin neurons across the sleep-wake cycle. Proc Natl Acad Sci U S A 106:2418-2422. CrossRef Medline
43. Hassani OK, Henny P, Lee MG, Jones BE (2010) GABAergic neurons intermingled with orexin and MCH neurons in the lateral hypothalamus discharge maximally during sleep. Eur J Neurosci 32:448-457. CrossRef Medline
44. Hoebel BG, Teitelbaum P (1962) Hypothalamic control of feeding and selfstimulation. Science 135:375-377. CrossRef Medline
45. Katz DB, Simon SA, Nicolelis MA (2001) Dynamic and multimodal responses of gustatory cortical neurons in awake rats. J Neurosci 21:4478-4489. Medline
46. Kirouac GJ, Ganguly PK (1995) Topographical organization in the nucleus accumbens of afferents from the basolateral amygdala and efferents to the lateral hypothalamus. Neuroscience 67:625-630. CrossRef Medline
47. Krettek JE, Price JL (1978) Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat. J Comp Neurol 178:225-254. CrossRef Medline
48. LeonardCM (1969) The prefrontal cortex of the rat. I. Cortical projection of the mediodorsal nucleus. II. Efferent connections. Brain Res 12:321-343. CrossRef Medline
49. Maier JX, Katz DB (2013) Neural dynamics in response to binary taste mixtures. J Neurophysiol 109:2108-2117. CrossRef Medline
50. Margules DL, Olds J (1962) Identical "feeding" and "rewarding" systems in the lateral hypothalamus of rats. Science 135:374-375. CrossRef Medline
51. Mileykovskiy BY, Kiyashchenko LI, Siegel JM (2005) Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron 46:787-798. CrossRef Medline
52. Nishijo H, Uwano T, Tamura R, Ono T (1998) Gustatory and multimodal neuronal responses in the amygdala during licking and discrimination of sensory stimuli in awake rats. J Neurophysiol 79:21-36. Medline
53. Norgren R (1970) Gustatory responses in the hypothalamus. Brain Res 21: 63-77. CrossRef Medline
54. Ogawa M, van der Meer MA, Esber GR, Cerri DH, Stalnaker TA, Schoenbaum G (2013) Risk-responsive orbitofrontal neurons track acquired salience. Neuron 77:251-258. CrossRef Medline
55. Ono T, Nakamura K, Nishijo H, Fukuda M (1986) Hypothalamic neuron involvement in integration of reward, aversion, and cue signals. J Neurophysiol 56:63-79. Medline
56. Ono T, Nakamura K, Fukuda M, Kobayashi T (1992) Catecholamine and acetylcholine sensitivity of rat lateral hypothalamic neurons related to learning. J Neurophysiol 67:265-279. Medline
57. Overduin J, Figlewicz DP, Bennett-Jay J, Kittleson S, Cummings DE (2012) Ghrelin increases the motivation to eat, but does not alter food palatability. Am J Physiol Regul Integr Comp Physiol 303:R259-R269. CrossRef Medline
58. Paton JJ, Belova MA, Morrison SE, Salzman CD (2006) The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 439:865-870. CrossRef Medline
59. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, Ed. 6. Amsterdam: Academic/Elsevier.
60. Peciña S, Berridge KC (2005) Hedonic hot spot in nucleus accumbens shell: where do mu-opioids cause increased hedonic impact of sweetness? J Neurosci 25:11777-11786. CrossRef Medline
61. Petrovich GD, Canteras NS, SwansonLW (2001) Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res Brain Res Rev 38:247-289. CrossRef Medline
62. Piette CE, Baez-Santiago MA, Reid EE, Katz DB, Moran A (2012) Inactivation of basolateral amygdala specifically eliminates palatability-related information in cortical sensory responses. J Neurosci 32:9981-9991. CrossRef Medline
63. Qu D, Ludwig DS, Gammeltoft S, Piper M, Pelleymounter MA, Cullen MJ, Mathes WF, Przypek R, Kanarek R, Maratos-Flier E (1996) A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature 380:243-247. CrossRef Medline
64. Rana SA, Parker LA (2008) Differential effects of neurotoxin-induced lesions of the basolateral amygdala and central nucleus of the amygdala on lithium-induced conditioned disgust reactions and conditioned taste avoidance. Behav Brain Res 189:284-297. CrossRef Medline
65. Reilly S, Pritchard TC (1996) Gustatory thalamus lesions in the rat: I. Innate taste preferences and aversions. Behav Neurosci 110:737-745. CrossRef Medline
66. Roitman JD, Shadlen MN (2002) Response of neurons in the lateral intraparietal area during a combined visual discrimination reaction time task. J Neurosci 22:9475-9489. Medline
67. Rolls ET (2009) Functional neuroimaging of umami taste: what makes umami pleasant? Am J Clin Nutr 90:804S-813S. CrossRef Medline
68. Rolls ET (2012) Taste, olfactory and food texture reward processing in the brain and the control of appetite. Proc Nutr Soc 71:488-501. CrossRef Medline
69. Rosen AM, Di LorenzoPM (2012) Neural coding of taste by simultaneously recorded cells in the nucleus of the solitary tract of the rat. J Neurophysiol 108:3301-3312. CrossRef Medline
70. Rosen AM, Roussin AT, Di Lorenzo PM (2010) Water as an independent taste modality. Front Neurosci 4:175. CrossRef Medline
71. Roth SR, Schwartz M, Teitelbaum P (1973) Failure of recovered lateral hypothalamic rats to learn specific food aversions. J Comp Physiol Psychol 83:184-197. CrossRef Medline
72. Sabatinelli D, Bradley MM, Lang PJ, Costa VD, Versace F (2007) Pleasure rather than salience activates human nucleus accumbens and medial prefrontal cortex. J Neurophysiol 98:1374-1379. CrossRef Medline
73. Sadacca BF, Rothwax JT, Katz DB (2012) Sodium concentration coding gives way to evaluative coding in cortex and amygdala. J Neurosci 32: 9999-10011. CrossRef Medline
74. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, Williams SC, Richardson JA, Kozlowski GP, Wilson S, Arch JR, Buckingham RE, Haynes AC, Carr SA, Annan RS, McNulty DE, Liu WS, Terrett JA, Elshourbagy NA, Bergsma DJ, et al (1998) Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92:573-585. CrossRef Medline
75. Samuelsen CL, Gardner MP, Fontanini A (2012) Effects of cue-triggered expectation on cortical processing of taste. Neuron 74:410-422. CrossRef Medline
76. Sano H, YokoiM (2007) Striatal medium spiny neurons terminate in a distinct region in the lateral hypothalamic area and do not directly innervate orexin/hypocretin-or melanin-concentrating hormone-containing neurons. J Neurosci 27:6948-6955. CrossRef Medline
77. Schmitt O, Usunoff KG, Lazarov NE, Itzev DE, Eipert P, Rolfs A, Wree A (2012) Orexinergic innervation of the extended amygdala and basal ganglia in the rat. Brain Struct Funct 217:233-256. CrossRef Medline
78. Schwartzbaum JS (1988) Electrophysiology of taste, feeding and reward in lateral hypothalamus of rabbit. Physiol Behav 44:507-526. CrossRef Medline
79. Schwartzbaum JS, Leventhal TO (1990) Neural substrates of behavioral aversion in lateral hypothalamus of rabbits. Brain Res 507:85-91. CrossRef Medline
80. Small DM, Gregory MD, Mak YE, Gitelman D, Mesulam MM, Parrish T (2003) Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron 39:701-711. CrossRef Medline
81. Smith DV, Travers JB (1979) A metric for the breadth of gustatory neurons. Chem Senses 4:215-229. CrossRef
82. Spector AC, Travers SP (2005) The representation of taste quality in the mammalian nervous system. Behav Cogn Neurosci Rev 4:143-191. CrossRef Medline
83. Stanley BG, Magdalin W, Seirafi A, Thomas WJ, Leibowitz SF (1993) The perifornical area: the major focus of (a) patchily distributed hypothalamic neuropeptide Y-sensitive feeding system(s). Brain Res 604:304-317. CrossRef Medline
84. Stewart RB, Russell RN, Lumeng L, Li TK, Murphy JM (1994) Consumption of sweet, salty, sour, and bitter solutions by selectively bred alcoholpreferring and alcohol-nonpreferring lines of rats. Alcohol Clin Exp Res 18:375-381. CrossRef Medline
85. Stratford TR, Kelley AE (1999) Evidence of a functional relationship between the nucleus accumbens shell and lateral hypothalamus subserving the control of feeding behavior. J Neurosci 19:11040-11048. Medline
86. Swanson LW, Sanchez-Watts G, Watts AG (2005) Comparison of melaninconcentrating hormone and hypocretin/orexin mRNA expression patterns in a new parceling scheme of the lateral hypothalamic zone. Neurosci Lett 387:80-84. CrossRef Medline
87. Taha SA, Fields HL (2005) Encoding of palatability and appetitive behaviors by distinct neuronal populations in the nucleus accumbens. J Neurosci 25:1193-1202. CrossRef Medline
88. Takahashi K, Lin JS, Sakai K (2008) Neuronal activity of orexin and nonorexin waking-active neurons during wake-sleep states in the mouse. Neuroscience 153:860-870. CrossRef Medline
89. Thompson RH, Swanson LW (2010) Hypothesis-driven structural connectivity analysis supports network over hierarchical model of brain architecture. Proc Natl Acad Sci U S A 107:15235-15239. CrossRef Medline
90. Touzani K, Sclafani A (2001) Conditioned flavor preference and aversion: role of the lateral hypothalamus. Behav Neurosci 115:84-93. CrossRef Medline
91. Touzani K, Sclafani A (2002) Lateral hypothalamic lesions impair flavournutrient and flavour-toxin trace learning in rats. Eur J Neurosci 16:2425-2433. CrossRef Medline
92. Travers JB, Norgren R (1986) Electromyographic analysis of the ingestion and rejection of sapid stimuli in the rat. Behav Neurosci 100:544-555. CrossRef Medline
93. Tsumori T, Yokota S, Kishi T, Qin Y, Oka T, Yasui Y (2006) Insular cortical and amygdaloid fibers are in contact with posterolateral hypothalamic neurons projecting to the nucleus of the solitary tract in the rat. Brain Res 1070:139-144. CrossRef Medline
94. Tucci S, Rada P, Hernandez L (1998) Role of glutamate in the amygdala and lateral hypothalamus in conditioned taste aversion. Brain Res 813:44-49. CrossRef Medline
95. West HL, Mark GP, Hoebel BG (1991) Effects of conditioned taste aversion on extracellular serotonin in the lateral hypothalamus and hippocampus of freely moving rats. Brain Res 556:95-100. CrossRef Medline
96. Yamamoto T, Yuyama N, Kato T, Kawamura Y (1985) Gustatory responses of cortical neurons in rats. II. Information processing of taste quality. J Neurophysiol 53:1356-1369. Medline
97. Yamamoto T, Matsuo R, Kiyomitsu Y, Kitamura R (1989) Response properties of lateral hypothalamic neurons during ingestive behavior with special reference to licking of various taste solutions. Brain Res 481:286-297. CrossRef Medline
98. Zald DH, Hagen MC, Pardo JV (2002) Neural correlates of tasting concentrated quinine and sugar solutions. J Neurophysiol 87:1068-1075. Medline