μ-Opioid modulation in the rostral solitary nucleus and reticular formation alters taste reactivity: Evidence for a suppressive effect on consummatory behavior

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 301, Issue 3, 2011, Pages

  Kinzeler, Nicole R ^a   Travers, Susan P ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

Feeding; Gaping; Licking; Nucleus of the solitary tract

Indexed keywords

ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; MU OPIATE RECEPTOR; QUININE;

AMPLITUDE MODULATION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AVERSIVE BEHAVIOR; BRAIN STEM; FEEDING BEHAVIOR; FOREBRAIN; LICKING; MALE; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; RAT; RETICULAR FORMATION; SOLITARY TRACT NUCLEUS; TASTE ACUITY;

ANALGESICS, OPIOID; ANALYSIS OF VARIANCE; ANIMALS; CONSUMMATORY BEHAVIOR; EATING; ELECTROMYOGRAPHY; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; INFUSIONS, PARENTERAL; INJECTIONS; MALE; MOTOR ACTIVITY; QUININE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, MU; RETICULAR FORMATION; SOLITARY NUCLEUS; SUCROSE; TASTE; TIME FACTORS;

EID: 80052395827     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00142.2011     Document Type: Article

References (76)

1. Appleyard SM, Bailey TW, Doyle MW, Jin YH, Smart JL, Low MJ, Andresen MC. Proopiomelanocortin neurons in nucleus tractus solitaries are activated by visceral afferents: regulation by cholecystokinin and opioids. J Neurosci 25: 3578-3585, 2005.
2. Bakshi VP, Kelley AE. Feeding induced by opioid stimulation of the ventral striatum: role of opiate receptor subtypes. J Pharmacol Exp Ther 265: 1253-1260, 1993.
3. Bodnar RJ. Endogenous opioids and feeding behavior: a 30-year historical perspective. Peptides 25: 697-725, 2004.
4. Boxwell AY, Y; Travers SP, Travers JB. Activation of mu opiate receptors presynaptically suppresses afferent input to rNST neurons. 2011, http://www.achems.org/files/2011%20Meeting%20Files/FINAL ABSTRACTS. pdf.
5. Chen Z, Travers JB. Inactivation of amino acid receptors in medullary reticular formation modulates and suppresses ingestion and rejection responses in the awake rat. Am J Physiol Regul Integr Comp Physiol 285: R68-R83, 2003.
6. Chen Z, Travers SP, Travers JB. Muscimol infusions in the brain stem reticular formation reversibly block ingestion in the awake rat. Am J Physiol Regul Integr Comp Physiol 280: R1085-R1094, 2001.
7. Cheng PY, Liu-Chen LY, Chen C, Pickel VM. Immunolabeling of Mu opioid receptors in the rat nucleus of the solitary tract: extrasynaptic plasmalemmal localization and association with Leu5-enkephalin. J Comp Neurol 371: 522-536, 1996.
8. Chieng B, Christie MJ. Inhibition by opioids acting on mu-receptors of GABAergic and glutamatergic postsynaptic potentials in single rat periaqueductal gray neurones in vitro. Br J Pharmacol 113: 303-309, 1994.
9. Davis BJ, Kream RM. Distribution of tachykininand opioid-expressing neurons in the hamster solitary nucleus: an immunoand in situ hybridization histochemical study. Brain Res 616: 6-16, 1993.
10. DiNardo LA, Travers JB. Distribution of fos-like immunoreactivity in the medullary reticular formation of the rat after gustatory elicited ingestion and rejection behaviors. J Neurosci 17: 3826-3839, 1997.
11. Doyle TG, Berridge KC, Gosnell BA. Morphine enhances hedonic taste palatability in rats. Pharmacol Biochem Behav 46: 745-749, 1993.
12. Drake CT, Milner TA. Mu opioid receptors are in somatodendritic and axonal compartments of GABAergic neurons in rat hippocampal formation. Brain Res 849: 203-215, 1999.
13. Feldman JL, and Del Negro CA. Looking for inspiration: new perspectives on respiratory rhythm. Nat Rev Neurosci 7: 232-242, 2006.
14. Fields HL, Heinricher MM, Mason P. Neurotransmitters in nociceptive modulatory circuits. Annu Rev Neurosci 14: 219-245, 1991.
15. Flynn FW, Grill HJ. Intraoral intake and taste reactivity responses elicited by sucrose and sodium chloride in chronic decerebrate rats. Behav Neurosci 102: 934-941, 1988.
16. Giraudo SQ, Kotz CM, Billington CJ, Levine AS. Association between the amygdala and nucleus of the solitary tract in mu-opioid induced feeding in the rat. Brain Res 802: 184-188, 1998.
17. Glass MJ, Billington CJ, Levine AS. Opioids and food intake: distributed functional neural pathways? Neuropeptides 33: 360-368, 1999.
18. Gray PA, Rekling JC, Bocchiaro CM, Feldman JL. Modulation of respiratory frequency by peptidergic input to rhythmogenic neurons in the preBotzinger complex. Science 286: 1566-1568, 1999.
19. Grill HJ, Norgren R. The taste reactivity test. I. Mimetic responses to gustatory stimuli in neurologically normal rats. Brain Res 143: 263-279, 1978.
20. Grill HJ, Norgren R. The taste reactivity test. II. Mimetic responses to gustatory stimuli in chronic thalamic and chronic decerebrate rats. Brain Res 143: 281-297, 1978.
21. Grill HJ, Schwartz GJ, Travers JB. The contribution of gustatory nerve input to oral motor behavior and intake-based preference. I. Effects of chorda tympani or glossopharyngeal nerve section in the rat. Brain Res 573: 95-104, 1992.
22. Haji A, Takeda R, Okazaki M. Neuropharmacology of control of respiratory rhythm and pattern in mature mammals. Pharmacol Ther 86: 277-304, 2000.
23. Halsell CB, Travers SP, Travers JB. Ascending and descending projections from the rostral nucleus of the solitary tract originate from separate neuronal populations. Neuroscience 72: 185-197, 1996.
24. Heinricher MM, Morgan MM, Tortorici V, Fields HL. Disinhibition of off-cells and antinociception produced by an opioid action within the rostral ventromedial medulla. Neuroscience 63: 279-288, 1994.
25. Hellman KM, Mendelson SJ, Mendez-Duarte MA, Russell JL, Mason P. Opioid microinjection into raphe magnus modulates cardiorespiratory function in mice and rats. Am J Physiol Regul Integr Comp Physiol 297: R1400-R1408, 2009.
26. Herman MA, Alayan A, Sahibzada N, Bayer B, Verbalis J, Dretchen KL, Gillis RA. micro-Opioid receptor stimulation in the medial subnucleus of the tractus solitarius inhibits gastric tone and motility by reducing local GABA activity. Am J Physiol Gastrointest Liver Physiol 299: G494-G506, 2010.
27. Huang J, Wang H, Pickel VM. Rostrocaudal variation in targeting of N-methyl-D-aspartate and mu-opioid receptors in the rat medial nucleus of the solitary tract. J Comp Neurol 421: 400-411, 2000.
28. Huang W, Chen JX, Li YM, Lu YC, Wu XJ. Structures and connections of enkephalinand gamma-aminobutyric acid-immunoreactive profiles in the gustatory region of the nucleus tractus solitarius: a light and electron microscopic study. Neurol Sci 32: 53-58, 2010.
29. Johnson SM, Smith JC, Feldman JL. Modulation of respiratory rhythm in vitro: role of Gi/o protein-mediated mechanisms. J Appl Physiol 80: 2120-2133, 1996.
30. Kalyuzhny AE, Dooyema J, Wessendorf MW. Opioidand GABA(A)receptors are co-expressed by neurons in rat brain. Neuroreport 11: 2625-2628, 2000.
31. Kalyuzhny AE, Wessendorf MW. Relationship of muand delta-opioid receptors to GABAergic neurons in the central nervous system, including antinociceptive brainstem circuits. J Comp Neurol 392: 528-547, 1998.
32. Kelley AE, Bakshi VP, Haber SN, Steininger TL, Will MJ, Zhang M. Opioid modulation of taste hedonics within the ventral striatum. Physiol Behav 76: 365-377, 2002.
33. Kim EM, Quinn JG, Spanswick D, O'Hare E. Feeding association between the nucleus of the solitary tract and the ventral tegmental area. Appetite 53: 457-460, 2009.
34. Kinzeler NR, Travers SP. Licking and gaping elicited by microstimulation of the nucleus of the solitary tract. Am J Physiol Regul Integr Comp Physiol 295: R436-R448, 2008.
35. Kotz CM, Billington CJ, Levine AS. Opioids in the nucleus of the solitary tract are involved in feeding in the rat. Am J Physiol Regul Integr Comp Physiol 272: R1028-R1032, 1997.
36. Kotz CM, Glass MJ, Levine AS, Billington CJ. Regional effect of naltrexone in the nucleus of the solitary tract in blockade of NPY-induced feeding. Am J Physiol Regul Integr Comp Physiol 278: R499-R503, 2000.
37. Levine AS, Atkinson RL. Opioids in the regulation of food intake and energy expenditure. Fed Proc 46: 159-162, 1987.
38. Levine AS, Billington CJ. Opioids as agents of reward-related feeding: a consideration of the evidence. Physiol Behav 82: 57-61, 2004.
39. Levine AS, Weldon DT, Grace M, Cleary JP, Billington CJ. Naloxone blocks that portion of feeding driven by sweet taste in food-restricted rats. Am J Physiol Regul Integr Comp Physiol 268: R248-R252, 1995.
40. Li CS, Davis BJ, Smith DV. Opioid modulation of taste responses in the nucleus of the solitary tract. Brain Res 965: 21-34, 2003.
41. Lonergan T, Goodchild AK, Christie MJ, Pilowsky PM. Mu opioid receptors in rat ventral medulla: effects of endomorphin-1 on phrenic nerve activity. Respir Physiol Neurobiol 138: 165-178, 2003.
42. Mansour A, Fox CA, Burke S, Meng F, Thompson RC, Akil H, Watson SJ. Mu, delta, and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J Comp Neurol 350: 412-438, 1994.
43. Marks-Kaufman R. Increased fat consumption induced by morphine administration in rats. Pharmacol Biochem Behav 16: 949-955, 1982.
44. Martin-Schild S, Gerall AA, Kastin AJ, Zadina JE. Differential distribution of endomorphin 1and endomorphin 2-like immunoreactivities in the CNS of the rodent. J Comp Neurol 405: 450-471, 1999.
45. Mellen NM, Janczewski WA, Bocchiaro CM, Feldman JL. Opioidinduced quantal slowing reveals dual networks for respiratory rhythm generation. Neuron 37: 821-826, 2003.
46. Monteillet-Agius G, Fein J, Anton B, Evans CJ. ORL-1 and mu opioid receptor antisera label different fibers in areas involved in pain processing. J Comp Neurol 399: 373-383, 1998.
47. Moriwaki A, Wang JB, Svingos A, van Bockstaele E, Cheng P, Pickel V, Uhl GR. mu Opiate receptor immunoreactivity in rat central nervous system. Neurochem Res 21: 1315-1331, 1996.
48. Murakami S, Okamura H, Pelletier G, Ibata Y. Differential colocalization of neuropeptide Yand methionine-enkephalin-Arg6-Gly7-Leu8like immunoreactivity in catecholaminergic neurons in the rat brain stem. J Comp Neurol 281: 532-544, 1989.
49. Mustapic S, Radocaj T, Sanchez A, Dogas Z, Stucke AG, Hopp FA, Stuth EA, Zuperku EJ. Clinically relevant infusion rates of mu-opioid agonist remifentanil cause bradypnea in decerebrate dogs but not via direct effects in the pre-Botzinger complex region. J Neurophysiol 103: 409-418, 2010.
50. Mutolo D, Bongianni F, Einum J, Dubuc R, Pantaleo T. Opioidinduced depression in the lamprey respiratory network. Neuroscience 150: 720-729, 2007.
51. Nason MW Jr, Mason P. Medullary raphe neurons facilitate brown adipose tissue activation. J Neurosci 26: 1190-1198, 2006.
52. Parker LA, Maier S, Rennie M, Crebolder J. Morphineand naltrexone-induced modification of palatability: analysis by the taste reactivity test. Behav Neurosci 106: 999-1010, 1992.
53. Pecina S, Berridge KC. Opioid site in nucleus accumbens shell mediates eating and hedonic 'liking' for food: map based on microinjection Fos plumes. Brain Res 863: 71-86, 2000.
54. Pecina S, Smith KS, Berridge KC. Hedonic hot spots in the brain. Neuroscientist 12: 500-511, 2006.
55. Pickel VM, Colago EE. Presence of mu-opioid receptors in targets of efferent projections from the central nucleus of the amygdala to the nucleus of the solitary tract. Synapse 33: 141-152, 1999.
56. Pierce TL, Wessendorf MW. Immunocytochemical mapping of endomorphin-2-immunoreactivity in rat brain. J Chem Neuroanat 18: 181-207, 2000.
57. Poole SL, Deuchars J, Lewis DI, Deuchars SA. Subdivision-specific responses of neurons in the nucleus of the tractus solitarius to activation of mu-opioid receptors in the rat. J Neurophysiol 98: 3060-3071, 2007.
58. Rhim H, Miller RJ. Opioid receptors modulate diverse types of calcium channels in the nucleus tractus solitarius of the rat. J Neurosci 14: 7608-7615, 1994.
59. Sanders RD, Brian D, Maze M. G-protein-coupled receptors. Handb Exp Pharmacol 93-117, 2008.
60. Smith DV, Li CS. Tonic GABAergic inhibition of taste-responsive neurons in the nucleus of the solitary tract. Chem Senses 23: 159-169, 1998.
61. Smith KS, Berridge KC. Opioid limbic circuit for reward: interaction between hedonic hotspots of nucleus accumbens and ventral pallidum. J Neurosci 27: 1594-1605, 2007.
62. Smith KS, Berridge KC. The ventral pallidum and hedonic reward: neurochemical maps of sucrose "liking" and food intake. J Neurosci 25: 8637-8649, 2005.
63. Sykes KT, White SR, Hurley RW, Mizoguchi H, Tseng LF, Hammond DL. Mechanisms responsible for the enhanced antinociceptive effects of micro-opioid receptor agonists in the rostral ventromedial medulla of male rats with persistent inflammatory pain. J Pharmacol Exp Ther 322: 813-821, 2007.
64. Taha SA, Katsuura Y, Noorvash D, Seroussi A, Fields HL. Convergent, not serial, striatal and pallidal circuits regulate opioid-induced food intake. Neuroscience 161: 718-733, 2009.
65. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467: 60-79, 2003.
66. Travers JB, Grill HJ, Norgren R. The effects of glossopharyngeal and chorda tympani nerve cuts on the ingestion and rejection of sapid stimuli: an electromyographic analysis in the rat. Behav Brain Res 25: 233-246, 1987.
67. Travers JB, Herman K, Travers SP. Suppression of third ventricular NPY-elicited feeding following medullary reticular formation infusions of muscimol. Behav Neurosci 124: 225-233, 2010.
68. Travers JB, Norgren R. Electromyographic analysis of the ingestion and rejection of sapid stimuli in the rat. Behav Neurosci 100: 544-555, 1986.
69. Travers JB, Travers SP. Microcircuitry of the rostral nucleus of the solitary tract. In: Handbook of Brain Microcircuits, p. 284-289, 2010.
70. Wang M, Bradley RM. Properties of GABAergic neurons in the rostral solitary tract nucleus in mice. J Neurophysiol 103: 3205-3218, 2010.
71. Ward HG, Simansky KJ. Chronic prevention of mu-opioid receptor (MOR) G-protein coupling in the pontine parabrachial nucleus persistently decreases consumption of standard but not palatable food. Psychopharmacology (Berl) 187: 435-446, 2006.
72. Will MJ, Franzblau EB, Kelley AE. Nucleus accumbens mu-opioids regulate intake of a high-fat diet via activation of a distributed brain network. J Neurosci 23: 2882-2888, 2003.
73. Wilson JD, Nicklous DM, Aloyo VJ, Simansky KJ. An orexigenic role for mu-opioid receptors in the lateral parabrachial nucleus. Am J Physiol Regul Integr Comp Physiol 285: R1055-R1065, 2003.
74. Zhang M, Gosnell BA, Kelley AE. Intake of high-fat food is selectively enhanced by mu opioid receptor stimulation within the nucleus accumbens. J Pharmacol Exp Ther 285: 908-914, 1998.
75. Zhang M, Kelley AE. Opiate agonists microinjected into the nucleus accumbens enhance sucrose drinking in rats. Psychopharmacology (Berl) 132: 350-360, 1997.
76. Zhu M, Cho YK, Li CS. Activation of delta-opioid receptors reduces excitatory input to putative gustatory cells within the nucleus of the solitary tract. J Neurophysiol 101: 258-268, 2009.