Effect of orexin-B-saporin-induced lesions of the lateral hypothalamus on performance on a progressive ratio schedule

Journal of Psychopharmacology

Volumn 26, Issue 6, 2012, Pages 871-886

  Olarte Sanchez C M ^a   Valencia Torres, L ^a   Body, S ^a   Cassaday, H J ^a   Bradshaw, C M ^a   Szabadi, E ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Incentive value; motor performance; operant behaviour; orexin saporin; orexins; progressive ratio schedule

Indexed keywords

OREXIN 2 RECEPTOR; OREXIN B; SAPORIN;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BRAIN DAMAGE; CONTROLLED STUDY; FEMALE; FOOD INTAKE; INSTRUMENTAL CONDITIONING; LATERAL HYPOTHALAMUS; LOCOMOTION; MENTAL CAPACITY; MENTAL PERFORMANCE; MOTIVATION; MOTOR PERFORMANCE; NEUROTRANSMISSION; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; REINFORCEMENT;

ANIMALS; BEHAVIOR, ANIMAL; BODY WEIGHT; CONDITIONING, OPERANT; EATING; FEMALE; HYPOTHALAMIC AREA, LATERAL; HYPOTHALAMUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MOTIVATION; MOTOR ACTIVITY; NEURONS; NEUROPEPTIDES; PERFORMANCE-ENHANCING SUBSTANCES; PSYCHOMOTOR PERFORMANCE; RATS; RATS, WISTAR; REINFORCEMENT (PSYCHOLOGY); REINFORCEMENT SCHEDULE; RIBOSOME INACTIVATING PROTEINS, TYPE 1;

EID: 84862132693     PISSN: 02698811     EISSN: 14617285     Source Type: Journal    
DOI: 10.1177/0269881111409607     Document Type: Article

References (93)

1. Aberman JE, Ward SJ, Salamone JD. Effects of dopamine antagonists and accumbens dopamine depletions on time-constrained progressive-ratio performance. Pharmacol Biochem Behav. 1998 ; 61: 341-348
2. Akbari E, Motamedi F, Naghdi N, Noorbakhshina M. The effect of antagonization of orexin 1 receptors in CA1 and dentate gyrus regions on memory processing in passive avoidance task. Behav Brain Res. 2008 ; 187: 172-177
3. Akbari E, Naghdi N, Motamedi F. functional inactivation of orexin 1 receptors in CA1 region impairs acquisition, consolidation and retrieval in Morris water maze task. Behav Brain Res. 2006 ; 173: 47-52
4. Anaclet C, Parmentier R, Ouk K, Guidon G, Buda C, Sastre J-P, et al. Orexin/hypocretin and histamine: distinct roles in the control of wakefulness demonstrated using knock-out mouse models. J Neurosci. 2009 ; 29: 14423-14438
5. Anaclet C, Pedersen NP, Fuller PM, Lu J. Brainstem circuitry regulating phasic activation of trigeminal motoneurones during REM sleep. PLoS ONE. 2010 ; 5: e8788
6. Arnold JM, Roberts DCS. A critique of fixed and progressive ratio schedules used to examine the neural substrates of drug reinforcement. Pharmacol Biochem Behav. 1997 ; 57: 441-447
7. Aston-Jones G, Smith RJ, Moorman DE, Richardson KA. Role of lateral hypothalamic orexin neurons in reward processing and addiction. Neuropharmacology. 2009 ; 56: 112-121
8. Barr AM, Phillips AG. Withdrawal following repeated exposure to d-amphetamine decreases responding for a sucrose solution as measured by a progressive ratio schedule of reinforcement. Psychopharmacology. 1999 ; 141: 99-106
9. Berridge CW, Espana RA, Vittoz NM. Hypocretin/orexin in arousal and stress. Brain Res. 2010 ; 1314: 91-102
10. Bezzina G, Body S, Cheung THC, Hampson CL, Deakin JFW, Anderson IM, et al. Effect of quinolinic acid-induced lesions of the nucleus accumbens core on performance on a progressive ratio schedule of reinforcement: implications for inter-temporal choice. Psychopharmacology. 2008a ; 197: 339-350
11. Bezzina G, Cheung THC, Asgari K, Hampson CL, Body S, Bradshaw CM, et al. Effects of quinolinic acid-induced lesions of the nucleus accumbens core on inter-temporal choice: a quantitative analysis. Psychopharmacology. 2007 ; 195: 71-84
12. Bezzina G, den Boon FS, Hampson CL, Cheung THC, Body S, Bradshaw CM, et al. Effect of quinolinic acid-induced lesions of the subthalamic nucleus on performance on a progressive-ratio schedule of reinforcement: a quantitative analysis. Behav Brain Res. 2008b ; 195: 223-230
13. Bizo LA, Killeen PR. Models of ratio schedule performance. J Exp Psychol: Anim Behav Proc. 1997 ; 23: 351-367
14. Bizo LA, Kettle LC, Killeen PR. Rats don't always respond faster for more food. Anim Learn Behav. 2001 ; 29: 66-78
15. Blanco-Centurion C, Gerashchenko D, Salin-Pascual RJ, Shiromani PJ. Effect of hypocretin2-saporin and antidopamine-ββ-hydroxylase-saporin neurotoxic lesions of the dorsolateral pons on sleep and muscle tone. Eur J Neurosci. 2004 ; 19: 2741-2752
16. Blanco-Centurion C, Gerashchenko D, Shiromani PJ. Effect of saporin-induced lesions of three arousal populations on daily levels of sleep and wake. J Neurosci. 2007 ; 27: 14041-14048
17. Borgland SL, Chang SJ, Bowers MS, Thompson JL, Vittoz N, Floresco SB, et al. Orexin A/hypocretin-1 selectively promotes motivation for positive reinforcers. J Neurosci. 2009 ; 29: 11215-11225
18. Bowman EM, Brown VJ. Effects of excitotoxic lesions of the rat ventral striatum on the perception of reward cost. Exp Brain Res. 1998 ; 123: 439-448
19. Cason AM, Smith RJ, Tahsili-Fahadan P, Moorman DE, Sartor GC, Aston-Jones G. Role of orexin/hypocretin in reward-seeking and addiction: Implications for obesity. Physiol Behav. 2010 ; 100: 419-428
20. Cheeta S, Brooks S, Willner P. Effects of reinforcer sweetness and the D2/D3 antagonist raclopride on progressive ratio operant performance. Behav Pharmacol. 1995 ; 6: 127-132
21. Choi DL, Davis JF, Fitzgerald ME, Benoit SC. The role of orexin-A in food motivation, reward-based feeding behavior and food-induced neuronal activation in rats. Neuroscience. 2010 ; 167: 11-20
22. Clegg DJ, Air EL, Woods SC, Seeley RJ. Eating elicited by orexin-A, but not melanin-concentrating hormone, is opioid mediated. Endocrinology. 2002 ; 143: 2995-3000
23. Cummings DE, Purnell JQ, Frayo RS, Schmidova K, Wisse BE, Weigle DS. A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes. 2001 ; 50: 1714-1719
24. Date Y, Ueta Y, Yamashita H, Yamaguchi H, Matsukura S, Kangawa K, et al. Orexins, orexigenic hypothalamic peptides, interact with autonomic, neuroendocrine and neuroregulatory systems. Proc Natl Acad Sci U S A. 1999 ; 96: 748-753
25. De Lecea L, Sutcliffe JG. The hypocretins/orexins: novel hypothalamic neuropeptides involved in different physiological systems. Cell Mol Life Sci. 1999 ; 56: 473-480
26. De Lecea L, Kilduff TS, Peyron C, Gao X, Foye PE, Danielson PE, et al. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci U S A. 1998 ; 95: 322-327
27. De Wit S, Barker RA, Cickinson A, Cools R. Habitual versus goal-directed action control in Parkinson's disease. J Cogn Neurosci. 2010 ; 23: 1218-1229
28. Di Sebastiano AR, Yong-Yow S, Wagner L, Lehman MN, Coolen LM. Orexin mediates initiation of sexual behavior in sexually naive male rats, but is not critical for sexual performance. Horm Behav. 2010 ; 58: 397-404
29. Di Sebastiano AR, Wilson-Pérez HE, Lehman MN, Coolen LM. Lesions of orexin neurons block conditioned place preference for sexual behavior in male rats. Horm Behav. 2011 ; 59: 1-8
30. Dickinson A. Actions and habits: The development of behavioural autonomy. Phil Trans Roy Soc Lond Series B Biol Sci. 1985 ; 308: 67-78
31. Dube MG, Kalra SP, Kalra PS. Food intake elicited by central administration of orexins/hypocretins: identification of hypothalamic sites of action. Brain Res. 1999 ; 842: 473-477
32. Farr SA, Banks WA, Kumar VB, Morley JE. Orexin-A-induced feeding is dependent on nitric oxide. Peptides. 2005 ; 26: 759-765
33. Frederick-Duus D, Guyton MF, Fadel J. Food-elicited increases in cortical acetylcholine release require orexin transmission. Neuroscience. 2007 ; 149: 499-507
34. Furlong T, Carrive P. Neurotoxic lesions centered on the perifornical hypothalamus abolish the cardiovascular and behavioral responses of conditioned fear to context but not of restraint. Brain Res. 2007 ; 1128: 107-119
35. Gerard C, Mollereau C, Vassart G, Parmentier M. Nucleotide sequence of a human cannabinoid receptor cDNA. Nucleic Acids Res. 1990 ; 18: 7142
36. Gerashchenko D, Blanco-Centurion C, Greco MA, Shiromani PJ. Effects of lateral hypothalamic lesion with the neurotoxin hypocretin-2-saporin on sleep in Long-Evans rats. Neuroscience. 2003 ; 116: 223-235
37. Gerashchenko D, Blanco-Centurion C, Miller JD, Shiromani PJ. Insomnia following hypocretin2-saporin lesions of the substantia nigra. Neuroscience. 2006 ; 137: 29-36
38. Gerashchenko D, Kohls MD, Greco M, Waleh NS, Salin-Pascual R, Kilduff TS, et al. Hypocretin-2-saporin lesions of the lateral hypothalamus produce narcoleptic-like sleep behavior in the rat. J Neurosci. 2001 ; 21: 7273-7283
39. Hara J, Beuckmann CT, Nambu T, Willie JT, Chemelli RM, Sinton CM, et al. Genetic ablation of orexin neurons in mice results in narcolepsy, hypophagia, and obesity. Neuron. 2001 ; 30: 345-354
40. Harris GC, Aston-Jones G. Arousal and reward: a dichotomy in orexin function. Trends Neurosci. 2006 ; 29: 571-577
41. Harris GC, Wimmer M, Aston-Jones G. A role for lateral hypothalamic orexin neurons in reward seeking. Nature. 2005 ; 437: 556-559
42. Harris GC, Wimmer M, Ransall-Thompson J, Aston-Jones G. Lateral hypothalamic orexin neurons are critically involved in learning to associate an environment with morphine reward. Behav Brain Res. 2007 ; 183: 43-51
43. Ho M-Y, Body S, Kheramin S, Bradshaw CM, Szabadi E. Effects of 8-OH-DPAT and WAY-100635 on performance on a time-constrained progressive-ratio schedule. Psychopharmacology. 2003 ; 167: 137-144
44. Hodos W. Progressive ratio as a measure of reward strength. Science. 1961 ; 134: 943-944
45. Hodos W, Kalman G. Effects of increment size and reinforcer volume on progressive ratio performance. J Exp Anal Behav. 1963 ; 6: 387-392
46. Ida T, Nakahara K, Katayama T, Murakami N, Nakazato M. Effect of lateral cerebroventricular injection of the appetite-stimulating neuropeptide, orexin and neuropeptide Y, on the various behavioral activities of rats. Brain Res. 1999 ; 821: 526-529
47. Jones DNC, Gartlon J, Parker F, Taylor SG, Routledge C, Hemmati P, et al. Effects of centrally administered orexin-B and orexin-A: o role for orexin-1 receptors in orexin-B-induced hyperactivity. Psychopharmacology. 2001 ; 153: 210-218
48. Jongen-Relo AL, Feldon J. Specific neuronal protein: a new tool for histological evaluation of excitotoxic lesions. Physiol Behav. 2002 ; 76: 449-456
49. Kheramin S, Body S, Miranda Herrera F, Bradshaw CM, Szabadi E, et al. The effect of orbital prefrontal cortex lesions on performance on a progressive ratio schedule: implications for models of inter-temporal choice. Behav Brain Res. 2005 ; 156: 145-152
50. Killeen PR. Mathematical principles of reinforcement. Behav Brain Sci. 1994 ; 17: 105-172
51. Killeen PR, Sitomer MT. MPR. Behav Proc. 2003 ; 62: 49-64
52. Killeen PR, Posadas-Sanchez D, Johansen EB, Thrailkill EA. Progressive ratio schedules of reinforcement. J Exp Psychol: Anim Behav Proc. 2009 ; 35: 35-50
53. Kiyashchenko LI, Mileykovskiy BY, Lai YY, Siegel JM. Increased and decreased muscle tone with orexin (hypocretin) microinjections in the locus coeruleus and pontine inhibitory area. J Neurophysiol. 2001 ; 85: 2008-2016
54. Luo T, Leung LS. Endogenous histamine facilitates long-term potentiation in the hippocampus during walking. J Neurosci. 2010 ; 30: 7845-7852
55. Meister B. Neurotransmitters in key neurons of the hypothalamus that regulate feeding behavior and body weight. Physiol Behav. 2007 ; 92: 263-271
56. Miles FJ, Everitt BJ, Dickinson A. Oral cocaine seeking by rats: action or habit?. Behav Neurosci. 2003 ; 117: 927-938
57. Mistlberger RE, Antle MC, Kilduff TS, Jones M. Food- and light-entrained circadian rhythms in rats with hypoicretin-2-saporin ablations on the lateral hypothalamus. Brain Res. 2003 ; 980: 161-168
58. Mobini S, Chiang T-J, Ho M-Y, Bradshaw CM, Szabadi E. Comparison of the effects of clozapine, haloperidol, chlorpromazine and d-amphetamine on performance on a time-constrained progressive ratio schedule and on locomotor behaviour in the rat. Psychopharmacology. 2000 ; 152: 47-54
59. Narita M, Nagumo Y, Hashimoto S, Naritya M, Khotib J, Miyatake M, et al. Direct involvement of orexinergic systems in the activation of the mesolimbic dopamine pathways and related behaviors induced by morphine. J Neurosci. 2006 ; 26: 398-405
60. Nair SG, Golden SA, Shaham Y. Differential effects of the hypocretin 1 receptor antagonist SB 334867 on high-fat food self-administration and reinstatement of food seeking in rats. Br J Pharmacol. 2008 ; 154: 406-416
61. Ocampo-Garces A, Ibáñez F, Pedermo P, Torrealba F. Orexin-B-saporin lesions in the lateral hypothalamus enhance photic masking of rapid eye movement sleep in the albino rat. J Sleep Res. 2011 ; 20: 3-11
62. Paxinos G, Watson C The rat brain in stereotaxic coordinates. San Diego: Academic Press ; 1998 :
63. Peyron C, Tighe DK, van den Pol AN, de Lecea L, Heller HC, Sutcliffe JG, et al. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci. 1998 ; 18: 9996-10015
64. Ping-Teng C, Lee ES, Konz SA, Richardson NR, Roberts DCS. Progressive ratio schedules in drug self-administration studies in rats: A method to evaluate reinforcing efficacy. J Neurosci Meth. 1996 ; 66: 1-11
65. Pinheiro JC, Bates DM Mixed-effects models in S and S-plus. New York: Springer ; 2004 :
66. Piper DC, Upton N, Smith MI, Hunter AJ. The novel brain neuropeptide, orexin-A, modulates the sleep-wake cycle of rats. Eur J Neurosci. 2000 ; 12: 726-730
67. Reilly MP. Extending mathematical principles of reinforcement into the domain of behavioral pharmacology. Behav Proc. 2003 ; 62: 75-88
68. Rickard JF, Body S, Zhang Z, Bradshaw CM, Szabadi E. Effect of reinforcer magnitude on performance maintained by progressive-ratio schedules. J Exp Anal Behav. 2009 ; 91: 75-87
69. Roberts DCS, Richardson NR Neuromethods Vol 24, Animal Models of Drug Addiction. Boulton A Baker G Wu PH, ed. New York: Humana ; 1992: 233-269.
70. Rowland NE, Mukherjee M, Robertson K. Effects of the cannabinoid receptor antagonist SR 141716, alone and in combination with dexfenfluramine or naloxone, on food intake in rats. Psychopharmacology. 2001 ; 159: 111-116
71. Sakurai T. Orexins and orexin receptors: implication in feeding behavior. Regul Pept. 1999 ; 85: 25-30
72. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, et al. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell. 1998 ; 92: 573-585
73. Saper CB, Scammell TE, Lu J. Hypothalamic regulation of sleep and circadian rhythms. Nature. 2005 ; 437: 1257-1263
74. Sharf R, Sarhan M, Brayton CE, Guarnieri DJ, Taylor JR, Dileone RJ. Orexin signaling via the orexin 1 receptor mediates operant responding for food reinforcement. Biol Psychiatry. 2010 ; 67: 753-760
75. Siegel JM. Hypocretin (orexin): role in normal behavior and neuropathology. Ann Rev Psychol. 2004 ; 55: 125-148
76. Siegel JM The Orexin/Hypocretin System: Physiology and Pathophysiology. Nishino S Sakurai T, ed. Humana Press ; 2005 :
77. Skjoldager P, Pierre PJ, Mittleman G. Reinforcer magnitude and progressive ratio responding in the rat: Effects of increased effort, prefeeding, and extinction. Learn Motiv. 1993 ; 24: 303-343
78. Smith HR, Pang KCH. Orexin-saporin lesions of the medial septum impair spatial memory. Neuroscience. 2005 ; 132: 261-271
79. Stafford D, Branch MN. Effects of step size and break-point criterion on progressive-ratio performance. J Exp Anal Behav. 1998 ; 70: 123-138
80. Stewart J. Pathways to relapse: the neurobiology of drug- and stress-induced relapse of drug-taking. J Psychiat Neurosci. 2000 ; 25: 125-136
81. Sweet DS, Levine AS, Billington CJ, Kotz CM. Feeding response to central orexins. Brain Res. 1999 ; 821: 535-538
82. Takakusaki K. Forebrain control of locomotor behaviors. Brain Res Rev. 2008 ; 57: 192-198
83. Thorpe AJ, Kotz CM. Orexin A in the nucleus accumbens stimulates feeding and locomotor activity. Brain Res. 2005 ; 1050: 156-162
84. Thorpe AJ, Cleary JP, Levine AS, Kotz CM. Centrally administered orexin A increases motivation for sweet pellets in rats. Psychopharmacology. 2005 ; 182: 75-83
85. Thorpe AJ, Doane DF, Sweet DC, Beverly JL, Kotz CM. Orexin A in the rostrolateral hypothalamic area induces feeding by modulating GABAergic transmission. Brain Res. 2006 ; 1125: 60-66
86. Torterolo P, Yamuy J, Sampogna S, Morales FR, Chase MH. Hypocretinergic neurons are primarily involved in activation of the somatomotor system. Sleep. 2003 ; 26: 25-28
87. Trivedi P, Yu H, MacNeil DJ, Van der Ploeg LH, Guan XM. Distribution of orexin receptor mRNA in the rat brain. FEBS Lett. 1998 ; 438: 71-75
88. Vetrivelan R, Fuller PM, Tong Q, Lu J. Medullary circuitry regulating rapid eye movement sleep and motor atonia. J Neurosci. 2009 ; 29: 9361-9369
89. Wu MF, John J, Maidment N, Lam HA, Siegel JM. Hypocretin release in normal and narcoleptic dogs after food and sleep deprivation, eating, and movement. Am J Physiol: Regul Integr Comp Physiol. 2002 ; 283: R1079 - R1086
90. Yamanaka A, Beuckmann CT, Willie JT, Hara J, Tsujino N, Mieda M, et al. Hypothalamic orexin neurons regulate arousal according to energy balance in mice. Neuron. 2003 ; 38: 701-713
91. Zhang Z, Rickard JF, Asgari K, Body S, Bradshaw CM, Szabadi E. Quantitative analysis of the effects of some "atypical" and "conventional" antipsychotics on progressive ratio schedule performance. Psychopharmacology. 2005a ; 179: 489-497
92. Zhang Z, Rickard JF, Body S, Asgari K, Bradshaw CM, Szabadi E. Comparison of the effects of clozapine and 8-hydroxy-2-(di-n-propylamino)tetralin (8-OH-DPAT) on progressive ratio schedule performance: evidence against the involvement of 5-HT1A receptors in the behavioural effects of clozapine. Psychopharmacology. 2005b ; 181: 381-391
93. Zheng H, Patterson LM, Berthoud HR. Orexin signaling in the ventral tegmental area is required for high-fat appetite induced by opioid stimulation of the nucleus accumbens. J Neurosci. 2007 ; 27: 11075-11082