Anhedonia, avolition, and anticipatory deficits: Assessments in animals with relevance to the negative symptoms of schizophrenia

European Neuropsychopharmacology

Volumn 24, Issue 5, 2014, Pages 744-758

  Barnes, Samuel A ^a   Der Avakian, Andre ^a   Markou, Athina ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Animal models; Brain reward; Contrast effects; Effort related choice; ICSS; Sucrose preference

Indexed keywords

ANHEDONIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTICIPATORY DEFECIT; ARTICLE; AVOLITION; BEHAVIOR DISORDER; BLUNTED AFFECT; BRAIN DEPTH STIMULATION; CLINICAL ASSESSMENT; CONDITIONING; LOCOMOTION; NEGATIVE SYNDROME; NONHUMAN; PRIORITY JOURNAL; PSYCHOSOCIAL WITHDRAWAL; REINFORCEMENT; REWARD; SCHIZOPHRENIA; SELF STIMULATION; SUCROSE PREFERENCE TEST; SYMPTOMATOLOGY; ANIMAL; ANTICIPATION; DISEASE MODEL; HUMAN; MOTIVATION; NEUROPSYCHOLOGICAL TEST; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY;

ANHEDONIA; ANIMALS; ANTICIPATION, PSYCHOLOGICAL; DISEASE MODELS, ANIMAL; HUMANS; MOTIVATION; NEUROPSYCHOLOGICAL TESTS; REWARD; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY;

EID: 84899804721     PISSN: 0924977X     EISSN: 18737862     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2013.10.001     Document Type: Article

References (119)

1. Aberman J.E., Salamone J.D. Nucleus accumbens dopamine depletions make rats more sensitive to high ratio requirements but do not impair primary food reinforcement. Neuroscience 1999, 92:545-552.
2. Allison D.B., Mentore J.L., Heo M., Chandler L.P., Cappelleri J.C., Infante M.C., Weiden P.J. Antipsychotic-induced weight gain: a comprehensive research synthesis. Am. J. Psychiatry 1999, 156:1686-1696.
3. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders 2013, American Psychiatric Association, Washington DC. 5th ed.
4. Arnold J.M., Roberts D.C.S. A critique of fixed and progressive ratio schedules used to examine the neural substrates of drug reinforcement. Pharmacol. Biochem. Behav. 1997, 57:441-447.
5. Baird J.P., Turgeon S., Wallman A., Hulick V. Behavioral processes mediating phencyclidine-induced decreases in voluntary sucrose consumption. Pharmacol. Biochem. Behav. 2008, 88:272-279.
6. Barbano M.F., Cador M. Differential regulation of the consummatory, motivational and anticipatory aspects of feeding behavior by dopaminergic and opioidergic drugs. Neuropsychopharmacology 2005, 31:1371-1381.
7. Barch D.M., Dowd E.C. Goal representations and motivational drive in schizophrenia: the role of prefrontal-striatal interactions. Schizophr. Bull. 2010, 36:919-934.
8. Bardgett M.E., Depenbrock M., Downs N., Points M., Green L. Dopamine modulates effort-based decision making in rats. Behav. Neurosci. 2009, 123:242-251.
9. Barr A.M., Fiorino D.F., Phillips A.G. Effects of withdrawal from an escalating dose schedule of d-amphetamine on sexual behavior in the male rat. Pharmacol. Biochem. Behav. 1999, 64:597-604.
10. Barr A.M., Markou A. Psychostimulant withdrawal as an inducing condition in animal models of depression. Neurosci. Biobehav. Rev. 2005, 29:675-706.
11. Barr A.M., Markou A., Phillips A.G. A "crash" course on psychostimulant withdrawal as a model of depression. Trends Pharmacol. Sci. 2002, 23:475-482.
12. Barr A.M., Phillips A.G. 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.
13. Barr A.M., Phillips A.G. Increased successive negative contrast in rats withdrawn from an escalating-dose schedule of d-amphetamine. Pharmacol. Biochem. Behav. 2002, 71:293-299.
14. Bedford J.A., Bailey L.P., Wilson M.C. Cocaine reinforced progressive ratio performance in the rhesus monkey. Pharmacol. Biochem. Behav. 1978, 9:631-638.
15. Beninger R., Gerdjikov T. Dopamine-glutamate interaction in reward-related incentive learning. Dopamine and Glutamate in Psychiatric Disorders 2005, Humana Press, Totowa. W. Schmidt, M.A. Reith (Eds.).
16. Bergner C.L., Smolinsky A.N., Hart P.C., Dufour B.D., Egan R.J., Laporte J.L., Kalueff A.V. Mouse models for studying depression-like states and antidepressant drugs. Methods Mol. Biol. 2010, 602:267-282.
17. Berlin I., Givry-Steiner L., Lecrubier Y., Puech A.J. Measures of anhedonia and hedonic responses to sucrose in depressive and schizophrenic patients in comparison with healthy subjects. Eur. Psychiatry 1998, 13:303-309.
18. Berridge K.C. Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns. Neurosci. Biobehav. Rev. 2000, 24:173-198.
19. Berridge K.C., Robinson T.E. Parsing reward. Trends Neurosci. 2003, 26:507-513.
20. Bleuer E. Textbook of Psychiatry 1924, Macmillan, New York.
21. Botvinick M.M., Huffstetler S., McGuire J.T. Effort discounting in human nucleus accumbens. Cogn. Affect. Behav. Neurosci. 2009, 9:16-27.
22. Brebion G., Bressan R.A., Pilowsky L.S., Davis A.S. Depression, avolition, and attention disorders in patients with schizophrenia: associations with verbal memory efficiency. J. Neuropsychiatry Clin. Neurosci. 2009, 21:206-215.
23. Brody S.A., Dulawa S.C., Conquet F., Geyer M.A. Assessment of a prepulse inhibition deficit in a mutant mouse lacking mGlu5 receptors. Mol. Psychiatry 2004, 9:35-41.
24. Campbell K.A., Evans G., Gallistel C.R. A microcomputer-based method for physiologically interpretable measurement of the rewarding efficacy of brain stimulation. Physiol. Behav. 1985, 35:395-403.
25. Carlezon W.A., Chartoff E.H. Intracranial self-stimulation (ICSS) in rodents to study the neurobiology of motivation. Nat. Protoc. 2007, 2:2987-2995.
26. Carroll M.E., Kohl E.A., Johnson K.M., Lanasa R.M. Increased impulsive choice for saccharin during PCP withdrawal in female monkeys: influence of menstrual cycle phase. Psychopharmacology (Berl.) 2013, 227:413-424.
27. Cassens G., Actor C., Cling M., Schildkraut J.J. Amphetamine withdrawal: effects on threshold of intracranial reinforcement. Psychopharmacology 1981, 73:318-322.
28. Cocker P.J., Hosking J.G., Benoit J., Winstanley C.A. Sensitivity to cognitive effort mediates psychostimulant effects on a novel rodent cost/benefit decision-making task. Neuropsychopharmacology 2012, 37:1825-1837.
29. Cousins M.S., Atherton A., Turner L., Salamone J.D. Nucleus accumbens dopamine depletions alter relative response allocation in a T-maze cost/benefit task. Behav. Brain Res. 1996, 74:189-197.
30. Crespi L.P. Quantitative variation of incentive and performance in the white rat. Am. J. Psychol. 1942, 55:467-517.
31. Croxson P.L., Walton M.E., O'Reilly J.X., Behrens T.E., Rushworth M.F. Effort-based cost-benefit valuation and the human brain. J. Neurosci. 2009, 29:4531-4541.
32. Der-Avakian A., Markou A. Withdrawal from chronic exposure to amphetamine, but not nicotine, leads to an immediate and enduring deficit in motivated behavior without affecting social interaction in rats. Behav. Pharmacol. 2010, 21:359-368.
33. Der-Avakian A., Markou A. The neurobiology of anhedonia and other reward-related deficits. Trends Neurosci. 2012, 35:68-77.
34. Dowd E.C., Barch D.M. Pavlovian reward prediction and receipt in schizophrenia: relationship to anhedonia. PloS One 2012, 7:e35622.
35. 2 receptors impairs operant motivation and interval timing. J. Neurosci. 2007, 27:7731-7739.
36. Ellenbroek B.A., Cools A.R. Animal models for the negative symptoms of schizophrenia. Behav. Pharmacol. 2000, 11:223-233.
37. Elliott M.H. The Effect of Change of Reward on the Maze Performance of Rats 1928, University of California Press, Berkeley.
38. Esposito R., Kornetsky C. Morphine lowering of self-stimulation thresholds: lack of tolerance with long-term administration. Science 1977, 195:189-191.
39. Flaherty C. Incentive contrast: a review of behavioral changes following shifts in reward. Anim. Learn. Behav. 1982, 10:409-440.
40. Flaherty C.F. Incentive Relativity 1996, Cambridge University Press, Cambridge.
41. Floresco S.B., Onge J.R.S., Ghods-Sharifi S., Winstanley C.A. Cortico-limbic-striatal circuits subserving different forms of cost-benefit decision making. Cogn. Affect. Behav. Neurosci. 2008, 8:375-389.
42. Foussias G., Remington G. Negative symptoms in schizophrenia: avolition and Occam's razor. Schizophr. Bull. 2010, 36:359-369.
43. Gallistel C.R., Freyd G. Quantitative determination of the effects of catecholaminergic agonists and antagonists on the rewarding efficacy of brain stimulation. Pharmacol. Biochem. Behav. 1987, 26:731-741.
44. Gard D.E., Kring A.M., Gard M.G., Horan W.P., Green M.F. Anhedonia in schizophrenia: distinctions between anticipatory and consummatory pleasure. Schizophr. Res. 2007, 93:253-260.
45. Geyer M.A., Markou A. Animal models of psychiatric disorders. Psychopharmacology: The Fourth Generation of Progress 1995, 787-798. Raven Press, New York. F.E. Bloom, D.J. Kupfer (Eds.).
46. Gold J.M., Waltz J.A., Prentice K.J., Morris S.E., Heerey E.A. Reward processing in schizophrenia: a deficit in the representation of value. Schizophr. Bull. 2008, 34:835-847.
47. Gold J.M, Strauss G.P., Waltz J.A., Robinson B.M., Brown J.K., Frank M.J. Negative symptoms of schizophrenia are associated with abnormal effort-cost computations. Biol. Psychiatry 2013, 74:130-136.
48. 2-family receptors. Neurobiol. Learn. Mem. 2009, 92:243-248.
49. Heerey E.A., Gold J.M. Patients with schizophrenia demonstrate dissociation between affective experience and motivated behavior. J. Abnorm. Psychol. 2007, 116:268-278.
50. Ho B.C., Nopoulos P., Flaum M., Arndt S., Andreasen N.C. Two-year outcome in first-episode schizophrenia: predictive value of symptoms for quality of life. Am. J. Psychiatry 1998, 155:1196-1201.
51. Hodos W. Progressive ratio as a measure of reward strength. Science 1961, 134:943-944.
52. Horan W.P., Kring A.M., Blanchard J.J. Anhedonia in schizophrenia: a review of assessment strategies. Schizophr. Bull. 2006, 32:259-273.
53. Howes O.D., Kapur S. The dopamine hypothesis of schizophrenia: version III. The final common pathway. Schizophr. Bull. 2009, 35:549-562.
54. Hsu C.T., Patton D.F., Mistlberger R.E., Steele A.D. Palatable meal anticipation in mice. PloS One 2010, 5:e12903.
55. Hyman S.E., Fenton W.S. Medicine: what are the right targets for psychopharmacology?. Science 2003, 299:350-351.
56. Izquierdo A., Belcher A.M. Rodent models of adaptive decision making. Methods Mol. Biol. 2012, 829:85-101.
57. Jenkins T.A., Harte M.K., Reynolds G.P. Effect of subchronic phencyclidine administration on sucrose preference and hippocampal parvalbumin immunoreactivity in the rat. Neurosci. Lett. 2010, 471:144-147.
58. Jentsch J.D., Redmond D.E., Elsworth J.D., Taylor J.R., Youngren K.D., Roth R.H. Enduring cognitive deficits and cortical dopamine dysfunction in monkeys after long-term administration of phencyclidine. Science 1997, 277:953-955.
59. Jentsch J.D., Tran A., Le D., Youngren K.D., Roth R.H. Subchronic phencyclidine administration reduces mesoprefrontal dopamine utilization and impairs prefrontal cortical-dependent cognition in the rat. Neuropsychopharmacology 1997, 17:92-99.
60. Jentsch J.D., Taylor J.R., Roth R.H. Subchronic phencyclidine administration increases mesolimbic dopaminergic system responsivity and augments stress- and psychostimulant-induced hyperlocomotion. Neuropsychopharmacology 1998, 19:105-113.
61. Jentsch J.D., Roth R.H. The neuropsychopharmacology of phencyclidine: from NMDA receptor hypofunction to the dopamine hypothesis of schizophrenia. Neuropsychopharmacology 1999, 20(3):201-225.
62. 2 receptors in the striatum causes persistent abnormalities in prefrontal cortex functioning. Neuron 2006, 49:603-615.
63. Kirkpatrick B., Fenton W.S., Carpenter W.T., Marder S.R. The NIMH-MATRICS consensus statement on negative symptoms. Schizophr. Bull. 2006, 32:214-219.
64. Kornetsky C., Esposito R.U. Euphorigenic drugs: effects on the reward pathways of the brain. Fed. Proc. 1979, 38:2473-2476.
65. Kraepelin E. Dementia praecox and paraphrenia. J. Nerv. Ment. Dis. 1921, 54:384.
66. Leith N., Barrett R. Amphetamine and the reward system: evidence for tolerance and post-drug depression. Psychopharmacologia 1976, 46:19-25.
67. Liebman J.M. Discriminating between reward and performance: a critical review of intracranial self-stimulation methodology. Neurosci. Biobehav. Rev. 1983, 7:45-72.
68. Lipska B.K., Aultman J.M., Verma A., Weinberger D.R., Moghaddam B. Neonatal damage of the ventral hippocampus impairs working memory in the rat. Neuropsychopharmacology 2002, 27:47-54.
69. Lodge D.J., Grace A.A. Aberrant hippocampal activity underlies the dopamine dysregulation in an animal model of schizophrenia. J. Neurosci. 2007, 27:11424-11430.
70. Markou A., Chiamulera C., Geyer M.A., Tricklebank M., Steckler T. Removing obstacles in neuroscience drug discovery: the future path for animal models. Neuropsychopharmacology 2009, 34:74-89.
71. Markou A., Koob G.F. Postcocaine anhedonia: an animal model of cocaine withdrawal. Neuropsychopharmacology 1991, 4:17-26.
72. Markou A., Koob G.F. Construct validity of a self-stimulation threshold paradigm: effects of reward and performance manipulations. Physiol. Behav. 1992, 51:111-119.
73. Markou A., Koob G.F. Intracranial self-stimulation thresholds as a measure of reward. Behavioural Neuroscience: A Practical Approach 1993, vol. 2:93-115. IRL Press, Oxford.
74. Mendelson S.D., Pfaus J.G. Level searching: a new assay of sexual motivation in the male rat. Physiol. Behav. 1989, 45:337-341.
75. Mendoza J., Angeles-Castellanos M., Escobar C. Entrainment by a palatable meal induces food-anticipatory activity and c-Fos expression in reward-related areas of the brain. Neuroscience 2005, 133:293-303.
76. Morris B.J., Cochran S.M., Pratt J.A. PCP: from pharmacology to modelling schizophrenia. Curr. Opin. Pharmacol. 2005, 5:101-106.
77. Murray G.A., Cheng F., Clark L., Barnett J.H., Blackwell A.D., Fletcher P.C., Robbins T.W., Bullmore E.T., Jones P.B. Reinforcement and reversal learning in first-episode psychosis. Schizophr. Bull. 2008, 34:848-855.
78. Muscat R., Kyprianou T., Osman M., Phillips G., Willner P. Sweetness-dependent facilitation of sucrose drinking by raclopride is unrelated to calorie content. Pharmacol. Biochem. Behav. 1991, 40:209-213.
79. Muscat R., Willner P. Effects of dopamine receptor antagonists on sucrose consumption and preference. Psychopharmacology 1989, 99:98-102.
80. Neill J.C., Barnes S., Cook S., Grayson B., Idris N.F., McLean S.L., Snigdha S., Rajagopal L., Harte M.K. Animal models of cognitive dysfunction and negative symptoms of schizophrenia: focus on NMDA receptor antagonism. Pharmacol. Ther. 2010, 128:419-432.
81. O'Tuathaigh C.M.P., Waddington J.L. Mutant mouse models: phenotypic relationships to domains of psychopathology and pathobiology in schizophrenia. Schizophr. Bull. 2010, 36:243-245.
82. Olds J., Milner P. Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. J. Comp. Physiol. Psychol. 1954, 47:419-427.
83. Olney J.W., Newcomer J.W., Farber N.B. NMDA receptor hypofunction model of schizophrenia. J. Psychiatr. Res. 1999, 33:523-533.
84. Overstreet D.H. Modeling depression in animal models. Psychiatric Disorders: Methods and Protocols. In: Methods in Molecular Biology 2012, vol. 829:125-144. Humana Press, New York.
85. Paterson N., Markou A. The metabotropic glutamate receptor 5 antagonist MPEP decreased break points for nicotine, cocaine and food in rats. Psychopharmacology 2005, 179:255-261.
86. Paterson N.E., Myers C., Markou A. Effects of repeated withdrawal from continuous amphetamine administration on brain reward function in rats. Psychopharmacology 2000, 152:440-446.
87. Pellegrini S., Mustaca A. Consummatory successive negative contrast with solid food. Learn. Motiv. 2000, 31:200-209.
88. Pfaus J.G., Phillips A.G. Role of dopamine in anticipatory and consummatory aspects of sexual behavior in the male rat. Behav. Neurosci. 1991, 105:727-743.
89. Pratt J.A., Winchester C., Egerton A., Cochran S.M., Morris B.J. Modelling prefrontal cortex deficits in schizophrenia: implications for treatment. Br. J. Pharmacol. 2008, 153(Suppl. 1):S465-S470.
90. Reynolds G.S., Limpo A.J. Negative contrast after prolonged discrimination maintenance. Psychonom. Sci. 1968, 10:323-324.
91. Richardson N.R., Roberts D.C.S. Progressive ratio schedules in drug self-administration studies in rats: a method to evaluate reinforcing efficacy. J. Neurosci. Methods 1996, 66:1-11.
92. Roane H.S. On the applied use of progressive-ratio schedules of reinforcement. J. Appl. Behav. Anal. 2008, 41:155-161.
93. Roberts D.S., Richardson N. Self-administration of psychomotor stimulants using progressive ratio schedules of reinforcement. Animal Models of Drug Addiction. In: Neuromethods 1993, vol. 24:233-269. Humana Press, Totawa NJ.
94. Rodriguiz R.M., Chu R., Caron M.G., Wetsel W.C. Aberrant responses in social interaction of dopamine transporter knockout mice. Behav. Brain Res. 2004, 148:185-198.
95. Rummel C., Kissling W., Leucht S. Antidepressants for the negative symptoms of schizophrenia. Cochrane Database Syst. Rev. 2006, 3:CD005581.
96. Salamone J.D. Dopamine, effort, and decision making: theoretical comment on Bardgett et al. (2009). Behav. Neurosci. 2009, 123:463-467.
97. Salamone J.D., Correa M., Farrar A., Mingote S.M. Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits. Psychopharmacology 2007, 191:461-482.
98. Salamone J.D., Correa M., Mingote S., Weber S.M. Nucleus accumbens dopamine and the regulation of effort in food-seeking behavior: implications for studies of natural motivation, psychiatry, and drug abuse. J. Pharmacol. Exp. Ther. 2003, 305:1-8.
99. Salamone J.D., Cousins M.S., Bucher S. Anhedonia or anergia? Effects of haloperidol and nucleus accumbens dopamine depletion on instrumental response selection in a T-maze cost/benefit procedure. Behav. Brain Res. 1994, 65:221-229.
100. Salamone J.D., Cousins M.S., Snyder B.J. Behavioral functions of nucleus accumbens dopamine: empirical and conceptual problems with the anhedonia hypothesis. Neurosci. Biobehav. Rev. 1997, 21:341-359.
101. Salamone J.D., Steinpreis R.E., McCullough L.D., Smith P., Grebel D., Mahan K. Haloperidol and nucleus accumbens dopamine depletion suppress lever pressing for food but increase free food consumption in a novel food choice procedure. Psychopharmacology 1991, 104:515-521.
102. Simpson E.H., Kellendonk C., Ward R.D., Richards V., Lipatova O., Fairhurst S., Kandel E.R., Balsam P.D. Pharmacologic rescue of motivational deficit in an animal model of the negative symptoms of schizophrenia. Biol. Psychiatry 2011, 69:928-935.
103. Simpson E.H., Waltz J.A., Kellendonk C., Balsam P.D. Schizophrenia in translation: dissecting motivation in schizophrenia and rodents. Schizophr. Bull. 2012, 38:1111-1117.
104. Spielewoy C., Markou A. Withdrawal from chronic phencyclidine treatment induces long-lasting depression in brain reward function. Neuropsychopharmacology 2003, 28:1106-1116.
105. Stefurak T.L., Van Der Kooy D. Saccharin's rewarding, conditioned reinforcing, and memory-improving properties: mediation by isomorphic or independent processes?. Behav. Neurosci. 1992, 106:125-139.
106. Stoker A.K., Markou A. The intracranial self-stimulation procedure provides quantitative measures of brain reward function. Mood and Anxiety Related Phenotypes in Mice: Characterization Using Behavioral Tests, Volume II. In: Neuromethods 2011, vol. 63:307-331. Humana Press, New York.
107. Strauss G.P., Gold J.M. A new perspective on anhedonia in schizophrenia. Am. J. Psychiatry 2012, 169:364-373.
108. Strekalova T., Spanagel R., Bartsch D., Henn F.A., Gass P. Stress-induced anhedonia in mice is associated with deficits in forced swimming and exploration. Neuropsychopharmacology 2004, 29:2007-2017.
109. 1-like dopamine receptors. Psychopharmacology 1999, 144:95-110.
110. Turgeon S.M., Hoge S.G. Prior exposure to phencyclidine decreases voluntary sucrose consumption and operant performance for food reward. Pharmacol. Biochem. Behav. 2003, 76:393-400.
111. Vacca G., Phillips A.G. Inhibition of successive positive contrast in rats withdrawn from an escalating dose schedule of d-amphetamine. Int. J. Comp. Psychol. 2005, 18:298-306.
112. Vlachou S., Markou A. Intracranial self-stimulation. Animal Models of Drug Addiction. In: Neuromethods 2010, vol. 53:3-56. Humana Press, New York.
113. Vogel J.R., Mikulka P.J., Spear N.E. Effects of shifts in sucrose and saccharine concentrations on licking behavior in the rat. J. Comp. Physiol. Psychol. 1968, 66:661-666.
114. Wang C., McInnis J., Ross-Sanchez M., Shinnick-Gallagher P., Wiley J.L., Johnson K.M. Long-term behavioral and neurodegenerative effects of perinatal phencyclidine administration: implications for schizophrenia. Neuroscience 2001, 107:535-550.
115. Ward R.D., Simpson E.H., Richards V.L., Deo G., Taylor K., Glendinning J.I., Kandel E.R., Balsam P.D. Dissociation of hedonic reaction to reward and incentive motivation in an animal model of the negative symptoms of schizophrenia. Neuropsychopharmacology 2012, 37:1699-1707.
116. Willner P., Towell A., Sampson D., Sophokleous S., Muscat R. Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology 1987, 93:358-364.
117. Young J.W., Powell S.B., Risbrough V., Marston H.M., Geyer M.A. Using the MATRICS to guide development of a preclinical cognitive test battery for research in schizophrenia. Pharmacol. Ther. 2009, 122:150-202.
118. 1 receptors?. Biol. Psychiatry 2010, 67:784-787.
119. Young J.W., Meves J., Tarantino I., Caldwell S., Geyer M.A. Delayed procedural learning in α7-nicotinic acetylcholine receptor knockout mice. Genes Brain Behav. 2011, 10:720-733.