Methylphenidate and atomoxetine inhibit social play behavior through prefrontal and subcortical limbic mechanisms in rats

Journal of Neuroscience

Volumn 35, Issue 1, 2015, Pages 161-169

  Marijke Achterberg, E J ^a   Van Kerkhof, Linda W M ^b   Damsteegt, Ruth ^b   Trezza, Viviana ^c   Vanderschuren, Louk J M J ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c ROMA TRE UNIVERSITY   (Italy)

Author keywords

Amygdala; Habenula; Methylphenidate; Noradrenaline; Prefrontal cortex; Social play behavior

Indexed keywords

ATOMOXETINE; DIMETHYL SULFOXIDE; METHYLPHENIDATE; CENTRAL STIMULANT AGENT; PROPYLAMINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR CINGULATE; ARTICLE; BASOLATERAL AMYGDALA; BRAIN FUNCTION; BRAIN REGION; COGNITIVE DEVELOPMENT; CONTROLLED STUDY; EMOTION; EXECUTIVE FUNCTION; EXPERIMENTAL BEHAVIORAL TEST; HABENULA; HISTOPATHOLOGY; LIMBIC CORTEX; LOCOMOTION; MALE; NERVE CELL NETWORK; NEUROTRANSMISSION; NONHUMAN; NORADRENERGIC SYSTEM; PREFRONTAL CORTEX; RAT; SOCIAL INTERACTION; ANIMAL; DRUG EFFECTS; EXPLORATORY BEHAVIOR; HUMAN RELATION; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; LIMBIC SYSTEM; PHYSIOLOGY; RECREATION;

ANIMALS; ATOMOXETINE HYDROCHLORIDE; CENTRAL NERVOUS SYSTEM STIMULANTS; EXPLORATORY BEHAVIOR; INJECTIONS, INTRAVENTRICULAR; INTERPERSONAL RELATIONS; LIMBIC SYSTEM; MALE; METHYLPHENIDATE; PLAY AND PLAYTHINGS; PREFRONTAL CORTEX; PROPYLAMINES; RATS;

EID: 84920522820     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2945-14.2015     Document Type: Article

References (113)

1. Achterberg EJM, Trezza V, Vanderschuren LJMJ (2012) /3-Adrenoreceptor stimulation mediates reconsolidation of social reward-related memories. PLoS One 7:e39639.
2. Achterberg EJM, Trezza V, Siviy SM, Schrama L, Schoffelmeer ANM, Vanderschuren LJMJ (2014) Amphetamine and cocaine suppress social play behavior in rats through distinct mechanisms. Psychopharmacology 231:1503–1515.
3. Adolphs R (2003) Cognitive neuroscience of human social behaviour. Nat RevNeurosci 4:165–178.
4. Andersen SL (2005) Stimulants and the developing brain. Trends Pharmacol Sci 26:237–243.
5. Arnsten AF (2011) Catecholamine influences on dorsolateral prefrontal cortical networks. Biol Psychiatry 69:e89–e99.
6. Authier N, Dupuis E, Kwasiborski A, Eschalier A, Coudore F (2002) Behavioural assessment of dimethylsulfoxide neurotoxicity in rats. Toxicol Lett 132:117–121.
7. Baarendse PJJ, Counotte DS, O’Donnell P, Vanderschuren LJMJ (2013) Early social experience is critical for the development of cognitive control and dopamine modulation of prefrontal cortex function. Neuropsycho-pharmacology 38:1485–1494.
8. Baenninger LP (1967) Comparison of behavioural development in socially isolated and grouped rats. Anim Behav 15:312–323.
9. Bari A, Mar AC, Theobald DE, Elands SA, Oganya KC, Eagle DM, Robbins TW (2011) Prefrontal and monoaminergic contributions to stop-signal task performance in rats. J Neurosci 31:9254–9263.
10. Baxter MG, Murray EA (2002) The amygdala and reward. Nat Rev Neurosci 3:563–573.
11. Beatty WW, Dodge AM, Dodge LJ, White K, Panksepp J (1982) Psychomotor stimulants, social deprivation and play in juvenile rats. Pharmacol Biochem Behav 16:417–422.
12. Beatty WW, Costello KB, Berry SL (1984) Suppression of play fighting by amphetamine: effects of catecholamine antagonists, agonists and synthesis inhibitors. Pharmacol Biochem Behav 20:747–755.
13. Bell HC, McCaffrey DR, Forgie ML, Kolb B, Pellis SM (2009) The role of the medial prefrontal cortex in the play fighting of rats. Behav Neurosci 123: 1158–1168.
14. Berridge CW, Stratford TL, Foote SL, Kelley AE (1997) Distribution of dopamine beta-hydroxylase-like immunoreactive fibers within the shell subregion of the nucleus accumbens. Synapse 27:230–241.
15. Berridge KC, Kringelbach ML (2013) Neuroscience of affect: brain mechanisms of pleasure and displeasure. Curr Opin Neurobiol 23:294–303.
16. Blakemore SJ (2008) The social brain in adolescence. Nat Rev Neurosci 9:267–277.
17. Block AE, Dhanji H, Thompson-Tardif SF, Floresco SB (2007) Thalamic-prefrontal cortical-ventral striatal circuitry mediates dissociable components of strategy set shifting. Cereb Cortex 17:1625–1636.
18. Bolles RC, Woods PJ (1964) The ontogeny of behavior in the albino rat. Animal Behavior 12:427–441.
19. Buffalari DM, Grace AA (2007) Noradrenergic modulation of basolateral amygdala neuronal activity: opposing influences of alpha-2 and beta receptor activation. J Neurosci 27:12358–12366.
20. Cardinal RN, Parkinson JA, Hall J, Everitt BJ (2002) Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 26:321–352.
21. Cavaletti G, Oggioni N, Sala F, Pezzoni G, Cavalltti E, Marmiroli P, Petruc-cioli MG, Frattola L, Tredici G (2000) Effect on the peripheral nervous system of systemically administered dimethylsulfoxide in the rat: a neu-rophysiological and pathological study. Toxicol Lett 118:103–107.
22. Chamberlain SR, Sahakian BJ (2007) The neuropsychiatry of impulsivity. Curr Opin Psychiatry 20:255–261.
23. Chudasama Y, Bussey TJ, Muir JL (2001) Effects of selective thalamic and prelimbic cortex lesions on two types of visual discrimination and reversal learning. Eur J Neurosci 14:1009–1020.
24. Chudasama Y, Passetti F, Desai A, Rhodes SE, Lopian D, Robbins TW (2003) Dissociable aspects of performance on the 5-choice serial reaction time task following lesions of the dorsal anterior cingulate, infralimbic and orbitofrontal cortex in the rat: differential effects on selectivity, impulsiv-ity and compulsivity. Behav Brain Res 146:105–119.
25. Churchwell JC, Morris AM, Heurtelou NM, Kesner RP (2009) Interactions between the prefrontal cortex and amygdala during delay discounting and reversal. Behav Neurosci 123:1185–1196.
26. Daenen EW, Wolterink G, Gerrits MAFM, Van Ree JM (2002) The effects of neonatal lesions inthe amygdala or ventral hippocampus on social behavior later in life. Behav Brain Res 136:571–582.
27. Dalley JW, Cardinal RN, Robbins TW (2004) Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neuro-sci Biobehav Rev 28:771–784.
28. Del Campo N, Chamberlain SR, Sahakian BJ, Robbins TW (2011) The roles of dopamine and noradrenaline in the pathophysiology and treatment of attention-deficit/hyperactivity disorder. Biol Psychiatry 69:e145–e157.
29. Delfs JM, Zhu Y, Druhan JP, Aston-Jones GS (1998) Origin of noradrener-gic afferents to the shell subregion of the nucleus accumbens: anterograde and retrograde tract-tracing studies in the rat. Brain Res 806:127–140.
30. De Olmos JS, Beltramico CA, Alheid G (2004) Amygdala and extended amygdala of the rat: a cytoarchitectonical, fibroarchitectonical, and che-moarchitectonical survey. In: The rat nervous system (Paxinos G, ed), pp 509–603. San Diego: Elsevier Academic.
31. Eagle DM, Bari A, Robbins TW (2008) The neuropsychopharmacology of action inhibition: cross-species translation of the stop-signal and go/ no-go tasks. Psychopharmacology 199:439–456.
32. Economidou D, Theobald DE, Robbins TW, Everitt BJ, Dalley JW (2012) Norepinephrine and dopamine modulate impulsivity on the five-choice serial reaction time task through opponent actions in the shell and core sub-regions of the nucleus accumbens. Neuropsychopharmacology 37: 2057–2066.
33. Fagen R (1981) Animal play behavior. Oxford, Oxford UP.
34. Feldman HM, Reiff MI (2014) Clinical practice. Attention deficit-hyperactivity disorder in children and adolescents. N Engl J Med 370: 838–846.
35. Ferris RM, Tang FL (1979) Comparison of the effects of the isomers of amphetamine, methylphenidate and deoxypipradrol on the uptake of l-[3H]norepinephrine and [3H]dopamine by synaptic vesicles from rat whole brain, striatum and hypothalamus. JPharmacol Exp Ther 210:422–428.
36. Ferry B, Magistretti PJ, Pralong E (1997) Noradrenaline modulates glutamate-mediated neurotransmission inthe rat basolateral amygdala in vitro. Eur J Neurosci 9:1356–1364.
37. File SE, Seth P (2003) A review of 25 years of the social interaction test. Eur J Pharmacol 463:35–53.
38. Gottesfeld Z (1983) Origin and distributionof noradrenergic innervation in the habenula: a neurochemical study. Brain Res 275:299–304.
39. Gourley SL, Lee AS, Howell JL, Pittenger C, Taylor JR (2010) Dissociable regulation of instrumental action within mouse prefrontal cortex. Eur J Neurosci 32:1726–1734.
40. Graham KL, Burghardt GM (2010) Current perspectives on the biological study of play: signs of progress. Q Rev Biol 85:393–418.
41. Groenewegen HJ (1988) Organization of the afferent connections of the mediodorsal thalamic nucleus in the rat, related to the mediodorsal-prefrontal topography. Neuroscience 24:379–431.
42. Hikosaka O (2010) The habenula: from stress evasion to value-based decision-making. Nat Rev Neurosci 11:503–513.
43. Hoover WB, Vertes RP (2007) Anatomical analysisofafferent projections to the medial prefrontal cortex in the rat. Brain Struct Funct 212:149–179.
44. Jodo E, Chiang C, Aston-Jones G (1998) Potent excitatory influence of pre-frontal cortex activity on noradrenergic locus ceruleus neurons. Neuro-science 83:63–79.
45. Johnson LR, Hou M, Prager EM, Ledoux JE (2011) Regulation of the fear network by mediators of stress: norepinephrine alters the balance between cortical and subcortical afferent excitation of the lateral amygdala. Front Behav Neurosci 5:23.
46. Killcross S, Coutureau E (2003) Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb Cortex 13:400–408.
47. Kratochvil CJ, Wilens TE, Greenhill LL, Gao H, Baker KD, Feldman PD, Gelowitz DL (2006) Effects of long-term atomoxetine treatment for young children with attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 45:919–927.
48. Kutcher S, Aman M, Brooks SJ, Buitelaar J, van Daalen E, Fegert J, Findling RL, Fisman S, Greenhill LL, Huss M, Kusumakar V, Pine D, Taylor E, Tyano S (2004) International consensus statement on attention-deficit/ hyperactivity disorder (ADHD) and disruptive behavior disorders (DBDs): clinical implications and treatment practice suggestions. Eur Neuropsychopharmacol 14:11–28.
49. Lecourtier L, Kelly PH (2005) Bilateral lesions of the habenula induce atten-tional disturbances in rats. Neuropsychopharmacology 30:484–496.
50. Lecourtier L, Kelly PH (2007) A conductor hidden in the orchestra? Role of the habenular complex in monoamine transmission and cognition. Neu-rosci Biobehav Rev 31:658–672.
51. McAlonan GM, Robbins TW, Everitt BJ (1993) Effects of medial dorsal tha-lamic and ventral pallidal lesions on the acquisitionof a conditioned place preference: further evidence for the involvement of the ventral striatopal-lidal system in reward-related processes. Neuroscience 52:605–620.
52. McGaughy J, Ross RS, Eichenbaum H (2008) Noradrenergic, but not cho-linergic, deafferentation of prefrontal cortex impairs attentional set-shifting. Neuroscience 153:63–71.
53. Meaney MJ, Dodge AM, Beatty WW (1981) Sex-dependent effects of amygdaloid lesionsonthe social play ofprepubertal rats. Physiol Behav 26:467–472.
54. Miller EK, Cohen JD (2001) An integrative theory ofprefrontal cortex function. Annu Rev Neurosci 24:167–202.
55. Moore RY, Bloom FE (1979) Central catecholamine neuron systems: anatomy and physiology of the norepinephrine and epinephrine systems. Annu Rev Neurosci 2:113–168.
56. Morón JA, Brockington A, Wise RA, Rocha BA, Hope BT (2002) Dopamine uptake through the norepinephrine transporter in brain regions with low levelsof the dopamine transporter: evidence from knock-out mouse lines. J Neurosci 22:389–395.
57. Morrison SE, Salzman CD (2010) Re-valuing the amygdala. Curr Opin Neurobiol 20:221–230.
58. Newman LA, Darling J, McGaughy J (2008) Atomoxetine reverses atten-tional deficits produced by noradrenergic deafferentation of medial pre-frontal cortex. Psychopharmacology 200:39–50.
59. Panksepp J, Beatty WW (1980) Social deprivation and play in rats. Behav Neural Biol 30:197–206.
60. Panksepp J, Siviy S, Normansell L (1984) The psychobiology of play: theoretical and methodological perspectives. Neurosci Biobehav Rev 8:465–492.
61. Panksepp J, Normansell L, Cox JF, Siviy SM (1994) Effects of neonatal de-cortication on the social play of juvenile rats. Physiol Behav 56:429–443.
62. Pattij T, Vanderschuren LJMJ (2008) The neuropharmacology of impulsive behavior. Trends Pharmacol Sci 29:192–199.
63. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates. London, Academic.
64. Pellis SM, McKenna MM (1992) Intrinsic and extrinsic influences on play fighting in rats: effects of dominance, partner’s playfulness, temperament and neonatal exposure to testosterone propionate. Behav Brain Res 50: 135–145.
65. Pellis SM, Pellis VC (1987) Play-fighting differs from serious fighting in both target of attack and tactics of fighting in the laboratory rat Rattus norvegicus. Aggressive Behavior 13:227–242.
66. Pellis SM, Pellis VC (1998) Play fighting of rats in comparative perspective: a schema for neurobehavioral analyses. Neurosci Biobehav Rev 23:87–101.
67. Pellis SM, Pellis VC (2009) The playful brain. Oxford: OneWorld Publications.
68. Pellis SM, Pellis VC, Dewsbury DA (1989) Different levels of complexity in the play-fighting by muroid rodents appear to result from different levels of intensity of attack and defense. Aggressive Behavior 15:297–310.
69. Pellis SM, Hastings E, Shimizu T, Kamitakahara H, Komorowska J, Forgie ML, Kolb B (2006) The effects of orbital frontal cortex damage on the modulationofdefensive responsesbyrats inplayful and nonplayful social contexts. Behav Neurosci 120:72–84.
70. Peters J, Kalivas PW, Quirk GJ (2009) Extinction circuits for fear and addiction overlap in prefrontal cortex. Learn Mem 16:279–288.
71. Phelps EA, LeDoux JE (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48:175–187.
72. Pitkänen A (2000) Connectivity of the rat amygdaloid complex. In: The amygdala: a functional analysis (Aggleton JP, ed). pp 32–115. Oxford, OUP.
73. Poole TB, Fish J (1975) Investigation of playful behavior in Rattus norvegi-cus and Mus musculus (Mammalia). Journal of Zoology 175:61–71.
74. Porrino LJ, Lucignani G (1987) Different patterns of local brain energy metabolism associated with high and low doses of methylphenidate: relevance to its action in hyperactive children. Biol Psychiatry 22:126–138.
75. Radley JJ, Williams B, Sawchenko PE (2008) Noradrenergic innervation of the dorsal medial prefrontal cortex modulates hypothalamo-pituitary-adrenal responses to acute emotional stress. J Neurosci 28:5806–5816.
76. Rilling JK, King-Casas B, Sanfey AG (2008) The neurobiology of social decision-making. Curr Opin Neurobiol 18:159–165.
77. Ritz MC, Lamb RJ, Goldberg SR, Kuhar MJ (1987) Cocaine receptors on dopamine transporters are related to self-administration of cocaine. Science 237:1219–1223.
78. Robbins TW, Arnsten AF (2009) The neuropsychopharmacology of fronto-executive function: monoaminergic modulation. Annu Rev Neurosci 32: 267–287.
79. Roozendaal B, McEwen BS, Chattarji S (2009) Stress, memory and the amygdala. Nat Rev Neurosci 10:423–433.
80. Sah P, Faber ES, Lopez De Armentia M, Power J (2003) The amygdaloid complex: anatomy and physiology. Physiol Rev 83:803–834.
81. Schneider M, Koch M (2005) Deficient social and play behavior in juvenile and adult rats after neonatal cortical lesion: effects of chronic pubertal cannabinoid treatment. Neuropsychopharmacology 30:944–957.
82. Schoenbaum G, Setlow B, Nugent SL, Saddoris MP, Gallagher M (2003) Lesions of orbitofrontal cortex and basolateral amygdala complex disrupt acquisition of odor-guided discriminations and reversals. Learn Mem 10:129–140.
83. Schoenbaum G, Roesch MR, Stalnaker TA, Takahashi YK (2009) A new perspective on the role of the orbitofrontal cortex in adaptive behaviour. Nat Rev Neurosci 10:885–892.
84. Shin LM, Liberzon I (2010) The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 35:169–191.
85. Siviy SM, Panksepp J (1985) Dorsomedial diencephalic involvement in the juvenile play of rats. Behav Neurosci 99:1103–1113.
86. Siviy SM, Panksepp J (2011) In search of the neurobiological substrates for social playfulness inmammalian brains. Neurosci Biobehav Rev 35:1821–1830.
87. Špinka M, Newberry RC, Bekoff M (2001) Mammalian play: training for the unexpected. Q Rev Biol 76:141–168.
88. Sutton ME, Raskin LA (1986) A behavioral analysis ofthe effects of amphetamine on play and locomotor activity in the post-weaning rat. Pharmacol Biochem Behav 24:455–461.
89. Tait DS, Brown VJ, Farovik A, Theobald DE, Dalley JW, Robbins TW (2007) Lesions of the dorsal noradrenergic bundle impair attentional set-shifting in the rat. Eur J Neurosci 25:3719–3724.
90. Tanda G, Pontieri FE, Frau R, Di Chiara G (1997) Contribution of blockade of the noradrenaline carrier to the increase of extracellular dopamine in the rat prefrontal cortex by amphetamine and cocaine. Eur J Neurosci 9:2077–2085.
91. Thor DH, Holloway WR Jr (1983) Play soliciting in juvenile male rats: effects of caffeine, amphetamine and methylphenidate. Pharmacol Biochem Behav 19:725–727.
92. Trezza V, Vanderschuren LJMJ (2008) Cannabinoid and opioid modulation of social play behavior in adolescent rats: differential behavioral mechanisms. Eur Neuropsychopharmacol 18:519–530.
93. Trezza V, Baarendse PJJ, Vanderschuren LJMJ (2009a) Prosocial effects of nicotine and ethanol in adolescent rats through partially dissociable neu-robehavioral mechanisms. Neuropsychopharmacology 34:2560–2573.
94. Trezza V, Damsteegt R, Vanderschuren LJMJ (2009b) Conditioned place-preference induced by social play behavior: parametrics, extinction, reinstatement and disruption by methylphenidate. Eur Neuropsychopharmacol 19: 659–669.
95. Trezza V, Baarendse PJJ, Vanderschuren LJMJ (2010) The pleasures of play: pharmacological insights into social reward mechanisms. Trends Pharmacol Sci 31:463–469.
96. Trezza V, Damsteegt R, Achterberg EJM, Vanderschuren LJMJ (2011a) Nucleus accumbens mu-opioid receptors mediate social reward. J Neurosci 31:6362–6370.
97. Trezza V, Campolongo P, Vanderschuren LJMJ (2011b) Evaluating the rewarding nature of social interactions in laboratory animals. Dev Cogn Neurosci 1:444–458.
98. Trezza V, Damsteegt R, Manduca A, Petrosino S, van Kerkhof LWM, Pas-terkamp RJ, Zhou Y, Campolongo P, Cuomo V, Di Marzo V, Vander-schuren LJMJ (2012) Endocannabinoids in amygdala and nucleus accumbens mediate social play reward in adolescent rats. J Neurosci 32: 14899–14908.
99. Tye KM, Tye LD, Cone JJ, Hekkelman EF, Janak PH, Bonci A (2010) Meth-ylphenidate facilitates learning-induced amygdala plasticity. Nat Neuro-sci 13:475–481.
100. Unnerstall JR, Kopajtic TA, Kuhar MJ (1984) Distribution of alpha 2 agonist binding sites in the rat and human central nervous system: analysis of some functional, anatomic correlates of the pharmacologic effects of clo-nidine and related adrenergic agents. Brain Res 319:69–101.
101. van Kerkhof LWM, Achterberg EJM, Lesscher HMB, Trezza V, Vander-schuren LJMJ (2012) Dissociating the rewarding and motivational properties of social play behaviorin adolescent rats: the roleof dopamine, opioids and endocannabinoids. Soc Neurosci Abs 295.06.
102. van Kerkhof LWM, Damsteegt R, Trezza V, Voorn P, Vanderschuren LJMJ (2013a) Social play behavior in adolescent rats is mediated by functional activity in medial prefrontal cortex and striatum. Neuropsychopharma-cology 38:1899–1909.
103. van Kerkhof LWM, Damsteegt R, Trezza V, Voorn P, Vanderschuren LJMJ (2013b) Functional integrity of the habenula is necessary for social play behavior in adolescent rats. Eur J Neurosci 38:3465–3475.
104. van Kerkhof LWM, Trezza V, Mulder T, Gao P, Voorn P, Vanderschuren LJMJ (2014) Cellular activation in limbic brain systems during social play behaviour in rats. Brain Struct Funct 219:1181–1211.
105. Vanderschuren LJMJ (2010) How the brain makes play fun. American Journal of Play 2:315–337.
106. Vanderschuren LJMJ, Trezza V (2014) What the laboratory rat has taught us about social play behavior: role in behavioral development and neural mechanisms. Curr Top Behav Neurosci 16:189–212.
107. Vanderschuren LJMJ, Spruijt BM, Hol T, Niesink RJM, Van Ree JM (1995) Sequential analysis of social play behavior in juvenile rats: effects of morphine. Behav Brain Res 72:89–95.
108. Vanderschuren LJMJ, Niesink RJM, Van Ree JM (1997) The neurobiology of social play behavior in rats. Neurosci Biobehav Rev 21:309–326.
109. Vanderschuren LJMJ, Trezza V, Griffioen-Roose S, Schiepers OJ, Van Leeu-wen N, De Vries TJ, Schoffelmeer ANM (2008) Methylphenidate disrupts social play behavior in adolescent rats. Neuropsychopharmacology 33:2946–2956.
110. Veeneman MMJ, Boleij H, Broekhoven MH, Snoeren EMS, Guitart Masip M, Cousijn J, Spooren W, Vanderschuren LJMJ (2011) Dissociable roles of mGlu5 and dopamine receptors in the rewarding and sensitizing properties of morphine and cocaine. Psychopharmacology 214:863–876.
111. Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32–58.
112. Yamamoto BK, Novotney S (1998) Regulation of extracellular dopamine by the norepinephrine transporter. J Neurochem 71:274–280.
113. Zheng X, Liu F, Wu X, Li B (2008) Infusion of methylphenidate into the basolateral nucleus of amygdala or anterior cingulate cortex enhances fear memory consolidation in rats. Sci China C Life Sci 51:808–813.