Noradrenergic modulation of risk/reward decision making

Psychopharmacology

Volumn 232, Issue 15, 2015, Pages 2681-2696

  Montes, David R ^a   Stopper, Colin M ^a   Floresco, Stan B ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Decision making; Noradrenaline; Probabilistic discounting; Rat; Risk; 2 Receptors

Indexed keywords

ALPHA 2A ADRENERGIC RECEPTOR; ATOMOXETINE; CLONIDINE; GUANFACINE; NORADRENALIN; YOHIMBINE; ALPHA 2 ADRENERGIC RECEPTOR BLOCKING AGENT; ALPHA 2 ADRENERGIC RECEPTOR STIMULATING AGENT;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR CHANGE; CONTROLLED STUDY; DECISION MAKING; DOPAMINERGIC TRANSMISSION; EXECUTIVE FUNCTION; MALE; NEGATIVE FEEDBACK; NEUROMODULATION; NEUROPHYSIOLOGY; NONHUMAN; NORADRENERGIC SYSTEM; PRIORITY JOURNAL; RAT; REWARD; SENSITIVITY ANALYSIS; ANIMAL; DRUG EFFECTS; HIGH RISK BEHAVIOR; INSTRUMENTAL CONDITIONING; LONG EVANS RAT; PROBABILITY; RISK;

ADRENERGIC ALPHA-2 RECEPTOR AGONISTS; ADRENERGIC ALPHA-2 RECEPTOR ANTAGONISTS; ANIMALS; BEHAVIOR, ANIMAL; CHOICE BEHAVIOR; CLONIDINE; CONDITIONING, OPERANT; DECISION MAKING; GUANFACINE; MALE; PROBABILITY; RATS; RATS, LONG-EVANS; REWARD; RISK; RISK-TAKING; YOHIMBINE;

EID: 84937735104     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-015-3904-3     Document Type: Article

References (71)

1. Abela AR, Chudasama Y (2014) Noradrenergic α2A-receptor stimulation in the ventral hippocampus reduces impulsive decision-making. Psychopharmacology (Berl) 231:521-531. doi: 10.1007/s00213-013-3262-y
2. Arnsten AFT (2011) Catecholamine influences on dorsolateral prefrontal cortical networks. Biol Psychiatry 69:e89-e99. doi: 10.1016/j.biopsych.2011.01.027
3. Arnsten AFT, Jin LE (2012) Guanfacine for the treatment of cognitive disorders: a century of discoveries at Yale. Yale J Biol Med 85:45-58
4. Arnsten AFT, Pliszka SR (2011) Catecholamine influences on prefrontal cortical function: relevance to treatment of attention deficit/hyperactivity disorder and related disorders. Pharmacol Biochem Behav 99:211-216. doi: 10.1016/j.pbb.2011.01.020
5. Arnsten AFT, Cai J, Goldman-Rakic PS (1988) The alpha-2 adrenergic agonist guanfacine improves memory in aged monkeys without sedative or hypotensive side effects: evidence for alpha-2 receptor subtypes. J Neurosci 8:4287-4298
6. Arnsten AF, Mathew R, Ubriani R et al (1999) Alpha-1 noradrenergic receptor stimulation impairs prefrontal cortical cognitive function. Biol Psychiatry 45:26-31
7. Arnsten AFT, Wang MJ, Paspalas CD (2012) Neuromodulation of thought: flexibilities and vulnerabilities in prefrontal cortical network synapses. Neuron 76:223-239. doi: 10.1016/j.neuron.2012.08.038
8. Aston-Jones G, Cohen JD (2005) An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci 28:403-450. doi: 10.1146/annurev.neuro.28.061604.135709
9. Avery RA, Franowicz JS, Studholme C et al (2000) The alpha-2A-adrenoceptor agonist, guanfacine, increases regional cerebral blood flow in dorsolateral prefrontal cortex of monkeys performing a spatial working memory task. Neuropsychopharmacology 23:240-249. doi: 10.1016/S0893-133X(00)00111-1
10. Baarendse PJJ, Winstanley CA, Vanderschuren LJMJ (2013) Simultaneous blockade of dopamine and noradrenaline reuptake promotes disadvantageous decision making in a rat gambling task. Psychopharmacology (Berl) 225:719-731. doi: 10.1007/s00213-012-2857-z
11. Bari A, Theobald DE, Caprioli D et al (2010) Serotonin modulates sensitivity to reward and negative feedback in a probabilistic reversal learning task in rats. Neuropsychopharmacology 35:1290-1301. doi: 10.1038/npp.2009.233
12. Birnbaum SG, Podell DM, Arnsten AFT (2000) Noradrenergic alpha-2 receptor agonists reverse working memory deficits induced by the anxiogenic drug, FG7142, in rats. Pharmacol Biochem Behav 67:397-403
13. Birnbaum SG, Yuan PX, Wang M et al (2004) Protein kinase C overactivity impairs prefrontal cortical regulation of working memory. Science 306:882-884. doi: 10.1126/science.1100021
14. Bukstein OG, Head J (2012) Guanfacine ER for the treatment of adolescent attention-deficit/hyperactivity disorder. Expert Opin Pharmacother 13:2207-2213. doi: 10.1517/14656566.2012.721778
15. Bymaster FP, Katner JS, Nelson DL et al (2002) Atomoxetine increases extracellular levels of norepinephrine and dopamine in prefrontal cortex of rat: a potential mechanism for efficacy in attention deficit/hyperactivity disorder. Neuropsychopharmacology 27:699-711. doi: 10.1016/S0893-133X(02)00346-9
16. Cardinal RN, Howes NJ (2005) Effects of lesions of the nucleus accumbens core on choice between small certain rewards and large uncertain rewards in rats. BMC Neurosci 6:37. doi: 10.1186/1471-2202-6-37
17. Cedarbaum JM, Aghajanian GK (1977) Catecholamine receptors on the locus coeruleus neurons: pharmacological characterization. Eur J Pharmacol 44:375-385
18. Crespi F (2009) Anxiolytics antagonize yohimbine-induced central noradrenergic activity: a concomitant in vivo voltammetry - electrophysiology model of anxiety. J Neurosci 180:97-105. doi: 10.1016/j.jneumeth.2009.03.007
19. Croxtall JD (2011) Clonidine extended-release in attention-deficit hyperactivity disorder. Adis Drug Profile 13:329-336
20. Devoto P, Flore G, Pani L, Gessa GL (2001) Evidence for co-release of noradrenaline and dopamine from noradrenergic neurons in the cerebral cortex. Mol Psychiatry 6:657-664. doi: 10.1038/sj.mp.4000904
21. Drew GM, Gower AJ, Marriott AS (1979) Alpha-2-adrenoceptors mediate clonidine-induced sedation in the rat. Br J Pharmacol 67:133-141
22. Engberg G, Eriksson E (1991) Effects of alpha 2-adrenoceptor agonists on locus coeruleus firing rate and brain noradrenaline turnover in N-ethoxycarbonyl-2-ethoxy-1,2-dihydroquinoline (EEDQ)-treated rats. Naunyn Schmiedebergs Arch Pharmacol 343:472-477
23. Fernando ABP, Economidou D, Theobald DE et al (2012) Modulation of high impulsivity and attentional performance in rats by selective direct and indirect dopaminergic and noradrenergic receptor agonists. Psychopharmacology (Berl) 219:341-352. doi: 10.1007/s00213-011-2408-z
24. Franowicz JS, Kessler LE, Borja CMD et al (2002) Mutation of the alpha2A-adrenoceptor impairs working memory performance and annuls cognitive enhancement by guanfacine. J Neurosci 22:8771-8777
25. Gamo NJ, Wang M, Arnsten AFT (2010) Methylphenidate and atomoxetine enhance prefrontal function through α2-adrenergic and dopamine D1 receptors. J Am Acad Child Adolesc Psychiatry 49:1011-1023. doi: 10.1016/j.jaac.2010.06.015
26. Georges F, Caillé S, Vouillac C et al (2005) Role of imidazoline receptors in the anti-aversive properties of clonidine during opiate withdrawal in rats. Eur J Neurosci 22:1812-1816. doi: 10.1111/j.1460-9568.2005.04356.x
27. Ghods-Sharifi S, St Onge JR, Floresco SB (2009) Fundamental contribution by the basolateral amygdala to different forms of decision making. J Neurosci 29:5251-5259. doi: 10.1523/JNEUROSCI. 0315-09.2009
28. Green L, Myerson J (2004) A discounting framework for choice with delayed and probabilistic rewards. Psychol Bull 130:769-792. doi: 10.1037/0033-2909.130.5.769
29. Holmberg G, Gershon S (1961) Autonomic and psychic effects of yohimbine hydrochloride. Psychopharmacologia 2:93-106
30. Jentsch JD, Anzivino LA (2004) A low dose of the alpha2 agonist clonidine ameliorates the visual attention and spatial working memory deficits produced by phencyclidine administration to rats. Psychopharmacology (Berl) 175:76-83. doi: 10.1007/s00213-004-1772-3
31. Ji X-H, Ji J-Z, Zhang H, Li B-M (2008) Stimulation of alpha2-adrenoceptors suppresses excitatory synaptic transmission in the medial prefrontal cortex of rat. Neuropsychopharmacology 33:2263-2271. doi: 10.1038/sj.npp.1301603
32. Jordan CJ, Harvey RC, Baskin BB et al (2014) Cocaine-seeking behavior in a genetic model of attention-deficit/hyperactivity disorder following adolescent methylphenidate or atomoxetine treatments. Drug Alcohol Depend 140:25-32. doi: 10.1016/j.drugalcdep.2014.04.020
33. Kim S, Bobeica I, Gamo NJ et al (2012) Effects of α-2A adrenergic receptor agonist on time and risk preference in primates. Psychopharmacology (Berl) 219:363-375. doi: 10.1007/s00213-011-2520-0
34. Li BM, Mao ZM, Wang M, Mei ZT (1999) Alpha-2 adrenergic modulation of prefrontal cortical neuronal activity related to spatial working memory in monkeys. Neuropsychopharmacology 21:601-610. doi: 10.1016/S0893-133X(99)00070-6
35. Mao ZM, Arnsten AF, Li BM (1999) Local infusion of an alpha-1 adrenergic agonist into the prefrontal cortex impairs spatial working memory performance in monkeys. Biol Psychiatry 46:1259-1265
36. Marrs W, Kuperman J, Avedian T et al (2005) Alpha-2 adrenoceptor activation inhibits phencyclidine-induced deficits of spatial working memory in rats. Neuropsychopharmacology 30:1500-1510. doi: 10.1038/sj.npp.1300700
37. Mendez IA, Gilbert RJ, Bizon JL, Setlow B (2012) Effects of acute administration of nicotinic and muscarinic cholinergic agonists and antagonists on performance in different cost-benefit decision making tasks in rats. Psychopharmacology (Berl) 224:489-499. doi: 10.1007/s00213-012-2777-y
38. Michelson D, Adler L, Spencer T et al (2003) Atomoxetine in adults with ADHD: two randomized, placebo-controlled studies. Biol Psychiatry 53:112-120. doi: 10.1016/S0006-3223(02)01671-2
39. Milstein JA, Lehmann O, Theobald DEH et al (2007) Selective depletion of cortical noradrenaline by anti-dopamine beta-hydroxylase-saporin impairs attentional function and enhances the effects of guanfacine in the rat. Psychopharmacology (Berl) 190:51-63. doi: 10.1007/s00213-006-0594-x
40. Newman LA, Darling J, McGaughy J (2008) Atomoxetine reverses attentional deficits produced by noradrenergic deafferentation of medial prefrontal cortex. Psychopharmacology (Berl) 200:39-50. doi: 10.1007/s00213-008-1097-8
41. Pardey MC, Kumar NN, Goodchild AK, Cornish JL (2013) Catecholamine receptors differentially mediate impulsive choice in the medial prefrontal and orbitofrontal cortex. J Psychopharmacol 27:203-212. doi: 10.1177/0269881112465497
42. Reis DJ, Piletz JE (1997) The imidazoline receptor in control of blood pressure by clonidine and allied drugs. Am J Physiol 273:1569-1571
43. Riba J, Krämer UM, Heldmann M et al (2008) Dopamine agonist increases risk taking but blunts reward-related brain activity. PLoS One 3:e2479. doi: 10.1371/journal.pone.0002479
44. Rivalan M, Valton V, Seriès P et al (2013) Elucidating poor decision-making in a rat gambling task. PLoS One 8:e82052. doi: 10.1371/journal.pone.0082052
45. Robbins TW, Arnsten AFT (2009) The neuropsychopharmacology of fronto-executive function: monoaminergic modulation. Annu Rev Neurosci 32:267-287. doi: 10.1146/annurev.neuro.051508.135535
46. Robert F, Bert L, Lambás-Señas L et al (1996) In vivo monitoring of extracellular noradrenaline and glutamate from rat brain cortex with 2-min microdialysis sampling using capillary electrophoresis with laser-induced fluorescence detection. J Neurosci Methods 70:153-162. doi: 10.1016/S0165-0270(96)00113-6
47. Robinson ESJ (2012) Blockade of noradrenaline re-uptake sites improves accuracy and impulse control in rats performing a five-choice serial reaction time tasks. Psychopharmacology (Berl) 219:303-312. doi: 10.1007/s00213-011-2420-3
48. Robinson ESJ, Eagle DM, Mar AC et al (2008) Similar effects of the selective noradrenaline reuptake inhibitor atomoxetine on three distinct forms of impulsivity in the rat. Neuropsychopharmacology 33:1028-1037. doi: 10.1038/sj.npp.1301487
49. Schwager AL, Haack AK, Taha SA (2014) Impaired flexibility in decision making in rats after administration of the pharmacological stressor yohimbine. Psychopharmacology (Berl). doi: 10.1007/s00213-014-3529-y
50. Simon NW, Montgomery KS, Beas BS et al (2011) Dopaminergic modulation of risky decision-making. J Neurosci 31:17460-17470. doi: 10.1523/JNEUROSCI. 3772-11.2011
51. Spencer T, Biederman J, Wilens T et al (1998) Effectiveness and tolerability of tomoxetine in adults with attention deficit hyperactivity disorder. Am J Psychiatry 155:693-695
52. Spyraki C, Fibiger HC (1982) Clonidine-induced sedation in rats: evidence for mediation by postsynaptic cr2-adrenoreceptors. J Neural Transm 163:153-163
53. St. Onge JR, Floresco SB (2009) Dopaminergic modulation of risk-based decision making. Neuropsychopharmacology 34:681-697. doi: 10.1038/npp.2008.121
54. St. Onge JR, Floresco SB (2010) Prefrontal cortical contribution to risk-based decision making. Cereb Cortex 20:1816-1828. doi: 10.1093/cercor/bhp250
55. St. Onge JR, Chiu YC, Floresco SB (2010) Differential effects of dopaminergic manipulations on risky choice. Psychopharmacology (Berl) 211:209-221. doi: 10.1007/s00213-010-1883-y
56. St. Onge JR, Abhari H, Floresco SB (2011) Dissociable contributions by prefrontal D1 and D2 receptors to risk-based decision making. J Neurosci 31:8625-8633. doi: 10.1523/JNEUROSCI. 1020-11.2011
57. St. Onge JR, Stopper CM, Zahm DS, Floresco SB (2012) Separate prefrontal-subcortical circuits mediate different components of risk-based decision making. J Neurosci 32:2886-2899. doi: 10.1523/JNEUROSCI. 5625-11.2012
58. Stopper CM, Floresco SB (2011) Contributions of the nucleus accumbens and its subregions to different aspects of risk-based decision making. Cogn Affect Behav Neurosci 11:97-112. doi: 10.3758/s13415-010-0015-9
59. Stopper CM, Floresco SB (2014) What's better for me? Fundamental role for lateral habenula in promoting subjective decision biases. Nat Neurosci 17:33-35. doi: 10.1038/nn.3587
60. Stopper CM, Khayambashi S, Floresco SB (2013) Receptor-specific modulation of risk-based decision making by nucleus accumbens dopamine. Neuropsychopharmacology 38:715-728. doi: 10.1038/npp.2012.240
61. Stopper CM, Green EB, Floresco SB (2014) Selective involvement by the medial orbitofrontal cortex in biasing risky, but not impulsive, choice. Cereb Cortex 24:154-162. doi: 10.1093/cercor/bhs297
62. Sun H, Green TA, Theobald DEH et al (2010) Yohimbine increases impulsivity through activation of cAMP response element binding in the orbitofrontal cortex. Biol Psychiatry 67:649-656. doi: 10.1016/j.biopsych.2009.11.030
63. Sun H, Cocker PJ, Zeeb FD, Winstanley CA (2012) Chronic atomoxetine treatment during adolescence decreases impulsive choice, but not impulsive action, in adult rats and alters markers of synaptic plasticity in the orbitofrontal cortex. Psychopharmacology (Berl) 219:285-301. doi: 10.1007/s00213-011-2419-9
64. Svensson TH, Bunney BS, Aghajanian GK (1975) Inhibition of both noradrenergic and serotonergic neurons in the brain by the alpha-adrenergic agonist clonidine. Brain Res 92:291-306
65. Takahashi H, Matsui H, Camerer C et al (2010) Dopamine D1 receptors and nonlinear probability weighting in risky choice. J Neurosci 30:16567-16572. doi: 10.1523/JNEUROSCI. 3933-10.2010
66. Tanda G, Bassareo V, Di Chiara G (1996) Mianserin markedly and selectively increases extracellular dopamine in the prefrontal cortex as compared to the nucleus accumbens of the rat. Psychopharmacology (Berl) 123:127-130
67. Umehara M, Ago Y, Fujita K et al (2013) Effects of serotonin-norepinephrine reuptake inhibitors on locomotion and prefrontal monoamine release in spontaneously hypertensive rats. Eur J Pharmacol 702:250-257. doi: 10.1016/j.ejphar.2013.01.033
68. Van Gaalen MM, van Koten R, Schoffelmeer ANM, Vanderschuren LJMJ (2006) Critical involvement of dopaminergic neurotransmission in impulsive decision making. Biol Psychiatry 60:66-73. doi: 10.1016/j.biopsych.2005.06.005
69. Wilhelm CJ, Mitchell SH (2008) Rats bred for high alcohol drinking are more sensitive to delayed and probabilistic outcomes. Genes Brain Behav 7:705-713. doi: 10.1111/j.1601-183X.2008.00406.x
70. Zeeb FD, Robbins TW, Winstanley CA (2009) Serotonergic and dopaminergic modulation of gambling behavior as assessed using a novel rat gambling task. Neuropsychopharmacology 34:2329-2343. doi: 10.1038/npp.2009.62
71. Zoratto F, Sinclair E, Manciocco A et al (2014) Individual differences in gambling proneness among rats and common marmosets: an automated choice task. Biomed Res Int 2014:927685