Genetic deletion of PDE10A selectively impairs incentive salience attribution and decreases medium spiny neuron excitability

Behavioural Brain Research

Volumn 268, Issue , 2014, Pages 48-54

  Piccart, Elisabeth ^a   De Backer, Jean François ^b   Gall, David ^b   Lambot, Laurie ^b   Raes, Adam ^a   Vanhoof, Greet ^c   Schiffmann, Serge ^b   D'Hooge, Rudi ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^c JANSSEN RESEARCH FOUNDATION   (Belgium)

Author keywords

Incentive salience; Medium spiny neurons; PDE10A; Schizophrenia; Striatum

Indexed keywords

PHOSPHODIESTERASE; PHOSPHODIESTERASE 10A; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; PDE10A PROTEIN, MOUSE;

ACTION POTENTIAL; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONDITIONED TASTE AVERSION; CONTROLLED STUDY; GENE DELETION; LATENT INHIBITION; MALE; MEDIUM SPINY NEURON; MOUSE; NERVE CELL; NERVE EXCITABILITY; NERVOUS SYSTEM FUNCTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PREPULSE INHIBITION; PRIORITY JOURNAL; SALIENCE ATTRIBUTION; STARTLE REFLEX; ANIMAL; ASSOCIATION; ATTENTION; AVOIDANCE BEHAVIOR; C57BL MOUSE; CONDITIONING; DEFICIENCY; GENETICS; INHIBITION (PSYCHOLOGY); KNOCKOUT MOUSE; NEUROPSYCHOLOGICAL TEST; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; REINFORCEMENT; REWARD; TASTE;

ACTION POTENTIALS; ANIMALS; ATTENTION; AVOIDANCE LEARNING; CONDITIONING (PSYCHOLOGY); CUES; GABAERGIC NEURONS; INHIBITION (PSYCHOLOGY); MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUROPSYCHOLOGICAL TESTS; PATCH-CLAMP TECHNIQUES; PHOSPHORIC DIESTER HYDROLASES; PREPULSE INHIBITION; REINFORCEMENT (PSYCHOLOGY); REWARD; TASTE PERCEPTION;

EID: 84898928806     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2014.03.016     Document Type: Article

References (56)

1. Graybiel A.M. The basal ganglia. Curr Biol 2000, 10:R509-R511.
2. Packard M.G., Knowlton B.J. Learning and memory functions of the Basal Ganglia. Annu Rev Neurosci 2002, 25:563-593.
3. Kreitzer A.C., Malenka R.C. Striatal plasticity and basal ganglia circuit function. Neuron 2008, 60:543-554.
4. Joel D. Open interconnected model of basal ganglia-thalamocortical circuitry and its relevance to the clinical syndrome of Huntington's disease. Mov Disord 2001, 16:407-423.
5. Kawaguchi Y. Neostriatal cell subtypes and their functional roles. Neurosci Res 1997, 27:1-8.
6. Kreitzer A.C. Physiology and pharmacology of striatal neurons. Annu Rev Neurosci 2009, 32:127-147.
7. Gerfen C.R. Synaptic organization of the striatum. J Electron Microsc Tech 1988, 10:265-281.
8. Calabresi P., Pisani A., Centonze D., Bernardi G. Synaptic plasticity and physiological interactions between dopamine and glutamate in the striatum. Neurosci Biobehav Rev 1997, 21:519-523.
9. Surmeier D.J., Ding J., Day M., Wang Z., Shen W. D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci 2007, 30:228-235.
10. Horvitz J.C. Dopamine gating of glutamatergic sensorimotor and incentive motivational input signals to the striatum. Behav Brain Res 2002, 137:65-74.
11. Calabresi P., Mercuri N., Stanzione P., Stefani A., Bernardi G. Intracellular studies on the dopamine-induced firing inhibition of neostriatal neurons in vitro: evidence for D1 receptor involvement. Neuroscience 1987, 20:757-771.
12. Schiffmann S.N., Lledo P.M., Vincent J.D. Dopamine D1 receptor modulates the voltage-gated sodium current in rat striatal neurones through a protein kinase A. J Physiol 1995, 483(Pt 1):95-107.
13. Levine M.S., Altemus K.L., Cepeda C., Cromwell H.C., Crawford C., Ariano M.A., et al. Modulatory actions of dopamine on NMDA receptor-mediated responses are reduced in D1A-deficient mutant mice. J Neurosci 1996, 16:5870-5882.
14. Levine M.S., Cepeda C. Dopamine modulation of responses mediated by excitatory amino acids in the neostriatum. Adv Pharmacol 1998, 42:724-729.
15. Robinson T.E., Berridge K.C. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 1993, 18:247-291.
16. Toates F. Models and theories of motivation. Motivational systems. Problems in the behavioural sciences 1986, vol. 4. Cambridge University Press.
17. Mahler S.V., Berridge K.C. Which cue to "want?" Central amygdala opioid activation enhances and focuses incentive salience on a prepotent reward cue. J Neurosci 2009, 29:6500-6513.
18. Kapur S., Mizrahi R., Li M. From dopamine to salience to psychosis - linking biology: pharmacology and phenomenology of psychosis. Schizophr Res 2005, 79:59-68.
19. Roiser J.P., Stephan K.E., den Ouden H.E., Barnes T.R., Friston K.J., Joyce E.M. Do patients with schizophrenia exhibit aberrant salience?. Psychol Med 2009, 39:199-209.
20. Bender A.T., Beavo J.A. Cyclic nucleotide phosphodiesterases: molecular regulation to clinical use. Pharmacol Rev 2006, 58:488-520.
21. Lugnier C. Cyclic nucleotide phosphodiesterase (PDE) superfamily: a new target for the development of specific therapeutic agents. Pharmacol Ther 2006, 109:366-398.
22. Girault J.A., Greengard P. The neurobiology of dopamine signaling. Arch Neurol 2004, 61:641-644.
23. Greengard P. The neurobiology of dopamine signaling. Biosci Rep 2001, 21:247-269.
24. Siuciak J.A., McCarthy S.A., Chapin D.S., Fujiwara R.A., James L.C., Williams R.D., et al. Genetic deletion of the striatum-enriched phosphodiesterase PDE10A: evidence for altered striatal function. Neuropharmacology 2006, 51:374-385.
25. Kebabian J.W., Beaulieu M., Itoh Y. Pharmacological and biochemical evidence for the existence of two categories of dopamine receptor. Can J Neurol Sci 1984, 11:114-117.
26. Svenningsson P., Nishi A., Fisone G., Girault J.A., Nairn A.C., Greengard P. DARPP-32: an integrator of neurotransmission. Annu Rev Pharmacol Toxicol 2004, 44:269-296.
27. Piccart E., Langlois X., Vanhoof G., D'Hooge R. Selective inhibition of phosphodiesterase 10A impairs appetitive and aversive conditioning and incentive salience attribution. Neuropharmacology 2013, 75C:437-444.
28. Weber M., Breier M., Ko D., Thangaraj N., Marzan D.E., Swerdlow N.R. Evaluating the antipsychotic profile of the preferential PDE10A inhibitor: papaverine. Psychopharmacology (Berl) 2009, 203:723-735.
29. Tam G.W., van de Lagemaat L.N., Redon R., Strathdee K.E., Croning M.D., Malloy M.P., et al. Confirmed rare copy number variants implicate novel genes in schizophrenia. Biochem Soc Trans 2010, 38:445-451.
30. Naert A., Callaerts-Vegh Z., Moechars D., Meert T., D'Hooge R. Vglut2 haploinsufficiency enhances behavioral sensitivity to MK-801 and amphetamine in mice. Prog Neuropsychopharmacol Biol Psychiatry 2011, 35:1316-1321.
31. Menniti F.S., Chappie T.A., Humphrey J.M., Schmidt C.J. Phosphodiesterase 10A inhibitors: a novel approach to the treatment of the symptoms of schizophrenia. Curr Opin Investig Drugs 2007, 8:54-59.
32. Siuciak J.A., Chapin D.S., Harms J.F., Lebel L.A., McCarthy S.A., Chambers L., et al. Inhibition of the striatum-enriched phosphodiesterase PDE10A: a novel approach to the treatment of psychosis. Neuropharmacology 2006, 51:386-396.
33. Siuciak J.A., McCarthy S.A., Chapin D.S., Martin A.N., Harms J.F., Schmidt C.J. Behavioral characterization of mice deficient in the phosphodiesterase-10A (PDE10A) enzyme on a C57/Bl6N congenic background. Neuropharmacology 2008, 54:417-427.
34. Flagel S.B., Akil H., Robinson T.E. Individual differences in the attribution of incentive salience to reward-related cues: implications for addiction. Neuropharmacology 2009, 56(Suppl. 1):139-148.
35. Uslaner J.M., Acerbo M.J., Jones S.A., Robinson T.E. The attribution of incentive salience to a stimulus that signals an intravenous injection of cocaine. Behav Brain Res 2006, 169:320-324.
36. Schenk S., Partridge B. Influence of a conditioned light stimulus on cocaine self-administration in rats. Psychopharmacology (Berl) 2001, 154:390-396.
37. Kelley A.E., Delfs J.M. Dopamine and conditioned reinforcement. I. Differential effects of amphetamine microinjections into striatal subregions. Psychopharmacology (Berl) 1991, 103:187-196.
38. Robinson S., Sandstrom S.M., Denenberg V.H., Palmiter R.D. Distinguishing whether dopamine regulates liking: wanting, and/or learning about rewards. Behav Neurosci 2005, 119:5-15.
39. Drew M.R., Simpson E.H., Kellendonk C., Herzberg W.G., Lipatova O., Fairhurst S., et al. Transient overexpression of striatal D2 receptors impairs operant motivation and interval timing. J Neurosci 2007, 27:7731-7739.
40. Peleg-Raibstein D., Sydekum E., Feldon J. Differential effects on prepulse inhibition of withdrawal from two different repeated administration schedules of amphetamine. Int J Neuropsychopharmacol 2006, 9:737-749.
41. Swerdlow N.R., Geyer M.A., Braff D.L. Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology (Berl) 2001, 156:194-215.
42. Tenn C.C., Fletcher P.J., Kapur S. Amphetamine-sensitized animals show a sensorimotor gating and neurochemical abnormality similar to that of schizophrenia. Schizophr Res 2003, 64:103-114.
43. Zhang J., Forkstam C., Engel J.A., Svensson L. Role of dopamine in prepulse inhibition of acoustic startle. Psychopharmacology (Berl) 2000, 149:181-188.
44. Young A.M., Moran P.M., Joseph M.H. The role of dopamine in conditioning and latent inhibition: what, when, where and how?. Neurosci Biobehav Rev 2005, 29:963-976.
45. Binder E.B., Kinkead B., Owens M.J., Kilts C.D., Nemeroff C.B. Enhanced neurotensin neurotransmission is involved in the clinically relevant behavioral effects of antipsychotic drugs: evidence from animal models of sensorimotor gating. J Neurosci 2001, 21:601-608.
46. Lacroix L., Broersen L.M., Feldon J., Weiner I. Effects of local infusions of dopaminergic drugs into the medial prefrontal cortex of rats on latent inhibition, prepulse inhibition and amphetamine induced activity. Behav Brain Res 2000, 107:111-121.
47. Lacroix L., Broersen L.M., Weiner I., Feldon J. The effects of excitotoxic lesion of the medial prefrontal cortex on latent inhibition, prepulse inhibition, food hoarding, elevated plus maze, active avoidance and locomotor activity in the rat. Neuroscience 1998, 84:431-442.
48. Threlfell S., Sammut S., Menniti F.S., Schmidt C.J., West A.R. Inhibition of phosphodiesterase 10A increases the responsiveness of striatal projection neurons to cortical stimulation. J Pharmacol Exp Ther 2009, 328:785-795.
49. Sotty F., Montezinho L.P., Steiniger-Brach B., Nielsen J. Phosphodiesterase 10A inhibition modulates the sensitivity of the mesolimbic dopaminergic system to D-amphetamine: involvement of the D1-regulated feedback control of midbrain dopamine neurons. J Neurochem 2009, 109:766-775.
50. + currents through a cAMP-dependent protein kinase A-independent mechanism. Neuroscience 2010, 167:678-690.
51. Schiffmann S.N., Desdouits F., Menu R., Greengard P., Vincent J.D., Vanderhaeghen J.J., et al. Modulation of the voltage-gated sodium current in rat striatal neurons by DARPP-32, an inhibitor of protein phosphatase. Eur J Neurosci 1998, 10:1312-1320.
52. 2+ conductance. J Neurosci 1997, 17:3334-3342.
53. Kelly M.P., Adamowicz W., Bove S., Hartman A.J., Mariga A., Pathak G., et al. Select 3',5'-cyclic nucleotide phosphodiesterases exhibit altered expression in the aged rodent brain. Cell Signal 2014, 26:383-397.
54. Kotera J., Sasaki T., Kobayashi T., Fujishige K., Yamashita Y., Omori K. Subcellular localization of cyclic nucleotide phosphodiesterase type 10A variants, and alteration of the localization by cAMP-dependent protein kinase-dependent phosphorylation. J Biol Chem 2004, 279:4366-4375.
55. Charych E.I., Jiang L.X., Lo F., Sullivan K., Brandon N.J. Interplay of palmitoylation and phosphorylation in the trafficking and localization of phosphodiesterase 10A: implications for the treatment of schizophrenia. J Neurosci 2010, 30:9027-9037.
56. Nishi A., Kuroiwa M., Miller D.B., O'Callaghan J.P., Bateup H.S., Shuto T., et al. Distinct roles of PDE4 and PDE10A in the regulation of cAMP/PKA signaling in the striatum. J Neurosci 2008, 28:10460-10471.