Adolescent-onset GABAAα1 silencing regulates reward-related decision making

European Journal of Neuroscience

Volumn 42, Issue 4, 2015, Pages 2114-2121

  Butkovich, Laura M ^a   Depoy, Lauren M ^a,b   Allen, Amanda G ^a,b   Shapiro, Lauren P ^a,b   Swanson, Andrew M ^a,b   Gourley, Shannon L ^a,b  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

GABAA; Addiction; Habit; Mouse; Response outcome

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; COCAINE; 4 AMINOBUTYRIC ACID A RECEPTOR; DOPAMINE UPTAKE INHIBITOR; GABRA1 PROTEIN, MOUSE; GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 70;

ADOLESCENT; ADULT; ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; ASSOCIATIVE MEMORY; BRAIN MATURATION; CONTROLLED STUDY; DECISION MAKING; DRUG SEEKING BEHAVIOR; GENE SILENCING; HABIT; MALE; MEDIAL PREFRONTAL CORTEX; MOTIVATION; MOUSE; NONHUMAN; ONSET AGE; PRELIMBIC CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REINFORCEMENT; REWARD; STATE DEPENDENT LEARNING; STIMULUS RESPONSE; TASK PERFORMANCE; AGE; ANIMAL; C57BL MOUSE; DRUG EFFECTS; DRUG SELF ADMINISTRATION; FOOD; GENETICS; INSTRUMENTAL CONDITIONING; METABOLISM; PHYSIOLOGY; PREFRONTAL CORTEX; TRANSGENIC MOUSE;

AGE FACTORS; ANIMALS; COCAINE; CONDITIONING, OPERANT; DECISION MAKING; DOPAMINE UPTAKE INHIBITORS; FOOD; GREEN FLUORESCENT PROTEINS; HSP70 HEAT-SHOCK PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PREFRONTAL CORTEX; RECEPTORS, GABA-A; REWARD; SELF ADMINISTRATION;

EID: 84939255227     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12995     Document Type: Article

References (51)

1. Balleine, B.W. & Dickinson, A. (1998) Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology, 37, 407-419.
2. Balleine, B.W. & O'Doherty, J.P. (2010) Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology, 35, 48-69.
3. Barker, J.M., Torregrossa, M.M. & Taylor, J.R. (2013) Bidirectional modulation of infralimbic dopamine D1 and D2 receptor activity regulates flexible reward seeking. Front. Neurosci., 7, 126.
4. Caldji, C., Diorio, J. & Meaney, M.J. (2000) Variations in maternal care in infancy regulate the development of stress reactivity. Biol. Psychiat., 48, 1164-1174.
5. Carmichael, S.T. & Price, J.L. (1996) Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. J. Comp. Neurol., 371, 179-207.
6. Cass, D.K., Thomases, D.R., Caballero, A. & Tseng, K.Y. (2013) Developmental disruption of gamma-aminobutyric acid function in the medial prefrontal cortex by noncontingent cocaine exposure during early adolescence. Biol. Psychiat., 74, 490-501.
7. Chen, Y. (2014) GABA-A receptor-dependent mechanisms prevent excessive spine elimination during postnatal maturation of the mouse cortex in vivo. FEBS Lett., 588, 4551-4560.
8. Corbit, L.H. & Balleine, B.W. (2003) The role of prelimbic cortex in instrumental conditioning. Behav. Brain Res., 146, 145-157.
9. Crozatier, C., Guerriero, R.M., Mathieu, F., Giros, B., Nosten-Bertrand, M. & Kosofsky, B.E. (2003) Altered cocaine-induced behavioral sensitization in adult mice exposed to cocaine in utero. Brain Res. Dev. Brain Res., 147, 97-105.
10. Datta, D., Arion, D. & Lewis, D.A. (2015) Developmental expression patterns of GABAA receptor subunits in layer 3 and 5 pyramidal cells of monkey prefrontal cortex. Cereb. Cortex, 25, 2295-2305.
11. DePoy, L.M., Noble, B., Allen, A.G. & Gourley, S.L. (2013) Developmentally divergent effects of Rho-kinase inhibition on cocaine- and BDNF-induced behavioral plasticity. Behav. Brain Res., 243, 171-175.
12. Dickinson, A. (1980) Contemporary Animal Learning Theory. Cambridge University Press, Cambridge.
13. Duncan, C.E., Webster, M.J., Rothmond, D.A., Bahn, S., Elashoff, M. & Shannon Weickert, C. (2010) Prefrontal GABA(A) receptor alpha-subunit expression in normal postnatal human development and schizophrenia. J. Psychiatr. Res., 44, 673-681.
14. Dutech, A., Coutureau, E. & Marchand, A.R. (2011) A reinforcement learning approach to instrumental contingency degradation in rats. J. Physiol. Paris, 105, 36-44.
15. Fritschy, J.M., Paysan, J., Enna, A. & Mohler, H. (1994) Switch in the expression of rat GABAA-receptor subtypes during postnatal development: an immunohistochemical study. J. Neurosci., 14, 5302-5324.
16. Gourley, S.L., Lee, A.S., Howell, J.L., Pittenger, C. & Taylor, J.R. (2010) Dissociable regulation of goal-directed action within mouse prefrontal cortex. Eur. J. Neurosci., 32, 1726-1734.
17. Gourley, S.L., Swanson, A.M., Jacobs, A.M., Howell, J.L., Mo, M., DiLeone, R.J., Koleske, A.J. & Taylor, J.R. (2012) Action control is mediated by prefrontal BDNF and glucocorticoid receptor binding. Proc. Natl. Acad. Sci. USA, 109, 20714-20719.
18. Gourley, S.L., Olevska, A., Zimmermann, K.S., Ressler, K.J., DiLeone, R.J. & Taylor, J.R. (2013) The orbitofrontal cortex regulates outcome-based decision-making via the lateral striatum. Eur. J. Neurosci., 38, 2382-2388.
19. Green, M.R. & McCormick, C.M. (2013) Effects of stressors in adolescence on learning and memory in rodent models. Horm. Behav., 64, 364-379.
20. Gremel, C.M. & Costa, R.M. (2013) Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual action. Nat. Commun., 4, 2264.
21. Grimm, J., Shaham, Y. & Hope, B. (2002) Effect of cocaine and sucrose withdrawal period on extinction behavior, cue-induced reinstatement, and protein levels of the dopamine transporter and tyrosine hydroxylase in limbic and cortical areas in rats. Behav. Pharmacol., 13, 379-388.
22. Hashimoto, T., Nguyen, Q.L., Rotaru, D., Keenan, T., Arion, D., Beneyto, M., Gonzalez-Burgos, G. & Lewis, D.A. (2009) Protracted developmental trajectories of GABAA receptor α1 and α2 subunit expression in the primate prefrontal cortex. Biol. Psychiat., 65, 1015-1023.
23. Heinen, K., Baker, R.E., Spijker, S., Rosahl, T., van Pelt, J. & Brussaard, A.B. (2003) Impaired dendritic spine maturation in GABAA receptor alpha1 subunit knock out mice. Neuroscience, 122, 699-705.
24. Heldt, S.A. & Ressler, K.J. (2010) Amygdala-specific reduction of alpha1-GABAA receptors disrupts the anticonvulsant, locomotor, and sedative, but not anxiolytic, effects of benzodiazepines in mice. J. Neurosci., 30, 7139-7151.
25. Hinton, E.A., Wheeler, M.G. & Gourley, S.L. (2014) Early-life cocaine interferes with BDNF-mediated behavioral plasticity. Learn. Memory, 21, 253-257.
26. Hsu, F.C., Zhang, G.J., Raol, Y.S., Valentino, R.J., Coulter, D.A. & Brooks-Kaval, A.R. (2003) Repeated neonatal handling with maternal separation permanently alters hippocampal GABAA receptors and behavioral stress responses. Proc. Natl. Acad. Sci. USA, 100, 12213-12218.
27. Huang, C.C., Liang, Y.C. & Hsu, K.S. (2011) Prenatal cocaine exposure enhances long-term potentiation induction in rat medial prefrontal cortex. Int. J. Neuropsychop., 14, 431-443.
28. Killcross, S. & Coutureau, E. (2003) Coordination of actions and habits in the medial prefrontal cortex. Cereb. Cortex, 13, 400-408.
29. Kruzich, P.J. (2007) Does response-contingent access to cocaine reinstate previously extinguished cocaine-seeking behavior in C57BL/6J mice? Brain Res., 1149, 165-171.
30. Lai, C.S., Franke, T.F. & Gan, W.B. (2012) Opposite effects of fear conditioning and extinction on dendritic spine remodeling. Nature, 483, 87-91.
31. LaLumiere, R.T., Niehoff, K.E. & Kalivas, P.W. (2010) The infralimbic cortex regulates the consolidation of extinction after cocaine self-administration. Learn. Memory, 17, 168-175.
32. Lu, H., Lim, B. & Poo, M.M. (2009) Cocaine exposure in utero alters synaptic plasticity in the medial prefrontal cortex of postnatal rats. J. Neurosci., 29, 12664-12674.
33. Maroteaux, M., Valjent, E., Longueville, S., Topilko, P., Girault, J.A. & Hervé, D. (2014) Role of the plasticity-associated transcription factor zif268 in the early phase of instrumental learning. PLoS One, 9, e81868.
34. Moorman, D.E., James, M.H., McGlinchey, E.M. & Aston-Jones, G. (2014) Differential roles of medial prefrontal subregions in the regulation of drug seeking. Brain Res., doi: 10.1016/j.brainres.2014.12.024. [Epub ahead of print].
35. A receptors: subtypes provide diversity of function and pharmacology. Neuropharmacology, 56, 141-148.
36. Ongur, D. & Price, J.L. (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb. Cortex, 10, 206-219.
37. Ostlund, S.B. & Balleine, B.W. (2005) Lesions of medial prefrontal cortex disrupt the acquisition but not the expression of goal-directed learning. J. Neurosci., 25, 7763-7770.
38. Rosen, G., Williams, A.G., Capra, J.A., Connolly, M.T., Cruz, B., Lu, L., Airey, D.C., Kulkarni, K. & Williams, R.W. (2000) The mouse brain library at www.Mbl.Org. International Mouse Genome Conference, 14, 166.
39. Salas-Ramirez, K.Y., Frankfurt, M., Alexander, A., Luine, V.N. & Friedman, E. (2010) Prenatal cocaine exposure increases anxiety, impairs cognitive function and increases dendritic spine density in adult rats: influence of sex. Neuroscience, 169, 1287-1295.
40. Sanders, J., Cowansage, K., Baumgartel, K. & Mayford, M. (2012) Elimination of dendritic spines with long-term memory is specific to active circuits. J. Neurosci., 32, 12570-12578.
41. Schilman, E.A., Uylings, H.B., Galis-de Graaf, Y., Joel, D. & Groenewegen, H.J. (2008) The orbital cortex in rats topographically projects to central parts of the caudate-putamen complex. Neurosci. Lett., 432, 40-45.
42. Sesack, S.R., Deutch, A.Y., Roth, R.H. & Bunney, B.S. (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J. Comp. Neurol., 290, 213-242.
43. Simansky, K.J. & Kachelries, W.J. (1996) Prenatal exposure to cocaine selectively disrupts motor responding to D-amphetamine in young and mature rabbits. Neuropharmacology, 35, 71-78.
44. Spear, L.P. (2000) The adolescent brain and age-related behavioral manifestations. Neurosci. Biobehav. R., 24, 417-463.
45. Swanson, A.M., Shapiro, L.P., Whyte, A.J. & Gourley, S.L. (2013) Glucocorticoid receptor regulation of action selection and prefrontal cortical dendritic spines. Commun. Int. Biol., 6, e26068.
46. Aα1-mediated plasticity in the orbitofrontal cortex regulates context-dependent action selection. Neuropsychopharmacology, 40, 1027-1036.
47. Thomsen, M. & Caine, S.B. (2005) Chronic intravenous drug self-administration in rats and mice. Curr. Protoc. Neurosci., 9, 9.20.
48. Tran-tu-Yen, D.A., Marchand, A.R., Pape, J.R., Di Scala, G. & Coutureau, E. (2009) Transient role of the rat prelimbic cortex in goal-directed behaviour. Eur. J. Neurosci., 30, 464-471.
49. Vicini, S., Ferguson, C., Prybylowski, K., Kralic, J., Morrow, A.L. & Homanics, G.E. (2001) GABA(A) receptor alpha1 subunit deletion prevents developmental changes of inhibitory synaptic currents in cerebellar neurons. J. Neurosci., 21, 3009-3016.
50. Wang, W., Nitulescu, I., Lewis, J.S., Lemos, J.C., Bamford, I.J., Posielski, N.M., Storey, G.P., Phillips, P.E. & Bamford, N.S. (2013) Overinhibition of corticostriatal activity following prenatal cocaine exposure. Ann. Neurol., 73, 355-369.
51. Yin, H.H., Ostlund, S.B. & Balleine, B.W. (2008) Reward-guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico-basal ganglia networks. Eur. J. Neurosci., 28, 1437-1448.