Prefrontal nicotinic receptors control novel social interaction between mice

FASEB Journal

Volumn 25, Issue 7, 2011, Pages 2145-2155

  Avale, Maria Elena ^a,d   Chabout, Jonathan ^c   Pons, Stéphanie ^a   Serreau, Pierre ^a,c   De Chaumont, Fabrice ^b   Olivo Marin, Jean Christophe ^b   Bourgeois, Jean Pierre ^a,b   Maskos, Uwe ^a   Changeux, Jean Pierre ^a   Granon, Sylvie ^a,c  

^a CNRS   (France)

^b INSTITUT PASTEUR   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Acetylcholine; Executive behavior; Gene rescue; Prelimbic cortex

Indexed keywords

NICOTINIC RECEPTOR; RECEPTOR SUBUNIT;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; MOTIVATION; MOUSE; NONHUMAN; OPEN FIELD BEHAVIOR; PREFRONTAL CORTEX; PRIORITY JOURNAL; SOCIAL INTERACTION; TASK PERFORMANCE;

ANIMALS; AUTORADIOGRAPHY; BICYCLO COMPOUNDS, HETEROCYCLIC; BINDING, COMPETITIVE; BRAIN; EXPLORATORY BEHAVIOR; FEMALE; GENETIC COMPLEMENTATION TEST; HEK293 CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; IODINE RADIOISOTOPES; LENTIVIRUS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; PREFRONTAL CORTEX; PROTO-ONCOGENE PROTEINS C-FOS; PYRIDINES; RECEPTORS, NICOTINIC; SOCIAL BEHAVIOR; TRANSFECTION;

MAMMALIA; MUS;

EID: 79960152766     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-178558     Document Type: Article

References (51)

1. Hill, J. A., Jr., Zoli, M., Bourgeois, J. P., and Changeux, J. P. (1993) Immunocytochemical localization of a neuronal nicotinic receptor: the beta 2-subunit. J. Neurosci. 13, 1551-1568 (Pubitemid 23095398)
2. Changeux, J. P., and Edelstein, S. J. (2005) Allosteric mechanisms of signal transduction. Science 308, 1424-1428
3. Picciotto, M. R., Zoli, M., Lena, C., Bessis, A., Lallemand, Y., Le Novere, N., Vincent, P., Pich, E. M., Brulet, P., and Changeux, J. P. (1995) Abnormal avoidance learning in mice lacking functional high-affinity nicotine receptor in the brain. Nature 374, 65-67
4. Changeux, J. P. (2010) Nicotine addiction and nicotinic receptors: lessons from genetically modified mice. Nat. Rev. Neurosci. 11, 389-401
5. Maskos, U. (2007) Emerging concepts: novel integration of in vivo approaches to localize the function of nicotinic receptors. J. Neurochem. 100, 596-602
6. Granon, S., Faure, P., and Changeux, J. P. (2003) Executive and social behaviors under nicotinic receptor regulation. Proc. Natl. Acad. Sci. U. S. A. 100, 9596-9601 (Pubitemid 37033973)
7. Wiklund, A., Granon, S., Cloez-Tayarani, I., Faure, P., le Sourd, A. M., Sundman, E., Changeux, J. P., and Eriksson, L. I. (2008) Sevoflurane anesthesia alters exploratory and anxiety-like behavior in mice lacking the beta2 nicotinic acetylcholine receptor subunit. Anesthesiology 109, 790-798
8. Zoli, M., Picciotto, M. R., Ferrari, R., Cocchi, D., and Changeux, J. P. (1999) Increased neurodegeneration during ageing in mice lacking high-affinity nicotine receptors. EMBO J. 18, 1235-1244 (Pubitemid 29110308)
9. Adolphs, R. Conceptual challenges and directions for social neuroscience. Neuron 65, 752-767
10. Amodio, D. M., and Frith, C. D. (2006) Meeting of minds: the medial frontal cortex and social cognition. Nat. Rev. Neurosci. 7, 268-277
11. Kording, K. (2007) Decision theory: what "should" the nervous system do? Science 318, 606-610
12. Yoshida, W., and Ishii, S. (2006) Resolution of uncertainty in prefrontal cortex. Neuron 50, 781-789 (Pubitemid 43775741)
13. Zahn, R., Moll, J., Paiva, M., Garrido, G., Krueger, F., Huey, E. D., and Grafman, J. (2009) The neural basis of human social values: evidence from functional MRI. Cereb. Cortex 19, 276-283
14. Izuma, K., Saito, D. N., and Sadato, N. (2008) Processing of social and monetary rewards in the human striatum. Neuron 58, 284-294 (Pubitemid 351539006)
15. Deaner, R. O., Khera, A. V., and Platt, M. L. (2005) Monkeys pay per view: adaptive valuation of social images by rhesus macaques. Curr. Biol. 15, 543-548
16. Panksepp, J. B., and Lahvis, G. P. (2007) Social reward among juvenile mice. Genes Brain Behav. 6, 661-671 (Pubitemid 47476188)
17. Robbins, T. W. (1996) Dissociating executive functions of the prefrontal cortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 351, 1463-1470; discussion 1470-1461
18. Besson, M., Suarez, S., Cormier, A., Changeux, J. P., and Granon, S. (2008) Chronic nicotine exposure has dissociable behavioural effects on control and beta2-/- mice. Behav. Genet. 38, 503-514
19. Bisler, S., Schleicher, A., Gass, P., Stehle, J. H., Zilles, K., and Staiger, J. F. (2002) Expression of c-Fos, ICER, Krox-24 and JunB in the whisker-to-barrel pathway of rats: time course of induction upon whisker stimulation by tactile exploration of an enriched environment. J. Chem. Neuroanat. 23, 187-198
20. Olivo-Marin, J. C. (2002) Extraction of spots in biological images using multiscale products. Pattern Recog. 35, 1989-1996
21. Paxinos, G., and Franklin, K. B. (2001) The Mouse Brain in Stereotaxic Coordinates, Academic Press, San Diego, CA, USA
22. Maskos, U., Molles, B. E., Pons, S., Besson, M., Guiard, B. P., Guilloux, J. P., Evrard, A., Cazala, P., Cormier, A., Mameli-Engvall, M., Dufour, N., Cloez-Tayarani, I., Bemelmans, A. P., Mallet, J., Gardier, A. M., David, V., Faure, P., Granon, S., and Changeux, J. P. (2005) Nicotine reinforcement and cognition restored by targeted expression of nicotinic receptors. Nature 436, 103-107 (Pubitemid 40966193)
23. Avale, M. E., Faure, P., Pons, S., Robledo, P., Deltheil, T., David, D. J., Gardier, A. M., Maldonado, R., Granon, S., Changeux, J. P., and Maskos, U. (2008) Interplay of beta2* nicotinic receptors and dopamine pathways in the control of spontaneous locomotion. Proc. Natl. Acad. Sci. U. S. A. 105, 15991-15996
24. Rasband, W. S. (1997-2009) ImageJ, U.S. National Institutes of Health, Bethesda, MD, USA; http://rsb.info.nih.gov/ij/
25. Granon, S., Save, E., Buhot, M. C., and Poucet, B. (1996) Effortful information processing in a spontaneous spatial situation by rats with medial prefrontal lesions. Behav. Brain Res. 78, 147-154 (Pubitemid 26252883)
26. Mogensen, J., Lauritsen, K. T., Elvertorp, S., Hasman, A., Moustgaard, A., and Wortwein, G. (2004) Place learning and object recognition by rats subjected to transection of the fimbria-fornix and/or ablation of the prefrontal cortex. Brain Res. Bull. 63, 217-236 (Pubitemid 38622579)
27. Birrell, J. M., and Brown, V. J. (2000) Medial frontal cortex mediates perceptual attentional set shifting in the rat. J. Neurosci. 20, 4320-4324 (Pubitemid 30365702)
28. Ragozzino, M. E., Detrick, S., and Kesner, R. P. (1999) Involvement of the prelimbic-infralimbic areas of the rodent prefrontal cortex in behavioral flexibility for place and response learning. J. Neurosci. 19, 4585-4594 (Pubitemid 29241106)
29. Rich, E. L., and Shapiro, M. (2009) Rat prefrontal cortical neurons selectively code strategy switches. J. Neurosci. 29, 7208-7219
30. Gorelova, N., and Yang, C. R. (1997) The course of neural projection from the prefrontal cortex to the nucleus accumbens in the rat. Neuroscience 76, 689-706
31. Vertes, R. P. (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51, 32-58
32. Smith, D. V., Hayden, B. Y., Truong, T. K., Song, A. W., Platt, M. L., and Huettel, S. A. Distinct value signals in anterior and posterior ventromedial prefrontal cortex. J. Neurosci. 30, 2490-2495
33. Moroni, M., Zwart, R., Sher, E., Cassels, B. K., and Bermudez, I. (2006) alpha4beta2 nicotinic receptors with high and low acetylcholine sensitivity: pharmacology, stoichiometry, and sensitivity to long-term exposure to nicotine. Mol. Pharmacol. 70, 755-768 (Pubitemid 44092336)
34. Mameli-Engvall, M., Evrard, A., Pons, S., Maskos, U., Svensson, T. H., Changeux, J. P., and Faure, P. (2006) Hierarchical control of dopamine neuron-firing patterns by nicotinic receptors. Neuron 50, 911-921 (Pubitemid 43850688)
35. Floresco, S. B., Zhang, Y., and Enomoto, T. (2009) Neural circuits subserving behavioral flexibility and their relevance to schizophrenia. Behav. Brain Res. 204, 396-409
36. Ito, M., and Doya, K. (2009) Validation of decision-making models and analysis of decision variables in the rat basal ganglia. J. Neurosci. 29, 9861-9874
37. Granon, S., Poucet, B., Thinus-Blanc, C., Changeux, J. P., and Vidal, C. (1995) Nicotinic and muscarinic receptors in the rat prefrontal cortex: differential roles in working memory, response selection and effortful processing. Psychopharmacology (Berl.) 119, 139-144
38. Everitt, B. J., and Robbins, T. W. (1997) Central cholinergic systems and cognition. Annu. Rev. Psychol. 48, 649-684
39. Sarter, M., and Bruno, J. P. (1997) Cognitive functions of cortical acetylcholine: toward a unifying hypothesis. Brain Res. Brain Res. Rev. 23, 28-46 (Pubitemid 27090748)
40. Ross, R. S., McGaughy, J., and Eichenbaum, H. (2005) Acetylcholine in the orbitofrontal cortex is necessary for the acquisition of a socially transmitted food preference. Learn. Mem. 12, 302-306 (Pubitemid 40958341)
41. Howe, W. M., Ji, J., Parikh, V., Williams, S., Mocaer, E., Trocme-Thibierge, C., and Sarter, M. (2010) Enhancement of attentional performance by selective stimulation of alpha4beta2(*) nAChRs: underlying cholinergic mechanisms. Neuropsychopharmacology 35, 1391-1401
42. Mansvelder, H. D., Mertz, M., and Role, L. W. (2009) Nicotinic modulation of synaptic transmission and plasticity in corticolimbic circuits. Semin. Cell. Dev. Biol. 20, 432-440
43. Couey, J. J., Meredith, R. M., Spijker, S., Poorthuis, R. B., Smit, A. B., Brussaard, A. B., and Mansvelder, H. D. (2007) Distributed network actions by nicotine increase the threshold for spike-timing-dependent plasticity in prefrontal cortex. Neuron 54, 73-87
44. Ballesteros-Yanez, I., Benavides-Piccione, R., Bourgeois, J. P., Changeux, J. P., and DeFelipe, J. Alterations of cortical pyramidal neurons in mice lacking high-affinity nicotinic receptors. Proc. Natl. Acad. Sci. U. S. A. 107, 11567-11572
45. Lambe, E. K., Picciotto, M. R., and Aghajanian, G. K. (2003) Nicotine induces glutamate release from thalamocortical terminals in prefrontal cortex. Neuropsychopharmacology 28, 216-225
46. Tolu, S., Avale, M. E., Nakatani, H., Pons, S., Parnaudeau, S., Tronche, F., Vogt, A., Monyer, H., Vogel, R., de Chaumont, F., Olivo-Marin, J. C., Changeux, J. P., and Maskos, U. (2010) A versatile system for the neuronal subtype specific expression of lentiviral vectors. FASEB J. 24, 723-730
47. Del Arco, A., and Mora, F. (2009) Neurotransmitters and prefrontal cortex-limbic system interactions: implications for plasticity and psychiatric disorders. J. Neural Transm. 116, 941-952
48. Sesack, S. R., and Grace, A. A. (2010) Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 35, 27-47
49. Uylings, H. B., Groenewegen, H. J., and Kolb, B. (2003) Do rats have a prefrontal cortex? Behav. Brain Res. 146, 3-17 (Pubitemid 37476129)
50. Granon, S., and Poucet, B. (2000) Involvement of the rat prefrontal cortex in cognitive functions: a central role for the prelimbic area. Psychobiology 28, 229-237 (Pubitemid 30480478)
51. Dehaene, S., Kerszberg, M., and Changeux, J. P. (1998) A neuronal model of a global workspace in effortful cognitive tasks. Proc. Natl. Acad. Sci. U. S. A. 95, 14529-14534 (Pubitemid 28549401)