Endocannabinoid Modulation of Orbitostriatal Circuits Gates Habit Formation

Neuron

Volumn 90, Issue 6, 2016, Pages 1312-1324

  Gremel, Christina M ^a,b   Chancey, Jessica H ^a   Atwood, Brady K ^a   Luo, Guoxiang ^a   Neve, Rachael ^c   Ramakrishnan, Charu ^d   Deisseroth, Karl ^d   Lovinger, David M ^a   Costa, Rui M ^e  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d Stanford University   (United States)

^e CHAMPALIMAUD CENTRE FOR THE UNKNOWN   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CANNABINOID 1 RECEPTOR; ENDOCANNABINOID; CLOZAPINE; CLOZAPINE N-OXIDE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN FUNCTION; BRAIN NERVE CELL; CONTROLLED STUDY; CORPUS STRIATUM; CORTICAL-STRIATAL PATHWAY; FEMALE; FRONTAL CORTEX; GENE DELETION; GOAL DIRECTED ACTION; HABIT FORMATION; HABITUAL ACTION; MALE; MOUSE; NERVE CELL NETWORK; NERVE TRACT; NEUROMODULATION; NONHUMAN; ORBITAL FRONTAL CORTEX; ORBITOSTRIATAL CIRCUIT; PRIORITY JOURNAL; ANALOGS AND DERIVATIVES; ANIMAL; DRUG EFFECTS; GENE SILENCING; GENETICS; HABIT; INSTRUMENTAL CONDITIONING; NERVE CELL INHIBITION; PHYSIOLOGY; PREFRONTAL CORTEX;

ANIMALS; CLOZAPINE; CONDITIONING, OPERANT; CORPUS STRIATUM; ENDOCANNABINOIDS; GENE KNOCKDOWN TECHNIQUES; HABITS; MALE; MICE; NEURAL INHIBITION; NEURAL PATHWAYS; PREFRONTAL CORTEX; RECEPTOR, CANNABINOID, CB1;

EID: 84969932223     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.04.043     Document Type: Article

References (58)

1. Adams C.D. Variations in the sensitivity of instrumental responding to reinforcer devaluation. Q. J. Exp. Psychol. B 1982, 34:77-98.
2. Adams C.D., Dickinson A. Instrumental responding following reinforcer devaluation. Q. J. Exp. Psychol. B 1981, 33:109-121.
3. Ahmari S.E., Spellman T., Douglass N.L., Kheirbek M.A., Simpson H.B., Deisseroth K., Gordon J.A., Hen R. Repeated cortico-striatal stimulation generates persistent OCD-like behavior. Science 2013, 340:1234-1239.
4. Armbruster B.N., Li X., Pausch M.H., Herlitze S., Roth B.L. Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc. Natl. Acad. Sci. USA 2007, 104:5163-5168.
5. Barnes T.D., Kubota Y., Hu D., Jin D.Z., Graybiel A.M. Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories. Nature 2005, 437:1158-1161.
6. Belin D., Everitt B.J. Cocaine seeking habits depend upon dopamine-dependent serial connectivity linking the ventral with the dorsal striatum. Neuron 2008, 57:432-441.
7. Belin D., Belin-Rauscent A., Murray J.E., Everitt B.J. Addiction: failure of control over maladaptive incentive habits. Curr. Opin. Neurobiol. 2013, 23:564-572.
8. Bradfield L.A., Dezfouli A., van Holstein M., Chieng B., Balleine B.W. Medial orbitofrontal cortex mediates outcome retrieval in partially observable task situations. Neuron 2015, 88:1268-1280.
9. Burguière E., Monteiro P., Feng G., Graybiel A.M. Optogenetic stimulation of lateral orbitofronto-striatal pathway suppresses compulsive behaviors. Science 2013, 340:1243-1246.
10. Burguière E., Monteiro P., Mallet L., Feng G., Graybiel A.M. Striatal circuits, habits, and implications for obsessive-compulsive disorder. Curr. Opin. Neurobiol. 2015, 30:59-65.
11. Colwill R.M., Rescorla R.A. Postconditioning devaluation of a reinforcer affects instrumental responding. J. Exp. Psychol. Anim. Behav. Process. 1985, 11:120-132.
12. Corbit L.H., Nie H., Janak P.H. Habitual alcohol seeking: time course and the contribution of subregions of the dorsal striatum. Biol. Psychiatry 2012, 72:389-395.
13. DePoy L., Daut R., Brigman J.L., MacPherson K., Crowley N., Gunduz-Cinar O., Pickens C.L., Cinar R., Saksida L.M., et al. Chronic alcohol produces neuroadaptations to prime dorsal striatal learning. Proc. Natl. Acad. Sci. USA 2013, 110:14783-14788.
14. Derusso A.L., Fan D., Gupta J., Shelest O., Costa R.M., Yin H.H. Instrumental uncertainty as a determinant of behavior under interval schedules of reinforcement. Front. Integr. Nuerosci. 2010, 4:17.
15. Dias-Ferreira E., Sousa J.C., Melo I., Morgado P., Mesquita A.R., Cerqueira J.J., Costa R.M., Sousa N. Chronic stress causes frontostriatal reorganization and affects decision-making. Science 2009, 325:621-625.
16. Dickinson A. Actions and habits: the development of behavioural autonomy. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1985, 308:67-78.
17. Dickinson A., Wood N., Smith J.W. Alcohol seeking by rats: action or habit?. Q. J. Exp. Psychol. B 2002, 55:331-348.
18. Fenno L.E., Mattis J., Ramakrishnan C., Hyun M., Lee S.Y., He M., Tucciarone J., Selimbeyoglu A., Berndt A., Grosenick L., et al. Targeting cells with single vectors using multiple-feature Boolean logic. Nat. Methods 2014, 11:763-772.
19. Gerdeman G., Lovinger D.M. CB1 cannabinoid receptor inhibits synaptic release of glutamate in rat dorsolateral striatum. J. Neurophysiol. 2001, 85:468-471.
20. Gerdeman G.L., Ronesi J., Lovinger D.M. Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat. Neurosci. 2002, 5:446-451.
21. Gillan C.M., Papmeyer M., Morein-Zamir S., Sahakian B.J., Fineberg N.A., Robbins T.W., de Wit S. Disruption in the balance between goal-directed behavior and habit learning in obsessive-compulsive disorder. Am. J. Psychiatry 2011, 168:718-726.
22. Goldstein R.Z., Volkow N.D. Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat. Rev. Neurosci. 2011, 12:652-669.
23. Gourley S.L., Olevska A., Zimmermann K.S., Ressler K.J., Dileone R.J., Taylor J.R. The orbitofrontal cortex regulates outcome-based decision-making via the lateral striatum. Eur. J. Neurosci. 2013, 38:2382-2388.
24. Graybiel A.M. Habits, rituals, and the evaluative brain. Annu. Rev. Neurosci. 2008, 31:359-387.
25. Gremel C.M., Costa R.M. Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions. Nat. Commun. 2013, 4:2264.
26. Griffiths K.R., Morris R.W., Balleine B.W. Translational studies of goal-directed action as a framework for classifying deficits across psychiatric disorders. Front. Syst. Neurosci. 2014, 8:101.
27. Hilário M.R.F., Clouse E., Yin H.H., Costa R.M. Endocannabinoid signaling is critical for habit formation. Front. Integr. Nuerosci. 2007, 1:6.
28. Hilario M., Holloway T., Jin X., Costa R.M. Different dorsal striatum circuits mediate action discrimination and action generalization. Eur. J. Neurosci. 2012, 35:1105-1114.
29. Hoover W.B., Vertes R.P. Projections of the medial orbital and ventral orbital cortex in the rat. J. Comp. Neurol. 2011, 519:3766-3801.
30. Kano M., Ohno-Shosaku T., Hashimotodani Y., Uchigashima M., Watanabe M. Endocannabinoid-mediated control of synaptic transmission. Physiol. Rev. 2009, 89:309-380.
31. Killcross S., Coutureau E. Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb. Cortex 2003, 13:400-408.
32. Lovinger D.M. Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum. Neuropharmacology 2010, 58:951-961.
33. Marsicano G., Goodenough S., Monory K., Hermann H., Eder M., Cannich A., Azad S.C., Cascio M.G., Gutiérrez S.O., van der Stelt M., et al. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 2003, 302:84-88.
34. Mátyás F., Yanovsky Y., Mackie K., Kelsch W., Misgeld U., Freund T.F. Subcellular localization of type 1 cannabinoid receptors in the rat basal ganglia. Neuroscience 2006, 137:337-361.
35. Nazzaro C., Greco B., Cerovic M., Baxter P., Rubino T., Trusel M., Parolaro D., Tkatch T., Benfenati F., Pedarzani P., Tonini R. SK channel modulation rescues striatal plasticity and control over habit in cannabinoid tolerance. Nat. Neurosci. 2012, 15:284-293.
36. Ostlund S.B., Balleine B.W. The contribution of orbitofrontal cortex to action selection. Ann. N Y Acad. Sci. 2007, 1121:174-192.
37. Pan W.X., Mao T., Dudman J.T. Inputs to the dorsal striatum of the mouse reflect the parallel circuit architecture of the forebrain. Front. Neuroanat. 2010, 4:147.
38. Remijnse P.L., Nielen M.M.A., van Balkom A.J.L.M., Cath D.C., van Oppen P., Uylings H.B.M., Veltman D.J. Reduced orbitofrontal-striatal activity on a reversal learning task in obsessive-compulsive disorder. Arch. Gen. Psychiatry 2006, 63:1225-1236.
39. Rhodes S.E.V., Murray E.A. Differential effects of amygdala, orbital prefrontal cortex, and prelimbic cortex lesions on goal-directed behavior in rhesus macaques. J. Neurosci. 2013, 33:3380-3389.
40. Rolls E.T., Everitt B.J., Roberts A. The orbitofrontal cortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 1996, 351:1433-1443. discussion 1443-1444.
41. Rothermel M., Brunert D., Zabawa C., Díaz-Quesada M., Wachowiak M. Transgene expression in target-defined neuron populations mediated by retrograde infection with adeno-associated viral vectors. J. Neurosci. 2013, 33:15195-15206.
42. Samson H.H., Cunningham C.L., Czachowski C.L., Chappell A., Legg B., Shannon E. Devaluation of ethanol reinforcement. Alcohol 2004, 32:203-212.
43. Schilman E.A., Uylings H.B.M., Galis-de Graaf Y., Joel D., Groenewegen H.J. The orbital cortex in rats topographically projects to central parts of the caudate-putamen complex. Neurosci. Lett. 2008, 432:40-45.
44. Schoenbaum G., Shaham Y. The role of orbitofrontal cortex in drug addiction: a review of preclinical studies. Biol. Psychiatry 2008, 63:256-262.
45. Shepherd G.M.G. Corticostriatal connectivity and its role in disease. Nat. Rev. Neurosci. 2013, 14:278-291.
46. Smith K.S., Graybiel A.M. A dual operator view of habitual behavior reflecting cortical and striatal dynamics. Neuron 2013, 79:361-374.
47. Stachniak T.J., Ghosh A., Sternson S.M. Chemogenetic synaptic silencing of neural circuits localizes a hypothalamus→midbrain pathway for feeding behavior. Neuron 2014, 82:797-808.
48. Stalnaker T.A., Calhoon G.G., Ogawa M., Roesch M.R., Schoenbaum G. Neural correlates of stimulus-response and response-outcome associations in dorsolateral versus dorsomedial striatum. Front. Integr. Nuerosci. 2010, 4:12.
49. Stalnaker T.A., Cooch N.K., Schoenbaum G. What the orbitofrontal cortex does not do. Nat. Neurosci. 2015, 18:620-627.
50. Thorn C.A., Atallah H., Howe M., Graybiel A.M. Differential dynamics of activity changes in dorsolateral and dorsomedial striatal loops during learning. Neuron 2010, 66:781-795.
51. Uchigashima M., Narushima M., Fukaya M., Katona I., Kano M., Watanabe M. Subcellular arrangement of molecules for 2-arachidonoyl-glycerol-mediated retrograde signaling and its physiological contribution to synaptic modulation in the striatum. J. Neurosci. 2007, 27:3663-3676.
52. Wall N.R., De La Parra M., Callaway E.M., Kreitzer A.C. Differential innervation of direct- and indirect-pathway striatal projection neurons. Neuron 2013, 79:347-360.
53. Yin H.H., Knowlton B.J. The role of the basal ganglia in habit formation. Nat. Rev. Neurosci. 2006, 7:464-476.
54. Yin H.H., Knowlton B.J., Balleine B.W. Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur. J. Neurosci. 2004, 19:181-189.
55. Yin H.H., Knowlton B.J., Balleine B.W. Blockade of NMDA receptors in the dorsomedial striatum prevents action-outcome learning in instrumental conditioning. Eur. J. Neurosci. 2005, 22:505-512.
56. Yin H.H., Ostlund S.B., Knowlton B.J., Balleine B.W. The role of the dorsomedial striatum in instrumental conditioning. Eur. J. Neurosci. 2005, 22:513-523.
57. Yin H.H., Knowlton B.J., Balleine B.W. Inactivation of dorsolateral striatum enhances sensitivity to changes in the action-outcome contingency in instrumental conditioning. Behav. Brain Res. 2006, 166:189-196.
58. Znamenskiy P., Zador A.M. Corticostriatal neurons in auditory cortex drive decisions during auditory discrimination. Nature 2013, 497:482-485.