Shifted pallidal co-release of GABA and glutamate in habenula drives cocaine withdrawal and relapse

Nature Neuroscience

Volumn 19, Issue 8, 2016, Pages 1019-1024

  Meye, Frank J ^a,b   Soiza Reilly, Mariano ^a,b   Smit, Tamar ^a,b,c   Diana, Marco A ^b   Schwarz, Martin K ^d   Mameli, Manuel ^a,b  

^a INSTITUT DU FER À MOULIN   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c UTRECHT UNIVERSITY   (Netherlands)

^d UNIVERSITY HOSPITAL BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; COCAINE; GLUTAMIC ACID; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; VESICULAR GLUTAMATE TRANSPORTER 2;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVERSION; CONDITIONED PLACE PREFERENCE TEST; CONTROLLED STUDY; DRUG DEPENDENCE; ELEVATED PLUS MAZE TEST; ENTOPEDUNCULAR NUCLEUS; FORCED SWIM TEST; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; GLOBUS PALLIDUS; HABENULA; LOCOMOTION; MALE; MOLECULAR BIOLOGY; MOUSE; NERVE CELL; NERVE CELL STIMULATION; NEUROTRANSMISSION; NONHUMAN; OPTOGENETICS; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDORABIES VIRUS; RELAPSE; SIGNAL TRANSDUCTION; STRESS; SYNAPSE; TAIL SUSPENSION TEST; WITHDRAWAL SYNDROME; ANIMAL; DRUG EFFECTS; MESENCEPHALON; METABOLISM; NERVE TRACT; PHYSIOLOGY; RECURRENT DISEASE; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE;

ANIMALS; COCAINE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HABENULA; MALE; MESENCEPHALON; MICE; MICE, TRANSGENIC; NEURAL PATHWAYS; NEURONS; RECURRENCE; SYNAPSES; SYNAPTIC TRANSMISSION; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 84976320727     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4334     Document Type: Article

References (35)

1. Lammel, S., et al. Input-specific control of reward and aversion in the ventral tegmental area. Nature 491, 212-217 (2012).
2. Stamatakis, A.M., & Stuber, G.D. Activation of lateral habenula inputs to the ventral midbrain promotes behavioral avoidance. Nat. Neurosci. 15, 1105-1107 (2012).
3. Ide, J.S., & Li, C.S. Error-related functional connectivity of the habenula in humans. Front. Hum. Neurosci. 5, 25 (2011).
4. Brown, R.M., Short, J.L., & Lawrence, A.J. Identification of brain nuclei implicated in cocaine-primed reinstatement of conditioned place preference: A behaviour dissociable from sensitization. PLoS One 5, e15889 (2010).
5. Gill, M.J., Ghee, S.M., Harper, S.M., & See, R.E. Inactivation of the lateral habenula reduces anxiogenic behavior and cocaine seeking under conditions of heightened stress. Pharmacol. Biochem. Behav. 111, 24-29 (2013).
6. Jhou, T.C., et al. Cocaine drives aversive conditioning via delayed activation of dopamine-responsive habenular and midbrain pathways. J. Neurosci. 33, 7501-7512 (2013).
7. Meye, F.J., et al. Cocaine-evoked negative symptoms require AMPA receptor trafficking in the lateral habenula. Nat. Neurosci. 18, 376-378 (2015).
8. Shabel, S.J., Proulx, C.D., Trias, A., Murphy, R.T., & Malinow, R. Input to the lateral habenula from the basal ganglia is excitatory, aversive, and suppressed by serotonin. Neuron 74, 475-481 (2012).
9. Shabel, S.J., Proulx, C.D., Piriz, J., & Malinow, R. Mood regulation. GABA/glutamate co-release controls habenula output and is modified by antidepressant treatment. Science 345, 1494-1498 (2014).
10. Hong, S., & Hikosaka, O. The globus pallidus sends reward-related signals to the lateral habenula. Neuron 60, 720-729 (2008).
11. Ishida, Y., Denovan-Wright, E., Hebb, M.O., & Robertson, H.A. Amphetamine-induced Fos expression is evident in gamma-Aminobutyric acid neurons in the globus pallidus and entopeduncular nucleus in rats treated with intrastriatal c-fos antisense oligodeoxynucleotides. Exp. Neurol. 175, 275-281 (2002).
12. Porrino, L.J. Functional consequences of acute cocaine treatment depend on route of administration. Psychopharmacology (Berl.) 112, 343-351 (1993).
13. Pignatelli, M., & Bonci, A. Role of dopamine neurons in reward and aversion: A synaptic plasticity perspective. Neuron 86, 1145-1157 (2015).
14. Micheva, K.D., & Smith, S.J. Array tomography: A new tool for imaging the molecular architecture and ultrastructure of neural circuits. Neuron 55, 25-36 (2007).
15. Soiza-Reilly, M., Anderson, W.B., Vaughan, C.W., & Commons, K.G. Presynaptic gating of excitation in the dorsal raphe nucleus by GABA. Proc. Natl. Acad. Sci. USA 110, 15800-15805 (2013).
16. Edwards, R.H. The neurotransmitter cycle and quantal size. Neuron 55, 835-858 (2007).
17. Erickson, J.D., De Gois, S., Varoqui, H., Schafer, M.K., & Weihe, E. Activity-dependent regulation of vesicular glutamate and GABA transporters: A means to scale quantal size. Neurochem. Int. 48, 643-649 (2006).
18. Wang, L., Tu, P., Bonet, L., Aubrey, K.R., & Supplisson, S. Cytosolic transmitter concentration regulates vesicle cycling at hippocampal GABAergic terminals. Neuron 80, 143-158 (2013).
19. Tritsch, N.X., Ding, J.B., & Sabatini, B.L. Dopaminergic neurons inhibit striatal output through non-canonical release of GABA. Nature 490, 262-266 (2012).
20. Chillon, M., & Kremer, E.J. Trafficking and propagation of canine adenovirus vectors lacking A known integrin-interacting motif. Hum. Gene Ther. 12, 1815-1823 (2001).
21. Barr, A.M., Markou, A., & Phillips, A.G.A. A crash course on psychostimulant withdrawal as A model of depression. Trends Pharmacol. Sci. 23, 475-482 (2002).
22. Koob, G.F., & Volkow, N.D. Neurocircuitry of addiction. Neuropsychopharmacology 35, 217-238 (2010).
23. Mantsch, J.R., Baker, D.A., Funk, D., Le, A.D., & Shaham, Y. Stress-induced reinstatement of drug seeking: 20 years of progress. Neuropsychopharmacology 41, 335-356 (2016).
24. Hatzigiakoumis, D.S., Martinotti, G., Giannantonio, M.D., & Janiri, L. Anhedonia and substance dependence: clinical correlates and treatment options. Front. Psychiatry 2, 10 (2011).
25. Li, B., et al. Synaptic potentiation onto habenula neurons in the learned helplessness model of depression. Nature 470, 535-539 (2011).
26. Ji, H., & Shepard, P.D. Lateral habenula stimulation inhibits rat midbrain dopamine neurons through A GABAA receptor-mediated mechanism. J. Neurosci. 27, 6923-6930 (2007).
27. Dunlop, B.W., & Nemeroff, C.B. The role of dopamine in the pathophysiology of depression. Arch. Gen. Psychiatry 64, 327-337 (2007).
28. Tye, K.M., et al. Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 493, 537-541 (2013).
29. Radke, A.K., & Gewirtz, J.C. Increased dopamine receptor activity in the nucleus accumbens shell ameliorates anxiety during drug withdrawal. Neuropsychopharmacology 37, 2405-2415 (2012).
30. Twining, R.C., et al. Aversive stimuli drive drug seeking in A state of low dopamine tone. Biol. Psychiatry 77, 895-902 (2015).
31. Rah, J.C., et al. Thalamocortical input onto layer 5 pyramidal neurons measured using quantitative large-scale array tomography. Front. Neural Circuits 7, 177 (2013).
32. Micheva, K.D., Busse, B., Weiler, N.C., O'Rourke, N., & Smith, S.J. Single-synapse analysis of A diverse synapse population: proteomic imaging methods and markers. Neuron 68, 639-653 (2010).
33. Soiza-Reilly, M., & Commons, K.G. Quantitative analysis of glutamatergic innervation of the mouse dorsal raphe nucleus using array tomography. J. Comp. Neurol. 519, 3802-3814 (2011).
34. Seo, S., & Leitch, B. Synaptic changes in GABAA receptor expression in the thalamus of the stargazer mouse model of absence epilepsy. Neuroscience 306, 28-38 (2015).
35. Woo, J., et al. The adhesion protein IgSF9b is coupled to neuroligin 2 via S-SCAM to promote inhibitory synapse development. J. Cell Biol. 201, 929-944 (2013).