Ventral tegmental area GABA projections pause accumbal cholinergic interneurons to enhance associative learning

Nature

Volumn 492, Issue 7429, 2012, Pages 452-456

  Brown, Matthew T C ^a   Tan, Kelly R ^a   O'Connor, Eoin C ^a   Nikonenko, Irina ^a   Muller, Dominique ^a   Lüscher, Christian ^a,b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID;

INHIBITION; LEARNING; NEUROLOGY; PHYSIOLOGY; RODENT; SIGNALING;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CELL POPULATION; CHOLINERGIC NERVE CELL; CHOLINERGIC SYSTEM; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; MOUSE; NERVE PROJECTION; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; STATE DEPENDENT LEARNING; STIMULUS RESPONSE; SYNAPTIC TRANSMISSION; VENTRAL TEGMENTUM;

ANIMALS; AXONS; CHOLINERGIC NEURONS; DOPAMINE; GABAERGIC NEURONS; GAMMA-AMINOBUTYRIC ACID; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; LEARNING; MICE; NUCLEUS ACCUMBENS; OPTOGENETICS; PATCH-CLAMP TECHNIQUES; SYNAPSES; VENTRAL TEGMENTAL AREA;

ANIMALIA; MUS;

EID: 84871427418     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature11657     Document Type: Article

References (30)

1. Everitt, B. J. et al. Associative processes in addiction and reward. The role of amygdala-ventral striatal subsystems. Ann. NY Acad. Sci. 877, 412-438 (1999).
2. Mirenowicz, J. & Schultz, W. Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature 379, 449-451 (1996).
3. Robinson, T. E. & Berridge, K. C. The neural basis of drug craving: an incentivesensitization theory of addiction. Brain Res. Brain Res. Rev. 18, 247-291 (1993).
4. Tan, K. R. et al. GABA neurons of the VTA drive conditioned place aversion. Neuron 73, 1173-1183 (2012).
5. van Zessen, R., Phillips, J. L., Budygin, E. A. & Stuber, G. D. Activation of VTA GABA neurons disrupts reward consumption. Neuron 73, 1184-1194 (2012).
6. Van Bockstaele, E. J. & Pickel, V. M. GABA-containing neurons in the ventral tegmental area project to the nucleus accumbens in rat brain. Brain Res. 682, 215-221 (1995).
7. Margolis, E. B. et al. k opioids selectively control dopaminergic neurons projecting to the prefrontal cortex. Proc. Natl Acad. Sci. USA 103, 2938-2942 (2006).
8. Kimura, M., Rajkowski, J. & Evarts, E. Tonically discharging putamen neurons exhibit set-dependent responses. Proc. Natl Acad. Sci. USA81, 4998-5001(1984).
9. Aosaki, T. et al. Responses of tonically active neurons in the primate's striatum undergo systematic changes during behavioral sensorimotor conditioning. J. Neurosci. 14, 3969-3984 (1994).
10. Goldberg, J. A. & Reynolds, J. N. J. Spontaneous firing and evoked pauses in the tonically active cholinergic interneurons of the striatum. Neuroscience 198, 27-43 (2011).
11. Apicella, P. Leading tonically active neurons of the striatumfromreward detection to context recognition. Trends Neurosci. 30, 299-306 (2007).
12. Joshua, M., Adler, A., Mitelman, R., Vaadia, E. & Bergman, H. Midbrain dopaminergic neurons and striatal cholinergic interneurons encode the difference between reward and aversive events at different epochs of probabilistic classical conditioning trials. J. Neurosci. 28, 11673-11684 (2008).
13. Kätzel, D., Zemelman, B. V., Buetfering, C., Wö lfel, M. & Miesenböck, G. The columnar and laminar organization of inhibitory connections to neocortical excitatory cells. Nature Neurosci. 14, 100-107 (2011).
14. English, D. F. et al. GABAergic circuitsmediate the reinforcement-related signals of striatal cholinergic interneurons. Nature Neurosci. 15, 123-130 (2012).
15. Ding, J. B., Guzman, J. N., Peterson, J. D., Goldberg, J. A. & Surmeier, D. J. Thalamic gating of corticostriatal signaling by cholinergic interneurons. Neuron 67, 294-307 (2010).
16. Rymar, V. V., Sasseville, R., Luk, K. C. & Sadikot, A. F. Neurogenesis and stereological morphometry of calretinin-immunoreactive GABAergic interneurons of the neostriatum. J. Comp. Neurol. 469, 325-339 (2004).
17. Cohen, J. Y., Haesler, S., Vong, L., Lowell, B. B. & Uchida, N. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482, 85-88 (2012).
18. Inokawa, H., Yamada, H., Matsumoto, N., Muranishi, M. & Kimura, M. Juxtacellular labeling of tonically active neurons and phasically active neurons in the rat striatum. Neuroscience 168, 395-404 (2010).
19. Apicella, P., Ravel, S., Deffains, M. & Legallet, E. The role of striatal tonically active neurons in reward prediction error signaling during instrumental task performance. J. Neurosci. 31, 1507-1515 (2011).
20. Matsumoto, N., Minamimoto, T., Graybiel, A. M. & Kimura, M. Neurons in the thalamic CM-Pf complex supply striatal neurons with information about behaviorally significant sensory events. J. Neurophysiol. 85, 960-976 (2001).
21. Schulz, J. M., Oswald, M. J. & Reynolds, J. N. J. Visual-inducedexcitationleadsto firing pauses in striatal cholinergic interneurons. J. Neurosci. 31, 11133-11143 (2011).
22. Ligorio, M., Descarries, L. & Warren, R. A. Cholinergic innervation and thalamic input in rat nucleus accumbens. J. Chem. Neuroanat. 37, 33-45 (2009).
23. Cragg, S. J. Meaningful silences: how dopamine listens to the ACh pause. Trends Neurosci. 29, 125-131 (2006).
24. Threlfell, S. et al. Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron 75, 58-64 (2012).
25. Cachope, R. et al. Selective activation of cholinergic interneurons enhances accumbal phasic dopamine release: setting the tone for reward processing. Cell Rep. 2, 33-41 (2012).
26. Pratt, W. E., Spencer, R. C. & Kelley, A. E. Muscarinic receptor antagonism of the nucleus accumbens core causes avoidance to flavor and spatial cues. Behav. Neurosci. 121, 1215-1223 (2007).
27. Hikida, T. et al. Increased sensitivity to cocaine by cholinergic cell ablation in nucleus accumbens. Proc. Natl Acad. Sci. USA 98, 13351-13354 (2001).
28. Witten, I. B. et al. Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 330, 1677-1681 (2010).
29. Nugent, F. S., Penick, E. C. & Kauer, J. A. Opioids block long-term potentiation of inhibitory synapses. Nature 446, 1086-1090 (2007).
30. Padgett, C. L. et al. Methamphetamine-evoked depression of GABAB receptor signaling in GABA neurons of the VTA. Neuron 73, 978-989 (2012).