Optogenetics: illuminating the neural bases of rodent behavior

References

• Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci. 2005;8(9):1263–1268.
   PubMed Web of Science ®Google Scholar
• Zhang F, Aravanis AM, Adamantidis A, de Lecea L, Deisseroth K. Circuit-breakers: Optical technologies for probing neural signals and systems. Nat Rev Neurosci. 2007;8(8):577–581.
   PubMed Web of Science ®Google Scholar
• Yizhar O, Fenno LE, Davidson TJ, Mogri M, Deisseroth K. Optogenetics in neural systems. Neuron. 2011;71(1):9–34.
   PubMed Web of Science ®Google Scholar
• Nagel G, Szellas T, Huhn W, et al. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci U S A. 2003;100(24):13940–13945.
   PubMed Web of Science ®Google Scholar
• Lin JY. A user’s guide to channelrhodopsin variants: Features, limitations and future developments. Exp Physiol. 2011;96(1):19–25.
   PubMed Web of Science ®Google Scholar
• Airan RD, Thompson KR, Fenno LE, Bernstein H, Deisseroth K. Temporally precise in vivo control of intracellular signalling. Nature. 2009;458(7241):1025–1029.
   PubMed Web of Science ®Google Scholar
• Spoida K, Masseck OA, Deneris ES, Herlitze S. Gq/5-HT2c receptor signals activate a local GABAergic inhibitory feedback circuit to modulate serotonergic firing and anxiety in mice. Proc Natl Acad Sci U S A. 2014;111(17):6479–6484.
   Web of Science ®Google Scholar
• Masseck OA, Spoida K, Dalkara D, et al. Vertebrate cone opsins enable sustained and highly sensitive rapid control of gi/o signaling in anxiety circuitry. Neuron. 2014;81(6):1263–1273.
   Web of Science ®Google Scholar
• Oh E, Maejima T, Liu C, Deneris E, Herlitze S. Substitution of 5-HT1A receptor signaling by a light-activated G protein-coupled receptor. J Biol Chem. 2010;285(40):30825–30836.
   PubMed Web of Science ®Google Scholar
• Stierl M, Stumpf P, Udwari D, et al. Light modulation of cellular cAMP by a small bacterial photoactivated adenylyl cyclase, bPAC, of the soil bacterium beggiatoa. J Biol Chem. 2011;286(2):1181–1188.
   Web of Science ®Google Scholar
• Ryu MH, Moskvin OV, Siltberg-Liberles J, Gomelsky M. Natural and engineered photoactivated nucleotidyl cyclases for optogenetic applications. J Biol Chem. 2010;285(53):41501–41508.
   Web of Science ®Google Scholar
• Dietz DM, Sun H, Lobo MK, et al. Rac1 is essential in cocaine-induced structural plasticity of nucleus accumbens neurons. Nat Neurosci. 2012;15(6):891–896.
   Web of Science ®Google Scholar
• Hahn KM, Kuhlman B. Hold me tightly LOV. Nat Methods. 2010;7(8): 595, 597.
   Web of Science ®Google Scholar
• Konermann S, Brigham MD, Trevino AE, et al. Optical control of mammalian endogenous transcription and epigenetic states. Nature. 2013;500(7463):472–476.
   PubMed Web of Science ®Google Scholar
• Motta-Mena LB, Reade A, Mallory MJ, et al. An optogenetic gene expression system with rapid activation and deactivation kinetics. Nat Chem Biol. 2014;10(3):196–202.
   PubMed Web of Science ®Google Scholar
• Sparta DR, Stamatakis AM, Phillips JL, Hovelso N, van Zessen R, Stuber GD. Construction of implantable optical fibers for long-term optogenetic manipulation of neural circuits. Nat Protoc. 2011;7(1):12–23.
   Web of Science ®Google Scholar
• Britt JP, McDevitt RA, Bonci A. Use of channelrhodopsin for activation of CNS neurons. Curr Protoc Neurosci. 2012;Chapter 2:Unit2.16.
   Google Scholar
• Francis TC, Lobo MK.. Optogenetic regulation of dopamine receptor-expressing neurons. In: Mario Tiberi WW, editors. Dopamine Receptor Technologies. Neuromethods ed. Springer Protocols. In Press 2014.
   Google Scholar
• Kim TI, McCall JG, Jung YH, et al. Injectable, cellular-scale optoelectronics with applications for wireless optogenetics. Science. 2013;340(6129):211–216.
   PubMed Web of Science ®Google Scholar
• Lin JY, Knutsen PM, Muller A, Kleinfeld D, Tsien RY. ReaChR: A red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation. Nat Neurosci. 2013;16(10):1499–1508.
   PubMed Web of Science ®Google Scholar
• Madisen L, Mao T, Koch H, et al. A toolbox of cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat Neurosci. 2012;15(5):793–802.
   PubMed Web of Science ®Google Scholar
• Gradinaru V, Thompson KR, Zhang F, et al. Targeting and readout strategies for fast optical neural control in vitro and in vivo. J Neurosci. 2007;27(52):14231–14238.
   PubMed Web of Science ®Google Scholar
• Arenkiel BR, Peca J, Davison IG, et al. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron. 2007;54(2):205–218.
   PubMed Web of Science ®Google Scholar
• Fenno LE, Mattis J, Ramakrishnan C, et al. Targeting cells with single vectors using multiple-feature boolean logic. Nat Methods. 2014;11(7):763–772.
   Web of Science ®Google Scholar
• Adrover MF, Shin JH, Alvarez VA. Glutamate and dopamine transmission from midbrain dopamine neurons share similar release properties but are differentially affected by cocaine. J Neurosci. 2014;34(9):3183–3192.
   Web of Science ®Google Scholar
• Betley JN, Cao ZF, Ritola KD, Sternson SM. Parallel, redundant circuit organization for homeostatic control of feeding behavior. Cell. 2013;155(6):1337–1350.
   Web of Science ®Google Scholar
• Krashes MJ, Kravitz AV. Optogenetic and chemogenetic insights into the food addiction hypothesis. Front Behav Neurosci. 2014;8:57.
   Web of Science ®Google Scholar
• Lim DH, Ledue J, Mohajerani MH, Vanni MP, Murphy TH. Optogenetic approaches for functional mouse brain mapping. Front Neurosci. 2013;7:54.
   Web of Science ®Google Scholar
• Gerfen CR, Paletzki R, Heintz N. GENSAT BAC cre-recombinase driver lines to study the functional organization of cerebral cortical and basal ganglia circuits. Neuron. 2013;80(6):1368–1383.
   Web of Science ®Google Scholar
• Tsai HC, Zhang F, Adamantidis A, et al. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science. 2009;324(5930):1080–1084.
   PubMed Web of Science ®Google Scholar
• Zhang F, Gradinaru V, Adamantidis AR, et al. Optogenetic interrogation of neural circuits: Technology for probing mammalian brain structures. Nat Protoc. 2010;5(3):439–456.
   PubMed Web of Science ®Google Scholar
• Sohal VS, Zhang F, Yizhar O, Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature. 2009;459(7247):698–702.
   PubMed Web of Science ®Google Scholar
• Atasoy D, Aponte Y, Su HH, Sternson SM. A FLEX switch targets channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J Neurosci. 2008;28(28):7025–7030.
   Web of Science ®Google Scholar
• Yang XW, Model P, Heintz N. Homologous recombination based modification in escherichia coli and germline transmission in transgenic mice of a bacterial artificial chromosome. Nat Biotechnol. 1997;15(9):859–865.
   Web of Science ®Google Scholar
• Fenno L, Yizhar O, Deisseroth K. The development and application of optogenetics. Annu Rev Neurosci. 2011;34:389–412.
   PubMed Web of Science ®Google Scholar
• Zhu P, Narita Y, Bundschuh ST, et al. Optogenetic dissection of neuronal circuits in zebrafish using viral gene transfer and the Tet system. Front Neural Circuits. 2009;3:21.
   PubMed Web of Science ®Google Scholar
• Liu X, Ramirez S, Pang PT, et al. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature. 2012;484(7394):381–385.
   PubMed Web of Science ®Google Scholar
• Ramirez S, Liu X, Lin PA, et al. Creating a false memory in the hippocampus. Science. 2013;341(6144):387–391.
   PubMed Web of Science ®Google Scholar
• Lammel S, Lim BK, Ran C, et al. Input-specific control of reward and aversion in the ventral tegmental area. Nature. 2012;491(7423):212–217.
   PubMed Web of Science ®Google Scholar
• Chaudhury D, Walsh JJ, Friedman AK, et al. Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature. 2013;493(7433):532–536.
   PubMed Web of Science ®Google Scholar
• Walsh JJ, Friedman AK, Sun H, et al. Stress and CRF gate neural activation of BDNF in the mesolimbic reward pathway. Nat Neurosci. 2014;17(1):27–29.
   PubMed Web of Science ®Google Scholar
• Rothermel M, Brunert D, Zabawa C, Diaz-Quesada M, Wachowiak M. Transgene expression in target-defined neuron populations mediated by retrograde infection with adeno-associated viral vectors. J Neurosci. 2013;33(38):15195–15206.
   Web of Science ®Google Scholar
• Senn V, Wolff SB, Herry C, et al. Long-range connectivity defines behavioral specificity of amygdala neurons. Neuron. 2014;81(2):428–437.
   Web of Science ®Google Scholar
• Mattis J, Tye KM, Ferenczi EA, et al. Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins. Nat Methods. 2011;9(2):159–172.
   Web of Science ®Google Scholar
• Gunaydin LA, Yizhar O, Berndt A, Sohal VS, Deisseroth K, Hegemann P. Ultrafast optogenetic control. Nat Neurosci. 2010;13(3):387–392.
   PubMed Web of Science ®Google Scholar
• Berndt A, Yizhar O, Gunaydin LA, Hegemann P, Deisseroth K. Bi-stable neural state switches. Nat Neurosci. 2009;12(2):229–234.
   PubMed Web of Science ®Google Scholar
• Christie IN, Wells JA, Southern P, et al. fMRI response to blue light delivery in the naive brain: Implications for combined optogenetic fMRI studies. Neuroimage. 2012;66C:634–641.
   Google Scholar
• Gradinaru V, Zhang F, Ramakrishnan C, et al. Molecular and cellular approaches for diversifying and extending optogenetics. Cell. 2010;141(1):154–165.
   PubMed Web of Science ®Google Scholar
• Raimondo JV, Kay L, Ellender TJ, Akerman CJ. Optogenetic silencing strategies differ in their effects on inhibitory synaptic transmission. Nat Neurosci. 2012;15(8):1102–1104.
   Web of Science ®Google Scholar
• Kato HE, Zhang F, Yizhar O, et al. Crystal structure of the channelrhodopsin light-gated cation channel. Nature. 2012;482(7385):369–374.
   Web of Science ®Google Scholar
• Wietek J, Wiegert JS, Adeishvili N, et al. Conversion of channelrhodopsin into a light-gated chloride channel. Science. 2014;344(6182):409–412.
   PubMed Web of Science ®Google Scholar
• Berndt A, Lee SY, Ramakrishnan C, Deisseroth K. Structure-guided transformation of channelrhodopsin into a light-activated chloride channel. Science. 2014;344(6182):420–424.
   PubMed Web of Science ®Google Scholar
• Berglund K, Birkner E, Augustine GJ, Hochgeschwender U. Light-emitting channelrhodopsins for combined optogenetic and chemical-genetic control of neurons. PLoS One. 2013;8(3):e59759.
   PubMed Web of Science ®Google Scholar
• Land BB, Brayton CE, Furman KE, Lapalombara Z, Dileone RJ. Optogenetic inhibition of neurons by internal light production. Front Behav Neurosci. 2014;8:108.
   PubMed Web of Science ®Google Scholar
• Masseck OA, Rubelowski JM, Spoida K, Herlitze S. Light- and drug-activated G-protein-coupled receptors to control intracellular signalling. Exp Physiol. 2011;96(1):51–56.
   Web of Science ®Google Scholar
• Schmidt D, Tillberg PW, Chen F, Boyden ES. A fully genetically encoded protein architecture for optical control of peptide ligand concentration. Nat Commun. 2014;5:3019.
   Web of Science ®Google Scholar
• Strickland D, Moffat K, Sosnick TR. Light-activated DNA binding in a designed allosteric protein. Proc Natl Acad Sci U S A. 2008;105(31):10709–10714.
   Web of Science ®Google Scholar
• Gutierrez DV, Mark MD, Masseck O, et al. Optogenetic control of motor coordination by gi/o protein-coupled vertebrate rhodopsin in cerebellar purkinje cells. J Biol Chem. 2011;286(29):25848–25858.
   Web of Science ®Google Scholar
• Gittis AH, Kreitzer AC. Striatal microcircuitry and movement disorders. Trends Neurosci. 2012;35(9):557–564.
   Web of Science ®Google Scholar
• Vazey EM, Aston-Jones G. New tricks for old dogmas: Optogenetic and designer receptor insights for parkinson’s disease. Brain Res. 2013;1511:153–163.
   Web of Science ®Google Scholar
• Lobo MK, Nestler EJ, Covington HE 3rd. Potential utility of optogenetics in the study of depression. Biol Psychiatry. 2012;71(12):1068–1074.
   Web of Science ®Google Scholar
• Nieh EH, Kim SY, Namburi P, Tye KM. Optogenetic dissection of neural circuits underlying emotional valence and motivated behaviors. Brain Res. 2013;1511:73–92.
   PubMed Web of Science ®Google Scholar
• Tye KM, Deisseroth K. Optogenetic investigation of neural circuits underlying brain disease in animal models. Nat Rev Neurosci. 2012;13(4):251–266.
   PubMed Web of Science ®Google Scholar
• Lenz JD, Lobo MK. Optogenetic insights into striatal function and behavior. Behav Brain Res. 2013;255:44–54.
   PubMed Web of Science ®Google Scholar
• Lammel S, Tye KM, Warden MR. Progress in understanding mood disorders: Optogenetic dissection of neural circuits. Genes Brain Behav. 2014;13(1):38–51.
   PubMed Web of Science ®Google Scholar
• Sidor MM, McClung CA. Timing matters: Using optogenetics to chronically manipulate neural circuitry and rhythms. Front Behav Neurosci. 2014;8:41.
   Web of Science ®Google Scholar
• Carr FB, Zachariou V. Nociception and pain: Lessons from optogenetics. Front Behav Neurosci. 2014;8:69.
   Web of Science ®Google Scholar
• Iyer SM, Montgomery KL, Towne C, et al. Virally mediated optogenetic excitation and inhibition of pain in freely moving nontransgenic mice. Nat Biotechnol. 2014;32(3):274–278.
   PubMed Web of Science ®Google Scholar
• Hickey L, Li Y, Fyson SJ, et al. Optoactivation of locus ceruleus neurons evokes bidirectional changes in thermal nociception in rats. J Neurosci. 2014;34(12):4148–4160.
   PubMed Web of Science ®Google Scholar
• Browne LE, Woolf CJ. Casting light on pain. Nat Biotechnol. 2014;32(3):240–241.
   Web of Science ®Google Scholar
• Wykes RC, Heeroma JH, Mantoan L, et al. Optogenetic and potassium channel gene therapy in a rodent model of focal neocortical epilepsy. Sci Transl Med. 2012;4(161):161ra152.
   PubMed Web of Science ®Google Scholar
• Tonnesen J, Sorensen AT, Deisseroth K, Lundberg C, Kokaia M. Optogenetic control of epileptiform activity. Proc Natl Acad Sci U S A. 2009;106(29):12162–12167.
   PubMed Web of Science ®Google Scholar
• Krook-Magnuson E, Armstrong C, Oijala M, Soltesz I. On-demand optogenetic control of spontaneous seizures in temporal lobe epilepsy. Nat Commun. 2013;4:1376.
   PubMed Web of Science ®Google Scholar
• Paz JT, Davidson TJ, Frechette ES, et al. Closed-loop optogenetic control of thalamus as a tool for interrupting seizures after cortical injury. Nat Neurosci. 2013;16(1):64–70.
   PubMed Web of Science ®Google Scholar
• Aravanis AM, Wang LP, Zhang F, et al. An optical neural interface: In vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology. J Neural Eng. 2007;4(3):S143–S156.
   Web of Science ®Google Scholar
• Albin RL, Young AB, Penney JB. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989;12(10):366–375.
   PubMed Web of Science ®Google Scholar
• Gerfen CR, Engber TM, Mahan LC, et al. D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science. 1990;250(4986):1429–1432.
   PubMed Web of Science ®Google Scholar
• Kravitz AV, Freeze BS, Parker PR, et al. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature. 2010;466(7306):622–626.
   PubMed Web of Science ®Google Scholar
• Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K. Optical deconstruction of parkinsonian neural circuitry. Science. 2009;324(5925):354–359.
   PubMed Web of Science ®Google Scholar
• Heiney SA, Kim J, Augustine GJ, Medina JF. Precise control of movement kinematics by optogenetic inhibition of purkinje cell activity. J Neurosci. 2014;34(6):2321–2330.
   Web of Science ®Google Scholar
• Maia TV, Frank MJ. From reinforcement learning models to psychiatric and neurological disorders. Nat Neurosci. 2011;14(2):154–162.
   PubMed Web of Science ®Google Scholar
• Kravitz AV, Tye LD, Kreitzer AC. Distinct roles for direct and indirect pathway striatal neurons in reinforcement. Nat Neurosci. 2012;15(6):816–818.
   PubMed Web of Science ®Google Scholar
• Lobo MK, Nestler EJ. The striatal balancing act in drug addiction: Distinct roles of direct and indirect pathway medium spiny neurons. Front Neuroanat. 2011;5:41.
   PubMed Web of Science ®Google Scholar
• Lobo MK, Covington HE 3rd, Chaudhury D, et al. Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science. 2010;330(6002):385–390.
   PubMed Web of Science ®Google Scholar
• Koo JW, Lobo MK, Chaudhury D, et al. Loss of BDNF signaling in D1R expressing NAc neurons enhances morphine reward by reducing GABA inhibition. Neuropsychopharmacology. 2014;39(11):2646–2653.
   Google Scholar
• Xia Y, Driscoll JR, Wilbrecht L, Margolis EB, Fields HL, Hjelmstad GO. Nucleus accumbens medium spiny neurons target non-dopaminergic neurons in the ventral tegmental area. J Neurosci. 2011;31(21):7811–7816.
   Web of Science ®Google Scholar
• Bocklisch C, Pascoli V, Wong JC, et al. Cocaine disinhibits dopamine neurons by potentiation of GABA transmission in the ventral tegmental area. Science. 2013;341(6153):1521–1525.
   Web of Science ®Google Scholar
• Smith RJ, Lobo MK, Spencer S, Kalivas PW. Cocaine-induced adaptations in D1 and D2 accumbens projection neurons (a dichotomy not necessarily synonymous with direct and indirect pathways). Curr Opin Neurobiol. 2013;23(4):546–552.
   Web of Science ®Google Scholar
• Chandra R, Lenz JD, Gancarz AM, et al. Optogenetic inhibition of D1R containing nucleus accumbens neurons alters cocaine-mediated regulation of Tiam1. Front Mol Neurosci. 2013;6:13.
   Web of Science ®Google Scholar
• Stefanik MT, Kupchik YM, Brown RM, Kalivas PW. Optogenetic evidence that pallidal projections, not nigral projections, from the nucleus accumbens core are necessary for reinstating cocaine seeking. J Neurosci. 2013;33(34):13654–13662.
   Web of Science ®Google Scholar
• Tai LH, Lee AM, Benavidez N, Bonci A, Wilbrecht L. Transient stimulation of distinct subpopulations of striatal neurons mimics changes in action value. Nat Neurosci. 2012;15(9):1281–1289.
   Web of Science ®Google Scholar
• Francis TC, Chandra R, Friend DM, et al. Nucleus accumbens medium spiny neuron subtypes mediate depression-related outcomes to social defeat stress. Biol Psychiatry. Epub July 28, 2014.
   Google Scholar
• Witten IB, Lin SC, Brodsky M, et al. Cholinergic interneurons control local circuit activity and cocaine conditioning. Science. 2010;330(6011):1677–1681.
   Web of Science ®Google Scholar
• Cachope R, Mateo Y, Mathur BN, et al. Selective activation of cholinergic interneurons enhances accumbal phasic dopamine release: Setting the tone for reward processing. Cell Rep. 2012;2(1):33–41.
   PubMed Web of Science ®Google Scholar
• Threlfell S, Lalic T, Platt NJ, Jennings KA, Deisseroth K, Cragg SJ. Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron. 2012;75(1):58–64.
   PubMed Web of Science ®Google Scholar
• Nelson AB, Hammack N, Yang CF, Shah NM, Seal RP, Kreitzer AC. Striatal cholinergic interneurons drive GABA release from dopamine terminals. Neuron. 2014;82(1):63–70.
   Web of Science ®Google Scholar
• Witten IB, Steinberg EE, Lee SY, et al. Recombinase-driver rat lines: Tools, techniques, and optogenetic application to dopamine-mediated reinforcement. Neuron. 2011;72(5):721–733.
   Web of Science ®Google Scholar
• Ilango A, Kesner AJ, Broker CJ, Wang DV, Ikemoto S. Phasic excitation of ventral tegmental dopamine neurons potentiates the initiation of conditioned approach behavior: Parametric and reinforcement-schedule analyses. Front Behav Neurosci. 2014;8:155.
   Web of Science ®Google Scholar
• Steinberg EE, Keiflin R, Boivin JR, Witten IB, Deisseroth K, Janak PH. A causal link between prediction errors, dopamine neurons and learning. Nat Neurosci. 2013;16(7):966–973.
   Web of Science ®Google Scholar
• Koo JW, Mazei-Robison MS, Chaudhury D, et al. BDNF is a negative modulator of morphine action. Science. 2012;338(6103):124–128.
   PubMed Web of Science ®Google Scholar
• Adamantidis AR, Tsai HC, Boutrel B, et al. Optogenetic interrogation of dopaminergic modulation of the multiple phases of reward-seeking behavior. J Neurosci. 2011;31(30):10829–10835.
   PubMed Web of Science ®Google Scholar
• Bass CE, Grinevich VP, Gioia D, et al. Optogenetic stimulation of VTA dopamine neurons reveals that tonic but not phasic patterns of dopamine transmission reduce ethanol self-administration. Front Behav Neurosci. 2013;7:173.
   Web of Science ®Google Scholar
• Valenti O, Gill KM, Grace AA. Different stressors produce excitation or inhibition of mesolimbic dopamine neuron activity: Response alteration by stress pre-exposure. Eur J Neurosci. 2012;35(8):1312–1321.
   PubMed Web of Science ®Google Scholar
• Friedman AK, Walsh JJ, Juarez B, et al. Enhancing depression mechanisms in midbrain dopamine neurons achieves homeostatic resilience. Science. 2014;344(6181):313–319.
   PubMed Web of Science ®Google Scholar
• Krishnan V, Han MH, Graham DL, et al. Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell. 2007;131(2):391–404.
   PubMed Web of Science ®Google Scholar
• Cao JL, Covington HE 3rd, Friedman AK, et al. Mesolimbic dopamine neurons in the brain reward circuit mediate susceptibility to social defeat and antidepressant action. J Neurosci. 2010;30(49):16453–16458.
   PubMed Web of Science ®Google Scholar
• Tye KM, Mirzabekov JJ, Warden MR, et al. Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature. 2013;493(7433):537–541.
   PubMed Web of Science ®Google Scholar
• Brischoux F, Chakraborty S, Brierley DI, Ungless MA. Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. Proc Natl Acad Sci U S A. 2009;106(12):4894–4899.
   PubMed Web of Science ®Google Scholar
• Brown MT, Tan KR, O’Connor EC, Nikonenko I, Muller D, Luscher C. Ventral tegmental area GABA projections pause accumbal cholinergic interneurons to enhance associative learning. Nature. 2012;492(7429):452–456.
   Web of Science ®Google Scholar
• van Zessen R, Phillips JL, Budygin EA, Stuber GD. Activation of VTA GABA neurons disrupts reward consumption. Neuron. 2012;73(6):1184–1194.
   Web of Science ®Google Scholar
• Tan KR, Yvon C, Turiault M, et al. GABA neurons of the VTA drive conditioned place aversion. Neuron. 2012;73(6):1173–1183.
   Web of Science ®Google Scholar
• Stamatakis AM, Jennings JH, Ung RL, et al. A unique population of ventral tegmental area neurons inhibits the lateral habenula to promote reward. Neuron. 2013;80(4):1039–1053.
   Web of Science ®Google Scholar
• Stamatakis AM, Stuber GD. Activation of lateral habenula inputs to the ventral midbrain promotes behavioral avoidance. Nat Neurosci. 2012;15(8):1105–1107.
   PubMed Web of Science ®Google Scholar
• Covington HE 3rd, Lobo MK, Maze I, et al. Antidepressant effect of optogenetic stimulation of the medial prefrontal cortex. J Neurosci. 2010;30(48):16082–16090.
   PubMed Web of Science ®Google Scholar
• Vialou V, Bagot RC, Cahill ME, et al. Prefrontal cortical circuit for depression- and anxiety-related behaviors mediated by cholecystokinin: Role of DeltaFosB. J Neurosci. 2014;34(11):3878–3887.
   Web of Science ®Google Scholar
• Kumar S, Black SJ, Hultman R, et al. Cortical control of affective networks. J Neurosci. 2013;33(3):1116–1129.
   Web of Science ®Google Scholar
• Warden MR, Selimbeyoglu A, Mirzabekov JJ, et al. A prefrontal cortex-brainstem neuronal projection that controls response to behavioural challenge. Nature. 2012;492(7429):428–432.
   Web of Science ®Google Scholar
• Challis C, Beck SG, Berton O. Optogenetic modulation of descending prefrontocortical inputs to the dorsal raphe bidirectionally bias socioaffective choices after social defeat. Front Behav Neurosci. 2014;8:43.
   Web of Science ®Google Scholar
• Challis C, Boulden J, Veerakumar A, et al. Raphe GABAergic neurons mediate the acquisition of avoidance after social defeat. J Neurosci. 2013;33(35):13978–13988.
   Web of Science ®Google Scholar
• Yizhar O, Fenno LE, Prigge M, et al. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature. 2011;477(7363):171–178.
   PubMed Web of Science ®Google Scholar
• Stefanik MT, Moussawi K, Kupchik YM, et al. Optogenetic inhibition of cocaine seeking in rats. Addict Biol. 2013;18(1):50–53.
   PubMed Web of Science ®Google Scholar
• Sparta DR, Hovelso N, Mason AO, et al. Activation of prefrontal cortical parvalbumin interneurons facilitates extinction of reward-seeking behavior. J Neurosci. 2014;34(10):3699–3705.
   Web of Science ®Google Scholar
• Gremel CM, Costa RM. Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions. Nat Commun. 2013;4:2264.
   PubMed Web of Science ®Google Scholar
• Smith KS, Graybiel AM. A dual operator view of habitual behavior reflecting cortical and striatal dynamics. Neuron. 2013;79(2):361–374.
   PubMed Web of Science ®Google Scholar
• Narayanan NS, Land BB, Solder JE, Deisseroth K, DiLeone RJ. Prefrontal D1 dopamine signaling is required for temporal control. Proc Natl Acad Sci U S A. 2012;109(50):20726–20731.
   Web of Science ®Google Scholar
• Chen BT, Yau HJ, Hatch C, et al. Rescuing cocaine-induced prefrontal cortex hypoactivity prevents compulsive cocaine seeking. Nature. 2013;496(7445):359–362.
   Web of Science ®Google Scholar
• Burguiere E, Monteiro P, Feng G, Graybiel AM. Optogenetic stimulation of lateral orbitofronto-striatal pathway suppresses compulsive behaviors. Science. 2013;340(6137):1243–1246.
   PubMed Web of Science ®Google Scholar
• Ahmari SE, Spellman T, Douglass NL, et al. Repeated cortico-striatal stimulation generates persistent OCD-like behavior. Science. 2013;340(6137):1234–1239.
   PubMed Web of Science ®Google Scholar
• Britt JP, Benaliouad F, McDevitt RA, Stuber GD, Wise RA, Bonci A. Synaptic and behavioral profile of multiple glutamatergic inputs to the nucleus accumbens. Neuron. 2012;76(4):790–803.
   Web of Science ®Google Scholar
• Pascoli V, Terrier J, Espallergues J, Valjent E, O’Connor EC, Luscher C. Contrasting forms of cocaine-evoked plasticity control components of relapse. Nature. 2014;509(7501):459–464.
   PubMed Web of Science ®Google Scholar
• Stuber GD, Sparta DR, Stamatakis AM, et al. Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature. 2011;475(7356):377–380.
   PubMed Web of Science ®Google Scholar
• Land BB, Narayanan NS, Liu RJ, et al. Medial prefrontal D1 dopamine neurons control food intake. Nat Neurosci. 2014;17(2):248–253.
   Web of Science ®Google Scholar
• Calu DJ, Kawa AB, Marchant NJ, et al. Optogenetic inhibition of dorsal medial prefrontal cortex attenuates stress-induced reinstatement of palatable food seeking in female rats. J Neurosci. 2013;33(1):214–226.
   Web of Science ®Google Scholar
• McCarthy MM, Arnold AP, Ball GF, Blaustein JD, De Vries GJ. Sex differences in the brain: The not so inconvenient truth. J Neurosci. 2012;32(7):2241–2247.
   PubMed Web of Science ®Google Scholar
• Atasoy D, Betley JN, Su HH, Sternson SM. Deconstruction of a neural circuit for hunger. Nature. 2012;488(7410):172–177.
   PubMed Web of Science ®Google Scholar
• Jennings JH, Sparta DR, Stamatakis AM, et al. Distinct extended amygdala circuits for divergent motivational states. Nature. 2013;496(7444):224–228.
   Web of Science ®Google Scholar
• Adolphs R, Tranel D. Impaired judgments of sadness but not happiness following bilateral amygdala damage. J Cogn Neurosci. 2004;16(3):453–462.
   PubMed Web of Science ®Google Scholar
• Adolphs R, Baron-Cohen S, Tranel D. Impaired recognition of social emotions following amygdala damage. J Cogn Neurosci. 2002;14(8):1264–1274.
   PubMed Web of Science ®Google Scholar
• Kim SY, Adhikari A, Lee SY, et al. Diverging neural pathways assemble a behavioural state from separable features in anxiety. Nature. 2013;496(7444):219–223.
   PubMed Web of Science ®Google Scholar
• Tye KM, Prakash R, Kim SY, et al. Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature. 2011;471(7338):358–362.
   PubMed Web of Science ®Google Scholar
• Felix-Ortiz AC, Beyeler A, Seo C, Leppla CA, Wildes CP, Tye KM. BLA to vHPC inputs modulate anxiety-related behaviors. Neuron. 2013;79(4):658–664.
   Web of Science ®Google Scholar
• Felix-Ortiz AC, Tye KM. Amygdala inputs to the ventral hippocampus bidirectionally modulate social behavior. J Neurosci. 2014;34(2):586–595.
   PubMed Web of Science ®Google Scholar
• Hubner C, Bosch D, Gall A, Luthi A, Ehrlich I. Ex vivo dissection of optogenetically activated mPFC and hippocampal inputs to neurons in the basolateral amygdala: Implications for fear and emotional memory. Front Behav Neurosci. 2014;8:64.
   Web of Science ®Google Scholar
• Cho JH, Deisseroth K, Bolshakov VY. Synaptic encoding of fear extinction in mPFC-amygdala circuits. Neuron. 2013;80(6):1491–1507.
   PubMed Web of Science ®Google Scholar
• Johansen JP, Hamanaka H, Monfils MH, et al. Optical activation of lateral amygdala pyramidal cells instructs associative fear learning. Proc Natl Acad Sci U S A. 2010;107(28):12692–12697.
   PubMed Web of Science ®Google Scholar
• Huff ML, Miller RL, Deisseroth K, Moorman DE, LaLumiere RT. Posttraining optogenetic manipulations of basolateral amygdala activity modulate consolidation of inhibitory avoidance memory in rats. Proc Natl Acad Sci U S A. 2013;110(9):3597–3602.
   Web of Science ®Google Scholar
• Goshen I. The optogenetic revolution in memory research. Trends Neurosci. 2014;37(9):511–522.
   Web of Science ®Google Scholar
• Kheirbek MA, Drew LJ, Burghardt NS, et al. Differential control of learning and anxiety along the dorsoventral axis of the dentate gyrus. Neuron. 2013;77(5):955–968.
   PubMed Web of Science ®Google Scholar
• Andrews-Zwilling Y, Gillespie AK, Kravitz AV, et al. Hilar GABAergic interneuron activity controls spatial learning and memory retrieval. PLoS One. 2012;7(7):e40555.
   Web of Science ®Google Scholar
• Cruz FC, Koya E, Guez-Barber DH, et al. New technologies for examining the role of neuronal ensembles in drug addiction and fear. Nat Rev Neurosci. 2013;14(11):743–754.
   Web of Science ®Google Scholar
• Garner AR, Rowland DC, Hwang SY, et al. Generation of a synthetic memory trace. Science. 2012;335(6075):1513–1516.
   Web of Science ®Google Scholar
• Lin D, Boyle MP, Dollar P, et al. Functional identification of an aggression locus in the mouse hypothalamus. Nature. 2011;470(7333):221–226.
   Web of Science ®Google Scholar
• Wu Z, Autry AE, Bergan JF, Watabe-Uchida M, Dulac CG. Galanin neurons in the medial preoptic area govern parental behaviour. Nature. 2014;509(7500):325–330.
   PubMed Web of Science ®Google Scholar
• Albrecht U. Circadian clocks and mood-related behaviors. Handb Exp Pharmacol. 2013;(217):227–239.
   Google Scholar
• Burgess CR, Peever JH. A noradrenergic mechanism functions to couple motor behavior with arousal state. Curr Biol. 2013;23(18):1719–1725.
   PubMed Web of Science ®Google Scholar
• Adamantidis AR, Zhang F, Aravanis AM, Deisseroth K, de Lecea L. Neural substrates of awakening probed with optogenetic control of hypocretin neurons. Nature. 2007;450(7168):420–424.
   PubMed Web of Science ®Google Scholar
• Carter ME, Brill J, Bonnavion P, Huguenard JR, Huerta R, de Lecea L. Mechanism for hypocretin-mediated sleep-to-wake transitions. Proc Natl Acad Sci U S A. 2012;109(39):E2635–E2644.
   Web of Science ®Google Scholar
• Rolls A, Colas D, Adamantidis A, et al. Optogenetic disruption of sleep continuity impairs memory consolidation. Proc Natl Acad Sci U S A. 2011;108(32):13305–13310.
   PubMed Web of Science ®Google Scholar
• Konadhode RR, Pelluru D, Blanco-Centurion C, et al. Optogenetic stimulation of MCH neurons increases sleep. J Neurosci. 2013;33(25):10257–10263.
   Web of Science ®Google Scholar
• Crock LW, Kolber BJ, Morgan CD, et al. Central amygdala metabotropic glutamate receptor 5 in the modulation of visceral pain. J Neurosci. 2012;32(41):14217–14226.
   PubMed Web of Science ®Google Scholar
• Ballon DR, Flanary PL, Gladue DP, Konopka JB, Dohlman HG, Thorner J. DEP-domain-mediated regulation of GPCR signaling responses. Cell. 2006;126(6):1079–1093.
   PubMed Web of Science ®Google Scholar
• Gaspari S, Papachatzaki MM, Koo JW, et al. Nucleus accumbens-specific interventions in RGS9–2 activity modulate responses to morphine. Neuropsychopharmacology. 2014;39(8):1968–1977.
   Web of Science ®Google Scholar
• Cui G, Jun SB, Jin X, et al. Concurrent activation of striatal direct and indirect pathways during action initiation. Nature. 2013;494(7436):238–242.
   PubMed Web of Science ®Google Scholar
• Gerits A, Vanduffel W. Optogenetics in primates: A shining future? Trends Genet. 2013;29(7):403–411.
   Web of Science ®Google Scholar