Illuminating circuitry relevant to psychiatric disorders with optogenetics

Current Opinion in Neurobiology

Volumn 30, Issue , 2015, Pages 9-16

  Steinberg, Elizabeth E ^a   Christoffel, Daniel J ^a   Deisseroth, Karl ^a   Malenka, Robert C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CHANNELRHODOPSIN 2; COCAINE; CORTICOTROPIN RELEASING FACTOR RECEPTOR 2; DOPAMINE; FLUOXETINE; OREXIN; PSYCHOSTIMULANT AGENT; RHODOPSIN; UNCLASSIFIED DRUG;

ADAPTIVE BEHAVIOR; ADDICTION; ANXIETY DISORDER; BASOLATERAL AMYGDALA; BED NUCLEUS OF STRIA TERMINALIS; BEHAVIORAL SCIENCE; BRAIN FUNCTION; CHOLINERGIC SYSTEM; COCAINE DEPENDENCE; CONDITIONING; CORRELATIONAL STUDY; DOPAMINE RELEASE; DRUG SEEKING BEHAVIOR; EXCITATORY POSTSYNAPTIC POTENTIAL; FEAR; LATERAL HYPOTHALAMUS; LEARNING; MAJOR DEPRESSION; MEMORY DISORDER; MENTAL DISEASE; NERVE CELL NETWORK; NERVE PROJECTION; NERVE STIMULATION; NEUROPATHOLOGY; NEUROTRANSMISSION; NONHUMAN; NUCLEUS ACCUMBENS; OBSESSIVE COMPULSIVE DISORDER; OPTOGENETICS; PARABRACHIAL NUCLEUS; PATHOLOGICAL ANATOMY; PREFRONTAL CORTEX; REVIEW; SOCIAL DISABILITY; STRIA TERMINALIS; VENTRAL TEGMENTUM; BRAIN; HUMAN; METABOLISM; NERVE TRACT; PATHOLOGY; PHOTOSTIMULATION;

BRAIN; HUMANS; MENTAL DISORDERS; NERVE NET; NEURAL PATHWAYS; OPTOGENETICS; PHOTIC STIMULATION;

EID: 84907452552     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2014.08.004     Document Type: Review

References (72)

1. Samji H., Cescon A., Hogg R.S., Modur S.P., Althoff K.N., Buchacz K., Burchell A.N., Cohen M., Gebo K.A., Gill M.J., et al. Closing the gap: increases in life expectancy among treated HIV-positive individuals in the United States and Canada. PLOS ONE 2013, 8:e81355.
2. Nestler E.J. Antidepressant treatments in the 21st century. Biol Psychiatry 1998, 44:526-533.
3. Roth B.L. Contributions of molecular biology to antipsychotic drug discovery: promises fulfilled or unfulfilled?. Dialogues Clin Neurosci 2006, 8:303-309.
4. Hyman S.E. Revitalizing psychiatric therapeutics. Neuropsychopharmacology 2014, 39:220-229.
5. Weaver D.F., Weaver C.A. Exploring neurotherapeutic space: how many neurological drugs exist (or could exist)?. J Pharm Pharmacol 2011, 63:136-139.
6. Mayberg H.S., Lozano A.M., Voon V., McNeely H.E., Seminowicz D., Hamani C., Schwalb J.M., Kennedy S.H. Deep brain stimulation for treatment-resistant depression. Neuron 2005, 45:651-660.
7. Gabriëls L., Cosyns P., Nuttin B., Demeulemeester H., Gybels J. Deep brain stimulation for treatment-refractory obsessive-compulsive disorder: psychopathological and neuropsychological outcome in three cases. Acta Psychiatr Scand 2003, 107:275-282.
8. Kuhn J., Gründler T.O., Bauer R., Huff W., Fischer A.G., Lenartz D., Maarouf M., Bührle C., Klosterkötter J., Ullsperger M., et al. Successful deep brain stimulation of the nucleus accumbens in severe alcohol dependence is associated with changed performance monitoring. Addict Biol 2011, 16:620-623.
9. Davis K.D., Taub E., Houle S., Lang A.E., Dostrovsky J.O., Tasker R.R., Lozano A.M. Globus pallidus stimulation activates the cortical motor system during alleviation of parkinsonian symptoms. Nat Med 1997, 3:671-674.
10. Yizhar O., Fenno L.E., Davidson T.J., Mogri M., Deisseroth K. Optogenetics in neural systems. Neuron 2011, 71:9-34.
11. Deisseroth K. Circuit dynamics of adaptive and maladaptive behaviour. Nature 2014, 505:309-317.
12. Kessler R.C., Berglund P., Demler O., Jin R., Merikangas K.R., Walters E.E. Lifetime prevalence and age-of-onset distributions of DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 2005, 62:593-602.
13. Nestler E.J., Hyman S.E. Animal models of neuropsychiatric disorders. Nat Neurosci 2010, 13:1161-1169.
14. Jennings J.H., Sparta D.R., Stamatakis A.M., Ung R.L., Pleil K.E., Kash T.L., Stuber G.D. Distinct extended amygdala circuits for divergent motivational states. Nature 2013, 496:224-228.
15. Kim S., Adhikari A., Lee S.Y., Marshel J.H., Kim C.K., Mallory C.S., Lo M., Pak S., Mattis J., Lim B.K., et al. Diverging neural pathways assemble a behavioural state from separable features in anxiety. Nature 2013, 496:219-223.
16. Tye K.M., Prakash R., Kim S., Fenno L.E., Grosenick L., Zarabi H., Thompson K.R., Gradinaru V., Ramakrishnan C., Deisseroth K. Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 2011, 471:358-362.
17. Anthony T., Dee N., Bernard A., Lerchner W., Heintz N., Anderson D. Control of stress-induced persistent anxiety by an extra-amygdala septohypothalamic circuit. Cell 2014, 156:522-536.
18. Kheirbek M., Drew L., Burghardt N., Costantini D., Tannenholz L., Ahmari S., Zeng H., Fenton A., Hen R. Differential control of learning and anxiety along the dorsoventral axis of the dentate gyrus. Neuron 2013, 77:955-968.
19. LeDoux J.E. Emotion circuits in the brain. Annu Rev Neurosci 2000, 23:155-184.
20. Büchel C., Dolan R.J. Classical fear conditioning in functional neuroimaging. Curr Opin Neurobiol 2000, 10:219-223.
21. Rougemont-Bücking A., Linnman C., Zeffiro T.A., Zeidan M.A., Lebron-Milad K., Rodriguez-Romaguera J., Rauch S.L., Pitman R.K., Milad M.R. Altered processing of contextual information during fear extinction in PTSD: an fMRI study. CNS Neurosci Ther 2011, 17:227-236.
22. Wolff S.B., Gründemann J., Tovote P., Krabbe S., Jacobson G.A., Müller C., Herry C., Ehrlich I., Friedrich R.W., Letzkus J.J., et al. Amygdala interneuron subtypes control fear learning through disinhibition. Nature 2014, 509:453-458.
23. Courtin J., Chaudun F., Rozeske R.R., Karalis N., Gonzalez-Campo C., Wurtz H., Abdi A., Baufreton J., Bienvenu T.C., Herry C. Prefrontal parvalbumin interneurons shape neuronal activity to drive fear expression. Nature 2014, 505:92-96.
24. Letzkus J.J., Wolff S.B., Meyer E.M., Tovote P., Courtin J., Herry C., Lüthi A. A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 2011, 480:331-335.
25. Haubensak W., Kunwar P.S., Cai H., Ciocchi S., Wall N.R., Ponnusamy R., Biag J., Dong H., Deisseroth K., Callaway E.M., et al. Genetic dissection of an amygdala microcircuit that gates conditioned fear. Nature 2010, 468:270-276.
26. Ciocchi S., Herry C., Grenier F., Wolff S.B.E., Letzkus J.J., Vlachos I., Ehrlich I., Sprengel R., Deisseroth K., Stadler M.B., et al. Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 2010, 468:277-282.
27. Senn V., Wolff S.E., Herry C., Grenier F., Ehrlich I., Gründemann J., Fadok J., Müller C., Letzkus J., Lüthi A. Long-range connectivity defines behavioral specificity of amygdala neurons. Neuron 2014, 81:428-437.
28. Sparta D.R., Smithuis J., Stamatakis A.M., Jennings J.H., Kantak P.A., Ung R.L., Stuber G.D. Inhibition of projections from the basolateral amygdala to the entorhinal cortex disrupts the acquisition of contextual fear. Front Behav Neurosci 2014, 8-29.
29. Sears R.M., Fink A.E., Wigestrand M.B., Farb C.R., de Lecea L., Ledoux J.E. Orexin/hypocretin system modulates amygdala-dependent threat learning through the locus coeruleus. Proc Natl Acad Sci USA 2013, 110:20260-20265.
30. Cho J., Deisseroth K., Bolshakov V. Synaptic encoding of fear extinction in mPFC-amygdala circuits. Neuron 2013, 80:1491-1507.
31. Johansen J.P., Hamanaka H., Monfils M.H., Behnia R., Deisseroth K., Blair H.T., LeDoux J.E. Optical activation of lateral amygdala pyramidal cells instructs associative fear learning. Proc Natl Acad Sci USA 2010, 107:12692-12697.
32. Nabavi S., Fox R., Proulx C.D., Lin J.Y., Tsien R.Y., Malinow R. Engineering a memory with LTD and LTP. Nature 2014, 10.1038/nature13294.
33. Liu X., Ramirez S., Pang P.T., Puryear C.B., Govindarajan A., Deisseroth K., Tonegawa S. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 2012, 484:381-385.
34. Ramirez S., Liu X., Lin P-, Suh J., Pignatelli M., Redondo R.L., Ryan T.J., Tonegawa S. Creating a false memory in the hippocampus. Science 2013, 341:387-391.
35. Lüscher C., Malenka R.C. Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron 2011, 69:650-663.
36. Lammel S., Lim B.K., Malenka R.C. Reward and aversion in a heterogeneous midbrain dopamine system. Neuropharmacology 2014, 76(Pt. B):351-359.
37. Steinberg E.E., Janak P.H. Establishing causality for dopamine in neural function and behavior with optogenetics. Brain Res 2013, 1511:46-64.
38. Stuber G.D., Britt J.P., Bonci A. Optogenetic modulation of neural circuits that underlie reward seeking. Biol Psychiatry 2012, 71:1061-1067.
39. Pascoli V., Terrier J., Espallergues J., Valjent E., O'Connor E.C., Lüscher C. Contrasting forms of cocaine-evoked plasticity control components of relapse. Nature 2014, 509:459-464.
40. Britt J., Benaliouad F., McDevitt R., Stuber G., Wise R., Bonci A. Synaptic and behavioral profile of multiple glutamatergic inputs to the nucleus accumbens. Neuron 2012, 76:790-803.
41. Pascoli V., Turiault M., Lüscher C. Reversal of cocaine-evoked synaptic potentiation resets drug-induced adaptive behaviour. Nature 2011, 481:71-75.
42. Stefanik M.T., Moussawi K., Kupchik Y.M., Smith K.C., Miller R.L., Huff M.L., Deisseroth K., Kalivas P.W., LaLumiere R.T. Optogenetic inhibition of cocaine seeking in rats. Addict Biol 2013, 18:50-53.
43. Lee B.R., Ma Y., Huang Y.H., Wang X., Otaka M., Ishikawa M., Neumann P.A., Graziane N.M., Brown T.E., Suska A., et al. Maturation of silent synapses in amygdala-accumbens projection contributes to incubation of cocaine craving. Nat Neurosci. 2013, 16:1644-1651.
44. Stefanik M.T., Kalivas P.W. Optogenetic dissection of basolateral amygdala projections during cue-induced reinstatement of cocaine seeking. Front Behav Neurosci 2013, 7:213.
45. Lobo M.K., Covington H.E., Chaudhury D., Friedman A.K., Sun H., Damez-Werno D., Dietz D.M., Zaman S., Koo J.W., Kennedy P.J., et al. Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science 2010, 330:385-390.
46. Bock R., Shin J.H., Kaplan A.R., Dobi A., Markey E., Kramer P.F., Gremel C.M., Christensen C.H., Adrover M.F., Alvarez V.A. Strengthening the accumbal indirect pathway promotes resilience to compulsive cocaine use. Nat Neurosci 2013, 16:632-638.
47. Witten I.B., Lin S.C., Brodsky M., Prakash R., Diester I., Anikeeva P., Gradinaru V., Ramakrishnan C., Deisseroth K. Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 2010, 330:1677-1681.
48. Stefanik M.T., Kupchik Y.M., Brown R.M., Kalivas P.W. Optogenetic evidence that pallidal projections, not nigral projections, from the nucleus accumbens core are necessary for reinstating cocaine seeking. J Neurosci 2013, 33:13654-13662.
49. Kalivas P.W., Volkow N.D. New medications for drug addiction hiding in glutamatergic neuroplasticity. Mol Psychiatry 2011, 16:974-986.
50. Martín-García E., Courtin J., Renault P., Fiancette J., Wurtz H., Simonnet A., Levet F., Herry C., Deroche-Gamonet V. Frequency of cocaine self-administration influences drug seeking in the rat: optogenetic evidence for a role of the prelimbic cortex. Neuropsychopharmacology 2014, 10.1038/npp.2014.66.
51. van den Oever M.C., Rotaru D.C., Heinsbroek J.A., Gouwenberg Y., Deisseroth K., Stuber G.D., Mansvelder H.D., Smit A.B. Ventromedial prefrontal cortex pyramidal cells have a temporal dynamic role in recall and extinction of cocaine-associated memory. J Neurosci 2013, 33:18225-18233.
52. Chen B.T., Yau H., Hatch C., Kusumoto-Yoshida I., Cho S.L., Hopf F.W., Bonci A. Rescuing cocaine-induced prefrontal cortex hypoactivity prevents compulsive cocaine seeking. Nature 2013, 496:359-362.
53. Seif T., Chang S., Simms J.A., Gibb S.L., Dadgar J., Chen B.T., Harvey B.K., Ron D., Messing R.O., Bonci A., et al. Cortical activation of accumbens hyperpolarization-active NMDARs mediates aversion-resistant alcohol intake. Nat Neurosci 2013, 16:1094-1100.
54. Golden S.A., Covington H.E., Berton O., Russo S.J. A standardized protocol for repeated social defeat stress in mice. Nat Protoc 2011, 6:1183-1191.
55. Russo S.J., Nestler E.J. The brain reward circuitry in mood disorders. Nat Rev Neurosci 2013, 14:609-625.
56. Chaudhury D., Walsh J.J., Friedman A.K., Juarez B., Ku S.M., Koo J.W., Ferguson D., Tsai H., Pomeranz L., Christoffel D.J., et al. Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature 2013, 493:532-536.
57. Walsh J.J., Friedman A.K., Sun H., Heller E.A., Ku S.M., Juarez B., Burnham V.L., Mazei-Robison M.S., Ferguson D., Golden S.A., et al. Stress and CRF gate neural activation of BDNF in the mesolimbic reward pathway. Nat Neurosci 2013, 17:27-29.
58. Tye K.M., Mirzabekov J.J., Warden M.R., Ferenczi E.A., Tsai H., Finkelstein J., Kim S., Adhikari A., Thompson K.R., Andalman A.S., et al. Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 2012, 493:537-541.
59. Friedman A.K., Walsh J.J., Juarez B., Ku S.M., Chaudhury D., Wang J., Li X., Dietz D.M., Pan N., Vialou F.V., et al. Enhancing depression mechanisms in midbrain dopamine neurons achieves homeostatic resilience. Science 2014, 344:313-319.
60. Covington H.E., Lobo M.K., Maze I., Vialou V., Hyman J.M., Zaman S., LaPlant Q., Mouzon E., Ghose S., Tamminga C.A., et al. Antidepressant effect of optogenetic stimulation of the medial prefrontal cortex. J Neurosci 2010, 30:16082-16090.
61. Vialou V., Bagot R.C., Cahill M.E., Ferguson D., Robison A.J., Dietz D.M., Fallon B., Mazei-Robison M., Ku S.M., Harrigan E., et al. Prefrontal cortical circuit for depression- and anxiety-related behaviors mediated by cholecystokinin: role of FosB. J Neurosci 2014, 34:3878-3887.
62. Warden M., Selimbeyoglu A., Mirzabekov J., Lo M. A prefrontal cortex-brainstem neuronal projection that controls response to behavioural challenge. Nature 2012, 492:428-432.
63. Challis C., Beck S., 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.
64. Challis C., Boulden J., Veerakumar A., Espallergues J., Vassoler F.M., Pierce R.C., Beck S.G., Berton O. Raphe GABAergic neurons mediate the acquisition of avoidance after social defeat. J Neurosci 2013, 33:13978-13988.
65. Yizhar O., Fenno L.E., Prigge M., Schneider F., Davidson T.J., O'Shea D.J., Sohal V.S., Goshen I., Finkelstein J., Paz J.T., et al. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 2011, 477:171-178.
66. Felix-Ortiz A.C., Tye K.M. Amygdala inputs to the ventral hippocampus bidirectionally modulate social behavior. J Neurosci 2014, 34:586-595.
67. 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.
68. Smith K., Graybiel A. A dual operator view of habitual behavior reflecting cortical and striatal dynamics. Neuron 2013, 79:361-374.
69. Smith K.S., Virkud A., Deisseroth K., Graybiel A.M. Reversible online control of habitual behavior by optogenetic perturbation of medial prefrontal cortex. Proc Natl Acad Sci USA 2012, 109:18932-18937.
70. 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.
71. Burguiere E., Monteiro P., Feng G., Graybiel A.M. Optogenetic stimulation of lateral orbitofronto-striatal pathway suppresses compulsive behaviors. Science 2013, 340:1243-1246.
72. 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.