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17 - Optogenetics to Study Reward Learning and Addiction

from Part IV - Optogenetics in Learning, Neuropsychiatric Diseases, and Behavior

Published online by Cambridge University Press:  28 April 2017

Krishnarao Appasani
Affiliation:
GeneExpression Systems, Inc., Massachusetts
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Optogenetics
From Neuronal Function to Mapping and Disease Biology
, pp. 241 - 256
Publisher: Cambridge University Press
Print publication year: 2017

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References

Adamantidis, A. R., Tsai, H. C., Boutrel, B., Zhang, F., Stuber, G. D., Budygin, E. A., Tourino, C., Bonci, A., Deisseroth, K. & De Lecea, L. 2011. Optogenetic interrogation of dopaminergic modulation of the multiple phases of reward-seeking behavior. J Neurosci, 31, 10829–35.CrossRefGoogle ScholarPubMed
Albin, R. L., Young, A. B. & Penney, J. B. 1989. The functional anatomy of basal ganglia disorders. Trends Neurosci, 12, 366–75.CrossRefGoogle ScholarPubMed
Atkins, A. L., Mashhoon, Y. & Kantak, K. M. 2008. Hippocampal regulation of contextual cue-induced reinstatement of cocaine-seeking behavior. Pharmacol Biochem Behav, 90, 481–91.CrossRefGoogle ScholarPubMed
Berridge, K. C. 2007. The debate over dopamine’s role in reward: the case for incentive salience. Psychopharmacology (Berl), 191, 391431.CrossRefGoogle ScholarPubMed
Berridge, K. C. & Robinson, T. E. 1998. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev, 28, 309–69.CrossRefGoogle ScholarPubMed
Bremner, J. D., Krystal, J. H., Southwick, S. M. & Charney, D. S. 1996. Noradrenergic mechanisms in stress and anxiety: II. Clinical studies. Synapse, 23, 3951.3.0.CO;2-I>CrossRefGoogle ScholarPubMed
Brischoux, F., Chakraborty, S., Brierley, D. I. & Ungless, M. A. 2009. Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. Proc Natl Acad Sci U S A, 106, 4894–9.CrossRefGoogle ScholarPubMed
Britt, J. P., Benaliouad, F., Mcdevitt, R. A., Stuber, G. D., Wise, R. A. & Bonci, A. 2012. Synaptic and behavioral profile of multiple glutamatergic inputs to the nucleus accumbens. Neuron, 76, 790803.CrossRefGoogle ScholarPubMed
Bromberg-Martin, E. S., Matsumoto, M. & Hikosaka, O. 2010. Distinct tonic and phasic anticipatory activity in lateral habenula and dopamine neurons. Neuron, 67, 144–55.CrossRefGoogle ScholarPubMed
Brown, T. E., Lee, B. R., Mu, P., Ferguson, D., Dietz, D., Ohnishi, Y. N., Lin, Y., Suska, A., Ishikawa, M., Huang, Y. H., Shen, H., Kalivas, P. W., Sorg, B. A., Zukin, R. S., Nestler, E. J., Dong, Y. & Schluter, O. M. 2011. A silent synapse-based mechanism for cocaine-induced locomotor sensitization. J Neurosci, 31, 8163–74.CrossRefGoogle ScholarPubMed
Cohen, J. Y., Haesler, S., Vong, L., Lowell, B. B. & Uchida, N. 2012. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature, 482, 85–8.CrossRefGoogle ScholarPubMed
Cornwall, J., Cooper, J. D. & Phillipson, O. T. 1990. Projections to the rostral reticular thalamic nucleus in the rat. Exp Brain Res, 80, 157–71.CrossRefGoogle Scholar
Danjo, T., Yoshimi, K., Funabiki, K., Yawata, S. & Nakanishi, S. 2014. Aversive behavior induced by optogenetic inactivation of ventral tegmental area dopamine neurons is mediated by dopamine D2 receptors in the nucleus accumbens. Proc Natl Acad Sci U S A, 111, 6455–60.CrossRefGoogle ScholarPubMed
Di Ciano, P. & Everitt, B. J. 2004. Direct interactions between the basolateral amygdala and nucleus accumbens core underlie cocaine-seeking behavior by rats. J Neurosci, 24, 7167–73.CrossRefGoogle ScholarPubMed
Everitt, B. J. & Robbins, T. W. 2005. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci, 8, 1481–9.CrossRefGoogle ScholarPubMed
Ferguson, S. M., Eskenazi, D., Ishikawa, M., Wanat, M. J., Phillips, P. E., Dong, Y., Roth, B. L. & Neumaier, J. F. 2011. Transient neuronal inhibition reveals opposing roles of indirect and direct pathways in sensitization. Nat Neurosci, 14, 22–4.CrossRefGoogle ScholarPubMed
Fernando, A. B., Economidou, D., Theobald, D. E., Zou, M. F., Newman, A. H., Spoelder, M., Caprioli, D., Moreno, M., Hipolito, L., Aspinall, A. T., Robbins, T. W. & Dalley, J. W. 2012. Modulation of high impulsivity and attentional performance in rats by selective direct and indirect dopaminergic and noradrenergic receptor agonists. Psychopharmacology (Berl), 219, 341–52.CrossRefGoogle ScholarPubMed
Fields, H. L., Hjelmstad, G. O., Margolis, E. B. & Nicola, S. M. 2007. Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu Rev Neurosci, 30, 289316.CrossRefGoogle ScholarPubMed
Gerfen, C. R. 1992. The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia. Annu Rev Neurosci, 15, 285320.CrossRefGoogle ScholarPubMed
Hikida, T., Kimura, K., Wada, N., Funabiki, K. & Nakanishi, S. 2010. Distinct roles of synaptic transmission in direct and indirect striatal pathways to reward and aversive behavior. Neuron, 66, 896907.CrossRefGoogle ScholarPubMed
Horvitz, J. C. 2000. Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience, 96, 651–6.CrossRefGoogle ScholarPubMed
Ilango, A., Kesner, A. J., Broker, C. J., Wang, D. V. & Ikemoto, S. 2014a. Phasic excitation of ventral tegmental dopamine neurons potentiates the initiation of conditioned approach behavior: parametric and reinforcement-schedule analyses. Front Behav Neurosci, 8, 155.CrossRefGoogle ScholarPubMed
Ilango, A., Kesner, A. J., Keller, K. L., Stuber, G. D., Bonci, A. & Ikemoto, S. 2014b. Similar roles of substantia nigra and ventral tegmental dopamine neurons in reward and aversion. J Neurosci, 34, 817–22.CrossRefGoogle ScholarPubMed
Jhou, T. C., Fields, H. L., Baxter, M. G., Saper, C. B. & Holland, P. C. 2009. The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses. Neuron, 61, 786800.CrossRefGoogle ScholarPubMed
Johnson, S. W. & North, R. A. 1992. Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J Physiol, 450, 455–68.CrossRefGoogle ScholarPubMed
Kalivas, P. W. & Volkow, N. D. 2005. The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry, 162, 1403–13.CrossRefGoogle ScholarPubMed
Kaufling, J., Veinante, P., Pawlowski, S. A., FREUND-MERCIER, M. J. & Barrot, M. 2009. Afferents to the GABAergic tail of the ventral tegmental area in the rat. J Comp Neurol, 513, 597621.CrossRefGoogle Scholar
Kim, K. M., Baratta, M. V., Yang, A., Lee, D., Boyden, E. S. & Fiorillo, C. D. 2012. Optogenetic mimicry of the transient activation of dopamine neurons by natural reward is sufficient for operant reinforcement. PLoS One, 7, e33612.CrossRefGoogle ScholarPubMed
Kourrich, S., Rothwell, P. E., Klug, J. R. & Thomas, M. J. 2007. Cocaine experience controls bidirectional synaptic plasticity in the nucleus accumbens. J Neurosci, 27, 7921–8.CrossRefGoogle ScholarPubMed
Koya, E., Cruz, F. C., Ator, R., Golden, S. A., Hoffman, A. F., Lupica, C. R. & Hope, B. T. 2012. Silent synapses in selectively activated nucleus accumbens neurons following cocaine sensitization. Nat Neurosci, 15, 1556–62.CrossRefGoogle ScholarPubMed
Kravitz, A. V., Tye, L. D. & Kreitzer, A. C. 2012. Distinct roles for direct and indirect pathway striatal neurons in reinforcement. Nat Neurosci, 15, 816–8.CrossRefGoogle ScholarPubMed
Lalumiere, R. T., Smith, K. C. & Kalivas, P. W. 2012. Neural circuit competition in cocaine-seeking: roles of the infralimbic cortex and nucleus accumbens shell. Eur J Neurosci, 35, 614–22.CrossRefGoogle ScholarPubMed
Lammel, S., Lim, B. K., Ran, C., Huang, K. W., Betley, M. J., Tye, K. M., Deisseroth, K. & Malenka, R. C. 2012. Input-specific control of reward and aversion in the ventral tegmental area. Nature, 491, 212–7.CrossRefGoogle ScholarPubMed
Lee, B. R., Ma, Y. Y., Huang, Y. H., Wang, X., Otaka, M., Ishikawa, M., Neumann, P. A., Graziane, N. M., Brown, T. E., Suska, A., Guo, C., Lobo, M. K., Sesack, S. R., Wolf, M. E., Nestler, E. J., Shaham, Y., Schluter, O. M. & Dong, Y. 2013. Maturation of silent synapses in amygdala-accumbens projection contributes to incubation of cocaine craving. Nat Neurosci, 16, 1644–51.CrossRefGoogle ScholarPubMed
Lima, S. Q., Hromadka, T., Znamenskiy, P. & Zador, A. M. 2009. PINP: a new method of tagging neuronal populations for identification during in vivo electrophysiological recording. PLoS One, 4, e6099.CrossRefGoogle ScholarPubMed
Lobo, M. K., Covington, H. E. 3RD, Chaudhury, D., Friedman, A. K., Sun, H., DAMEZ-WERNO, D., Dietz, D. M., Zaman, S., Koo, J. W., Kennedy, P. J., Mouzon, E., Mogri, M., Neve, R. L., Deisseroth, K., Han, M. H. & Nestler, E. J. 2010. Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science, 330, 385–90.CrossRefGoogle ScholarPubMed
Lobo, M. K. & Nestler, E. J. 2011. The striatal balancing act in drug addiction: distinct roles of direct and indirect pathway medium spiny neurons. Front Neuroanat, 5, 41.CrossRefGoogle ScholarPubMed
Lodge, D. J. & Grace, A. A. 2006. The laterodorsal tegmentum is essential for burst firing of ventral tegmental area dopamine neurons. Proc Natl Acad Sci U S A, 103, 5167–72.CrossRefGoogle ScholarPubMed
Lu, X. Y., Ghasemzadeh, M. B. & Kalivas, P. W. 1998. Expression of D1 receptor, D2 receptor, substance P and enkephalin messenger RNAs in the neurons projecting from the nucleus accumbens. Neuroscience, 82, 767–80.Google ScholarPubMed
Ma, S. & Morilak, D. A. 2005. Norepinephrine release in medial amygdala facilitates activation of the hypothalamic-pituitary-adrenal axis in response to acute immobilisation stress. J Neuroendocrinol, 17, 22–8.CrossRefGoogle ScholarPubMed
Ma, Y. Y., Lee, B. R., Wang, X., Guo, C., Liu, L., Cui, R., Lan, Y., BALCITA-PEDICINO, J. J., Wolf, M. E., Sesack, S. R., Shaham, Y., Schluter, O. M., Huang, Y. H. & Dong, Y. 2014. Bidirectional modulation of incubation of cocaine craving by silent synapse-based remodeling of prefrontal cortex to accumbens projections. Neuron, 83, 1453–67.CrossRefGoogle ScholarPubMed
Maeda, H. & Mogenson, G. J. 1982. Effects of peripheral stimulation on the activity of neurons in the ventral tegmental area, substantia nigra and midbrain reticular formation of rats. Brain Res Bull, 8, 714.CrossRefGoogle ScholarPubMed
Mantz, J., Thierry, A. M. & Glowinski, J. 1989. Effect of noxious tail pinch on the discharge rate of mesocortical and mesolimbic dopamine neurons: selective activation of the mesocortical system. Brain Res, 476, 377–81.CrossRefGoogle ScholarPubMed
Matsumoto, M. & Hikosaka, O. 2007. Lateral habenula as a source of negative reward signals in dopamine neurons. Nature, 447, 1111–5.CrossRefGoogle ScholarPubMed
Matsumoto, M. & Hikosaka, O. 2009. Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature, 459, 837–41.CrossRefGoogle ScholarPubMed
Mcfarland, K., Lapish, C. C. & Kalivas, P. W. 2003. Prefrontal glutamate release into the core of the nucleus accumbens mediates cocaine-induced reinstatement of drug-seeking behavior. J Neurosci, 23, 3531–7.CrossRefGoogle ScholarPubMed
Mogenson, G. J., Jones, D. L. & Yim, C. Y. 1980. From motivation to action: functional interface between the limbic system and the motor system. Prog Neurobiol, 14, 6997.CrossRefGoogle ScholarPubMed
Pascoli, V., Terrier, J., Espallergues, J., Valjent, E., O’CONNOR, E. C. & Luscher, C. 2014. Contrasting forms of cocaine-evoked plasticity control components of relapse. Nature, 509, 459–64.CrossRefGoogle ScholarPubMed
Peters, J., Vallone, J., Laurendi, K. & Kalivas, P. W. 2008. Opposing roles for the ventral prefrontal cortex and the basolateral amygdala on the spontaneous recovery of cocaine-seeking in rats. Psychopharmacology (Berl), 197, 319–26.CrossRefGoogle ScholarPubMed
Redgrave, P., Prescott, T. J. & Gurney, K. 1999. Is the short-latency dopamine response too short to signal reward error? Trends Neurosci, 22, 146–51.CrossRefGoogle ScholarPubMed
Rescorla, R. A. & Wagner, A.R. 1972. A Theory of Pavlovian Condition: Variations in the Effectiveness of Reinforcement and Nonreinforcement. New York, Appleton-Century-Crofts.Google Scholar
Roitman, M. F., Stuber, G. D., Phillips, P. E., Wightman, R. M. & Carelli, R. M. 2004. Dopamine operates as a subsecond modulator of food seeking. J Neurosci, 24, 1265–71.CrossRefGoogle ScholarPubMed
Russo, S. J., Dietz, D. M., Dumitriu, D., Morrison, J. H., Malenka, R. C. & Nestler, E. J. 2010. The addicted synapse: mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci, 33, 267–76.CrossRefGoogle ScholarPubMed
Schultz, W. 1998. Predictive reward signal of dopamine neurons. J Neurophysiol, 80, 127.CrossRefGoogle ScholarPubMed
Schultz, W., Apicella, P. & Ljungberg, T. 1993. Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. J Neurosci, 13, 900–13.CrossRefGoogle ScholarPubMed
Schultz, W., Dayan, P. & Montague, P. R. 1997. A neural substrate of prediction and reward. Science, 275, 1593–9.CrossRefGoogle ScholarPubMed
Schultz, W. & Romo, R. 1987. Responses of nigrostriatal dopamine neurons to high-intensity somatosensory stimulation in the anesthetized monkey. J Neurophysiol, 57, 201–17.CrossRefGoogle ScholarPubMed
Setlow, B., Gallagher, M. & Holland, P. C. 2002. The basolateral complex of the amygdala is necessary for acquisition but not expression of CS motivational value in appetitive Pavlovian second-order conditioning. Eur J Neurosci, 15, 1841–53.CrossRefGoogle Scholar
Song, S. S., Kang, B. J., Wen, L., Lee, H. J., Sim, H. R., Kim, T. H., Yoon, S., Yoon, B. J., Augustine, G. J. & Baik, J. H. 2014. Optogenetics reveals a role for accumbal medium spiny neurons expressing dopamine D2 receptors in cocaine-induced behavioral sensitization. Front Behav Neurosci, 8, 336.CrossRefGoogle ScholarPubMed
Stamatakis, A. M. & Stuber, G. D. 2012. Activation of lateral habenula inputs to the ventral midbrain promotes behavioral avoidance. Nat Neurosci, 15, 1105–7.CrossRefGoogle Scholar
Stefanik, M. T. & Kalivas, P. W. 2013. Optogenetic dissection of basolateral amygdala projections during cue-induced reinstatement of cocaine seeking. Front Behav Neurosci, 7, 213.CrossRefGoogle ScholarPubMed
Stefanik, M. T., Kupchik, Y. M., Brown, R. M. & Kalivas, P. W. 2013a. Optogenetic evidence that pallidal projections, not nigral projections, from the nucleus accumbens core are necessary for reinstating cocaine seeking. J Neurosci, 33, 13654–62.CrossRefGoogle Scholar
Stefanik, M. T., Kupchik, Y. M. & Kalivas, P. W. 2016. Optogenetic inhibition of cortical afferents in the nucleus accumbens simultaneously prevents cue-induced transient synaptic potentiation and cocaine-seeking behavior. Brain Struct Funct, 221, 1681–9.CrossRefGoogle ScholarPubMed
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. 2013b. Optogenetic inhibition of cocaine seeking in rats. Addict Biol, 18, 50–3.CrossRefGoogle ScholarPubMed
Steinberg, E. E. & Janak, P. H. 2013. Establishing causality for dopamine in neural function and behavior with optogenetics. Brain Res, 1511, 4664.CrossRefGoogle ScholarPubMed
Steinberg, E. E., Keiflin, R., Boivin, J. R., Witten, I. B., Deisseroth, K. & Janak, P. H. 2013. A causal link between prediction errors, dopamine neurons and learning. Nat Neurosci, 16, 966–73.CrossRefGoogle ScholarPubMed
Stuber, G. D., Hnasko, T. S., Britt, J. P., Edwards, R. H. & Bonci, A. 2010. Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate. J Neurosci, 30, 8229–33.CrossRefGoogle Scholar
Stuber, G. D., Sparta, D. R., Stamatakis, A. M., Van Leeuwen, W. A., Hardjoprajitno, J. E., Cho, S., Tye, K. M., Kempadoo, K. A., Zhang, F., Deisseroth, K. & Bonci, A. 2011. Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature, 475, 377–80.CrossRefGoogle ScholarPubMed
Sun, W. & Rebec, G. V. 2003. Lidocaine inactivation of ventral subiculum attenuates cocaine-seeking behavior in rats. J Neurosci, 23, 10258–64.CrossRefGoogle ScholarPubMed
Suska, A., Lee, B. R., Huang, Y. H., Dong, Y. & Schluter, O. M. 2013. Selective presynaptic enhancement of the prefrontal cortex to nucleus accumbens pathway by cocaine. Proc Natl Acad Sci U S A, 110, 713–8.CrossRefGoogle ScholarPubMed
Sutton, R. S. 1988. Learning to predict by the methods of temporal differences. Machine Learning, 3, 944.CrossRefGoogle Scholar
Sutton, R. S. & Barto, A. G. 1998. Reinforcement Learning: An Introduction. Cambridge, MA: MIT Press.Google Scholar
Tan, K. R., Yvon, C., Turiault, M., Mirzabekov, J. J., Doehner, J., Labouebe, G., Deisseroth, K., Tye, K. M. & Luscher, C. 2012. GABA neurons of the VTA drive conditioned place aversion. Neuron, 73, 1173–83.CrossRefGoogle ScholarPubMed
Tanimoto, H., Heisenberg, M. & Gerber, B. 2004. Experimental psychology: event timing turns punishment to reward. Nature, 430, 983.CrossRefGoogle ScholarPubMed
Tsai, H. C., Zhang, F., Adamantidis, A., Stuber, G. D., Bonci, A., De Lecea, L. & Deisseroth, K. 2009. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science, 324, 1080–4.CrossRefGoogle ScholarPubMed
Ungless, M. A., Argilli, E. & Bonci, A. 2010. Effects of stress and aversion on dopamine neurons: implications for addiction. Neurosci Biobehav Rev, 35, 151–6.CrossRefGoogle ScholarPubMed
Ungless, M. A. & Grace, A. A. 2012. Are you or aren’t you? Challenges associated with physiologically identifying dopamine neurons. Trends Neurosci, 35, 422–30.CrossRefGoogle ScholarPubMed
Van Zessen, R., Phillips, J. L., Budygin, E. A. & Stuber, G. D. 2012. Activation of VTA GABA neurons disrupts reward consumption. Neuron, 73, 1184–94.Google ScholarPubMed
Wise, R. A. 2004. Dopamine, learning and motivation. Nat Rev Neurosci, 5, 483–94.CrossRefGoogle ScholarPubMed

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