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Stereotaxic Surgery in Rodents for Stimulation of the Brain Reward System

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The Brain Reward System

Part of the book series: Neuromethods ((NM,volume 165))

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Abstract

The use of stereotaxic surgery to implant devices like microdialysis probes or stimulating electrodes in specific regions of the central nervous system (CNS) is critical for our understanding of the neurobiology of reward and aversion in rodents. Here we review the different methodological approaches to the study of brain reward systems and outline the procedure for stereotaxic implantation of devices in reward-associated CNS sites in mice and rats. We also discuss applications that take advantage of our ability to target precisely defined regions in the CNS. Applications addressed include response to drugs and natural rewards (food), drug self-administration, electrical self-stimulation, delivery of viral constructs to alter gene expression, optogenetics to evaluate reward and avoidance behaviors, fiber photometry to measure transient calcium signaling, and real-time electrochemical detection through amperometry and fast-scan cyclic voltammetry. Using the knowledge gained by these experiments, we can move forward with new treatments for disorders related to disruptions in the reward systems of the CNS.

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References

  1. Schultz W (2010) Dopamine signals for reward value and risk: basic and recent data. Behav Brain Funct 6:24. https://doi.org/10.1186/1744-9081-6-24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Hu H (2016) Reward and Aversion. Annu Rev Neurosci 39:297–324. https://doi.org/10.1146/annurev-neuro-070815-014106

    Article  CAS  PubMed  Google Scholar 

  3. Berridge KC, Kringelbach ML (2015) Pleasure systems in the brain. Neuron 86(3):646–664. https://doi.org/10.1016/j.neuron.2015.02.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Berridge KC, Robinson TE (2003) Parsing reward. Trends Neurosci 26(9):507–513. https://doi.org/10.1016/S0166-2236(03)00233-9

    Article  CAS  PubMed  Google Scholar 

  5. Hernandez L, Hoebel BG (1990) Feeding can enhance dopamine turnover in the prefrontal cortex. Brain Res Bull 25(6):975–979

    Article  CAS  PubMed  Google Scholar 

  6. Hernandez L, Hoebel BG (1988) Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by microdialysis. Life Sci 42(18):1705–1712

    Article  CAS  PubMed  Google Scholar 

  7. Yoshida M et al (1992) Eating and drinking cause increased dopamine release in the nucleus accumbens and ventral tegmental area in the rat: measurement by in vivo microdialysis. Neurosci Lett 139(1):73–76

    Article  CAS  PubMed  Google Scholar 

  8. Mark GP et al (1992) Effects of feeding and drinking on acetylcholine release in the nucleus accumbens, striatum, and hippocampus of freely behaving rats. J Neurochem 58(6):2269–2274

    Article  CAS  PubMed  Google Scholar 

  9. Salamone JD et al (1991) Haloperidol and nucleus accumbens dopamine depletion suppress lever pressing for food but increase free food consumption in a novel food choice procedure. Psychopharmacology 104(4):515–521

    Article  CAS  PubMed  Google Scholar 

  10. Bradberry CW et al (1991) Individual differences in behavioral measures: correlations with nucleus accumbens dopamine measured by microdialysis. Pharmacol Biochem Behav 39(4):877–882

    Article  CAS  PubMed  Google Scholar 

  11. Mogenson GJ, Wu M (1982) Neuropharmacological and electrophysiological evidence implicating the mesolimbic dopamine system in feeding responses elicited by electrical stimulation of the medial forebrain bundle. Brain Res 253(1–2):243–251

    Article  CAS  PubMed  Google Scholar 

  12. Bromberg-Martin ES, Matsumoto M, Hikosaka O (2010) Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 68(5):815–834. https://doi.org/10.1016/j.neuron.2010.11.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Matsumoto M, Hikosaka O (2009) Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459(7248):837–841. https://doi.org/10.1038/nature08028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Eshel N et al (2015) Arithmetic and local circuitry underlying dopamine prediction errors. Nature 525(7568):243–246. https://doi.org/10.1038/nature14855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Cohen JY et al (2012) Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482(7383):85–88. https://doi.org/10.1038/nature10754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Umberg EN, Pothos EN (2011) Neurobiology of aversive states. Physiol Behav 104(1):69–75. https://doi.org/10.1016/j.physbeh.2011.04.045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Pothos E et al (1991) Dopamine microdialysis in the nucleus accumbens during acute and chronic morphine, naloxone-precipitated withdrawal and clonidine treatment. Brain Res 566(1–2):348–350. https://doi.org/10.1016/0006-8993(91)91724-f

    Article  CAS  PubMed  Google Scholar 

  18. Wise RA, Rompre PP (1989) Brain dopamine and reward. Annu Rev Psychol 40:191–225. https://doi.org/10.1146/annurev.ps.40.020189.001203

    Article  CAS  PubMed  Google Scholar 

  19. Kelley AE, Baldo BA, Pratt WE (2005) A proposed hypothalamic-thalamic-striatal axis for the integration of energy balance, arousal, and food reward. J Comp Neurol 493(1):72–85. https://doi.org/10.1002/cne.20769

    Article  CAS  PubMed  Google Scholar 

  20. Wassum KM et al (2009) Distinct opioid circuits determine the palatability and the desirability of rewarding events. Proc Natl Acad Sci U S A 106(30):12512–12517. https://doi.org/10.1073/pnas.0905874106

    Article  PubMed  PubMed Central  Google Scholar 

  21. Will MJ, Franzblau EB, Kelley AE (2004) The amygdala is critical for opioid-mediated binge eating of fat. Neuroreport 15(12):1857–1860

    Article  CAS  PubMed  Google Scholar 

  22. Zhang M, Gosnell BA, Kelley AE (1998) Intake of high-fat food is selectively enhanced by mu opioid receptor stimulation within the nucleus accumbens. J Pharmacol Exp Ther 285(2):908–914

    CAS  PubMed  Google Scholar 

  23. Kelley AE et al (2003) Restricted daily consumption of a highly palatable food (chocolate Ensure(R)) alters striatal enkephalin gene expression. Eur J Neurosci 18(9):2592–2598

    Article  CAS  PubMed  Google Scholar 

  24. Smith SL, Harrold JA, Williams G (2002) Diet-induced obesity increases mu opioid receptor binding in specific regions of the rat brain. Brain Res 953(1–2):215–222

    Article  CAS  PubMed  Google Scholar 

  25. Qi J et al (2014) A glutamatergic reward input from the dorsal raphe to ventral tegmental area dopamine neurons. Nat Commun 5:5390. https://doi.org/10.1038/ncomms6390

    Article  CAS  PubMed  Google Scholar 

  26. 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(3):900–913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Luo M, Zhou J, Liu Z (2015) Reward processing by the dorsal raphe nucleus: 5-HT and beyond. Learn Mem 22(9):452–460. https://doi.org/10.1101/lm.037317.114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Coenen VA et al (2019) Frontal white matter architecture predicts efficacy of deep brain stimulation in major depression. Transl Psychiatry 9(1):197. https://doi.org/10.1038/s41398-019-0540-4

    Article  PubMed  PubMed Central  Google Scholar 

  29. Mirzadeh Z et al (2016) Parkinson's disease outcomes after intraoperative CT-guided "asleep" deep brain stimulation in the globus pallidus internus. J Neurosurg 124(4):902–907. https://doi.org/10.3171/2015.4.JNS1550

    Article  PubMed  Google Scholar 

  30. Shaffie A et al (2018) A generalized deep learning-based diagnostic system for early diagnosis of various types of pulmonary nodules. Technol Cancer Res Treat 17:1533033818798800. https://doi.org/10.1177/1533033818798800

    Article  PubMed  PubMed Central  Google Scholar 

  31. Barbosa ACB et al (2012) Rapid method for acute intracerebroventricular injection in adult zebrafish. In: Kaleuff A, Stewart A (eds) Zebrafish protocols for neurobehavioral research. neuromethods, vol 66. Humana Press, c/o Springer Science+Business Media, New York

    Google Scholar 

  32. Maximino C, Herculano AM (2010) A review of monoaminergic neuropsychopharmacology in zebrafish. Zebrafish 7(4):359–378. https://doi.org/10.1089/zeb.2010.0669

    Article  CAS  PubMed  Google Scholar 

  33. Li P et al (2007) Cloning and spatial and temporal expression of the zebrafish dopamine D1 receptor. Dev Dyn 236(5):1339–1346. https://doi.org/10.1002/dvdy.21130

    Article  CAS  PubMed  Google Scholar 

  34. Boehmler W et al (2007) D4 Dopamine receptor genes of zebrafish and effects of the antipsychotic clozapine on larval swimming behaviour. Genes Brain Behav 6(2):155–166. https://doi.org/10.1111/j.1601-183X.2006.00243.x

    Article  CAS  PubMed  Google Scholar 

  35. Boehmler W et al (2004) Evolution and expression of D2 and D3 dopamine receptor genes in zebrafish. Dev Dyn 230(3):481–493. https://doi.org/10.1002/dvdy.20075

    Article  CAS  PubMed  Google Scholar 

  36. Yamamoto K, Vernier P (2011) The evolution of dopamine systems in chordates. Front Neuroanat 5:21. https://doi.org/10.3389/fnana.2011.00021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Tay TL et al (2011) Comprehensive catecholaminergic projectome analysis reveals single-neuron integration of zebrafish ascending and descending dopaminergic systems. Nat Commun 2:171. https://doi.org/10.1038/ncomms1171

    Article  CAS  PubMed  Google Scholar 

  38. Powers CM et al (2011) Silver exposure in developing zebrafish produces persistent synaptic and behavioral changes. Neurotoxicol Teratol 33(2):329–332. https://doi.org/10.1016/j.ntt.2010.10.006

    Article  CAS  PubMed  Google Scholar 

  39. Chatterjee D, Gerlai R (2009) High precision liquid chromatography analysis of dopaminergic and serotoninergic responses to acute alcohol exposure in zebrafish. Behav Brain Res 200(1):208–213. https://doi.org/10.1016/j.bbr.2009.01.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Anichtchik OV et al (2004) Neurochemical and behavioural changes in zebrafish Danio rerio after systemic administration of 6-hydroxydopamine and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. J Neurochem 88(2):443–453. https://doi.org/10.1111/j.1471-4159.2004.02190.x

    Article  CAS  PubMed  Google Scholar 

  41. Scerbina T, Chatterjee D, Gerlai R (2012) Dopamine receptor antagonism disrupts social preference in zebrafish: a strain comparison study. Amino Acids 43(5):2059–2072. https://doi.org/10.1007/s00726-012-1284-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Gomez-Laplaza LM, Gerlai R (2010) Latent learning in zebrafish (Danio rerio). Behav Brain Res 208(2):509–515. https://doi.org/10.1016/j.bbr.2009.12.031

    Article  PubMed  Google Scholar 

  43. Gerlai R (2011) Associative learning in zebrafish (Danio rerio). Methods Cell Biol 101:249–270. https://doi.org/10.1016/B978-0-12-387036-0.00012-8

    Article  PubMed  Google Scholar 

  44. Colwill RM et al (2005) Visual discrimination learning in zebrafish (Danio rerio). Behav Process 70(1):19–31. https://doi.org/10.1016/j.beproc.2005.03.001

    Article  Google Scholar 

  45. Pather S, Gerlai R (2009) Shuttle box learning in zebrafish (Danio rerio). Behav Brain Res 196(2):323–327. https://doi.org/10.1016/j.bbr.2008.09.013

    Article  PubMed  Google Scholar 

  46. Zala SM, Maattanen I (2013) Social learning of an associative foraging task in zebrafish. Naturwissenschaften 100(5):469–472. https://doi.org/10.1007/s00114-013-1017-6

    Article  CAS  PubMed  Google Scholar 

  47. Aoki R, Tsuboi T, Okamoto H (2015) Y-maze avoidance: an automated and rapid associative learning paradigm in zebrafish. Neurosci Res 91:69–72. https://doi.org/10.1016/j.neures.2014.10.012

    Article  PubMed  Google Scholar 

  48. Luchiari AC, Salajan DC, Gerlai R (2015) Acute and chronic alcohol administration: effects on performance of zebrafish in a latent learning task. Behav Brain Res 282:76–83. https://doi.org/10.1016/j.bbr.2014.12.013

    Article  CAS  PubMed  Google Scholar 

  49. Fernandes Y et al (2014) Embryonic alcohol exposure impairs associative learning performance in adult zebrafish. Behav Brain Res 265:181–187. https://doi.org/10.1016/j.bbr.2014.02.035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Sison M, Gerlai R (2010) Associative learning in zebrafish (Danio rerio) in the plus maze. Behav Brain Res 207(1):99–104. https://doi.org/10.1016/j.bbr.2009.09.043

    Article  PubMed  Google Scholar 

  51. Grossman L et al (2011) Effects of piracetam on behavior and memory in adult zebrafish. Brain Res Bull 85(1–2):58–63. https://doi.org/10.1016/j.brainresbull.2011.02.008

    Article  CAS  PubMed  Google Scholar 

  52. Ghosh DD et al (2016) Neural architecture of hunger-dependent multisensory decision making in C. elegans. Neuron 92(5):1049–1062. https://doi.org/10.1016/j.neuron.2016.10.030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Ezcurra M et al (2016) Neuropeptidergic signaling and active feeding state inhibit nociception in Caenorhabditis elegans. J Neurosci 36(11):3157–3169. https://doi.org/10.1523/JNEUROSCI.1128-15.2016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Bendesky A et al (2011) Catecholamine receptor polymorphisms affect decision-making in C. elegans. Nature 472(7343):313–318. https://doi.org/10.1038/nature09821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Stauffer WR et al (2016) Dopamine neuron-specific optogenetic stimulation in rhesus macaques. Cell 166(6):1564–1571. e1566. https://doi.org/10.1016/j.cell.2016.08.024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Baez-Mendoza R, van Coeverden CR, Schultz W (2016) A neuronal reward inequity signal in primate striatum. J Neurophysiol 115(1):68–79. https://doi.org/10.1152/jn.00321.2015

    Article  CAS  PubMed  Google Scholar 

  57. Freeman SM, Rebout N, Bales KL (2018) Effect of reward type on object discrimination learning in socially monogamous coppery titi monkeys (Callicebus cupreus). Am J Primatol 80(6):e22868. https://doi.org/10.1002/ajp.22868

    Article  PubMed  PubMed Central  Google Scholar 

  58. Chang SW et al (2015) Neural mechanisms of social decision-making in the primate amygdala. Proc Natl Acad Sci U S A 112(52):16012–16017. https://doi.org/10.1073/pnas.1514761112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Toda K et al (2012) Differential encoding of factors influencing predicted reward value in monkey rostral anterior cingulate cortex. PLoS One 7(1):e30190. https://doi.org/10.1371/journal.pone.0030190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Murray EA, Rudebeck PH (2018) Specializations for reward-guided decision-making in the primate ventral prefrontal cortex. Nat Rev Neurosci 19(7):404–417. https://doi.org/10.1038/s41583-018-0013-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Opris I, Hampson RE, Deadwyler SA (2009) The encoding of cocaine vs. natural rewards in the striatum of nonhuman primates: categories with different activations. Neuroscience 163(1):40–54. https://doi.org/10.1016/j.neuroscience.2009.06.002

    Article  CAS  PubMed  Google Scholar 

  62. Nakamura K et al (2012) Differential reward coding in the subdivisions of the primate caudate during an oculomotor task. J Neurosci 32(45):15963–15982. https://doi.org/10.1523/JNEUROSCI.1518-12.2012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Hampson RE et al (2011) Effects of cocaine rewards on neural representations of cognitive demand in nonhuman primates. Psychopharmacology 213(1):105–118. https://doi.org/10.1007/s00213-010-2017-2

    Article  CAS  PubMed  Google Scholar 

  64. Arsenault JT et al (2013) Dopaminergic reward signals selectively decrease fMRI activity in primate visual cortex. Neuron 77(6):1174–1186. https://doi.org/10.1016/j.neuron.2013.01.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Walantus W, Elias L, Kriegstein A (2007) In utero intraventricular injection and electroporation of E16 rat embryos. J Vis Exp 6:236. https://doi.org/10.3791/236

    Article  Google Scholar 

  66. Szot GL, Koudria P, Bluestone JA (2007) Transplantation of pancreatic islets into the kidney capsule of diabetic mice. J Vis Exp 9:404. https://doi.org/10.3791/404

    Article  Google Scholar 

  67. Geiger BM et al (2008) Survivable stereotaxic surgery in rodents. J Vis Exp 20:880. https://doi.org/10.3791/880

    Article  Google Scholar 

  68. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates. Academic Press, Amsterdam

    Google Scholar 

  69. Smits SM, Burbach JP, Smidt MP (2006) Developmental origin and fate of meso-diencephalic dopamine neurons. Prog Neurobiol 78(1):1–16. https://doi.org/10.1016/j.pneurobio.2005.12.003

    Article  CAS  PubMed  Google Scholar 

  70. Carlezon WA Jr, Thomas MJ (2009) Biological substrates of reward and aversion: a nucleus accumbens activity hypothesis. Neuropharmacology 56(Suppl 1):122–132

    Article  CAS  PubMed  Google Scholar 

  71. Proulx CD, Hikosaka O, Malinow R (2014) Reward processing by the lateral habenula in normal and depressive behaviors. Nat Neurosci 17(9):1146–1152. https://doi.org/10.1038/nn.3779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Hikosaka O (2010) The habenula: from stress evasion to value-based decision-making. Nat Rev Neurosci 11(7):503–513. https://doi.org/10.1038/nrn2866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Brunzell DH et al (2009) Nucleus accumbens CREB activity is necessary for nicotine conditioned place preference. Neuropsychopharmacology 34(8):1993–2001. https://doi.org/10.1038/npp.2009.11

    Article  CAS  PubMed  Google Scholar 

  74. Neumaier JF et al (2002) Elevated expression of 5-HT1B receptors in nucleus accumbens afferents sensitizes animals to cocaine. J Neurosci 22(24):10856–10863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Smedley EB, DiLeo A, Smith KS (2019) Circuit directionality for motivation: Lateral accumbens-pallidum, but not pallidum-accumbens, connections regulate motivational attraction to reward cues. Neurobiol Learn Mem 162:23–35. https://doi.org/10.1016/j.nlm.2019.05.001

    Article  PubMed  PubMed Central  Google Scholar 

  76. Dreyer JK et al (2016) Functionally distinct dopamine signals in nucleus accumbens core and shell in the freely moving rat. J Neurosci 36(1):98–112. https://doi.org/10.1523/JNEUROSCI.2326-15.2016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Fortin SM et al (2015) Sampling phasic dopamine signaling with fast-scan cyclic voltammetry in awake, behaving rats. Curr Protoc Neurosci 70:7.25.1–7.25.20. https://doi.org/10.1002/0471142301.ns0725s70

    Article  CAS  Google Scholar 

  78. Sackett DA, Saddoris MP, Carelli RM (2017) Nucleus accumbens shell dopamine preferentially tracks information related to outcome value of reward. eNeuro 4(3):ENEURO.0058-17.2017. https://doi.org/10.1523/ENEURO.0058-17.2017

    Article  PubMed  PubMed Central  Google Scholar 

  79. Saddoris MP et al (2015) Differential dopamine release dynamics in the nucleus accumbens core and shell reveal complementary signals for error prediction and incentive motivation. J Neurosci 35(33):11572–11582. https://doi.org/10.1523/JNEUROSCI.2344-15.2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Fortin SM, Roitman MF (2017) Central GLP-1 receptor activation modulates cocaine-evoked phasic dopamine signaling in the nucleus accumbens core. Physiol Behav 176:17–25. https://doi.org/10.1016/j.physbeh.2017.03.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Covey DP et al (2016) Amphetamine elevates nucleus accumbens dopamine via an action potential-dependent mechanism that is modulated by endocannabinoids. Eur J Neurosci 43(12):1661–1673. https://doi.org/10.1111/ejn.13248

    Article  PubMed  PubMed Central  Google Scholar 

  82. Pomeranz LE et al (2017) Gene expression profiling with cre-conditional pseudorabies virus reveals a subset of midbrain neurons that participate in reward circuitry. J Neurosci 37(15):4128–4144. https://doi.org/10.1523/JNEUROSCI.3193-16.2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Schelp SA et al (2017) A transient dopamine signal encodes subjective value and causally influences demand in an economic context. Proc Natl Acad Sci U S A 114(52):E11303–E11312. https://doi.org/10.1073/pnas.1706969114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Collins AL et al (2016) Nucleus accumbens acetylcholine receptors modulate dopamine and motivation. Neuropsychopharmacology 41(12):2830–2838. https://doi.org/10.1038/npp.2016.81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. O'Neill B et al (2014) Behavior of knock-in mice with a cocaine-insensitive dopamine transporter after virogenetic restoration of cocaine sensitivity in the striatum. Neuropharmacology 79:626–633. https://doi.org/10.1016/j.neuropharm.2013.12.023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Heller EA et al (2016) Targeted epigenetic remodeling of the Cdk5 gene in nucleus accumbens regulates cocaine- and stress-evoked behavior. J Neurosci 36(17):4690–4697. https://doi.org/10.1523/JNEUROSCI.0013-16.2016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Werner CT et al (2018) E3 ubiquitin-protein ligase SMURF1 in the nucleus accumbens mediates cocaine seeking. Biol Psychiatry 84(12):881–892. https://doi.org/10.1016/j.biopsych.2018.07.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Ferguson D et al (2015) SIRT1-FOXO3a regulate cocaine actions in the nucleus accumbens. J Neurosci 35(7):3100–3111. https://doi.org/10.1523/JNEUROSCI.4012-14.2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Foldi CJ, Milton LK, Oldfield BJ (2017) The role of mesolimbic reward neurocircuitry in prevention and rescue of the activity-based anorexia (ABA) phenotype in rats. Neuropsychopharmacology 42(12):2292–2300. https://doi.org/10.1038/npp.2017.63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Bailey MR et al (2018) An interaction between serotonin receptor signaling and dopamine enhances goal-directed vigor and persistence in mice. J Neurosci 38(9):2149–2162. https://doi.org/10.1523/JNEUROSCI.2088-17.2018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Kim HD et al (2016) SIRT1 mediates depression-like behaviors in the nucleus accumbens. J Neurosci 36(32):8441–8452. https://doi.org/10.1523/JNEUROSCI.0212-16.2016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Chen NA et al (2014) Knockdown of CRF1 receptors in the ventral tegmental area attenuates cue- and acute food deprivation stress-induced cocaine seeking in mice. J Neurosci 34(35):11560–11570. https://doi.org/10.1523/JNEUROSCI.4763-12.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Mikhailova MA et al (2016) Optogenetically-induced tonic dopamine release from VTA-nucleus accumbens projections inhibits reward consummatory behaviors. Neuroscience 333:54–64. https://doi.org/10.1016/j.neuroscience.2016.07.006

    Article  CAS  PubMed  Google Scholar 

  94. Wakabayashi KT et al (2016) Application of fast-scan cyclic voltammetry for the in vivo characterization of optically evoked dopamine in the olfactory tubercle of the rat brain. Analyst 141(12):3746–3755. https://doi.org/10.1039/c6an00196c

    Article  CAS  PubMed  Google Scholar 

  95. Singh S et al (2018) Axin-2 knockdown promote mitochondrial biogenesis and dopaminergic neurogenesis by regulating Wnt/beta-catenin signaling in rat model of Parkinson’s disease. Free Radic Biol Med 129:73–87. https://doi.org/10.1016/j.freeradbiomed.2018.08.033

    Article  CAS  PubMed  Google Scholar 

  96. Voronkov DN et al (2019) Immunohistochemical assessment of the compensatory responses in rat olfactory bulbs after 6-hydroxydopamine-induced lesion of the substantia nigra. Bull Exp Biol Med 166(6):811–815. https://doi.org/10.1007/s10517-019-04446-8

    Article  CAS  PubMed  Google Scholar 

  97. Ramalingam M, Huh YJ, Lee YI (2019) The Impairments of alpha-synuclein and mechanistic target of rapamycin in rotenone-induced SH-SY5Y cells and mice model of Parkinson’s disease. Front Neurosci 13:1028. https://doi.org/10.3389/fnins.2019.01028

    Article  PubMed  PubMed Central  Google Scholar 

  98. Shnitko TA, Robinson DL (2015) Regional variation in phasic dopamine release during alcohol and sucrose self-administration in rats. ACS Chem Neurosci 6(1):147–154. https://doi.org/10.1021/cn500251j

    Article  CAS  PubMed  Google Scholar 

  99. Hernandez G et al (2016) Ventral midbrain NMDA receptor blockade: from enhanced reward and dopamine inactivation. Front Behav Neurosci 10:161. https://doi.org/10.3389/fnbeh.2016.00161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Orsini CA et al (2017) Optogenetic inhibition reveals distinct roles for basolateral amygdala activity at discrete time points during risky decision making. J Neurosci 37(48):11537–11548. https://doi.org/10.1523/JNEUROSCI.2344-17.2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Mahoney CE et al (2017) GABAergic neurons of the central amygdala promote cataplexy. J Neurosci 37(15):3995–4006. https://doi.org/10.1523/JNEUROSCI.4065-15.2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Harasta AE et al (2015) Septal glucagon-like peptide 1 receptor expression determines suppression of cocaine-induced behavior. Neuropsychopharmacology 40(8):1969–1978. https://doi.org/10.1038/npp.2015.47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Cates HM et al (2019) A novel role for E2F3b in regulating cocaine action in the prefrontal cortex. Neuropsychopharmacology 44(4):776–784. https://doi.org/10.1038/s41386-018-0296-1

    Article  PubMed  Google Scholar 

  104. Steidl S et al (2017) Operant responding for optogenetic excitation of LDTg inputs to the VTA requires D1 and D2 dopamine receptor activation in the NAcc. Behav Brain Res 333:161–170. https://doi.org/10.1016/j.bbr.2017.06.045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Fakhoury M, Rompre PP, Boye SM (2016) Role of the dorsal diencephalic conduction system in the brain reward circuitry. Behav Brain Res 296:431–441. https://doi.org/10.1016/j.bbr.2015.10.038

    Article  PubMed  Google Scholar 

  106. Fakhoury M et al (2016) Effect of electrolytic lesions of the dorsal diencephalic conduction system on the distribution of Fos-like immunoreactivity induced by rewarding electrical stimulation. Neuroscience 334:214–225. https://doi.org/10.1016/j.neuroscience.2016.08.002

    Article  CAS  PubMed  Google Scholar 

  107. Bian J et al (2013) Lentiviral vector-mediated knockdown of Lrb in the arcuate nucleus promotes diet-induced obesity in rats. J Mol Endocrinol 51(1):27–35. https://doi.org/10.1530/JME-12-0212

    Article  CAS  PubMed  Google Scholar 

  108. Gaspar JM et al (2018) Downregulation of HIF complex in the hypothalamus exacerbates diet-induced obesity. Brain Behav Immun 73:550–561. https://doi.org/10.1016/j.bbi.2018.06.020

    Article  CAS  PubMed  Google Scholar 

  109. Fish EW et al (2014) Different contributions of dopamine D1 and D2 receptor activity to alcohol potentiation of brain stimulation reward in C57BL/6J and DBA/2J mice. J Pharmacol Exp Ther 350(2):322–329. https://doi.org/10.1124/jpet.114.216135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Robinson JE et al (2012) Mephedrone (4-methylmethcathinone) and intracranial self-stimulation in C57BL/6J mice: comparison to cocaine. Behav Brain Res 234(1):76–81. https://doi.org/10.1016/j.bbr.2012.06.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Fish EW et al (2010) Alcohol, cocaine, and brain stimulation-reward in C57Bl6/J and DBA2/J mice. Alcohol Clin Exp Res 34(1):81–89. https://doi.org/10.1111/j.1530-0277.2009.01069.x

    Article  CAS  PubMed  Google Scholar 

  112. Kolodziej A et al (2014) SPECT-imaging of activity-dependent changes in regional cerebral blood flow induced by electrical and optogenetic self-stimulation in mice. NeuroImage 103:171–180. https://doi.org/10.1016/j.neuroimage.2014.09.023

    Article  PubMed  Google Scholar 

  113. Simon MJ, Molina F, Puerto A (2009) Conditioned place preference but not rewarding self-stimulation after electrical activation of the external lateral parabrachial nucleus. Behav Brain Res 205(2):443–449. https://doi.org/10.1016/j.bbr.2009.07.028

    Article  PubMed  Google Scholar 

  114. Paxinos G, Watson C (2014) Paxino’s and Watson’s: The rat brain in stereotaxic coordinates. Seventh edition. edn. Elsevier/AP, Academic Press is an imprint of Elsevier, Amsterdam; Boston

    Google Scholar 

  115. Paxinos G et al (1985) Bregma, lambda and the interaural midpoint in stereotaxic surgery with rats of different sex, strain and weight. J Neurosci Methods 13(2):139–143

    Article  CAS  PubMed  Google Scholar 

  116. Brocka M et al (2018) Contributions of dopaminergic and non-dopaminergic neurons to VTA-stimulation induced neurovascular responses in brain reward circuits. NeuroImage 177:88–97. https://doi.org/10.1016/j.neuroimage.2018.04.059

    Article  CAS  PubMed  Google Scholar 

  117. Geiger BM et al (2009) Deficits of mesolimbic dopamine neurotransmission in rat dietary obesity. Neuroscience 159(4):1193–1199. https://doi.org/10.1016/j.neuroscience.2009.02.007

    Article  CAS  PubMed  Google Scholar 

  118. Pothos EN, Sulzer D, Hoebel BG (1998) Plasticity of quantal size in ventral midbrain dopamine neurons: possible implications for the neurochemistry of feeding and reward. Appetite 31(3):405. https://doi.org/10.1006/appe.1998.0210

    Article  CAS  PubMed  Google Scholar 

  119. Cederfjall E, Sahin G, Kirik D, Bjorklund T (2012) Design of a single AAV vector for coexpression of TH and GCH1 to establish continuous DOPA synthesis in a rat model of Parkinson's disease. Mol Ther 20:1315–1326

    Article  PubMed  PubMed Central  Google Scholar 

  120. Tokuoka H et al (2011) Compensatory regulation of dopamine after ablation of the tyrosine hydroxylase gene in the nigrostriatal projection. J Biol Chem 286(50):43549–43558. https://doi.org/10.1074/jbc.M111.284729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Bocarsly ME et al (2014) GS 455534 selectively suppresses binge eating of palatable food and attenuates dopamine release in the accumbens of sugar-bingeing rats. Behav Pharmacol 25(2):147–157. https://doi.org/10.1097/FBP.0000000000000029

    Article  CAS  PubMed  Google Scholar 

  122. Rada P et al (2010) Opioids in the hypothalamus control dopamine and acetylcholine levels in the nucleus accumbens. Brain Res 1312:1–9. https://doi.org/10.1016/j.brainres.2009.11.055

    Article  CAS  PubMed  Google Scholar 

  123. Avena N, Rada P, Hoebel B (2008) Evidence for sugar addiction: Behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci Biobehav Rev 32(1):20–39

    Article  CAS  PubMed  Google Scholar 

  124. Avena NM et al (2008) After daily bingeing on a sucrose solution, food deprivation induces anxiety and accumbens dopamine/acetylcholine imbalance. Physiol Behav 94(3):309–315. https://doi.org/10.1016/j.physbeh.2008.01.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Avena NM et al (2006) Sucrose sham feeding on a binge schedule releases accumbens dopamine repeatedly and eliminates the acetylcholine satiety response. Neuroscience 139(3):813–820. https://doi.org/10.1016/j.neuroscience.2005.12.037

    Article  CAS  PubMed  Google Scholar 

  126. Rada P, Avena NM, Hoebel BG (2005) Daily bingeing on sugar repeatedly releases dopamine in the accumbens shell. Neuroscience 134(3):737–744

    Article  CAS  PubMed  Google Scholar 

  127. Jamal M et al (2019) COA-Cl induces dopamine release and tyrosine hydroxylase phosphorylation: In vivo reverse microdialysis and in vitro analysis. Brain Res 1706:68–74. https://doi.org/10.1016/j.brainres.2018.10.026

    Article  CAS  PubMed  Google Scholar 

  128. Chefer VI et al (2006) Quantitative no-net-flux microdialysis permits detection of increases and decreases in dopamine uptake in mouse nucleus accumbens. J Neurosci Methods 155(2):187–193. https://doi.org/10.1016/j.jneumeth.2005.12.018

  129. Cremers TI et al (2009) Quantitative microdialysis using modified ultraslow microdialysis: direct rapid and reliable determination of free brain concentrations with the MetaQuant technique. J Neurosci Methods 178(2):249–254. https://doi.org/10.1016/j.jneumeth.2008.12.010

  130. de Vries MG et al (2003) Extracellular glucose in rat ventromedial hypothalamus during acute and recurrent hypoglycemia. Diabetes 52(11):2767–2773. https://doi.org/10.2337/diabetes.52.11.2767

  131. Justice JB, Jr (1993) Quantitative microdialysis of neurotransmitters. J Neurosci Methods 48(3):263–276. https://doi.org/10.1016/0165-0270(93)90097-b

  132. Unger EL et al (2014) Low brain iron effects and reversibility on striatal dopamine dynamics. Exp Neurol 261:462–468. https://doi.org/10.1016/j.expneurol.2014.06.023

  133. Borkar CD et al (2016) Neuropeptide Y system in accumbens shell mediates ethanol self-administration in posterior ventral tegmental area. Addict Biol 21(4):766–775. https://doi.org/10.1111/adb.12254

    Article  CAS  PubMed  Google Scholar 

  134. Burton AC et al (2018) Previous cocaine self-administration disrupts reward expectancy encoding in ventral striatum. Neuropsychopharmacology 43(12):2350–2360. https://doi.org/10.1038/s41386-018-0058-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Mogenson GJ et al (1979) Self-stimulation of the nucleus accumbens and ventral tegmental area of Tsai attenuated by microinjections of spiroperidol into the nucleus accumbens. Brain Res 171(2):247–259. https://doi.org/10.1016/0006-8993(79)90331-7

    Article  CAS  PubMed  Google Scholar 

  136. Jenkins OF, Atrens DM, Jackson DM (1983) Self-stimulation of the nucleus accumbens and some comparisons with hypothalamic self-stimulation. Pharmacol Biochem Behav 18(4):585–591. https://doi.org/10.1016/0091-3057(83)90285-x

    Article  PubMed  Google Scholar 

  137. Sasaki K et al (1984) The effects of feeding and rewarding brain stimulation on lateral hypothalamic unit activity in freely moving rats. Brain Res 322(2):201–211. https://doi.org/10.1016/0006-8993(84)90110-0

    Article  CAS  PubMed  Google Scholar 

  138. Farakhor S, Shalchyan V, Daliri MR (2019) Adaptation effects of medial forebrain bundle micro-electrical stimulation. Bioengineered 10(1):78–86. https://doi.org/10.1080/21655979.2019.1599628

    Article  PubMed  PubMed Central  Google Scholar 

  139. Katsidoni V, Kastellakis A, Panagis G (2013) Biphasic effects of Delta9-tetrahydrocannabinol on brain stimulation reward and motor activity. Int J Neuropsychopharmacol 16(10):2273–2284. https://doi.org/10.1017/S1461145713000709

    Article  CAS  PubMed  Google Scholar 

  140. Garcia R, Zafra MA, Puerto A (2015) Rewarding effects of electrical stimulation of the insular cortex: decayed effectiveness after repeated tests and subsequent increase in vertical behavioral activity and conditioned place aversion after naloxone administration. Neurobiol Learn Mem 118:64–73. https://doi.org/10.1016/j.nlm.2014.11.008

    Article  CAS  PubMed  Google Scholar 

  141. Grim TW et al (2015) Effects of acute and repeated dosing of the synthetic cannabinoid CP55,940 on intracranial self-stimulation in mice. Drug Alcohol Depend 150:31–37. https://doi.org/10.1016/j.drugalcdep.2015.01.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. van Wolfswinkel L, Seifert WF, van Ree JM (1988) Catecholamines and endogenous opioids in ventral tegmental self-stimulation reward. Pharmacol Biochem Behav 30(3):589–595. https://doi.org/10.1016/0091-3057(88)90070-6

    Article  PubMed  Google Scholar 

  143. Marcangione C, Rompre PP (2008) Topographical Fos induction within the ventral midbrain and projection sites following self-stimulation of the posterior mesencephalon. Neuroscience 154(4):1227–1241. https://doi.org/10.1016/j.neuroscience.2008.05.014

    Article  CAS  PubMed  Google Scholar 

  144. Fish EW et al (2014) Effects of the neuroactive steroid allopregnanolone on intracranial self-stimulation in C57BL/6J mice. Psychopharmacology 231(17):3415–3423. https://doi.org/10.1007/s00213-014-3600-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Gigante ED et al (2016) Optogenetic activation of a lateral hypothalamic-ventral tegmental drive-reward pathway. PLoS One 11(7):e0158885. https://doi.org/10.1371/journal.pone.0158885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Touzani K, Velley L (1998) Electrical self-stimulation in the central amygdaloid nucleus after ibotenic acid lesion of the lateral hypothalamus. Behav Brain Res 90(2):115–124. https://doi.org/10.1016/s0166-4328(97)00090-9

    Article  CAS  PubMed  Google Scholar 

  147. Garcia R, Simon MJ, Puerto A (2013) Conditioned place preference induced by electrical stimulation of the insular cortex: effects of naloxone. Exp Brain Res 226(2):165–174. https://doi.org/10.1007/s00221-013-3422-7

    Article  CAS  PubMed  Google Scholar 

  148. Bahi A, Dreyer JL (2008) Overexpression of plasminogen activators in the nucleus accumbens enhances cocaine-, amphetamine- and morphine-induced reward and behavioral sensitization. Genes Brain Behav 7(2):244–256. https://doi.org/10.1111/j.1601-183X.2007.00346.x

    Article  CAS  PubMed  Google Scholar 

  149. Runegaard AH et al (2018) Locomotor- and Reward-enhancing effects of cocaine are differentially regulated by chemogenetic stimulation of gi-signaling in dopaminergic neurons. eNeuro 5(3):ENEURO.0345-17.2018. https://doi.org/10.1523/ENEURO.0345-17.2018

    Article  PubMed  PubMed Central  Google Scholar 

  150. Towne C, Thompson KR (2016) Overview on research and clinical applications of optogenetics. Curr Protoc Pharmacol 75:11.19.11–11.19.21. https://doi.org/10.1002/cpph.13

    Article  Google Scholar 

  151. Deisseroth K (2011) Optogenetics. Nat Methods 8(1):26–29. https://doi.org/10.1038/nmeth.f.324

    Article  CAS  PubMed  Google Scholar 

  152. Deisseroth K et al (2006) Next-generation optical technologies for illuminating genetically targeted brain circuits. J Neurosci 26(41):10380–10386. https://doi.org/10.1523/JNEUROSCI.3863-06.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Berrios J et al (2016) Loss of UBE3A from TH-expressing neurons suppresses GABA co-release and enhances VTA-NAc optical self-stimulation. Nat Commun 7:10702. https://doi.org/10.1038/ncomms10702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Han X et al (2017) Role of dopamine projections from ventral tegmental area to nucleus accumbens and medial prefrontal cortex in reinforcement behaviors assessed using optogenetic manipulation. Metab Brain Dis 32(5):1491–1502. https://doi.org/10.1007/s11011-017-0023-3

    Article  CAS  PubMed  Google Scholar 

  155. van Zessen R et al (2012) Activation of VTA GABA neurons disrupts reward consumption. Neuron 73(6):1184–1194. https://doi.org/10.1016/j.neuron.2012.02.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Wolfman SL et al (2018) Nicotine aversion is mediated by GABAergic interpeduncular nucleus inputs to laterodorsal tegmentum. Nat Commun 9(1):2710. https://doi.org/10.1038/s41467-018-04654-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Shabel SJ et al (2012) Input to the lateral habenula from the basal ganglia is excitatory, aversive, and suppressed by serotonin. Neuron 74(3):475–481. https://doi.org/10.1016/j.neuron.2012.02.037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Lammel S et al (2012) Input-specific control of reward and aversion in the ventral tegmental area. Nature 491(7423):212–217. https://doi.org/10.1038/nature11527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Stamatakis AM et al (2013) A unique population of ventral tegmental area neurons inhibits the lateral habenula to promote reward. Neuron 80(4):1039–1053. https://doi.org/10.1016/j.neuron.2013.08.023

    Article  CAS  PubMed  Google Scholar 

  160. Sharpe MJ et al (2017) Lateral hypothalamic GABAergic neurons encode reward predictions that are relayed to the ventral tegmental area to regulate learning. Curr Biol 27(14):2089–2100. e2085. https://doi.org/10.1016/j.cub.2017.06.024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Barbano MF et al (2016) Feeding and reward are differentially induced by activating GABAergic lateral hypothalamic projections to VTA. J Neurosci 36(10):2975–2985. https://doi.org/10.1523/JNEUROSCI.3799-15.2016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Steidl S et al (2017) Optogenetic excitation in the ventral tegmental area of glutamatergic or cholinergic inputs from the laterodorsal tegmental area drives reward. Eur J Neurosci 45(4):559–571. https://doi.org/10.1111/ejn.13436

    Article  PubMed  Google Scholar 

  163. de Jong JW et al (2019) A neural circuit mechanism for encoding aversive stimuli in the mesolimbic dopamine system. Neuron 101(1):133–151. e137. https://doi.org/10.1016/j.neuron.2018.11.005

    Article  CAS  PubMed  Google Scholar 

  164. Wang D et al (2017) Learning shapes the aversion and reward responses of lateral habenula neurons. elife 6:e23045. https://doi.org/10.7554/eLife.23045

    Article  PubMed  PubMed Central  Google Scholar 

  165. Li Y et al (2016) Serotonin neurons in the dorsal raphe nucleus encode reward signals. Nat Commun 7:10503. https://doi.org/10.1038/ncomms10503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Moriya S et al (2018) Acute aversive stimuli rapidly increase the activity of ventral tegmental area dopamine neurons in awake mice. Neuroscience 386:16–23. https://doi.org/10.1016/j.neuroscience.2018.06.027

    Article  CAS  PubMed  Google Scholar 

  167. Zhong W et al (2017) Learning and stress shape the reward response patterns of serotonin neurons. J Neurosci 37(37):8863–8875. https://doi.org/10.1523/JNEUROSCI.1181-17.2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Wei C et al (2018) Response dynamics of midbrain dopamine neurons and serotonin neurons to heroin, nicotine, cocaine, and MDMA. Cell Discov 4:60. https://doi.org/10.1038/s41421-018-0060-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Rodeberg NT et al (2017) Hitchhiker’s guide to voltammetry: acute and chronic electrodes for in vivo fast-scan cyclic voltammetry. ACS Chem Neurosci 8(2):221–234. https://doi.org/10.1021/acschemneuro.6b00393

    Article  CAS  PubMed  Google Scholar 

  170. Colon-Gonzalez F et al (2013) Obesity pharmacotherapy: what is next? Mol Asp Med 34(1):71–83. https://doi.org/10.1016/j.mam.2012.10.005

    Article  CAS  Google Scholar 

  171. Klanker M et al (2017) Deep brain stimulation of the medial forebrain bundle elevates striatal dopamine concentration without affecting spontaneous or reward-induced phasic release. Neuroscience 364:82–92. https://doi.org/10.1016/j.neuroscience.2017.09.012

    Article  CAS  PubMed  Google Scholar 

  172. Oliva I, Wanat MJ (2019) Operant costs modulate dopamine release to self-administered cocaine. J Neurosci 39(7):1249–1260. https://doi.org/10.1523/JNEUROSCI.1721-18.2018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Chartoff EH et al (2016) Relative timing between kappa opioid receptor activation and cocaine determines the impact on reward and dopamine release. Neuropsychopharmacology 41(4):989–1002. https://doi.org/10.1038/npp.2015.226

    Article  CAS  PubMed  Google Scholar 

  174. Bobak MJ et al (2016) Modafinil activates phasic dopamine signaling in dorsal and ventral striata. J Pharmacol Exp Ther 359(3):460–470. https://doi.org/10.1124/jpet.116.236000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Ferreira NR et al (2018) Simultaneous measurements of ascorbate and glutamate in vivo in the rat brain using carbon fiber nanocomposite sensors and microbiosensor arrays. Bioelectrochemistry 121:142–150. https://doi.org/10.1016/j.bioelechem.2018.01.009

    Article  CAS  PubMed  Google Scholar 

  176. Zlebnik NE et al (2014) Long-term reduction of cocaine self-administration in rats treated with adenoviral vector-delivered cocaine hydrolase: evidence for enzymatic activity. Neuropsychopharmacology 39(6):1538–1546. https://doi.org/10.1038/npp.2014.3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Muir J et al (2018) In vivo fiber photometry reveals signature of future stress susceptibility in nucleus accumbens. Neuropsychopharmacology 43(2):255–263. https://doi.org/10.1038/npp.2017.122

    Article  CAS  PubMed  Google Scholar 

  178. Salinas-Hernandez XI et al (2018) Dopamine neurons drive fear extinction learning by signaling the omission of expected aversive outcomes. Elife 7:e38818. https://doi.org/10.7554/eLife.38818

    Article  PubMed  PubMed Central  Google Scholar 

  179. Menegas W et al (2017) Opposite initialization to novel cues in dopamine signaling in ventral and posterior striatum in mice. elife 6:e21886. https://doi.org/10.7554/eLife.21886

    Article  PubMed  PubMed Central  Google Scholar 

  180. Parker KE et al (2019) A paranigral VTA nociceptin circuit that constrains motivation for reward. Cell 178(3):653–671. e619. https://doi.org/10.1016/j.cell.2019.06.034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Itoga CA et al (2019) New viral-genetic mapping uncovers an enrichment of corticotropin-releasing hormone-expressing neuronal inputs to the nucleus accumbens from stress-related brain regions. J Comp Neurol 527(15):2474–2487. https://doi.org/10.1002/cne.24676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  182. Clark RA, Ewing AG (1997) Quantitative measurements of released amines from individual exocytosis events. Mol Neurobiol 15(1):1–16. https://doi.org/10.1007/BF02740612

    Article  CAS  PubMed  Google Scholar 

  183. Benoit-Marand M, Jaber M, Gonon F (2000) Release and elimination of dopamine in vivo in mice lacking the dopamine transporter: functional consequences. Eur J Neurosci 12(8):2985–2992. https://doi.org/10.1046/j.1460-9568.2000.00155.x

    Article  CAS  PubMed  Google Scholar 

  184. Sulzer D, Pothos EN (2000) Regulation of quantal size by presynaptic mechanisms. Rev Neurosci 11(2–3):159–212. https://doi.org/10.1515/revneuro.2000.11.2-3.159

    Article  CAS  PubMed  Google Scholar 

  185. Geiger BM et al (2008) Evidence for defective mesolimbic dopamine exocytosis in obesity-prone rats. FASEB J 22(8):2740–2746. https://doi.org/10.1096/fj.08-110759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Schuweiler DR et al (2018) Effects of an acute therapeutic or rewarding dose of amphetamine on acquisition of Pavlovian autoshaping and ventral striatal dopamine signaling. Behav Brain Res 336:191–203. https://doi.org/10.1016/j.bbr.2017.09.003

    Article  CAS  PubMed  Google Scholar 

  187. Hart AS, Clark JJ, Phillips PEM (2015) Dynamic shaping of dopamine signals during probabilistic Pavlovian conditioning. Neurobiol Learn Mem 117:84–92. https://doi.org/10.1016/j.nlm.2014.07.010

    Article  CAS  PubMed  Google Scholar 

  188. Aitken TJ, Greenfield VY, Wassum KM (2016) Nucleus accumbens core dopamine signaling tracks the need-based motivational value of food-paired cues. J Neurochem 136(5):1026–1036. https://doi.org/10.1111/jnc.13494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Sunsay C, Rebec GV (2014) Extinction and reinstatement of phasic dopamine signals in the nucleus accumbens core during Pavlovian conditioning. Behav Neurosci 128(5):579–587. https://doi.org/10.1037/bne0000012

    Article  PubMed  PubMed Central  Google Scholar 

  190. Jing M et al (2018) A genetically encoded fluorescent acetylcholine indicator for in vitro and in vivo studies. Nat Biotechnol 36(8):726–737. https://doi.org/10.1038/nbt.4184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. Marvin JS et al (2019) A genetically encoded fluorescent sensor for in vivo imaging of GABA. Nat Methods 16(8):763–770. https://doi.org/10.1038/s41592-019-0471-2

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The original research work of the authors cited in this chapter was funded by NIH/NIDA (F31 DA023760; BMG), NIH/NIDDK (R01 DK065872 and ARRA 3R01DK065872-04S1; ENP) as well as an Award of Excellence in Biomedical Research by the Smith Family Foundation (ENP). Fondly dedicated to late Prof. Bartley G. Hoebel who extensively contributed to our understanding of the neurobiology of reward .

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Authors and Affiliations

  1. Department of Biomedical and Nutritional Sciences, Zuckerberg College of Health Sciences, University of Massachusetts Lowell, Lowell, MA, USA

    Brenda M. Geiger & Monika Irene

  2. Program in Pharmacology and Experimental Therapeutics & Pharmacology and Drug Development, Graduate School of Biomedical Sciences, Department of Immunology (Former Integrative Physiology and Pathobiology), Tufts University School of Medicine, Boston, MA, USA

    Emmanuel N. Pothos

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  1. Brenda M. Geiger
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  2. Monika Irene
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  3. Emmanuel N. Pothos
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Correspondence to Brenda M. Geiger or Emmanuel N. Pothos .

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  1. Department of Natural Sciences, School of Arts and Sciences, Lebanese American University, Beirut, Lebanon

    Marc Fakhoury

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Geiger, B.M., Irene, M., Pothos, E.N. (2021). Stereotaxic Surgery in Rodents for Stimulation of the Brain Reward System. In: Fakhoury, M. (eds) The Brain Reward System. Neuromethods, vol 165. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-1146-3_2

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