Opposite initialization to novel cues in dopamine signaling in ventral and posterior striatum in mice

eLife

Volumn 6, Issue , 2017, Pages

  Menegas, William ^a   Babayan, Benedicte M ^a   Uchida, Naoshige ^a   Watabe Uchida, Mitsuko ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; CONDITIONED REFLEX; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EXCITATION; FLUOROMETRY; IMPLANTATION; LICKING; MALE; MICROSCOPY; MOUSE; NERVE CELL STIMULATION; NERVE FIBER MEMBRANE POTENTIAL; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; REWARD; SIGNAL TRANSDUCTION; STIMULUS RESPONSE; VENTRAL STRIATUM; ANIMAL; METABOLISM; PHYSIOLOGY;

ADRENERGIC RECEPTOR STIMULATING AGENT; DOPAMINE;

ANIMALS; CUES; DOPAMINE; DOPAMINERGIC NEURONS; FLUOROMETRY; MICE; SYMPATHOMIMETICS; VENTRAL STRIATUM;

EID: 85011015312     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.21886     Document Type: Article

References (92)

1. Adelsberger H, Garaschuk O, Konnerth A. 2005. Cortical calcium waves in resting newborn mice. Nature Neuroscience 8:988-990. doi: 10.1038/nn1502, PMID: 16007081
2. Akerboom J, Chen TW, Wardill TJ, Tian L, Marvin JS, Mutlu S, Calderón NC, Esposti F, Borghuis BG, Sun XR, Gordus A, Orger MB, Portugues R, Engert F, Macklin JJ, Filosa A, Aggarwal A, Kerr RA, Takagi R, Kracun S, et al. 2012. Optimization of a GCaMP calcium indicator for neural activity imaging. Journal of Neuroscience 32: 13819-13840. doi: 10.1523/JNEUROSCI.2601-12.2012, PMID: 23035093
3. Aransay A, Rodríguez-López C, García-Amado M, Clascá F, Prensa L. 2015. Long-range projection neurons of the mouse ventral tegmental area: a single-cell axon tracing analysis. Frontiers in Neuroanatomy 9:59. doi: 10.3389/fnana.2015.00059, PMID: 26042000
4. Barto AG, Fagg AH, Sitkoff N, Houk JC. 1999. A cerebellar model of timing and prediction in the control of reaching. Neural Computation 11:565-594. doi: 10.1162/089976699300016575, PMID: 10085421
5. Bayer HM, Glimcher PW. 2005. Midbrain dopamine neurons encode a quantitative reward prediction error signal. Neuron 47:129-141. doi: 10.1016/j.neuron.2005.05.020, PMID: 15996553
6. Beier KT, Steinberg EE, DeLoach KE, Xie S, Miyamichi K, Schwarz L, Gao XJ, Kremer EJ, Malenka RC, Luo L. 2015. Circuit architecture of VTA dopamine neurons revealed by systematic Input-Output mapping. Cell 162: 622-634. doi: 10.1016/j.cell.2015.07.015, PMID: 26232228
7. Boehnke SE, Berg DJ, Marino RA, Baldi PF, Itti L, Munoz DP. 2011. Visual adaptation and novelty responses in the superior colliculus. European Journal of Neuroscience 34:766-779. doi: 10.1111/j.1460-9568.2011.07805.x, PMID: 21864319
8. Braver TS, Cohen JD. 1999. Dopamine, cognitive control, and schizophrenia: the gating model. Progress in Brain Research 121:327-349. doi: 10.1016/S0079-6123(08)63082-4, PMID: 10551035
9. Brischoux F, Chakraborty S, Brierley DI, Ungless MA. 2009. Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. PNAS 106:4894-4899. doi: 10.1073/pnas.0811507106, PMID: 19261850
10. Bromberg-Martin ES, Matsumoto M, Hikosaka O. 2010. Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 68:815-834. doi: 10.1016/j.neuron.2010.11.022, PMID: 21144997
11. Brown J, Bullock D, Grossberg S. 1999. How the basal ganglia use parallel excitatory and inhibitory learning pathways to selectively respond to unexpected rewarding cues. Journal of Neuroscience 19:10502-10511. PMID: 10575046
12. Bäckman CM, Malik N, Zhang Y, Shan L, Grinberg A, Hoffer BJ, Westphal H, Tomac AC. 2006. Characterization of a mouse strain expressing cre recombinase from the 3' untranslated region of the dopamine transporter locus. Genesis 44:383-390. doi: 10.1002/dvg.20228, PMID: 16865686
13. Chen Q, Cichon J, Wang W, Qiu L, Lee SJ, Campbell NR, Destefino N, Goard MJ, Fu Z, Yasuda R, Looger LL, Arenkiel BR, Gan WB, Feng G. 2012. Imaging neural activity using Thy1-GCaMP transgenic mice. Neuron 76: 297-308. doi: 10.1016/j.neuron.2012.07.011, PMID: 23083733
14. Chen TW, Wardill TJ, Sun Y, Pulver SR, Renninger SL, Baohan A, Schreiter ER, Kerr RA, Orger MB, Jayaraman V, Looger LL, Svoboda K, Kim DS. 2013. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499:295-300. doi: 10.1038/nature12354, PMID: 23868258
15. Chung K, Deisseroth K. 2013. CLARITY for mapping the nervous system. Nature Methods 10:508-513. doi: 10.1038/nmeth.2481, PMID: 23722210
16. Clark JJ, Hollon NG, Phillips PE. 2012. Pavlovian valuation systems in learning and decision making. Current Opinion in Neurobiology 22:1054-1061. doi: 10.1016/j.conb.2012.06.004, PMID: 22749132
17. Cohen JY, Haesler S, Vong L, Lowell BB, Uchida N. 2012. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482:85-88. doi: 10.1038/nature10754, PMID: 22258508
18. Courchesne E, Hillyard SA, Galambos R. 1975. Stimulus novelty, task relevance and the visual evoked potential in man. Electroencephalography and Clinical Neurophysiology 39:131-143. doi: 10.1016/0013-4694(75)90003-6, PMID: 50210
19. Cui G, Jun SB, Jin X, Pham MD, Vogel SS, Lovinger DM, Costa RM. 2013. Concurrent activation of striatal direct and indirect pathways during action initiation. Nature 494:238-242. doi: 10.1038/nature11846, PMID: 23354054
20. Dayan P, Sejnowski TJ. 1996. Exploration bonuses and dual control. Machine Learning 25:5-22. doi: 10.1007/BF00115298
21. Dayan P, Niv Y. 2008. Reinforcement learning: the good, the bad and the ugly. Current Opinion in Neurobiology 18:185-196. doi: 10.1016/j.conb.2008.08.003, PMID: 18708140
22. Davis MD, Schmidt JJ. 2000. In vivo spectrometric calcium flux recordings of intrinsic Caudate-Putamen cells and transplanted IMR-32 neuroblastoma cells using miniature fiber optrodes in anesthetized and awake rats and monkeys. Journal of Neuroscience Methods 99:9-23. doi: 10.1016/S0165-0270(00)00209-0, PMID: 10936638
23. Fiorillo CD, Song MR, Yun SR. 2013. Multiphasic temporal dynamics in responses of midbrain dopamine neurons to appetitive and aversive stimuli. Journal of Neuroscience 33:4710-4725. doi: 10.1523/JNEUROSCI.3883-12.2013, PMID: 23486944
24. Geisler S, Zahm DS. 2005. Afferents of the ventral tegmental area in the rat-anatomical substratum for integrative functions. The Journal of Comparative Neurology 490:270-294. doi: 10.1002/cne.20668, PMID: 16082674
25. Geisler S, Derst C, Veh RW, Zahm DS. 2007. Glutamatergic afferents of the ventral tegmental area in the rat. Journal of Neuroscience 27:5730-5743. doi: 10.1523/JNEUROSCI.0012-07.2007, PMID: 17522317
26. Gershman SJ, Niv Y. 2015. Novelty and inductive generalization in human reinforcement learning. Topics in Cognitive Science 7:391-415. doi: 10.1111/tops.12138, PMID: 25808176
27. Grimm J, Mueller A, Hefti F, Rosenthal A. 2004. Molecular basis for catecholaminergic neuron diversity. PNAS 101:13891-13896. doi: 10.1073/pnas.0405340101, PMID: 15353588
28. Gunaydin LA, Grosenick L, Finkelstein JC, Kauvar IV, Fenno LE, Adhikari A, Lammel S, Mirzabekov JJ, Airan RD, Zalocusky KA, Tye KM, Anikeeva P, Malenka RC, Deisseroth K. 2014. Natural neural projection dynamics underlying social behavior. Cell 157:1535-1551. doi: 10.1016/j.cell.2014.05.017, PMID: 24949967
29. Haber SN. 2014. The place of dopamine in the cortico-basal ganglia circuit. Neuroscience 282:248-257. doi: 10.1016/j.neuroscience.2014.10.008
30. Hazy TE, Frank MJ, O’Reilly RC. 2010. Neural mechanisms of acquired phasic dopamine responses in learning. Neuroscience & Biobehavioral Reviews 34:701-720. doi: 10.1016/j.neubiorev.2009.11.019, PMID: 19944716
31. Hintiryan H, Foster NN, Bowman I, Bay M, Song MY, Gou L, Yamashita S, Bienkowski MS, Zingg B, Zhu M, Yang XW, Shih JC, Toga AW, Dong HW. 2016. The mouse cortico-striatal projectome. Nature Neuroscience 19: 1100-1114. doi: 10.1038/nn.4332, PMID: 27322419
32. Horvitz JC, Stewart T, Jacobs BL. 1997. Burst activity of ventral tegmental dopamine neurons is elicited by sensory stimuli in the awake cat. Brain Research 759:251-258. doi: 10.1016/S0006-8993(97)00265-5, PMID: 9221945
33. Houk JC, Adams JL. 1995. A model of how the basal ganglia generate and use neural signals that predict reinforcement. Models of Information Processing in the Basal Ganglia. p. 249.
34. Howe MW, Dombeck DA. 2016. Rapid signalling in distinct dopaminergic axons during locomotion and reward. Nature 535:505-510. doi: 10.1038/nature18942, PMID: 27398617
35. Ikemoto S. 2007. Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Research Reviews 56:27-78. doi: 10.1016/j.brainresrev.2007.05.004, PMID: 17574681
36. Kakade S, Dayan P. 2002. Dopamine: generalization and bonuses. Neural Networks 15:549-559. doi: 10.1016/S0893-6080(02)00048-5, PMID: 12371511
37. Kato HK, Chu MW, Isaacson JS, Komiyama T. 2012. Dynamic sensory representations in the olfactory bulb: modulation by wakefulness and experience. Neuron 76:962-975. doi: 10.1016/j.neuron.2012.09.037, PMID: 23217744
38. Kim HF, Ghazizadeh A, Hikosaka O. 2015. Dopamine neurons encoding Long-Term memory of object value for habitual behavior. Cell 163:1165-1175. doi: 10.1016/j.cell.2015.10.063, PMID: 26590420
39. Kim CK, Yang SJ, Pichamoorthy N, Young NP, Kauvar I, Jennings JH, Lerner TN, Berndt A, Lee SY, Ramakrishnan C, Davidson TJ, Inoue M, Bito H, Deisseroth K. 2016. Simultaneous fast measurement of circuit dynamics at multiple sites across the mammalian brain. Nature Methods 13:325-328. doi: 10.1038/nmeth.3770, PMID: 26878381
40. Kishiyama MM, Yonelinas AP, Knight RT. 2009. Novelty enhancements in memory are dependent on lateral prefrontal cortex. Journal of Neuroscience 29:8114-8118. doi: 10.1523/JNEUROSCI.5507-08.2009, PMID: 19553451
41. Klein S, Staring M, Murphy K, Viergever MA, Pluim JP. 2010. Elastix: a toolbox for intensity-based medical image registration. IEEE Transactions on Medical Imaging 29:196-205. doi: 10.1109/TMI.2009.2035616, PMID: 19923044
42. Knight R. 1996. Contribution of human hippocampal region to novelty detection. Nature 383:256-259. doi: 10.1038/383256a0, PMID: 8805701
43. Koester HJ, Sakmann B. 2000. Calcium dynamics associated with action potentials in single nerve terminals of pyramidal cells in layer 2/3 of the young rat neocortex. The Journal of Physiology 529 Pt 3:625-646. doi: 10.1111/j.1469-7793.2000.00625.x, PMID: 11118494
44. Kohonen T, Oja E. 1976. Fast adaptive formation of orthogonalizing filters and associative memory in recurrent networks of neuron-like elements. Biological Cybernetics 21:85-95. doi: 10.1007/BF01259390, PMID: 1244872
45. Kudo Y, Akita K, Nakamura T, Ogura A, Makino T, Tamagawa A, Ozaki K, Miyakawa A. 1992. A single optical fiber fluorometric device for measurement of intracellular Ca2+ concentration: its application to hippocampal neurons in vitro and in vivo. Neuroscience 50:619-625. doi: 10.1016/0306-4522(92)90451-7, PMID: 1436506
46. Lacey MG, Mercuri NB, North RA. 1989. Two cell types in rat substantia nigra zona compacta distinguished by membrane properties and the actions of dopamine and opioids. Journal of Neuroscience 9:1233-1241. PMID: 2703874
47. Lammel S, Hetzel A, Häckel O, Jones I, Liss B, Roeper J. 2008. Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 57:760-773. doi: 10.1016/j.neuron.2008.01.022, PMID: 18341995
48. Lee HJ, Youn JM, O MJ, Gallagher M, Holland PC. 2006. Role of substantia nigra-amygdala connections in surprise-induced enhancement of attention. Journal of Neuroscience 26:6077-6081. doi: 10.1523/JNEUROSCI.1316-06.2006, PMID: 16738251
49. Lee HJ, Youn JM, Gallagher M, Holland PC. 2008. Temporally limited role of substantia nigra-central amygdala connections in surprise-induced enhancement of learning. European Journal of Neuroscience 27:3043-3049. doi: 10.1111/j.1460-9568.2008.06272.x, PMID: 18588542
50. Lerner TN, Shilyansky C, Davidson TJ, Evans KE, Beier KT, Zalocusky KA, Crow AK, Malenka RC, Luo L, Tomer R, Deisseroth K. 2015. Intact-Brain analyses reveal distinct information carried by SNc dopamine subcircuits. Cell 162:635-647. doi: 10.1016/j.cell.2015.07.014, PMID: 26232229
51. Li S, Cullen WK, Anwyl R, Rowan MJ. 2003. Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty. Nature Neuroscience 6:526-531. doi: 10.1038/nn1049, PMID: 12704392
52. Ljungberg T, Apicella P, Schultz W. 1992. Responses of monkey dopamine neurons during learning of behavioral reactions. Journal of Neurophysiology 67:145-163. PMID: 1552316
53. Llano I, Tan YP, Caputo C. 1997. Spatial heterogeneity of intracellular Ca2+ signals in axons of basket cells from rat cerebellar slices. The Journal of Physiology 502:509-519. doi: 10.1111/j.1469-7793.1997.509bj.x, PMID: 9279804
54. Mackintosh NJ. 1975. A theory of attention: Variations in the associability of stimuli with reinforcement. Psychological Review 82:276-298. doi: 10.1037/h0076778
55. Marsland S, Shapiro J, Nehmzow U. 2002. A self-organising network that grows when required. Neural Networks 15:1041-1058. doi: 10.1016/S0893-6080(02)00078-3, PMID: 12416693
56. Matsumoto M, Hikosaka O. 2009. Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459:837-841. doi: 10.1038/nature08028, PMID: 19448610
57. Matsumoto M, Takada M. 2013. Distinct representations of cognitive and motivational signals in midbrain dopamine neurons. Neuron 79:1011-1024. doi: 10.1016/j.neuron.2013.07.002, PMID: 23932490
58. Menegas W, Bergan JF, Ogawa SK, Isogai Y, Umadevi Venkataraju K, Osten P, Uchida N, Watabe-Uchida M. 2015. Dopamine neurons projecting to the posterior striatum form an anatomically distinct subclass. eLife 4: e10032. doi: 10.7554/eLife.10032, PMID: 26322384
59. Metz CT, Klein S, Schaap M, van Walsum T, Niessen WJ. 2011. Nonrigid registration of dynamic medical imaging data using nD + T B-splines and a groupwise optimization approach. Medical Image Analysis 15:238-249. doi: 10.1016/j.media.2010.10.003, PMID: 21075672
60. Montague PR, Hyman SE, Cohen JD. 2004. Computational roles for dopamine in behavioural control. Nature 431:760-767. doi: 10.1038/nature03015, PMID: 15483596
61. Murayama M, Pérez-Garci E, Lüscher HR, Larkum ME. 2007. Fiberoptic system for recording dendritic calcium signals in layer 5 neocortical pyramidal cells in freely moving rats. Journal of Neurophysiology 98:1791-1805. doi: 10.1152/jn.00082.2007, PMID: 17634346
62. O’Reilly RC, Frank MJ, Hazy TE, Watz B. 2007. PVLV: the primary value and learned value pavlovian learning algorithm. Behavioral Neuroscience 121:31-49. doi: 10.1037/0735-7044.121.1.31, PMID: 17324049
63. Otmakhova N, Duzel E, Deutch AY, Lisman J. 2013. The hippocampal-VTA loop: the role of novelty and motivation in controlling the entry of information into long-term memory. Intrinsically Motivated Learning in Natural and Artificial Systems. Springer. p. 235-254.
64. Pan WX, Schmidt R, Wickens JR, Hyland BI. 2005. Dopamine cells respond to predicted events during classical conditioning: evidence for eligibility traces in the reward-learning network. Journal of Neuroscience 25:6235-6242. doi: 10.1523/JNEUROSCI.1478-05.2005, PMID: 15987953
65. Parker NF, Cameron CM, Taliaferro JP, Lee J, Choi JY, Davidson TJ, Daw ND, Witten IB. 2016. Reward and choice encoding in terminals of midbrain dopamine neurons depends on striatal target. Nature Neuroscience 19:845-854. doi: 10.1038/nn.4287, PMID: 27110917
66. Pavlov IP, Anrep GV. 1927. Conditioned Reflexes: An Investigation of the Physiological Activity of the Cerebral Cortex. London: Oxford University Press: Humphrey Milford.
67. Pearce JM, Hall G. 1980. A model for pavlovian learning: variations in the effectiveness of conditioned but not of unconditioned stimuli. Psychological Review 87:532-552. doi: 10.1037/0033-295X.87.6.532, PMID: 7443916
68. Redgrave P, Prescott TJ, Gurney K. 1999. Is the short-latency dopamine response too short to signal reward error? Trends in Neurosciences 22:146-151. doi: 10.1016/S0166-2236(98)01373-3, PMID: 10203849
69. Rescorla RA, Wagner AR. 1972. A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and non-reinforcement. In: Black AH, Prokasy WF (Eds). Classical Conditioning II: Current Research and Theory. p. 64-99.
70. Restorff H. 1933. Ueber die wirkung von bereichsbildungen im spurenfeld. analyse Von vorgängen im spurenfeld. I. Von W. Köhler und H. v. restorff. Psychologische Forschung 18:299-342. doi: 10.1007/BF02409636
71. Roeper J. 2013. Dissecting the diversity of midbrain dopamine neurons. Trends in Neurosciences 36:336-342. doi: 10.1016/j.tins.2013.03.003, PMID: 23582338
72. Schomaker J, Meeter M. 2015. Short- and long-lasting consequences of novelty, deviance and surprise on brain and cognition. Neuroscience & Biobehavioral Reviews 55:268-279. doi: 10.1016/j.neubiorev.2015.05.002, PMID: 25976634
73. Schultz W, Dayan P, Montague PR. 1997. A neural substrate of prediction and reward. Science 275:1593-1599. doi: 10.1126/science.275.5306.1593, PMID: 9054347
74. Schultz W. 2015. Neuronal reward and decision signals: From theories to data. Physiological Reviews 95:853-951. doi: 10.1152/physrev.00023.2014, PMID: 26109341
75. Sechenov I. 1935. Reflexes of the brain (1863). Selected Works: English Translation, State Publishing House for Biological and Medical Literature. Moscow-Leningrad.
76. Segovia G, Del Arco A, De Blas M, Garrido P, Mora F. 2010. Environmental enrichment increases the in vivo extracellular concentration of dopamine in the nucleus accumbens: a microdialysis study. Journal of Neural Transmission 117:1123-1130. doi: 10.1007/s00702-010-0447-y, PMID: 20706747
77. Sokolov EN. 1963. Higher nervous functions; the orienting reflex. Annual Review of Physiology 25:545-580. doi: 10.1146/annurev.ph.25.030163.002553, PMID: 13977960
78. Steinberg EE, Keiflin R, Boivin JR, Witten IB, Deisseroth K, Janak PH. 2013. A causal link between prediction errors, dopamine neurons and learning. Nature Neuroscience 16:966-973. doi: 10.1038/nn.3413, PMID: 23708143
79. Steinfels GF, Heym J, Strecker RE, Jacobs BL. 1983. Behavioral correlates of dopaminergic unit activity in freely moving cats. Brain Research 258:217-228. doi: 10.1016/0006-8993(83)91145-9, PMID: 6824912
80. Stuber GD, Hnasko TS, Britt JP, Edwards RH, Bonci A. 2010. Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate. Journal of Neuroscience 30:8229-8233. doi: 10.1523/JNEUROSCI.1754-10.2010, PMID: 20554874
81. Sutton RS. 1988. Learning to predict by the methods of temporal differences. Machine Learning 3:9-44. doi: 10.1007/BF00115009
82. Sutton RS, Barto AG. 1998. Reinforcement Learning: An Introduction. Cambridge, Mass: MIT Press.
83. Takeuchi T, Duszkiewicz AJ, Sonneborn A, Spooner PA, Yamasaki M, Watanabe M, Smith CC, Fernández G, Deisseroth K, Greene RW, Morris RG. 2016. Locus coeruleus and dopaminergic consolidation of everyday memory. Nature 537:357-362. doi: 10.1038/nature19325, PMID: 27602521
84. Threlfell S, Lalic T, Platt NJ, Jennings KA, Deisseroth K, Cragg SJ. 2012. Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron 75:58-64. doi: 10.1016/j.neuron.2012.04.038, PMID: 22794260
85. Tomer R, Ye L, Hsueh B, Deisseroth K. 2014. Advanced CLARITY for rapid and high-resolution imaging of intact tissues. Nature Protocols 9:1682-1697. doi: 10.1038/nprot.2014.123, PMID: 24945384
86. Uchida N, Mainen ZF. 2003. Speed and accuracy of olfactory discrimination in the rat. Nature Neuroscience 6: 1224-1229. doi: 10.1038/nn1142, PMID: 14566341
87. Wagner AR. 1978. Expectancies and the priming of STM. In: Hulse SH, Fowler H, Honig WK (eds). Cognitive Processes in Animal Behavior. p. 177-209.
88. Watabe-Uchida M, Zhu L, Ogawa SK, Vamanrao A, Uchida N. 2012. Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron 74:858-873. doi: 10.1016/j.neuron.2012.03.017, PMID: 22681690
89. Wesson DW, Carey RM, Verhagen JV, Wachowiak M. 2008. Rapid encoding and perception of novel odors in the rat. PLoS Biology 6:e82. doi: 10.1371/journal.pbio.0060082, PMID: 18399719
90. Wickersham IR, Lyon DC, Barnard RJ, Mori T, Finke S, Conzelmann KK, Young JA, Callaway EM. 2007. Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron 53:639-647. doi: 10.1016/j.neuron.2007.01.033, PMID: 17329205
91. Widrow B, Hoff ME. 1960. Adaptive Switching Circuits. IRE WESCON Convention Record, New York.
92. Zahm DS, Brog JS. 1992. On the significance of subterritories in the "accumbens" part of the rat ventral striatum. Neuroscience 50:751-767. doi: 10.1016/0306-4522(92)90202-D, PMID: 1448200