The Effect of Ethanol on the Neuronal Subserving of Behavior in the Hippocampus

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We have previously shown that both acute and chronic ethanol treatment depresses neural activity, specifically in the cingulate cortex. Minor influences were found in the motor cortex. The acute effect of ethanol in the hippocampus was intermediate to those in the cingulate and motor cortices. In the present study, we concentrate on the chronic effects of ethanol on the hippocampus. We demonstrate how the neuronal activity underlying food-acquisition behavior is modified after chronic ethanol treatment, and how the hippocampus subserves formation of newly-formed alcohol-acquisition behavior. Neuronal activity in CA1 was more sensitive to chronic ethanol than the Dg area. Acute administration of ethanol had a normalizing effect on the chronically-treated animals: their performance and the hippocampal neural activity approached a normal range. The sets of neurons involved in food-acquisition behavior formed before chronic ethanol treatment, and those involved in alcohol-acquisition behavior formed after treatment significantly overlapped supporting the view that the neuronal mechanisms of pre-existing behavior provide the basis for the formation of new behavior. Additionally, we also discovered alcohol-acquisition selective neurons. Assuming that the formation of new neuronal specializations underlies learning, we believe that alcohol-selective neurons are specialized during the formation of alcohol-acquisition behavior. Our data demonstrate several new findings on the effect of acute and chronic ethanol on hippocampus activity, and how the neuronal activity relates to behavior before and after ethanol treatment.

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Y. Alexandrov, Y. Grinchenko, D. Shevchenko, R. Averkin, V. Matz, S. Laukka and M. Sams, "The Effect of Ethanol on the Neuronal Subserving of Behavior in the Hippocampus," Journal of Behavioral and Brain Science, Vol. 3 No. 1, 2013, pp. 107-130. doi: 10.4236/jbbs.2013.31011.


[1] P. Somogyi “Hippocampus: Intrinsic Organization,” In: P. Shepherd and S. Grillner, Eds., Handbook of Brain Microcircuits, Oxford University Press, New York, 2010, pp. 148-164.
[2] O. S. Vinogradova, “Functional Organization of the Limbic System in the Process of Registration of Information: Facts and Hypotheses,” In: R. L. Isaakson and K. H. Pribram, Eds., The Hippocampus, Plenum Press, New York, 1984, pp. 1-69.
[3] L. R. Squire, “Memory and the Hippocampus: A Synthesis from Findings with Rats, Monkeys, and Humans,” Psychological Review, Vol. 99, No. 2, 1992, pp. 195-231. doi:10.1037/0033-295X.99.2.195
[4] H. Eichenbaum “The Hippocampal System and Declarative Memory in Animals,” Journal of Cognitive Neuroscience, Vol. 4, No. 3, 1992, pp. 217-231. doi:10.1162/jocn.1992.4.3.217
[5] G. Buzsaki, “The Hippocampo-Neocortical Dialogue,” Cereb Cortex, Vol. 6, No. 2, 1996, pp. 81-92. doi:10.1093/cercor/6.2.81
[6] D. B. Matthews and A. L. Morrow, “Effects of Acute and Chronic Ethanol Exposure on Spatial Cognitive Processing and Hippocampal Function in the Rat,” Hippocampus, Vol. 10, No. 1, 2000, pp. 122-130. doi:10.1002/(SICI)1098-1063(2000)10:1<122::AID-HIPO13>3.0.CO;2-V
[7] J. M. Silvers, S. Tokunaga, R. B. Berry, A. M. White and D. B. Matthews, “Impairments in Spatial Learning and Memory: Ethanol, Allopregnanolone, and the Hippocampus,” Brain Research Reviews, Vol. 43, No. 3, 2003, pp. 275-284. doi:10.1016/j.brainresrev.2003.09.002
[8] E. T. Rolls, “A Computational Theory of Episodic Memory Formation in the Hippocampus,” Behavioural Brain Research, Vol. 215, No. 2, 2010, pp. 180-196. doi:10.1016/j.bbr.2010.03.027
[9] M. F. Carr, S. P. Jadhav and L. M. Frank, “Hippocampal Replay in the Awake State: A Potential Substrate for Memory Consolidation and Retrieval,” Nature Neuroscience, Vol. 14, No. 2, 2011, pp. 147-153. doi:10.1038/nn.2732
[10] A. M. White and P. J. Best, “Effects of Ethanol on Hippocampal Place-Cell and Interneuron Activity,” Brain Research, Vol. 876, No. 1-2, 2000, pp. 154-165. doi:10.1016/S0006-8993(00)02629-9
[11] T. Miki, S. J. Harris, P. Wilce, Y. Takeuchi and K. S. Bedi, “Neurons in the Hilus Region of the Rat Hippocampus Are Depleted in Number by Exposure to Alcohol During Early Postnatal Life,” Hippocampus, Vol. 10, No. 3, 2000, pp. 284-295. doi:10.1002/1098-1063(2000)10:3<284::AID-HIPO9>3.0.CO;2-K
[12] B. Givens, J. M. Williams and T. M. Gill, “Septohippocampal Pathway as a Site for the Memory-Impairing Effects of Ethanol,” Hippocampus, Vol. 10, No. 1, 2000, pp. 111-121. doi:10.1002/(SICI)1098-1063(2000)10:1<111::AID-HIPO12>3.0.CO;2-1
[13] S. Kumar, P. Porcu, D. F. Werner, D. B. Matthews, J. L. Diaz-Granados, R. S. Helfand and A. L. Morrow, “The Role of GABA(A) Receptors in the Acute and Chronic Effects of Ethanol: A Decade of Progress,” Psychopharmacology, Vol. 205, No. 4, 2009, pp. 529-564. doi:10.1007/s00213-009-1562-z
[14] T. Tsurugizawa, A. Uematsu, H. Uneyama and K. Torii, “The Role of the Gabaergic and Dopaminergic Systems in the Brain Response to an Intragastric Load of Alcohol in Conscious Rats,” Neuroscience, Vol. 171, No. 2, 2010, pp. 451-460. doi:10.1016/j.neuroscience.2010.09.016
[15] L. M. Garcia-Moreno, N. M. Conejo, A. Capilla, O. Garcia-Sanchez, K. Senderek and J. L. Arias, “Chronic Ethanol Intake and Object Recognition in Young and Adult Rats,” Progress in Neuro-Psychopharmacology & Biological Psychiatry, Vol. 26, No. 5, 2002, pp. 831-837. doi:10.1016/S0278-5846(01)00327-X
[16] D. B. Matthews and J. R. Silvers, “The Use of Acute Ethanol Administration as a Tool to Investigate Multiple Memory Systems,” Neurobiology of Learning and Memory, Vol. 82, No. 3, 2004, pp. 299-308. doi:10.1016/j.nlm.2004.06.007
[17] E. J. Nestler and G. K. Aghajanian, “Molecular and Cellular Basis of Addiction,” Science, Vol. 278, No. 5335, 1997, pp. 58-63. doi:10.1126/science.278.5335.58
[18] T. W. Robbins and B. J. Everitt, “Drug Addiction: Bad Habits Add up,” Nature, Vol. 398, No. 6728, 1999, pp. 567-570. doi:10.1038/19208
[19] A. E. Kelley, “Memory and Addiction: Shared Neural Circuitry and Molecular Mechanisms,” Neuron, Vol. 44, No. 1, 2004, pp. 161-179. doi:10.1016/j.neuron.2004.09.016
[20] L. J. Chandler and P. W. Kalivas, “Neuroscience: Brain’s Defence against Cocaine,” Nature, Vol. 455, No. 7214, 2008, pp. 743-744. doi:10.1038/455743a
[21] B. Milner, L. R. Squire and E. R. Kandel, “Cognitive Neuroscience and the Study of Memory,” Neuron, Vol. 20, No. 3, 1998, pp. 445-468. doi:10.1016/S0896-6273(00)80987-3
[22] K. V. Anokhin, “Memory Consolidation: Narrowing the Gap between Systems and Molecular Genetic Neurosciences,” In: R. Miller, A. M. Ivanitsky and P. M. Balaban, Eds., Conceptual Advances in Brain Research, Complex Brain Functions Conceptual Advances in Russian Neuroscience, Harwood Academic Publishers, Amsterdam, 2000, pp. 53-72.
[23] O. E. Svarnik, Y. I. Alexandrov, V. V. Gavrilov, Y. V. Grinchenko and K. V. Anokhin, “Fos Expression and Task-Related Neuronal Activity in Rat Cerebral Cortex after Instrumental Learning,” Neuroscience, Vol. 136, No. 1, 2005, 33-42. doi:10.1016/j.neuroscience.2005.07.038
[24] O. E. Svarnik and Y. I. Alexandrov, “Differential c-Fos Activation in CA1, CA3 and Dentate Gyrus Areas of Hippocampus after Various Phases of Appetitive Instrumental Learning,” International Symposium “Hippocampus and Memory” Abstracts, Pushchino, 2006, p. 110.
[25] W. R. Klemm, C. G. Mallari, L. R. Dreyfus, J. C. Fiske, E. Forney and J. A. Mikeska, “Ethanol-Induced Regional and Dose-Response Differences in Multiple-Unit Activity in Rabbits,” Psychopharmacology, Vol. 49, No. 3, 1976, pp. 235-244. doi:10.1007/BF00426822
[26] S. F. Zornetzer, D. W. Walker and B. E. Hunter, “Neurophysiological Changes Produced by Alcohol,” In: Biomedical Processes and Consequences of Alcohol Use, Government Printing Office, Washington DC, 1982, pp. 95-128.
[27] A. M. White, D. B. Matthews and P. J. Best, “Ethanol, Memory, and Hippocampal Function: A Review of Recent Findings,” Hippocampus, Vol. 10, No. 1, 2000, pp. 88-93. doi:10.1002/(SICI)1098-1063(2000)10:1<88::AID-HIPO10>3.0.CO;2-L
[28] N. D. Volkow, Y. Ma, W. Zhu, J. S. Fowler, J. Li, M. Rao, K. Mueller, K. Pradhan, C. Wong and G. J. Wang, “Moderate Doses of Alcohol Disrupt the Functional Organization of the Human Brain,” Psychiatry Research, Vol. 162, No. 3, 2008, pp. 205-213. doi:10.1016/j.pscychresns.2007.04.010
[29] H. Morikawa and R. A. Morrisett, “Ethanol Action on Dopaminergic Neurons in the Ventral Tegmental Area: Interaction with Intrinsic Ion Channels and Neurotransmitter Inputs,” International Review of Neurobiology, Vol. 91, 2010, pp. 235-288. doi:10.1016/S0074-7742(10)91008-8
[30] C. P. Blomeley, S. Cains, R. Smith and E. Bracci, “Ethanol Affects Striatal Interneurons Directly and Projection Neurons through a Reduction in Cholinergic Tone,” Neuropsychopharmacology, Vol. 36, No. 5, 2011, pp. 10331046. doi:10.1038/npp.2010.241
[31] Y. I. Alexandrov, Y. V. Grinchenko, S. Laukka, T. Jarvilehto, V. N. Maz and I. A. Svetlajev, “Acute Effect of Ethanol on the Pattern of Behavioural Specialization of Neurons in the Limbic Cortex of the Freely Moving Rabbit,” Acta Physiologica Scandinavica, Vol. 140, No. 2, 1990, pp. 257-268. doi:10.1111/j.1748-1716.1990.tb08997.x
[32] P. K. Anokhin, “Biology and Neurophysiology of Conditioned Reflex and Its Role in Adaptive Behavior,” Pergamon Press, Oxford, 1973.
[33] V. B. Shvyrkov, “Behavioral Specialization of Neurons and the System-Selection Hypothesis of Learning,” In: F. Klix and H. Hagendorf, Eds., Human Memory and Cognitive Capabilities, Elsevier, Amsterdam, 1986, pp. 599611.
[34] Y. I. Alexandrov, “Learning and Memory: Traditional and Systems Approaches,” Neuroscience and Behavioral Physiology, Vol. 36, No. 9, 2006, pp. 969-985. doi:10.1007/s11055-006-0133-6
[35] Y. I. Alexandrov, “How We Fragment the World: The View from Inside versus the View from Outside,” Social Science Information, Vol. 47, No. 3, 2008, pp. 419-457. doi:10.1177/0539018408092580
[36] Y. I. Alexandrov, T. N. Grechenko, V. V. Gavrilov, A. G. Gorkin, D. G. Shevchenko, V. Grinchenko Yu, I. O. Aleksandrov, N. E. Maksimova, B. N. Bezdenezhnych and M. V. Bodunov, “Formation and Realization of Individual Experience,” Neuroscience and Behavioral Physiology, Vol. 27, No. 4, 2000, pp. 441-454. doi:10.1007/BF02462946
[37] Y. I. Alexandrov and A. V. Korpusova, “Role of Goal in Determination of Neuronal Activity of the Rabbit Motor and Visual Cortical Areas,” Neuroscience and Behavioral Physiology, Vol. 17, No. 6, 1987, pp. 473-479. doi:10.1007/BF01186344
[38] Y. I. Alexandrov, Y. V. Grinchenko, I. A. Svetlaev and O. Abdrashitov, “Factors Determining the Effect of Acute Ethanol Administration on Behavior Realization,” I.P. Pavlov Journal of Higher Nervous Activity, Vol. 39, 1989, pp. 1149-1151. (In Russian)
[39] Y. I. Alexandrov, Y. V. Grinchenko and T. Jarvilehto, “Change in the Pattern of Behavioural Specialization of Neurons in the Motor Cortex of the Rabbit Following Lesion of the Visual Cortex,” Acta Physiologica Scandinavica, Vol. 139, No. 1-2, 1990, pp. 371-385. doi:10.1111/j.1748-1716.1990.tb08936.x
[40] Y. I. Alexandrov, Y. V. Grinchenko, S. Laukka, T. Jarvilehto and V. N. Maz, “Acute Effects of Alcohol on Unit Activity in the Motor Cortex of Freely Moving Rabbits: Comparison with the Limbic Cortex,” Acta Physiologica Scandinavica, Vol. 142, No. 3, 1991, pp. 429-435. doi:10.1111/j.1748-1716.1991.tb09177.x
[41] L. I. Alexandrov and Y. I. Alexandrov, “Changes of Auditory-Evoked Potentials in Response to Behaviorally Meaningful Tones Induced by Acute Ethanol Intake in Altricial Nestlings at the Stage of Formation of Natural Behavior,” Alcohol, Vol. 10, No. 3, 1993, pp. 213-217. doi:10.1016/0741-8329(93)90038-P
[42] Y. I. Alexandrov, Y. V. Grinchenko, S. Laukka, T. Jarvilehto, V. N. Maz and A. V. Korpusova, “Effect of Ethanol on Hippocampal Neurons Depends on Their Behavioural Specialization,” Acta Physiologica Scandinavica, Vol. 149, No. 1, 1993, pp. 105-115. doi:10.1111/j.1748-1716.1993.tb09598.x
[43] Y. I. Alexandrov, A. V. Korpusova, Y. V. Grinchenko, V. N. Mats, S. Laukka and T. Jarvilehto, “Structural Changes and Reorganization of the Activity of the Cortical Neurons in the Behavior of Chronically Alcoholized Rabbits,” I.P. Pavlov Journal of Higher Nervous Activity, Vol. 44, 1994, pp. 1077-1085. (In Russian)
[44] Y. Alexandrov, M. Sams, J. Lavikainen, K. Reinikainen and R. Naatanen, “Differential Effects of Alcohol on the Cortical Processing of Foreign and Native Language,” International Journal of Psychophysiology, Vol. 28, 1998, pp. 1-10. doi:10.1016/S0167-8760(97)00066-4
[45] Y. I. Alexandrov, Y. V. Grinchenko, M. V. Bodunov, V. N. Matz, A. V. Korpusova, S. Laukka and M. Sams, “Neuronal Subserving of Behavior before and after Chronic Ethanol Treatment,” Alcohol, Vol. 22, No. 2, 2000, pp. 97-106. doi:10.1016/S0741-8329(00)00111-7
[46] Y. I. Alexandrov, Y. V. Grinchenko, D. G. Shevchenko, R. G. Averkin, V. N. Matz, S. Laukka and A. V. Korpusova, “A Subset of Cingulate Cortical Neurones Is Specifically Activated during Alcohol-Acquisition Behaviour,” Acta Physiologica Scandinavica, Vol. 171, No. 1, 2001, pp. 87-97.
[47] Y. I. Alexandrov, Y. V. Grinchenko, V. N. Mats, S. Laukka and A. V. Korpusova, “Involvement of Rabbit Motor Cortex Neurons in the Instrumental Behavior before and after Chronic Ethanol Consumption: A comparison with the Limbic Cortex,” I.P. Pavlov Journal of Higher Nervous Activity, Vol. 52, 2002, pp. 85-96. (In Russian)
[48] Y. I. Alexandrov, Y. V. Grinchenko, D. G. Shevchenko, V. N. Mats, S. Laukka and R. G. Averkin, “Neuron Activity in the Anterolateral Motor Cortex in Operant Food-Acquiring and Alcohol-Acquiring Behavior,” Neuroscience and Behavioral Physiology, Vol. 35, No. 5, 2005, pp. 501-509. doi:10.1007/s11055-005-0085-2
[49] V. V. Gavrilov, Y. V. Grinchenkо and Y. I. Alexandrov, “Comparison of the Sets of Behaviorally Specialized Limbic Cortex Neurons in Rats and Rabbits,” Forum of European Neuroscience, Berlin EJN Abstract Book, Vol. 10, 1998, p. 154.
[50] J. Y. Chang, S. F. Sawyer, R. S. Lee and D. J. Woodward, “Electrophysiological and Pharmacological Evidence for the Role of the Nucleus Accumbens in Cocaine Self-Administration in Freely Moving Rats,” Journal of Neuroscience, Vol. 14, No. 3, 1994, pp. 1224-1244.
[51] R. E. Hampson, J. D. Simeral and S. A. Deadwyler, “Distribution of Spatial and Nonspatial Information in Dorsal Hippocampus,” Nature, Vol. 402, No. 6762, 1999, pp. 610-614. doi:10.1038/45154
[52] E. S. Luschei, C. R. Garthwaite and M. E. Armstrong, “Relationship of Firing Patterns of Units in Face Area of Monkey Precentral Cortex to Conditioned Jaw Movements,” Journal of Neurophysiology, Vol. 34, No. 4, 1971, pp. 252-261.
[53] R. E. Martin, G. M. Murray, P. Kemppainen, Y. Masuda and B. J. Sessle, “Functional Properties of Neurons in the Primate Tongue Primary Motor Cortex during Swallowing,” Journal of Neurophysiology, Vol. 78, No. 3, 1997, pp. 1516-1530.
[54] J. B. Ranck Jr., “Studies on Single Neurons in Dorsal Hippocampal Formation and Septum in Unrestrained Rats. I. Behavioral Correlates and Firing Repertoires,” Experimental Neurology, Vol. 41, No. 2, 1973, pp. 461-531. doi:10.1016/0014-4886(73)90290-2
[55] K. Shima, K. Aya, H. Mushiake, M. Inase, H. Aizawa and J. Tanji, “Two Movement-Related Foci in the Primate Cingulate Cortex Observed in Signal-Triggered and SelfPaced Forelimb Movements,” Journal of Neurophysiology, Vol. 65, No. 2, 1991, pp. 188-202.
[56] R. W. Stackman and J. S. Taube, “Firing Properties of Rat Lateral Mammillary Single Units: Head Direction, Head Pitch, and Angular Head Velocity,” Journal of Neurophysiology, Vol. 18, No. 21, 1998, pp. 9020-9037.
[57] S. I. Wiener, “Spatial, Behavioral and Sensory Correlates of Hippocampal CA1 Complex Spike Cell Activity: Implications for Information Processing Functions,” Progress in Neurobiology, Vol. 49, No. 4, 1996, pp. 335-361.
[58] S. I. Wiener, C. A. Paul and H. Eichenbaum, “Spatial and Behavioral Correlates of Hippocampal Neuronal Activity,” Journal of Neuroscience, Vol. 9, No. 8, 1989, pp. 27372763.
[59] D. J. Woodward, P. H. Janak and J. Y. Chang, “Ethanol Action on Neural Networks Studied with Multineuron Recording in Freely Moving Animals,” Alcoholism: Clinical & Experimental Research, Vol. 22, No. 1, 1998, pp. 10-22. doi:10.1111/j.1530-0277.1998.tb03612.x
[60] Y. I. Alexandrov, “The Psychophsyiological Significance of Central and Peripheral Neuron Activity in Behavior,” Nauka Press, Moscow, 1989.
[61] Y. I. Alexandrov, “Systemogeny and Neuronal Death,” Neurochemistry, Vol. 21, 2004, pp. 5-14.
[62] A. G. Gorkin, K. G. Reymann and Y. I. Aleksandrov, “Long-Term Potentiation and Evoked Spike Responses in the Cingulate Cortex of Freely Mobile Rats,” Neuroscience and Behavioral Physiology, Vol. 33, No. 8, 2003, pp. 763-772. doi:10.1023/A:1025189013402
[63] A. E. Ryabinin, K. R. Melia, M. Cole, F. E. Bloom and M. C. Wilson, “Alcohol Selectively Attenuates Stress-Induced c-fos Expression in Rat Hippocampus,” Journal of Neuroscience, Vol. 15, No. 1, 1995, pp. 721-730.
[64] C. Vilpoux, V. Warnault, O. Pierrefiche, M. Daoust and M. Naassila, “Ethanol-Sensitive Brain Regions in Rat and Mouse: A Cartographic Review, Using Immediate Early Gene Expression,” Alcoholism: Clinical & Experimental Research, Vol. 33, No. 6, 2009, pp. 945-969. doi:10.1111/j.1530-0277.2009.00916.x
[65] N. Ludvig, B. T. Altura, S. E. Fox and B. M. Altura, “The Suppressant Effect of Ethanol, Delivered via Intrahippocampal Microdialysis, on the Firing of Local Pyramidal Cells in Freely Behaving Rats,” Alcohol, Vol. 12, No. 5, 1995, pp. 417-421. doi:10.1016/0741-8329(95)00012-G
[66] S. C. Steffensen and S. J. Henriksen, “Comparison of the Effects of Ethanol and Chlordiazepoxide on Electrophysiological Activity in the Fascia Dentata and Hippocampus Regio Superior,” Hippocampus, Vol. 2, No. 2, 1992, 201-211. doi:10.1002/hipo.450020210
[67] H. Yan, Q. Li, R. Madison, W. A. Wilson and H. S. Swartzwelder, “Differential Sensitivity of Hippocampal Interneurons to Ethanol in Adolescent and Adult Rats,” Journal of Pharmacology and Experimental Therapeutics, Vol. 335, No. 1, 2010, pp. 51-60. doi:10.1124/jpet.110.168450
[68] F. Fadda and Z. L. Rossetti, “Chronic Ethanol Consumption: From Neuroadaptation to Neurodegeneration,” Progress in Neurobiology, Vol. 56, No. 4, 1998, pp. 385-431. doi:10.1016/S0301-0082(98)00032-X
[69] D. W. Walker and B. E. Hunter, “Neuronal Adaptation in the Hippocampus Induced by Long-Term Ethanol Exposure,” NIDA—Research Monographs, Vol. 78, 1987, pp. 108-131.
[70] T. Miki, S. J. Harris, P. A. Wilce, Y. Takeuchi and K. S. Bedi, “Effects of Alcohol Exposure during Early Life on Neuron Numbers in the Rat Hippocampus. I. Hilus Neurons and Granule Cells,” Hippocampus, Vol. 13, No. 3, 2003, pp. 388-398. doi:10.1002/hipo.10072
[71] G. F. Koob and F. E. Bloom, “Cellular and Molecular Mechanisms of Drug Dependence,” Science, Vol. 242, No. 4879, 1988, pp. 715-723. doi:10.1126/science.2903550
[72] G. F. Koob, L. Stinus, M. Le Moal and F. E. Bloom, “Opponent Process Theory of Motivation: Neurobiological Evidence from Studies of Opiate Dependence,” Neuroscience & Biobehavioral Reviews, Vol. 13, No. 2-3, 1989, pp. 135-140. doi:10.1016/S0149-7634(89)80022-3
[73] K. V. Sudakov, “Motivation and Reinforcement in the Systemic Mechanisms of Behavior: Dynamic Reinforcement Engrams,” Neuroscience and Behavioral Physiology, Vol. 26, No. 5, 1996, pp. 445-453. doi:10.1007/BF02359406
[74] K. V. Sudakov and A. V. Kotov, “Functional Transswitching of Dominant Motivation in the Systemic Organization of Behavioral Acts,” Neuroscience and Behavioral Physiology, Vol. 17, No. 2, 1987, pp. 85-91. doi:10.1007/BF01184895
[75] P. J. Kenny, “Common Cellular and Molecular Mechanisms in Obesity and Drug Addiction,” Nature Reviews Neuroscience, Vol. 12, No. 11, 2011, pp. 638-651. doi:10.1038/nrn3105
[76] N. D. Volkow, G. J. Wang, J. S. Fowler and F. Telang, “Overlapping Neuronal Circuits in Addiction and Obesity: Evidence of Systems Pathology,” Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, No. 1507, 2008, pp. 3191-3200. doi:10.1098/rstb.2008.0107
[77] D. W. Walker, B. E. Hunter and W. C. Abraham, “Neuroanatomical and Functional Deficits Subsequent to Chronic Ethanol Administration in Animals,” Alcoholism: Clinical & Experimental Research, Vol. 5, No. 2, 1981, pp. 267-282. doi:10.1111/j.1530-0277.1981.tb04901.x
[78] T. K. Li, L. Lumeng, W. J. McBride, J. M. Murphy, J. C. Froehlich and S. Morzorati, “Pharmacology of Alcohol Preference in Rodents,” Advances in Alcohol & Substance Abuse, Vol. 7, No. 3-4, 1988, pp. 73-86. doi:10.1300/J251v07n03_11
[79] J. K. Chapin and D. J. Woodward, “Ethanol Withdrawal Increases Sensory Responsiveness of Single Somatosensory Cortical Neurons in the Awake, Behaving Rat,” Alcoholism: Clinical & Experimental Research, Vol. 13, No. 1, 1989, pp. 8-14. doi:10.1111/j.1530-0277.1989.tb00275.x
[80] J. M. Murphy, G. J. Gatto, W. J. McBride, L. Lumeng and T. K. Li, “Operant Responding for Oral Ethanol in the Alcohol-Preferring P and Alcohol-Nonpreferring NP Lines of Rats,” Alcohol, Vol. 6, No. 2, 1989, pp. 127-131. doi:10.1016/0741-8329(89)90037-2
[81] R. L. McBride and W. R. Klemm, “Stereotaxic Atlas of Rabbit Brain Based on the Rapid Method of Photography of Frozen, Unstained Sections,” Communications in Behavioral Biology, Vol. A2, 1968, pp. 179-215.
[82] Iu. V. Grinchenko and V. B. Shvyrkov, “A Simple Micromanipulator for Studying Neuronal Activity in Unrestrained Rabbits,” I.P. Pavlov Journal of Higher Nervous Activity, Vol. 24, 1974, pp. 870-872. (In Russian)
[83] D. Ferster, “Is Neural Noise Just a Nuisance?” Science, Vol. 273, No. 5283, 1996, p. 1812. doi:10.1126/science.273.5283.1812
[84] E. Vaadia, I. Haalman, M. Abeles, H. Bergman, Y. Prut, H. Slovin and A. Aertsen, “Dynamics of Neuronal Interactions in Monkey Cortex in Relation to Behavioural Events,” Nature, Vol. 373, No. 6514, 1995, pp. 515-518. doi:10.1038/373515a0
[85] V. Burov Iu, A. B. Kampov-Polevoi and O. P. Kashevskaia, “Formation of Experimental Alcoholism in a Population of Crossbred Rats,” Bulletin of Experimental Biology and Medicine, Vol. 96, 1983, pp. 67-68. (In Russian)
[86] J. O’Keefe, “Place Units in the Hippocampus of the Freely Moving Rat,” Experimental Neurology, Vol. 51, No. 1, 1976, pp. 78-109. doi:10.1016/0014-4886(76)90055-8
[87] E. R. Wood, P. A. Dudchenko and H. Eichenbaum, “The Global Record of Memory in Hippocampal Neuronal Activity,” Nature, Vol. 397, No. 6720, 1999, pp. 613-616. doi:10.1038/16564
[88] E. Pastalkova, V. Itskov, A. Amarasingham and G. Buzsaki, “Internally Generated Cell Assembly Sequences in the Rat Hippocampus,” Science, Vol. 321, No. 5894, 2008, pp. 1322-1327. doi:10.1126/science.1159775
[89] G. Buzsaki, “Hippocampus: Network Physiology,” In: P. Shepherd and S. Grillner, Eds., Handbook of Brain Microcircuits, Oxford University Press, New York, 2010, pp. 165-174.
[90] V. V. Gavrilov, S. I. Wiener and A. Berthoz, “Discharge Correlates of Hippocampal Complex Spike Neurons in Behaving Rats Passively Displaced on a Mobile Robot,” Hippocampus, Vol. 8, No. 5, 1998, pp. 475-490. doi:10.1002/(SICI)1098-1063(1998)8:5<475::AID-HIPO7>3.0.CO;2-H
[91] O. Bengoechea and L. M. Gonzalo, “Effect of Chronic Alcoholism on the Human Hippocampus,” Histology and Histopathology, Vol. 5, No. 3, 1990, pp. 349-357.
[92] P. A. McMullen, J. A. Saint-Cyr and P. L. Carlen, “Morphological Alterations in Rat CA1 Hippocampal Pyramidal Cell Dendrites Resulting from Chronic Ethanol Consumption and Withdrawal,” Journal of Comparative Neurology, Vol. 225, No. 1, 1984, pp. 111-118. doi:10.1002/cne.902250112
[93] T. Ribot, “Diseases of Memory,” Appleton-Century Crofts, New York, 1882,
[94] M. A. King, B. E. Hunter and D. W. Walker, “Alterations and Recovery of Dendritic Spine Density in Rat Hippocampus Following Long-Term Ethanol Ingestion,” Brain Research, Vol. 459, No. 2, 1988, pp. 381-385. doi:10.1016/0006-8993(88)90656-7
[95] M. M. Paula-Barbosa, F. Brandao, M. D. Madeira and A. Cadete-Leite, “Structural Changes in the Hippocampal Formation after Long-Term Alcohol Consumption and Withdrawal in the Rat,” Addiction, Vol. 88, No. 2, 1993, pp. 237-247. doi:10.1111/j.1360-0443.1993.tb00807.x
[96] D. B. Matthews, “Ethanol and the Hippocampal System: Behaviour to Molecular Biology,” Hippocampus, Vol. 10, No. 1, 2000, p. 87. doi:10.1002/(SICI)1098-1063(2000)10:1<87::AID-HIPO9>3.0.CO;2-J
[97] J. Schummers and M. D. Browning, “Evidence for a Role for GABA(A) and NMDA Receptors in Ethanol Inhibition of Long-Term Potentiation,” Molecular Brain Research, Vol. 94, No. 1-2, 2001, pp. 9-14. doi:10.1016/S0169-328X(01)00161-9
[98] T. P. Beresford, D. B. Arciniegas, J. Alfers, L. Clapp, B. Martin, Y. Du, D. Liu, D. Shen and C. Davatzikos, “Hippocampus Volume Loss Due to Chronic Heavy Drinking,” Alcoholism: Clinical & Experimental Research, Vol. 30, No. 11, 2006, pp. 1866-1870. doi:10.1111/j.1530-0277.2006.00223.x
[99] A. Cadete-Leite, M. A. Tavares, H. B. Uylings and M. Paula-Barbosa, “Granule Cell Loss and Dendritic Regrowth in the Hippocampal Dentate Gyrus of the Rat after Chronic Alcohol Consumption,” Brain Research, Vol. 473, No. 1, 1988, pp. 1-14. doi:10.1016/0006-8993(88)90309-5
[100] D. G. Smith, J. E. Learn, W. J. McBride, L. Lumeng, T. K. Li and J. M. Murphy, “Long-Term Effects of Alcohol Drinking on Cerebral Glucose Utilization in Alcohol-Preferring Rats,” Pharmacology Biochemistry and Behavior, Vol. 69, No. 3-4, 2001, pp. 543-553. doi:10.1016/S0091-3057(01)00553-6
[101] O. Bengoechea and L. M. Gonzalo, “Effects of Alcoholization on the Rat Hippocampus,” Neuroscience Letters, Vol. 123, No. 2, 1991, pp. 112-114. doi:10.1016/0304-3940(91)90170-X
[102] H. G. Kuhn, H. Dickinson-Anson and F. H. Gage, “Neurogenesis in the Dentate Gyrus of the Adult Rat: Age-Related Decrease of Neuronal Progenitor Proliferation,” Journal of Neuroscience, Vol. 16, No. 6, 1996, pp. 20272033.
[103] J. M. Parent, “Injury-Induced Neurogenesis in the Adult Mammalian Brain,” Neuroscientist, Vol. 9, No. 4, 2003, pp. 261-272. doi:10.1177/1073858403252680
[104] C. D. Clelland, M. Choi, C. Romberg, G. D. Clemenson Jr., A. Fragniere, P. Tyers, S. Jessberger, L. M. Saksida, R. A. Barker, F. H. Gage and T. J. Bussey, “A Functional Role for Adult Hippocampal Neurogenesis in Spatial Pattern Separation,” Science, Vol. 325, No. 5937, 2009, pp. 210-213. doi:10.1126/science.1173215
[105] E. Aberg, C. P. Hofstetter, L. Olson and S. Brene, “Moderate Ethanol Consumption Increases Hippocampal Cell Proliferation and Neurogenesis in the Adult Mouse,” International Journal of Neuropsychopharmacology, Vol. 8, No. 4, 2005, pp. 557-567. doi:10.1017/S1461145705005286
[106] M. Nilsson, E. Perfilieva, U. Johansson, O. Orwar and P. S. Eriksson, “Enriched Environment Increases Neurogenesis in the Adult Rat Dentate Gyrus and Improves Spatial Memory,” Journal of Neurobiology, Vol. 39, No. 4, 1999, pp. 569-578. doi:10.1002/(SICI)1097-4695(19990615)39:4<569::AID-NEU10>3.0.CO;2-F
[107] P. S. Eriksson, E. Perfilieva, T. Bjork-Eriksson, A. M. Alborn, C. Nordborg, D. A. Peterson and F. H. Gage, “Neurogenesis in the Adult Human Hippocampus,” Nature Medicine, Vol. 4, No. 11, 1998, pp. 1313-1317. doi:10.1038/3305
[108] E. Gould, A. Beylin, P. Tanapat, A. Reeves and T. J. Shors, “Learning Enhances Adult Neurogenesis in the Hippocampal Formation,” Nature Neuroscience, Vol. 2, No. 3, 1999, pp. 260-265. doi:10.1038/6365
[109] F. T. Crews, K. Nixon and M. E. Wilkie, “Exercise Reverses Ethanol Inhibition of Neural Stem Cell Proliferation,” Alcohol, Vol. 33, No. 1, 2004, pp. 63-71.
[110] J. N. Riley and D. W. Walker, “Morphological Alterations in Hippocampus after Long-Term Alcohol Consumption in Mice,” Science, Vol. 201, No. 4356, 1978, pp. 646-648. doi:10.1126/science.566953
[111] M. M. Airaksinen and P. Peura, “Mechanisms of Alcohol Withdrawal Syndrome,” Medical Biology, Vol. 65, No. 2-3, 1987, pp. 105-112.
[112] I. P. Anokhina, B. M. Kogan and A. Z. Drozdov, “Disturbances in Regulation of Catecholamine Neuromediation in Alcoholism,” Alcohol, Vol. 23, No. 5, 1988, pp. 343350.
[113] B. S. Bratus, “Psychological Analysis of Personality Changes in Alcoholics,” Edition of Moscow University, Moscow, 1974.
[114] R. J. Gibbins, H. Kalant, A. E. LeBlanc and J. W. Clark, “The Effects of Chronic Administration of Ethanol on Startle Thresholds in Rats,” Psychopharmacologia, Vol. 19, No. 2, 1971, pp. 95-104. doi:10.1007/BF00402633
[115] B. Kissin, “The Pharmacodynamics and Natural History of Alcoholism,” In: The Biology of Alcoholism, Plenum Press, New York, 1974, pp. 1-36.
[116] A. M. Ludwig, “Alcohol Input and Creative Output,” British Journal of Addiction, Vol. 85, No. 7, 1990, pp. 953-963. doi:10.1111/j.1360-0443.1990.tb03726.x
[117] D. E. Feldman and M. Brecht, “Map Plasticity in Somatosensory Cortex,” Science, Vol. 310, No. 5749, 2005, pp. 810-815. doi:10.1126/science.1115807
[118] I. V. Bondar, D. A. Leopold, B. J. Richmond, J. D. Victor and N. K. Logothetis, “Long-Term Stability of Visual Pattern Selective Responses of Monkey Temporal Lobe Neurons,” PLoS One, Vol. 4, No. 12, 2009, p. e8222. doi:10.1371/journal.pone.0008222
[119] P. M. Bradley, B. D. Burns, T. M. King and A. C. Webb, “Electrophysiological Correlates of Prior Training: An in Vitro Study of an Area of the Avian Brain Which Is Essential for Early Learning,” Brain Research, Vol. 708, No. 1, 1996, pp. 100-107. doi:10.1016/0006-8993(95)01470-5
[120] M. Brecht, M. Scneider and I. Manns, “Silent Neurons in Sensorimotor Cortices: Implication for Cortical Plasticity,” In: F. F. Ebner Ed., Neural Plasticity in Adult Somatic Sensory-Motor Systems, Taylor & Francis Group, Boca Raton, 2005, pp. 1-19.
[121] P. A. Greenberg and F. A. Wilson, “Functional Stability of Dorsolateral Prefrontal Neurons,” Journal of Neurophysiology, Vol. 92, No. 2, 2004, pp. 1042-1055. doi:10.1152/jn.00062.2004
[122] M. S. Jog, Y. Kubota, C. I. Connolly, V. Hillegaart and A. M. Graybiel, “Building Neural Representations of Habits,” Science, Vol. 286, No. 5445, 1999, pp. 1745-1749. doi:10.1126/science.286.5445.1745
[123] M. A. Nicolelis, A. A. Ghazanfar, B. M. Faggin, S. Votaw and L. M. Oliveira, “Reconstructing the Engram: Simultaneous, Multisite, Many Single Neuron Recordings,” Neuron, Vol. 18, No. 4, 1997, pp. 529-537. doi:10.1016/S0896-6273(00)80295-0
[124] E. M. Schmidt, M. J. Bak and J. S. McIntosh, “Long-Term Chronic Recording from Cortical Neurons,” Experimental Neurology, Vol. 52, No. 3, 1976, pp. 496-506. doi:10.1016/0014-4886(76)90220-X
[125] H. A. Swadlow and T. P. Hicks, “Subthreshold Receptive Fields and Baseline Excitability of, ‘Silent’ S1 Callosal Neurons in Awake Rabbits: Contributions of AMPA/Kainate and NMDA Receptors,” Experimental Brain Research, Vol. 115, No. 3, 1997, pp. 403-409. doi:10.1007/PL00005710
[126] L. T. Thompson and P. J. Best, “Long-Term Stability of the Place-Field Activity of Single Units Recorded from the Dorsal Hippocampus of Freely Behaving Rats,” Brain Research, Vol. 509, No. 2, 1990, pp. 299-308. doi:10.1016/0006-8993(90)90555-P
[127] J. C. Williams, R. L. Rennaker and D. R. Kipke, “Stability of Chronic Multichannel Neural Recordings: Implications for a Long-Term Neural Interface,” Neurocomputting, Vol. 26-27, 1999, pp. 1069-1076. doi:10.1016/S0925-2312(99)00106-X
[128] T. Xu, X. Yu, A. J. Perlik, W. F. Tobin, J. A. Zweig, K. Tennant, T. Jones and Y. Zuo, “Rapid Formation and Selective Stabilization of Synapses for Enduring Motor Memories,” Nature, Vol. 462, 2009, pp. 915-919. doi:10.1038/nature08389
[129] M. A. Wilson and B. L. McNaughton, “Dynamics of the Hippocampal Ensemble Code for Space,” Science, Vol. 261, No. 5124, 1993, pp. 1055-1058. doi:10.1126/science.8351520
[130] G. Yang, F. Pan and W. B. Gan, “Stably Maintained Dendritic Spines Are Associated with Lifelong Memories,” Nature, Vol. 462, No. 7275, 2009, pp. 920-924. doi:10.1038/nature08577
[131] L. M. Frank, G. B. Stanley and E. N. Brown, “Hippocampal Plasticity across Multiple Days of Exposure to Novel Environments,” Journal of Neuroscience, Vol. 24, No. 35, 2004, pp. 7681-7689. doi:10.1523/JNEUROSCI.1958-04.2004
[132] J. Epsztein, M. Brecht and A. K. Lee, “Intracellular Determinants of Hippocampal CA1 Place and Silent Cell Activity in a Novel Environment,” Neuron, Vol. 70, No. 1, 2011, pp. 109-120. doi:10.1016/j.neuron.2011.03.006
[133] A. Carleton, L. T. Petreanu, R. Lansford, A. AlvarezBuylla and P. M. Lledo, “Becoming a New Neuron in the Adult Olfactory Bulb,” Nature Neuroscience, Vol. 6, No. 5, 2003, pp. 507-518.
[134] T. J. Shors, G. Miesegaes, A. Beylin, M. Zhao, T. Rydel and E. Gould, “Neurogenesis in the Adult is Involved in the Formation of Trace Memories,” Nature, Vol. 410, No. 6826, 2001, pp. 372-376. doi:10.1038/35066584
[135] J. A. Paton and F. N. Nottebohm, “Neurons Generated in the Adult Brain Are Recruited into Functional Circuits,” Science, Vol. 225, No. 4666, 1984, pp. 1046-1048. doi:10.1126/science.6474166
[136] G. Kempermann, H. G. Kuhn and F. H. Gage, “Experience-Induced Neurogenesis in the Senescent Dentate Gyrus,” Journal of Neuroscience, Vol. 18, No. 9, 1998, pp. 3206-3212.
[137] K. V. Anokhin, A. A. Tiunova and S. P. Rose, “Reminder Effects—Reconsolidation or Retrieval Deficit? Pharmacological Dissection with Protein Synthesis Inhibitors Following Reminder for a Passive-Avoidance Task in Young Chicks,” European Journal of Neuroscience, Vol. 15, No. 11, 2002, pp. 1759-1765. doi:10.1046/j.1460-9568.2002.02023.x
[138] O. E. Svarnik, T. A. Fadeeva, K. V. Anokhin and Y. I. Alexandrov, “Learning Strategies and c-Fos Expression in the Rat Retrosplenial Cortex during Operant Skill Acquisition,” FENS Abstracts, Vol. 4, 2008.
[139] M. A. Castro-Alamancos, J. Borrell and L. M. GarciaSegura, “Performance in an Escape Task Induces FosLike Immunoreactivity in a Specific Area of the Motor Cortex of the Rat,” Neuroscience, Vol. 49, No. 1, 1992, 157-162. doi:10.1016/0306-4522(92)90083-E
[140] E. M. Bowman, T. G. Aigner and B. J. Richmond, “Neural Signals in the Monkey Ventral Striatum Related to Motivation for Juice and Cocaine Rewards,” Journal of Neurophysiology, Vol. 75, No. 3, 1996, pp. 1061-1073.
[141] R. M. Carelli and S. A. Deadwyler, “Cellular Mechanisms Underlying Reinforcement-Related Processing in the Nucleus Accumbens: Electrophysiological Studies in Behaving Animals,” Pharmacology Biochemistry and Behavior , Vol. 57, No. 3, 1997, pp. 495-504. doi:10.1016/S0091-3057(96)00442-X
[142] K. M. Kendrick and B. A. Baldwin, “The Effects of Sodium Appetite on the Responses of Cells in the Zona Incerta to the Sight or Ingestion of Food, Salt and Water in Sheep,” Brain Research, Vol. 492, No. 1-2, 1989, pp. 211-218. doi:10.1016/0006-8993(89)90903-7
[143] D. L. Robinson and R. M. Carelli, “Distinct Subsets of Nucleus Accumbens Neurons Encode Operant Responding for Ethanol versus Water,” European Journal of Neuroscience, Vol. 28, No. 9, 2008, pp. 1887-1894. doi:10.1111/j.1460-9568.2008.06464.x
[144] J. A. Ainge, M. Tamosiunaite, F. Woergoetter and P. A. Dudchenko, “Hippocampal CA1 Place Cells Encode Intended Destination on a Maze with Multiple Choice Points,” Journal of Neuroscience, Vol. 27, No. 36, 2007, pp. 9769-9779. doi:10.1523/JNEUROSCI.2011-07.2007
[145] C. R. Breese, R. E. Hampson and S. A. Deadwyler, “Hippocampal Place Cells: Stereotypy and Plasticity,” Journal of Neuroscience, Vol. 9, 1989, 1097-1111.
[146] P. J. Best and A. M. White, “Hippocampal Cellular Activity: A Brief History of Space,” Proceedings of the National Academy of Sciences, Vol. 95, No. 6, 1998, pp. 2717-2719. doi:10.1073/pnas.95.6.2717
[147] P. J. Best, A. M. White and A. Minai, “Spatial Processing in the Brain: The Activity of Hippocampal Place Cells,” Annual Review of Neuroscience, Vol. 24, No. 1, 2001, pp. 459-486. doi:10.1146/annurev.neuro.24.1.459
[148] T. Kobayashi, H. Nishijo, M. Fukuda, J. Bures and T. Ono, “Task-Dependent Representations in Rat Hippocampal place Neurons,” Journal of Neurophysiology, Vol. 78, No. 2, 1997, pp. 597-613.
[149] E. J. Markus, Y. L. Qin, B. Leonard, W. E. Skaggs, B. L. McNaughton and C. A. Barnes, “Interactions between Location and Task Affect the Spatial and Directional Firing of Hippocampal Neurons,” Journal of Neuroscience, Vol. 15, No. 11, 1995, pp. 7079-7094.
[150] I. Lee and J. Kim, “The Shift from a Response Strategy to Object-in-Place Strategy during Learning Is Accompanied by a Matching Shift in Neural Firing Correlates in the Hippocampus,” Learning & Memory, Vol. 17, No. 8, 2010, pp. 381-393. doi:10.1101/lm.1829110
[151] P. J. Kennedy and M. L. Shapiro, “Motivational States Activate Distinct Hippocampal Representations to Guide Goal-Directed Behaviors,” Proceedings of the National Academy of Sciences, Vol. 106, No. 26, 2009, pp. 1080510810. doi:10.1073/pnas.0903259106
[152] L. Zinyuk, S. Kubik, Y. Kaminsky, A. A. Fenton and J. Bures, “Understanding Hippocampal Activity by Using Purposeful Behavior: Place Navigation Induces Place Cell Discharge in Both Task-Relevant and Task-Irrelevant Spatial Reference Frames,” Proceedings of the National Academy of Sciences, Vol. 97, No. 7, 2000, pp. 3771-3776. doi:10.1073/pnas.97.7.3771
[153] M. A. Moita, S. Rosis, Y. Zhou, J. E. LeDoux and H. T. Blair, “Putting Fear in Its Place: Remapping of Hippocampal Place Cells during Fear Conditioning,” Journal of Neuroscience, Vol. 24, No. 31, 2004, pp. 7015-7023. doi:10.1523/JNEUROSCI.5492-03.2004
[154] E. R. Wood, P. A. Dudchenko, R. J. Robitsek and H. Eichenbaum, “Hippocampal Neurons Encode Information about Different Types of Memory Episodes Occurring in the Same Location,” Neuron, Vol. 27, No. 3, 2000, pp. 623-633. doi:10.1016/S0896-6273(00)00071-4
[155] A. J. Robison and E. J. Nestler, “Transcriptional and Epigenetic Mechanisms of Addiction,” Nature Reviews Neuroscience, Vol. 12, No. 11, 2011, pp. 623-637. doi:10.1038/nrn3111
[156] S. S. Schreiber and M. Baudry, “Selective Neuronal Vulnerability in the Hippocampus—a Role for Gene Expression?” Trends in Neurosciences, Vol. 18, No. 10, 1995, pp. 446-451. doi:10.1016/0166-2236(95)94495-Q
[157] V. V. Sherstnev, V. V. Iurasov, Z. I. Storozheva, M. A. Gruden and N. E. Iakovleva, “Biochemical Markers of Apoptosis in Different Brain Regions after Training,” I.P. Pavlov Journal of Higher Nervous Activity, Vol. 55, 2005, pp. 729733. (In Russian)
[158] C. H. Bailey and E. R. Kandel, “Structural Changes Accompanying Memory Storage,” Annual Review of Physiology, Vol. 55, No. 1, 1993, pp. 397-426. doi:10.1146/
[159] S. Pulipparacharuvil, W. Renthal, C. F. Hale, M. Taniguchi, G. Xiao, A. Kumar, S. J. Russo, D. Sikder, C. M. Dewey, M. M. Davis, P. Greengard, A. C. Nairn, E. J. Nestler and C. W. Cowan, “Cocaine Regulates MEF2 to Control Synaptic and Behavioral Plasticity,” Neuron, Vol. 59, No. 4, 2008, pp. 621-633. doi:10.1016/j.neuron.2008.06.020
[160] V. Deroche-Gamonet, D. Belin and P. V. Piazza, “Evidence for Addiction-Like Behavior in the Rat,” Science, Vol. 305, No. 5686, 2004, pp. 1014-1017. doi:10.1126/science.1099020

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