Brain reward circuitry beyond the mesolimbic dopamine system: a neurobiological theory

Ikemoto, Satoshi

doi:10.1016/j.neubiorev.2010.02.001

Cited by 454Neurotransmitter Receptor Influence on BehaviorNeural and Behavioral Psychology StudiesNeuroscience and Neuropharmacology Research

Brain reward circuitry beyond the mesolimbic dopamine system: a neurobiological theory

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Ikemoto, Satoshi·2010·Neuroscience & Biobehavioral Reviews

DOI 10.1016/j.neubiorev.2010.02.001PMC PMC2894302

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Abstract

Reductionist attempts to dissect complex mechanisms into simpler elements are necessary, but not sufficient for understanding how biological properties like reward emerge out of neuronal activity. Recent studies on intracranial self-administration of neurochemicals (drugs) found that rats learn to self-administer various drugs into the mesolimbic dopamine structures-the posterior ventral tegmental area, medial shell nucleus accumbens and medial olfactory tubercle. In addition, studies found roles of non-dopaminergic mechanisms of the supramammillary, rostromedial tegmental and midbrain raphe nuclei in reward. To explain intracranial self-administration and related effects of various drug manipulations, I outlined a neurobiological theory claiming that there is an intrinsic central process that coordinates various selective functions (including perceptual, visceral, and reinforcement processes) into a global function of approach. Further, this coordinating process for approach arises from interactions between brain structures including those structures mentioned above and their closely linked regions: the medial prefrontal cortex, septal area, ventral pallidum, bed nucleus of stria terminalis, preoptic area, lateral hypothalamic areas, lateral habenula, periaqueductal gray, laterodorsal tegmental nucleus and parabrachical area.

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The DAergic system, particularly the mesocorticolimbic pathway, is involved in drug addiction because DA modulates limbic and cortical sites for goal-directed behavior.
“The role of the DAergic system (in particular the mesocorticolimbic pathway) in drug addiction derives from DA’s ability to modulate many of the limbic and cortical sites involved in goal-directed behavior (Fig. 1) [18, 28–31].”
From Mechanistic insights into nicotine withdrawal (2011) · cites this paper as [30]
The LHb is a source of anti-reward signals that influences reward-related DA neuron activity.
“Studies conducted in recent years have identified the LHb as a source of anti-reward signals that plays an important role in determining the reward-related activity of DA neurons [18, 30, 68–70].”
From Mechanistic insights into nicotine withdrawal (2011) · cites this paper as [30]

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Collective dynamics of ‘small-world’ networks
Watts, D. J., & Strogatz, S. H. (1998) · Nature · doi:10.1038/30918 · Cited by 43,060 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Complex brain networks: graph theoretical analysis of structural and functional systems
Bullmore, E., & Sporns, O. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2575 · Cited by 11,820 · see citing works
Parallel organization of functionally segregated circuits linking basal ganglia and cortex
Alexander, G. E., DeLong, M. R., & Strick, P. L. (1986) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.09.030186.002041 · Cited by 8,527 · see citing works
Network biology: understanding the cell's functional organization
Barabási, A.-L., & Oltvai, Z. N. (2004) · Nature Reviews Genetics · doi:10.1038/nrg1272 · Cited by 7,903 · see citing works
Error and attack tolerance of complex networks
Albert, R., Jeong, H., & Barabási, A.-L. (2000) · Nature · doi:10.1038/35019019 · Cited by 7,534 · see citing works
Error and attack tolerance of complex networksPreprint
Albert, R., Jeong, H., & Barabási, A.-Ĺ. (2000) · Cited by 6,554 · see citing works
The Organization of Behavior; A Neuropsychological Theory.
Attneave, F., B., M., & Hebb, D. O. (1950) · The American Journal of Psychology · doi:10.2307/1418888 · Cited by 5,146 · see citing works
Rhythms of the Brain
Buzsáki, G. (2006) · doi:10.1093/acprof:oso/9780195301069.001.0001 · Cited by 4,873 · see citing works
Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats.
Di Chiara, G., & Imperato, A. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.14.5274 · Cited by 4,733 · see citing works
AChE-stained horizontal sections of the rat brain in stereotaxic coordinates
Paxinos, G., WATSON, C. R. R., & Emson, P. C. (1980) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(80)90021-7 · Cited by 4,497 · see citing works
What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?
Berridge, K. C., & Robinson, T. E. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00019-8 · Cited by 4,127 · see citing works
Untitled work
(1998) · Cited by 4,012 · see citing works
Neural systems of reinforcement for drug addiction: from actions to habits to compulsion
Everitt, B. J., & Robbins, T. W. (2005) · Nature Neuroscience · doi:10.1038/nn1579 · Cited by 3,785 · see citing works
From molecular to modular cell biology.
Hartwell, L. H., Hopfield, J. J., Leibler, S., & Murray, A. W. (1999) · Nature · doi:10.1038/35011540 · Cited by 3,632 · see citing works
The Human Connectome: A Structural Description of the Human Brain
Sporns, O., Tononi, G., & Kötter, R. (2005) · PLoS Computational Biology · doi:10.1371/journal.pcbi.0010042 · Cited by 3,260 · see citing works
Autoradiographic localization of dopamine D1 and D2 receptors in rat nucleus accumbens: Resistance to differential rearing conditions
Bardo, M. T., & Hammer, R. P. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90226-e · Cited by 3,229 · see citing works
Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain.
Olds, J., & Milner, P. (1954) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0058775 · Cited by 3,176 · see citing works
A psychomotor stimulant theory of addiction.
Wise, R. A., & Bozarth, M. A. (1987) · Psychological Review · doi:10.1037/0033-295x.94.4.469 · Cited by 2,747 · see citing works
Conditioned Reflexes: An Investigation of the Physiological Activity of the Cerebral Cortex.
Pavlov, P. I. (1930) · Archives of Neurology And Psychiatry · doi:10.1001/archneurpsyc.1930.02220110256018 · Cited by 2,681 · see citing works
Operant Behavior: Areas of Research and Application,
Honig, W. K. (1966) · Medical Entomology and Zoology · Cited by 2,656 · see citing works
Getting formal with dopamine and reward
Schultz, W. (2002) · Neuron · doi:10.1016/s0896-6273(02)00967-4 · Cited by 2,574 · see citing works
THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS
Mink, J. W. (1996) · Progress in Neurobiology · doi:10.1016/s0301-0082(96)00042-1 · Cited by 2,478 · see citing works
The role of the basal ganglia in habit formation
Yin, H. H., & Knowlton, B. J. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1919 · Cited by 2,402 · see citing works
Drives and the C. N. S. (conceptual nervous system).
Hebb, D. O. (1955) · Psychological Review · doi:10.1037/h0041823 · Cited by 2,090 · see citing works
Drugs of abuse: anatomy, pharmacology and function of reward pathways
Koob, G. F. (1992) · Trends in Pharmacological Sciences · doi:10.1016/0165-6147(92)90060-j · Cited by 2,070 · see citing works
Which elements are excited in electrical stimulation of mammalian central nervous system: A review
Ranck, J. B. (1975) · Brain Research · doi:10.1016/0006-8993(75)90364-9 · Cited by 2,024 · see citing works
Brain Maps: Structure of the Rat Brain
Swanson, L. W. (1992) · Medical Entomology and Zoology · Cited by 1,851 · see citing works
The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat
Swanson, L. W. (1982) · Brain Research Bulletin · doi:10.1016/0361-9230(82)90145-9 · Cited by 1,718 · see citing works
An opponent-process theory of motivation. I. Temporal dynamics of affect
Solomon, R. L., & Corbit, J. D. (1974) · Psychological Review · doi:10.1037/h0036128 · Cited by 1,704 · see citing works
Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: An anterograde tract‐tracing study with <i>Phaseolus vulgaris</i> leucoagglutinin
Sesack, S. R., Deutch, A. Y., Roth, R. H., & Bunney, B. S. (1989) · Journal of Comparative Neurology · doi:10.1002/cne.902900205 · Cited by 1,568 · see citing works
Differential projections of the infralimbic and prelimbic cortex in the rat
Vertes, R. P. (2004) · Synapse · doi:10.1002/syn.10279 · Cited by 1,550 · see citing works
The primate basal ganglia: Parallel and integrative networks
Haber, S. N. (2003) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2003.10.003 · Cited by 1,479 · see citing works
Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex
Ikemoto, S. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.004 · Cited by 1,477 · see citing works
Self-citation
Conditioned reflexes: An investigation of the physiological activity of the cerebral cortex
Pavlov, I. P. (2010) · Annals of Neurosciences · doi:10.5214/ans.0972-7531.1017309 · Cited by 1,466 · see citing works
The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking
Ikemoto, S., & Panksepp, J. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00023-5 · Cited by 1,450 · see citing works
Self-citation
Efferent connections of the substantia nigra and ventral tegmental area in the rat
Beckstead, R. M., Domesick, V. B., & Nauta, W. J. H. (1979) · Brain Research · doi:10.1016/0006-8993(79)91001-1 · Cited by 1,293 · see citing works
Lateral habenula as a source of negative reward signals in dopamine neurons
Matsumoto, M., & Hikosaka, O. (2007) · Nature · doi:10.1038/nature05860 · Cited by 1,292 · see citing works
Efferent connections of the parabrachial nucleus in the rat
Saper, C. B., & Loewy, A. D. (1980) · Brain Research · doi:10.1016/0006-8993(80)91117-8 · Cited by 1,217 · see citing works
Putting a spin on the dorsal-ventral divide of the striatum
Voorn, P., Vanderschuren, L. J. M. J., Groenewegen, H. J., Robbins, T. W., & Pennartz, C. M. A. (2004) · Trends in Neurosciences · doi:10.1016/j.tins.2004.06.006 · Cited by 1,188 · see citing works
Catecholamine innervation of the basal forebrain IV. Topography of the dopamine projection to the basal forebrain and neostriatum
Fallon, J. H., & Moore, R. Y. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901800310 · Cited by 1,172 · see citing works
The connections of the septal region in the rat
Swanson, L. W., & Cowan, W. M. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901860408 · Cited by 1,136 · see citing works
Structural plasticity associated with exposure to drugs of abuse
Robinson, T. E., & Kolb, B. E. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.06.025 · Cited by 1,104 · see citing works
Neuroleptics and operant behavior: The anhedonia hypothesis
Wise, R. A. (1982) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00010372 · Cited by 1,022 · see citing works
The mesolimbic dopamine system: The final common pathway for the reinforcing effect of drugs of abuse?
Pierce, R. C., & Kumaresan, V. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.016 · Cited by 913 · see citing works
Organization of projections from the medial nucleus of the amygdala: A PHAL study in the rat
Canteras, N. S., Simerly, R. B., & Swanson, L. W. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903600203 · Cited by 884 · see citing works
Organization of the projections from the subiculum to the ventral striatum in the rat. A study using anterograde transport of Phaseolus vulgaris leucoagglutinin
Groenewegen, H. J., Vermeulen‐Vanderzee, E., Kortschot, A. T., & Witter, M. P. (1987) · Neuroscience · doi:10.1016/0306-4522(87)90275-2 · Cited by 867 · see citing works
Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat
Hopkins, D. A., & Holstege, G. (1978) · Experimental Brain Research · doi:10.1007/bf00239551 · Cited by 866 · see citing works
Efferent connections of the habenular nuclei in the rat
Herkenham, M. A., & Nauta, W. J. H. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901870103 · Cited by 855 · see citing works
Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat
Berendse, H. W., Graaf, Y. G.-D., & Groenewegen, H. J. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903160305 · Cited by 847 · see citing works
A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat
Vertes, R. P. (1991) · Journal of Comparative Neurology · doi:10.1002/cne.903130409 · Cited by 842 · see citing works
Afferent connections of the habenular nuclei in the rat. A horseradish peroxidase study, with a note on the fiber‐of‐passage problem
Herkenham, M. A., & Nauta, W. J. H. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901730107 · Cited by 798 · see citing works
Formation of accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving
Conrad, K. L., Tseng, K. Y., Uejima, J. L., Reimers, J. M., Heng, L.-J., Shaham, Y., Marinelli, M., & Wolf, M. E. (2008) · Nature · doi:10.1038/nature06995 · Cited by 790 · see citing works
Uniform Inhibition of Dopamine Neurons in the Ventral Tegmental Area by Aversive Stimuli
Ungless, M. A., Magill, P. J., & Bolam, J. P. (2004) · Science · doi:10.1126/science.1093360 · Cited by 782 · see citing works
Catecholamine theories of reward: A critical review
Wise, R. A. (1978) · Brain Research · doi:10.1016/0006-8993(78)90253-6 · Cited by 769 · see citing works
Progress in physiological psychology
Stellar, E., & Sprague, J. M. (1966) · Academic Press eBooks · Cited by 765 · see citing works
Extinction and recovery of cocaine self-administration following 6-hydroxydopamine lesions of the nucleus accumbens
Roberts, D. C. S., Koob, G. F., Klonoff, P., & Fibiger, H. C. (1980) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(80)90166-5 · Cited by 730 · see citing works
On the role of ascending catecholaminergic systems in intravenous self-administration of cocaine
Roberts, D. C. S., Corcoran, M. E., & Fibiger, H. C. (1977) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(77)90084-3 · Cited by 728 · see citing works
Organization of cerebral cortical afferent systems in the rat. II. Magnocellular basal nucleus
Saper, C. B. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902220302 · Cited by 703 · see citing works
Neurobiological mechanisms for opponent motivational processes in addiction
Koob, G. F., & Moal, M. L. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0094 · Cited by 702 · see citing works
The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses.
Jhou, T. C., Fields, H. L., Baxter, M. G., Saper, C. B., & Holland, P. C. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.001 · Cited by 696 · see citing works
Connections of the rat lateral septal complex 1Published on the World Wide Web on 2 June 1997. 1
Risold, P. Y., & Swanson, L. W. (1997) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00009-x · Cited by 671 · see citing works
Circuit-breakers: optical technologies for probing neural signals and systems
Zhang, F., Aravanis, A. M., Adamantidis, A., de Lecea, L., & Deisseroth, K. A. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2192 · Cited by 623 · see citing works
Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear.
Kim, J. J., Rison, R. A., & Fanselow, M. S. (1993) · Behavioral Neuroscience · doi:10.1037/0735-7044.107.6.1093 · Cited by 615 · see citing works
Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum
Berendse, H. W., & Groenewegen, H. J. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902990206 · Cited by 598 · see citing works
Projections of the medial preoptic nucleus: A Phaseolus vulgaris leucoagglutinin anterograde tract‐tracing study in the rat
Simerly, R. B., & Swanson, L. W. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902700205 · Cited by 592 · see citing works
Convergence of autonomic and limbic connections in the insular cortex of the rat
Saper, C. B. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902100207 · Cited by 584 · see citing works
Localization of brain reinforcement mechanisms: intracranial self-administration and intracranial place-conditioning studies
McBride, W. J., Murphy, J. M., & Ikemoto, S. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(99)00022-4 · Cited by 574 · see citing works
Self-citation
Modeling the impact of lesions in the human brain
Alstott, J., Breakspear, M., Hagmann, P., Cammoun, L., & Sporns, O. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000408 · Cited by 561 · see citing works
Afferent projections to the ventral tegmental area of Tsai and interfascicular nucleus: A horseradish peroxidase study in the rat
Phillipson, O. T. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901870108 · Cited by 553 · see citing works
The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb
Luskin, M. B., & Price, J. L. (1983) · The Journal of Comparative Neurology · doi:10.1002/cne.902160305 · Cited by 552 · see citing works
Midbrain Dopamine Neurons Signal Preference for Advance Information about Upcoming Rewards
Bromberg-Martin, E. S., & Hikosaka, O. (2009) · Neuron · doi:10.1016/j.neuron.2009.06.009 · Cited by 548 · see citing works
Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: A retro‐ and antero‐grade transport and immunohistochemical study
Semba, K., & Fibiger, H. C. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903230307 · Cited by 544 · see citing works
NOVELTY AND CURIOSITY AS DETERMINANTS OF EXPLORATORY BEHAVIOUR 1
Berlyne, D. E. (1950) · British Journal of Psychology General Section · doi:10.1111/j.2044-8295.1950.tb00262.x · Cited by 537 · see citing works
The organization of neural inputs to the medial preoptic nucleus of the rat
Simerly, R. B., & Swanson, L. W. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902460304 · Cited by 523 · see citing works
Parallel and interactive learning processes within the basal ganglia: relevance for the understanding of addiction
Belin, D., Jonkman, S., Dickinson, A., Robbins, T. W., & Everitt, B. J. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.09.027 · Cited by 520 · see citing works
Neuroplasticity in the mesolimbic dopamine system and cocaine addiction
Thomas, M. J., Kalivas, P. W., & Shaham, Y. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.77 · Cited by 513 · see citing works
Approach‐avoidance analysis of rat diencephalon
OLDS, M. E., & Olds, J. (1963) · The Journal of Comparative Neurology · doi:10.1002/cne.901200206 · Cited by 512 · see citing works
An autoradiographic study of the efferent connections of the lateral hypothalamic area in the rat
Saper, C. B., Swanson, L. W., & Cowan, W. M. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901830402 · Cited by 509 · see citing works
The mesopontine rostromedial tegmental nucleus: A structure targeted by the lateral habenula that projects to the ventral tegmental area of tsai and substantia nigra compacta
Jhou, T. C., Geisler, S., Marinelli, M., Degarmo, B. A., & Zahm, D. S. (2009) · Journal of Comparative Neurology · doi:10.1002/cne.21891 · Cited by 503 · see citing works
Limbic-diencephalic mechanisms of voluntary movement.
Vanderwolf, C. H. (1971) · Psychological Review · doi:10.1037/h0030672 · Cited by 491 · see citing works
Cortical Dopaminergic Involvement in Cocaine Reinforcement
Goeders, N. E., & Smith, J. E. (1983) · Science · doi:10.1126/science.6879176 · Cited by 490 · see citing works
Hypothalamic Substrates of Reward
Olds, J. (1962) · Physiological Reviews · doi:10.1152/physrev.1962.42.4.554 · Cited by 472 · see citing works
A biological theory of reinforcement.
Glickman, S. E., & Schiff, B. B. (1967) · Psychological Review · doi:10.1037/h0024290 · Cited by 466 · see citing works
An Opponent-Process Theory of Motivation
Solomon, R. L., & Corbit, J. D. (2008) · Cited by 461 · see citing works
Destruction of dopaminergic nerve terminals in nucleus accumbens: Effect on d-amphetamine self-administration
Lyness, W. H., Friedle, N. M., & Moore, K. E. (1979) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(79)90040-6 · Cited by 457 · see citing works
Organization of the output of the ventral striatopallidal system in the rat: ventral pallidal efferents
Groenewegen, H. J., Berendse, H. W., & Haber, S. N. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90115-v · Cited by 456 · see citing works
Disruption of cocaine self-administration following 6-hydroxydopamine lesions of the ventral tegmental area in rats
Roberts, D. C. S., & Koob, G. F. (1982) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(82)90469-5 · Cited by 448 · see citing works
Efferent connections of the septal area in the rat: An analysis utilizing retrograde and anterograde transport methods
Meibach, R. C., & Siegel, A. (1977) · Brain Research · doi:10.1016/0006-8993(77)90088-9 · Cited by 438 · see citing works
Efferent connections of the ventral pallidum: Evidence of a dual striato pallidofugal pathway
Haber, S. N., Groenewegen, H. J., Grove, E. A., & Nauta, W. J. H. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902350304 · Cited by 432 · see citing works
The accumbens: beyond the core-shell dichotomy
Heimer, L., Alheid, G. F., de Olmos, J. S., Groenewegen, H. J., Haber, S. N., Harlan, R. E., & Zahm, D. S. (1997) · Journal of Neuropsychiatry · doi:10.1176/jnp.9.3.354 · Cited by 418 · see citing works
Reticulo-cortical activity and behavior: A critique of the arousal theory and a new synthesis
Vanderwolf, C. H., & Robinson, T. E. (1981) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00009869 · Cited by 412 · see citing works
Organization of cortical, basal forebrain, and hypothalamic afferents to the parabrachial nucleus in the rat
Moga, M. M., Herbert, H., Hurley, K. M., Yasui, Y., Gray, T. S., & Saper, C. B. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902950408 · Cited by 407 · see citing works
Self-Stimulation of the Brain
Olds, J. (1958) · Science · doi:10.1126/science.127.3294.315 · Cited by 404 · see citing works
Efferent projections of the paraventricular thalamic nucleus in the rat
Moga, M. M., Weis, R. P., & Moore, R. Y. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903590204 · Cited by 402 · see citing works
Cortical projection patterns of the medial septum‐diagonal band complex
Gaykema, R. P. A., Luiten, P. G. M., Nyakas, C. J., & Traber, J. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902930109 · Cited by 387 · see citing works
Afferents of the ventral tegmental area in the rat-anatomical substratum for integrative functions
Geisler, S., & Zahm, D. S. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20668 · Cited by 379 · see citing works
The pharmacology of mesolimbic dopamine neurons: a dual-probe microdialysis study in the ventral tegmental area and nucleus accumbens of the rat brain
Westerink, B. H. C., Kwint, H., & Devries, J. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-08-02605.1996 · Cited by 372 · see citing works
Glutamatergic neurons are present in the rat ventral tegmental area
Yamaguchi, T., Sheen, W., & Morales, M. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05263.x · Cited by 367 · see citing works
Self-injection of amphetamine directly into the brain
Hoebel, B. G., Monaco, A. P., Hernandez, L., Aulisi, E. F., Stanley, B. G., & Lenard, L. (1983) · Psychopharmacology · doi:10.1007/bf00429012 · Cited by 367 · see citing works
The projection field of the stria terminalis in the rat brain. An experimental study
de Olmos, J. S., & Ingram, W. R. (1972) · The Journal of Comparative Neurology · doi:10.1002/cne.901460303 · Cited by 355 · see citing works
The efferent projections of the periaqueductal gray in the rat: A Phaseolus vulgaris‐leucoagglutinin study. II. Descending projections
Cameron, A. A., Khan, I. A., Westlund, K. N., & Willis, W. D. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903510408 · Cited by 353 · see citing works
Afferents to the GABAergic tail of the ventral tegmental area in the rat
Kaufling, J., Veinante, P., Pawlowski, S. A., Freund‐Mercier, M., & Barrot, M. (2009) · Journal of Comparative Neurology · doi:10.1002/cne.21983 · Cited by 347 · see citing works
A portrait of the substrate for self-stimulation.
Gallistel, C. R., Shizgal, P., & Yeomans, J. S. (1981) · Psychological Review · doi:10.1037/0033-295x.88.3.228 · Cited by 337 · see citing works
Bed nucleus of the stria terminalis: Cytoarchitecture, immunohistochemistry, and projection to the parabrachial nucleus in the rat
Moga, M. M., Saper, C. B., & Gray, T. S. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902830302 · Cited by 333 · see citing works
Dissociation of dopamine release in the nucleus accumbens from intracranial self-stimulation
Garris, P. A., Kilpatrick, M., Bunin, M. A., Michael, D., Walker, Q. D., & Wightman, R. M. (1999) · Nature · doi:10.1038/18019 · Cited by 327 · see citing works
Rewarding Actions of Phencyclidine and Related Drugs in Nucleus Accumbens Shell and Frontal Cortex
Carlezon, & Wise, R. A. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-09-03112.1996 · Cited by 327 · see citing works
Origin of the dopaminergic innervation of the central extended amygdala and accumbens shell: A combined retrograde tracing and immunohistochemical study in the rat
Hasue, R. H., & Shammah‐Lagnado, S. J. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10420 · Cited by 306 · see citing works
Augmentation of drug reward by chronic food restriction
Carr, K. D. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00759-x · Cited by 300 · see citing works
PHA-L analysis of projections from the supramammillary nucleus in the rat
Vertes, R. P. (1992) · Journal of Comparative Neurology · doi:10.1002/cne.903260408 · Cited by 299 · see citing works
Afferent and efferent connections of the laterodorsal tegmental nucleus in the rat
Cornwall, J., Cooper, J. D., & Phillipson, O. T. (1990) · Brain Research Bulletin · doi:10.1016/0361-9230(90)90072-8 · Cited by 294 · see citing works
Drugs and Reinforcement Mechanisms: A Critical Review of the Catecholamine Theory
Fibiger, H. C. (1978) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pa.18.040178.000345 · Cited by 293 · see citing works
Efferent projections of infralimbic and prelimbic areas of the medial prefrontal cortex in the Japanese monkey, Macaca fuscata
Chiba, T., Kayahara, T., & Nakano, K. (2001) · Brain Research · doi:10.1016/s0006-8993(00)03013-4 · Cited by 290 · see citing works
Projections from bed nuclei of the stria terminalis, anteromedial area: Cerebral hemisphere integration of neuroendocrine, autonomic, and behavioral aspects of energy balance
Dong, H.-W., & Swanson, L. W. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.20788 · Cited by 290 · see citing works
Efferent projections of the infralimbic (area 25) region of the medial prefrontal cortex in the rat: an anterograde tracer PHA-L study
Takagishi, M., & Chiba, T. (1991) · Brain Research · doi:10.1016/0006-8993(91)91677-s · Cited by 284 · see citing works
The Olfactory Cortex and the Ventral Striatum
Heimer, L. (1978) · Springer eBooks · doi:10.1007/978-1-4757-0716-8_7 · Cited by 283 · see citing works
Complex interactions between nicotine and nonpharmacological stimuli reveal multiple roles for nicotine in reinforcement
Chaudhri, N., Caggiula, A. R., Donny, E. C., Palmatier, M. I., Liu, X., & Sved, A. F. (2006) · Psychopharmacology · doi:10.1007/s00213-005-0178-1 · Cited by 271 · see citing works
Autoradiographic analysis of ascending projections from the pontine and mesencephalic reticular formation and the median raphe nucleus in the rat
Vertes, R. P., & Martin, G. F. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902750404 · Cited by 267 · see citing works
Role of Dopamine D1and D2Receptors in the Nucleus Accumbens in Mediating Reward
Ikemoto, S., Glazier, B. S., Murphy, J. M., & McBride, W. J. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-21-08580.1997 · Cited by 257 · see citing works
Self-citation
Projections from bed nuclei of the stria terminalis, dorsomedial nucleus: Implications for cerebral hemisphere integration of neuroendocrine, autonomic, and drinking responses
Dong, H., & Swanson, L. W. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20790 · Cited by 249 · see citing works
Efferent projections from the parabrachial nucleus demonstrated with the anterograde tracer Phaseolus vulgaris leucoagglutinin
Krukoff, T. L., Harris, K. H., & Jhamandas, J. H. (1993) · Brain Research Bulletin · doi:10.1016/0361-9230(93)90054-f · Cited by 242 · see citing works
Behavior of Captive White-Footed Mice
Kavanau, J. L. (1967) · Science · doi:10.1126/science.155.3770.1623 · Cited by 238 · see citing works
Brain Stimulation Reward
Stolerman, I. P., & Price, L. H. (2015) · Springer eBooks · doi:10.1007/978-3-642-36172-2_200188 · Cited by 234 · see citing works
The role of affective processes in learning and motivation.
Young, P. T. (1959) · Psychological Review · doi:10.1037/h0045997 · Cited by 229 · see citing works
Decreased intracranial self-stimulation after neuroleptics or 6-hydroxydopamine: Evidence for mediation by motor deficits rather than by reduced reward
Fibiger, H. C., Carter, D. A., & Phillips, A. G. (1976) · Psychopharmacology · doi:10.1007/bf00428696 · Cited by 225 · see citing works
The supramammillary area: its organization, functions and relationship to the hippocampus
Pan, W.-X., & McNaughton, N. (2004) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2004.09.003 · Cited by 223 · see citing works
Dissociations between appetitive and consummatory responses by pharmacological manipulations of reward-relevant brain regions.
Ikemoto, S., & Panksepp, J. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.2.331 · Cited by 216 · see citing works
Self-citation
Brainstem projections from the lateral hypothalamic area in the rat, as studied with autoradiography
Hosoya, Y., & Matsushita, M. (1981) · Neuroscience Letters · doi:10.1016/0304-3940(81)90232-9 · Cited by 210 · see citing works
Brainstem pathways of reward.
Routtenberg, A., & Malsbury, C. W. (1969) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0027655 · Cited by 210 · see citing works
Mapping the differential effects of procaine on frequency and amplitude of reticularly elicited hippocampal rhythmical slow activity
Kirk, I. J., & McNaughton, N. (1993) · Hippocampus · doi:10.1002/hipo.450030411 · Cited by 208 · see citing works
Reward, Motivation, Cognition: Psychobiology of Mesotelencephalic Dopamine Systems
Fibiger, H. C., & Phillips, A. G. (1986) · Comprehensive physiology · doi:10.1002/cphy.cp010412 · Cited by 204 · see citing works
Influence of novel versus home environments on sensitization to the psychomotor stimulant effects of cocaine and amphetamine
Badiani, A., Browman, K. E., & Robinson, T. E. (1995) · Brain Research · doi:10.1016/0006-8993(95)00028-o · Cited by 204 · see citing works
The role of the exploratory drive in learning.
Montgomery, K. C. (1954) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0054833 · Cited by 199 · see citing works
Projections of the dorsal raphe nucleus to the brainstem: PHA‐L analysis in the rat
Vertes, R. P., & Kocsis, B. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903400103 · Cited by 198 · see citing works
Cholinergic and peptidergic projections from the medial septum and the nucleus of the diagonal band of broca to dorsal hippocampus, cingulate cortex and olfactory bulb: A combined wheatgerm agglutinin-apohorseradish peroxidase-gold immunohistochemical study
Senut, M., Menétrey, D., & Lamour, Y. A. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90260-1 · Cited by 194 · see citing works
The cytoarchitecture of the interfascicular nucleus and ventral tegmental area of tsai in the rat
Phillipson, O. T. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901870106 · Cited by 193 · see citing works
Intracranial Self-Administration of Ethanol within the Ventral Tegmental Area of Male Wistar Rats: Evidence for Involvement of Dopamine Neurons
Rodd, Z. A., Meléndez, R. I., Bell, R. L., Kuc, K. A., Zhang, Y., Murphy, J. M., & McBride, W. J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1319-03.2004 · Cited by 193 · see citing works
Purpose and cognition: the determiners of animal learning.
Tolman, E. C. (1925) · Psychological Review · doi:10.1037/h0072784 · Cited by 191 · see citing works
The role of dopamine in intracranial self-stimulation of the ventral tegmental area
Fibiger, H., LePiane, F., Jakubovic, A., & Phillips, A. (1987) · The Journal of Neuroscience · doi:10.1523/jneurosci.07-12-03888.1987 · Cited by 189 · see citing works
Involvement of the Olfactory Tubercle in Cocaine Reward: Intracranial Self-Administration Studies
Ikemoto, S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-28-09305.2003 · Cited by 183 · see citing works
Self-citation
Afferent and efferent connections of the medial preoptic area in the rat: A WGA-HRP study
Chiba, T., & Murata, Y. (1985) · Brain Research Bulletin · doi:10.1016/0361-9230(85)90091-7 · Cited by 182 · see citing works
Projections of GABAergic and cholinergic basal forebrain and GABAergic preoptic‐anterior hypothalamic neurons to the posterior lateral hypothalamus of the rat
Gritti, I., Mainville, L., & Jones, B. E. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903390206 · Cited by 179 · see citing works
Two brain sites for cannabinoid reward
Zangen, A., Solinas, M., Ikemoto, S., Goldberg, S. R., & Wise, R. A. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3554-05.2006 · Cited by 174 · see citing works
Habit-forming actions of nomifensine in nucleus accumbens
Carlezon, W. A., Devine, D. P., & Wise, R. A. (1995) · Psychopharmacology · doi:10.1007/bf02246095 · Cited by 170 · see citing works
Topographical organization of GABAergic neurons within the ventral tegmental area of the rat
Olson, V. G., & Nestler, E. J. (2006) · Synapse · doi:10.1002/syn.20345 · Cited by 170 · see citing works
Projections from the rhomboid nucleus of the bed nuclei of the stria terminalis: Implications for cerebral hemisphere regulation of ingestive behaviors
Dong, H., & Swanson, L. W. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10758 · Cited by 168 · see citing works
The efferent projections of the rat lateral habenular nucleus revealed by the PHA-L anterograde tracing method
Araki, M., McGeer, P. L., & Kimura, H. (1988) · Brain Research · doi:10.1016/0006-8993(88)91410-2 · Cited by 163 · see citing works
Effects of the availability of rewarding septal and hypothalamic stimulation on bar pressing for food under conditions of deprivation.
Routtenberg, A., & Lindy, J. (1965) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0022365 · Cited by 160 · see citing works
Primary reinforcing effects of nicotine are triggered from multiple regions both inside and outside the ventral tegmental area
Ikemoto, S., Qin, M., & Liu, Z.-H. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4542-05.2006 · Cited by 151 · see citing works
Self-citation
Learning when the onset of illumination is used as the reinforcing stimulus.
Kish, G. B. (1955) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0040782 · Cited by 150 · see citing works
Cocaine is self-administered into the shell but not the core of the nucleus accumbens of Wistar rats
Rodd-Henricks, Z. A., McKinzie, D. L., Li, T.-K., Murphy, J. M., & McBride, W. J. (2002) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.102.038950 · Cited by 150 · see citing works
The efferent projections of the periaqueductal gray in the rat: A Phaseolus vulgaris‐leucoagglutinin study. I. Ascending projections
Cameron, A. A., Khan, I. A., Westlund, K. N., Cliffer, K. D., & Willis, W. D. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903510407 · Cited by 149 · see citing works
Possible excitatory amino acid afferents to nucleus raphe dorsalis of the rat investigated with retrograde wheat germ agglutinin and d-[3H]aspartate tracing
Kalén, P., Karlson, M., & Wiklund, L. (1985) · Brain Research · doi:10.1016/0006-8993(85)91244-2 · Cited by 148 · see citing works
Addiction as a pathology in prefrontal cortical regulation of corticostriatal habit circuitry
Kalivas, P. W. (2008) · Neurotoxicity Research · doi:10.1007/bf03033809 · Cited by 148 · see citing works
Simultaneous dopamine and single-unit recordings reveal accumbens GABAergic responses: implications for intracranial self-stimulation
Cheer, J. F., Heien, M. L. A. V., Garris, P. A., Carelli, R. M., & Wightman, R. M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509607102 · Cited by 143 · see citing works
An experimental study of the ventral striatum of the golden hamster. II. Neuronal connections of the olfactory tubercle
Newman, R. S., & Winans, S. S. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901910204 · Cited by 142 · see citing works
Regional Heterogeneity for the Intracranial Self-Administration of Ethanol and Acetaldehyde within the Ventral Tegmental Area of Alcohol-Preferring (P) Rats: Involvement of Dopamine and Serotonin
Rodd, Z. A., Bell, R. L., Zhang, Y., Murphy, J. M., D, A. G. M., Zaffaroni, A., Li, T., & McBride, W. J. (2004) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300561 · Cited by 141 · see citing works
Afferents to the median raphe nucleus of the rat: Retrograde cholera toxin and wheat germ conjugated horseradish peroxidase tracing, and selectived-[3H]aspartate labelling of possible excitatory amino acid inputs
Behzadi, G., Kalén, P., Parvopassu, F., & Wiklund, L. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90194-9 · Cited by 140 · see citing works
Rewarding and psychomotor stimulant effects of endomorphin-1: anteroposterior differences within the ventral tegmental area and lack of effect in nucleus accumbens
Zangen, A., Ikemoto, S., Zadina, J. E., & Wise, R. A. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-16-07225.2002 · Cited by 138 · see citing works
Mapping of chemical trigger zones for reward
Ikemoto, S., & Wise, R. A. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.07.012 · Cited by 137 · see citing works
Self-citation
Ventral striatal anatomy of locomotor activity induced by cocaine, D-amphetamine, dopamine and D1/D2 agonists
Ikemoto, S. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00247-6 · Cited by 134 · see citing works
Self-citation
Projections of the Parabrachial Nucleus in the Old World Monkey
Pritchard, T. C., Hamilton, R. B., & Norgren, R. (2000) · Experimental Neurology · doi:10.1006/exnr.2000.7450 · Cited by 134 · see citing works
CNS connections with the median raphe nucleus: Retrograde tracing with WGA‐apoHRP‐gold complex in the rat
Marcinkiewicz, M., Morcos, R., & Chrétien, M. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902890103 · Cited by 134 · see citing works
Prefrontal cortical projections to the cholinergic neurons in the basal forebrain
Gaykema, R. P. A., Weeghel, R. V., Hersh, L. B., & Luiten, P. G. M. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903030405 · Cited by 134 · see citing works
Neuropharmacological assessment of cocaine self-administration into the medial prefrontal cortex
Goeders, N. E., Dworkin, S. I., & Smith, J. E. (1986) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(86)90206-6 · Cited by 133 · see citing works
Electrical stimulation of reward sites in the ventral tegmental area increases dopamine transmission in the nucleus accumbens of the rat
FIORINO, D., COURY, A., FIBIGER, H., & PHILLIPS, A. (1993) · Behavioural Brain Research · doi:10.1016/0166-4328(93)90109-4 · Cited by 131 · see citing works
Patterns of direct projections from the hippocampus to the medial septum-diagonal band complex: Anterograde tracing with Phaseolus vulgaris leucoagglutinin combined with immunohistochemistry of choline acetyltransferase
Gaykema, R. P. A., van der Kuil, J., Hersh, L. B., & Luiten, P. G. M. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90299-4 · Cited by 131 · see citing works
An autoradiographic study of projections ascending from the midbrain central gray, and from the region lateral to it, in the rat
Eberhart, J. A., Morrell, J. I., Krieger, M. S., & Pfaff, D. W. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902410305 · Cited by 126 · see citing works
CART peptide-immunoreactive neurones in the nucleus accumbens in monkeys: Ultrastructural analysis, colocalization studies, and synaptic interactions with dopaminergic afferents
Smith, Y., Kieval, J. Z., Couceyro, P. R., & Kuhar, M. J. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990517)407:4 · Cited by 122 · see citing works
The Functional Divide for Primary Reinforcement of D-Amphetamine Lies between the Medial and Lateral Ventral Striatum: Is the Division of the Accumbens Core, Shell, and Olfactory Tubercle Valid?: Figure 1.
Ikemoto, S., Qin, M., & Liu, Z. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0892-05.2005 · Cited by 120 · see citing works
Self-citation
The ventral striatopallidothalamic projection: I. The striatopallidal link originating in the striatal parts of the olfactory tubercle
Heimer, L., Zaborszky, L., Zahm, D. S., & Alheid, G. F. (1987) · Journal of Comparative Neurology · doi:10.1002/cne.902550409 · Cited by 117 · see citing works
Self-infusion of GABA-sub(A ) antagonists directly into the ventral tegmental area and adjacent regions.
Ikemoto, S., Murphy, J. M., & McBride, W. J. H. (1997) · Behavioral Neuroscience · doi:10.1037//0735-7044.111.2.369 · Cited by 117 · see citing works
Self-citation
Rewarding Effects of the Cholinergic Agents Carbachol and Neostigmine in the Posterior Ventral Tegmental Area
Ikemoto, S., & Wise, R. A. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-22-09895.2002 · Cited by 116 · see citing works
Self-citation
Ascending projections of the posterior nucleus of the hypothalamus: PHA‐L analysis in the rat
Vertes, R. P., Crane, A. M., Colom, L. V., & Bland, B. H. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903590107 · Cited by 116 · see citing works
Pharmacological suppression of the median raphe nucleus with serotonin1a agonists, 8-OH-DPAT and buspirone, produces hippocampal theta rhythm in the rat
Vertes, R. P., Kinney, G. G., Kocsis, B., & Fortin, W. J. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90255-0 · Cited by 111 · see citing works
Basal ganglia — possible role in motor coordination and learning
HIKOSAKA, O. (1991) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(05)80042-x · Cited by 111 · see citing works
Self-stimulation in the frontal cortex of rattus norvegicus
Routtenberg, A., & Sloan, M. A. (1972) · Behavioral Biology · doi:10.1016/s0091-6773(72)80218-9 · Cited by 110 · see citing works
Effects of nucleus accumbens amphetamine on lateral hypothalamic brain stimulation reward
Colle, L. M., & Wise, R. A. (1988) · Brain Research · doi:10.1016/0006-8993(88)90653-1 · Cited by 107 · see citing works
GABA in the ventral tegmental area: Differential regional effects on locomotion, aggression and food intake after microinjection of GABA agonists and antagonists
Arnt, J., & Scheel‐Krüger, J. (1979) · Life Sciences · doi:10.1016/0024-3205(79)90402-8 · Cited by 106 · see citing works
Prolonged rewarding stimulation of the rat medial forebrain bundle: Neurochemical and behavioral consequences.
Hernández, G., Hamdani, S., Rajabi, H., Conover, K. L., Stewart, J., Arvanitogiannis, A., & Shizgal, P. (2006) · Behavioral Neuroscience · doi:10.1037/0735-7044.120.4.888 · Cited by 105 · see citing works
Regional Differences Within the Rat Ventral Tegmental Area for Muscimol Self-Infusions
Ikemoto, S., Murphy, J. M., & McBride, W. J. H. (1998) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(98)00086-0 · Cited by 104 · see citing works
Self-citation
Direct catecholaminergic-cholinergic interactions in the basal forebrain. II. Substantia nigra-ventral tegmental area projections to cholinergic neurons
Gaykema, R. P. A., & Záborszky, L. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19961028)374:4 · Cited by 103 · see citing works
Organization of ventral tegmental area projections to the ventral tegmental area–nigral complex in the rat
Ferreira, J. G. P., Del-Fava, F., Hasue, R. H., & Shammah‐Lagnado, S. J. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.02.003 · Cited by 101 · see citing works
Effects of peripheral and central dopamine blockade on lateral hypothalamic self-stimulation: Evidence for both reward and motor deficits
Stellar, J. R. (1983) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(83)90466-5 · Cited by 101 · see citing works
Is the dopaminergic mesocorticolimbic system necessary for intracranial self-stimulation?
Simon, H., Stinus, L., Tassin, J., Lavielle, S., Blanc, G., Thierry, A. M., Glowinski, J., & Moal, M. L. (1979) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(79)91745-x · Cited by 100 · see citing works
Sniffing and motivated behavior in the rat
Clarke, S., & Trowill, J. A. (1971) · Physiology & Behavior · doi:10.1016/0031-9384(71)90013-8 · Cited by 99 · see citing works
The supramammillary nucleus: Is it necessary for the mediation of hippocampal theta rhythm?
Thinschmidt, J. S., Kinney, G. G., & Kocsis, B. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00045-k · Cited by 96 · see citing works
GABAergic agents on the medial septal nucleus affect hippocampal theta rhythm and acetylcholine utilization
Allen, C. N., & Crawford, I. L. (1984) · Brain Research · doi:10.1016/0006-8993(84)90116-1 · Cited by 96 · see citing works
Projections from the subfornical region of the lateral hypothalamic area
Goto, M., Canteras, N. S., Burns, G., & Swanson, L. W. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20764 · Cited by 95 · see citing works
Possible glutamatergic/aspartatergic projections to the supramammillary nucleus and their origins in the rat studied by selective [3H]D-aspartate labelling and immunocytochemistry
Kiss, J., Csáki, Á., Bokor, H., Kocsis, K., & Kocsis, B. (2002) · Neuroscience · doi:10.1016/s0306-4522(02)00037-4 · Cited by 95 · see citing works
Brain stimulation reward and dopamine terminal fields. I. Caudate-putamen, nucleus accumbens and amygdala
Prado-Alcalá, R. A., & Wise, R. A. (1984) · Brain Research · doi:10.1016/0006-8993(84)90567-5 · Cited by 94 · see citing works
Signalled versus unsignalled intravenous amphetamine: large differences in the acute psychomotor response and sensitization
Crombag, H. S., Badiani, A., & Robinson, T. E. (1996) · Brain Research · doi:10.1016/0006-8993(96)00066-2 · Cited by 91 · see citing works
Satiation effects in self-stimulation of the brain.
Olds, J. (1958) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0039616 · Cited by 91 · see citing works
Positive reinforcement of the barpressing response by a light stimulus following dark operant pretests with no aftereffect.
Marx, M. H., Henderson, R. L., & Roberts, C. L. (1955) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0045062 · Cited by 89 · see citing works
A quantitative demonstration of animal drive.
Dashiell, J. F. (1925) · Journal of comparative psychology · doi:10.1037/h0071833 · Cited by 89 · see citing works
Pontine and mesencephalic substrates of self-stimulation
Rompré, P.-P., & Miliaressis, E. (1985) · Brain Research · doi:10.1016/0006-8993(85)91435-0 · Cited by 88 · see citing works
Hypothalamic substrate for the positive reinforcing properties of morphine in the rat
OLDS, M. E. (1979) · Brain Research · doi:10.1016/0006-8993(79)90175-6 · Cited by 88 · see citing works
Strong positive reward in median raphe: specific inhibition bypara-chlorophenylalanine
Miliaressis, E., Bouchard, A., & Jacobowitz, D. M. (1975) · Brain Research · doi:10.1016/0006-8993(75)90521-1 · Cited by 88 · see citing works
Cortical projections of the nucleus of the diagonal band of broca and of the substantia innominata in the rat: An anatomical study using the anterograde transport of a conjugate of wheat germ agglutinin and horseradish peroxidase
Lamour, Y. A., Dutar, P., & Jobert, A. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90061-7 · Cited by 85 · see citing works
Regional neuroleptic microinjections indicate a role for nucleus accumbens in lateral hypothalamic self-stimulation reward
Stellar, J. R., & Corbett, D. (1989) · Brain Research · doi:10.1016/0006-8993(89)91400-5 · Cited by 83 · see citing works

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Heimer L Wilson RD Santini M The subcortical projections of the allocortex: similarities in the neural associations of the hippocampus, the piriform cortex, and the neocortex Golgi Centennial Symposium Proceedings 1975 New York Raven Press 177 193

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“Aversive, negative sensory input is processed by the habenular complex, an epithalamic structure involved in fear, anxiety, depression, and stress (Geisler et al. 2008, Ikemoto 2010, Winter et al. 2010).”
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“In addition, reward is an induced internal state that produces and reinforces approach behavior [3,4].”
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Authors: Ikemoto, S.
Affiliations: National Institutes of Health (US)
Corresponding author: Ikemoto, Satoshi
ORCID: Ikemoto, Satoshi
Venue: Neuroscience & Biobehavioral Reviews
Publisher: Elsevier BV
Published: 2010-11
Volume: 35
Issue: 2
Pages: 129-150
ISSN: 0149-7634 (ISSN-L)
DOI: 10.1016/j.neubiorev.2010.02.001
PMC: PMC2894302
OpenAlex: W2026626196
Cited by: 454
References: 277
Citations by year: 2026: 20 · 2025: 20 · 2024: 26 · 2023: 22 · 2022: 39 · 2021: 33 · 2020: 35 · 2019: 31 · 2018: 24 · 2017: 13 · 2016: 23 · 2015: 31 · 2014: 33 · 2013: 35 · 2012: 32
FWCI: 13.46
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience & Biobehavioral Reviews (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health
National Institute on Drug Abuse (ZIADA000480, Z01DA000439, ZIADA000439)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: brain reward system, mesolimbic dopamine system, drug reward, supramammillary nucleus, rostromedial tegmental nucleus, midbrain raphe nuclei, approach behavior, reinforcement, medial prefrontal cortex, septal area, ventral pallidum, bed nucleus of the stria terminalis, preoptic area, lateral hypothalamus, lateral habenula, periaqueductal gray, laterodorsal tegmental nucleus, parabrachial area
MeSH terms: Animals, Brain, Dopamine, Models, Neurological, Neural Pathways, Reward, Self Administration

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Brain reward circuitry beyond the mesolimbic dopamine system: a neurobiological theory

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