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Basal ganglia circuit loops, dopamine and motivation: A review and enquiry
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Dopamine neurons located in the midbrain play a role in motivation that regulates approach behavior (approach motivation). In addition, activation and inactivation of dopamine neurons regulate mood and induce reward and aversion, respectively. Accumulating evidence suggests that such motivational role of dopamine neurons is not limited to those located in the ventral tegmental area, but also in the substantia nigra. The present paper reviews previous rodent work concerning dopamine's role in approach motivation and the connectivity of dopamine neurons, and proposes two working models: One concerns the relationship between extracellular dopamine concentration and approach motivation. High, moderate and low concentrations of extracellular dopamine induce euphoric, seeking and aversive states, respectively. The other concerns circuit loops involving the cerebral cortex, basal ganglia, thalamus, epithalamus, and midbrain through which dopaminergic activity alters approach motivation. These models should help to generate hypothesis-driven research and provide insights for understanding altered states associated with drugs of abuse and affective disorders.
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“Intriguingly, the caudate nucleus receives projections from midbrain DA and is part of the nigrostriatal DA system, which, like the mesolimbic DA system, plays a role in reward and motivation (Ikemoto et al., 2015).”
From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Ikemoto et al., 2015
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BackgroundGaming Increases Craving to Gaming-Related Stimuli in Individuals With Internet Gaming Disorder
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“Connections comprising significant components (subnetworks) were assigned to motor, associative, or limbic circuits that constitute the cortico–basal ganglia–thalamocortical network (Galvan et al., 2015; Ikemoto et al., 2015).”
BackgroundSeeking motivation and reward: Roles of dopamine, hippocampus, and supramammillo-septal pathway
Kesner, A. J., Calva, C. B., & Ikemoto, S. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102252 · Cited by 61
“participate in producing seeking behavior toward goals by interacting with the thalamo-cortico-basal ganglia system (Ikemoto et al., 2015).”
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“Intriguingly, the caudate nucleus receives projections from midbrain DA and is part of the nigrostriatal DA system, which, like the mesolimbic DA system, plays a role in reward and motivation (Ikemoto et al., 2015).”
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“Still other findings identified circuit loops involving the cerebral cortex, basal ganglia, thalamus, epithalamus, and midbrain through which dopaminergic activity affected motivation [29].”
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“…habit learning and formation (Graybiel and Grafton 2015), multisensory integration (Coffey et al. 2016; Reig and Silberberg 2014), and emotional and motivational regulation (Francis et al. 2015; Haber and Knutson 2010; Ikemoto et al. 2015; Lobo et al. 2013, Révy et al. 2014; Sesack and Grace 2010).”
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“Social interaction is thought to produce an internal reward state which will, in turn, reinforce and promote approach behaviors (Ikemoto et al. 2015).”
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“…this respect, the nucleus accumbens, which is part of the dopaminergic system, is seen as part of the reward processing system which is mainly active during experiencing reward, and its activity may correlate with the reward value (Salimpoor et al., 2013, 2015; Ikemoto et al., 2015; Zatorre, 2015).”
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“Finally, antipsychotics have been suggested to directly cause amotivation and subsequent impairments in goal-directed behavior by the reduction of dopaminergic transmission (Ikemoto et al., 2015).”
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Striatal Activity and Reward Relativity: Neural Signals Encoding Dynamic Outcome Valuation
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“Introduction Stable neural representations have been important components of motivational neuroscience (Hikosaka et al., 2014; Bowman et al., 1996; Ikemoto et al., 2015; Morita and Kawaguchi, 2015) and historically helped strengthen the idea that a hierarchy of incentives can reliably guide behavior and brain function…”
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“cocaine, amphetamine, cannabis, ecstasy, opiates such as heroin and opium and alcohol among others) is known to increase DA signalling in mesocorticolimbic circuit and it had long been accepted that rewarding effects of drugs are related to dopamine transmission (Ikemoto et al. 2015; Volkow Nora and Morales 2015).”
BackgroundDetecting stable individual differences in the functional organization of the human basal ganglia
García-García, M., Nikolaidis, A., Bellec, P., Craddock, R. C., Cheung, B., Castellanos, F. X., & Milham, M. P. (2017) · NeuroImage · doi:10.1016/j.neuroimage.2017.07.029 · Cited by 22
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Increased alcohol consumption in sleep-restricted rats is mediated by delta FosB induction
García‐García, F., Priego-Fernández, S., López-Muciño, L. A., Acosta-Hernández, M. E., & Peña-Escudero, C. (2021) · Alcohol · doi:10.1016/j.alcohol.2021.02.004 · Cited by 21
Fransquet, P., Hutchinson, D. M., Olsson, C. A., Wilson, J., ALLSOP, S. J., Najman, J. M., Elliott, E. J., Mattick, R. P., Saffery, R., & Ryan, J. L. (2016) · Current Zoology · doi:10.1093/eep/dvw023 · Cited by 21
McLaughlin, T., Blum, K., Steinberg, B., Modestino, E. J., Fried, L., Baron, D. A., Siwicki, D., Braverman, E. R., & Badgaiyan, R. D. (2018) · Journal of Behavioral Addictions · doi:10.1556/2006.6.2017.081 · Cited by 24
“While much of this evidence points to the loci of this effect of DA being the ventral tegmental area (VTA), other evidence suggests that the motivational and other effects of DA on behavior may also derive from the substantia nigra (Ikemoto et al., 2015; Krawczyk et al., 2013).”
BackgroundMolecular Plasticity of the Nucleus Accumbens Revisited—Astrocytic Waves Shall Rise
Kardos, J., Dobolyi, Á., Szabó, Z. M., Simon, Á., Lourmet, G. S., Palkovits, M., & Héja, L. (2019) · Molecular Neurobiology · doi:10.1007/s12035-019-1641-z · Cited by 22
Troshev, D. V., Berezhnoy, D. S., Игоревна, К. О., Абаимов, Д. А., Muzychuk, O. A., Nalobin, D. S., Stvolinsky, S. L., & Федорова, Т. Н. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2021.04.006 · Cited by 21
Blázquez, G., Castañé, A., Saavedra, A., Masana, M., Alberch, J., & Pérez‐Navarro, E. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00317 · Cited by 22
Janíčková, H., Kljakic, O., Rosborough, K., Raulic, S., Matovic, S., Gros, R., Saksida, L. M., Bussey, T. J., Inoue, W., Prado, V. F., et al. (2019) · The FASEB Journal · doi:10.1096/fj.201802108r · Cited by 23
“It is also important to note that PPT/LDT cholinergic neurons critically influence activity of midbrain dopaminergic neurons (96–99), known to be involved in the modulation of stress responsiveness (100) and motivation (101).”
BackgroundLi, R., Wang, X., Lin, F., Song, T., Zhu, X., & Lei, H. C. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.116588 · Cited by 20
Selley, D. E., Lazenka, M. F., Sim‐Selley, L. J., McVoy, J. R. S., Potter, D. N., Chartoff, E. H., Carlezon, W. A., & Negus, S. S. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.107935 · Cited by 19
Hu, S., Wu, H., Xu, C., Wang, A., Wang, Y., Shen, T., Huang, F., Kan, H., & Li, C. (2019) · Frontiers in Neural Circuits · doi:10.3389/fncir.2019.00025 · Cited by 18
Extracellular Vesicles in Psychiatry Research in the Context of RDoC Criteria
Ilgın, C., & Topuzoǧlu, A. (2018) · Psychiatry Investigation · doi:10.30773/pi.2018.09.17 · Cited by 17
Sanchez, W. N., Pochapski, J. A., Jessen, L. F., Ellenberger, M., Schwarting, R. K. W., Robinson, D. L., Andreatini, R., & Cunha, C. D. (2021) · British Journal of Pharmacology · doi:10.1111/bph.15658 · Cited by 15
Batton, A. D., Blaha, C. D., Bieber, A. J., et al. (2018) · Synapse · doi:10.1002/syn.22073 · Cited by 15
Single-dose L-dopa increases upper brainstem GABA in Parkinson's disease: A preliminary study
Song, Y., Gong, T., Xiang, Y., Mikkelsen, M. E., Wang, G., & Edden, R. A. E. (2021) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2021.117309 · Cited by 16
Glueck, E., Ginder, D. E., Hyde, J., North, K., & Grimm, J. W. (2016) · Psychopharmacology · doi:10.1007/s00213-016-4516-2 · Cited by 15
“One possibility is that EE or loss of EE produces a state of low motivation, perhaps reflecting decreased dopamine signaling (Ikemoto et al. 2015; Salamone et al. 2016).”
Baldi, P., Alhassen, W., Chen, S., Nguyen, H. N., Khoudari, M., & Alachkar, A. (2021) · Journal of Neuroscience Research · doi:10.1002/jnr.24919 · Cited by 12
Fuenzalida‐Uribe, N., & Campusano, J. M. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.12.032 · Cited by 12
Dopamine modulates the optomotor response to unreliable visual stimuli in Drosophila melanogaster
Akiba, M., Sugimoto, K., Aoki, R., Murakami, R., Miyashita, T., Hashimoto, R., Hiranuma, A., Yamauchi, J., Ueno, T., & Morimoto, T. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14648 · Cited by 13
Group independent components underpin responses to items from a depression scale
Stoyanov, D., Khorev, V. S., Paunova, R., Kandilarova, S., Kurkin, S., & Calhoun, V. D. (2023) · Acta Neuropsychiatrica · doi:10.1017/neu.2023.22 · Cited by 13
Systematic review on resting-state fMRI in people with AUD and people who binge drink
Rodríguez, G. C., Russell, M. A., & Claus, E. D. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02796-y · Cited by 12
Modeling of Neurodegenerative Diseases Using Discrete Chaotic Systems
Shabestari, P. S., Rostami, Z., Pham, V., et al. (2019) · Communications in Theoretical Physics · doi:10.1088/0253-6102/71/10/1241 · Cited by 12
Grimm, O., Thomä, L., Kranz, T. M., & Reif, A. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02003-y · Cited by 11
“Caudate (Ca), putamen (Pu), and nucleus accumbens (NAcc) are important hubs of cognition and motivation in the basal ganglia [18].”
BackgroundLafragette, A., Bardo, M. T., Lardeux, V., Solinas, M., & Thiriet, N. (2016) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyw097 · Cited by 13
“…with previous work showing that Δ FosB accumulation in D1R(+) MSNs plays a major role in cocaine reward (Kelz et al., 1999; Colby et al., 2003; Grueter et al., 2013) and that the activation of D1R(+) cells in the striatum produces reinforcing effects (Kravitz et al., 2012; Ikemoto et al., 2015).”
InfluentialNeurophysiological correlates of stereotypic behaviour in a model carnivore species
Díez‐León, M., Kitchenham, L., Duprey, R., Bailey, C. D. C., Choleris, E., Lewis, M. H., & Mason, G. J. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112056 · Cited by 12
Gemikonakli, G., Keay, K. A., Kendig, M. D., Kang, J. W. M., Corbit, L. H., & Mor, D. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14518 · Cited by 12
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Relapse to cocaine seeking in an invertebrate
Amaning-Kwarteng, A. O., Asif-Malik, A., Pei, Y., & Canales, J. J. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.04.008 · Cited by 11
“…with common brain substrates, one of which is the dopaminergic system and its affiliated basal ganglia thalamo-cortical systems in mammals (Ikemoto et al., 2015, Volkow and Morales, 2015), and therefore it could be argued that such drugs can prime one another by reactivating…”
Cilia in the Striatum Mediate Timing-Dependent Functions
Alhassen, W., Alhassen, S., Chen, J., Monfared, R. V., & Alachkar, A. (2022) · Molecular Neurobiology · doi:10.1007/s12035-022-03095-9 · Cited by 12
Limbic-Basal Ganglia Circuits Parallel and Integrative Aspects
Groenewegen, H. J., Voorn, P., & Scheel‐Krüger, J. (2016) · Innovations in cognitive neuroscience · doi:10.1007/978-3-319-42743-0_2 · Cited by 11
Bao, D., Zhou, J., Ying, H., Yang, X., Jiao, W., Hu, Y., & Wang, X. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00654 · Cited by 11
Takeuchi, E., Yamada, D., Suzuki, S., Saitoh, A., Itoh, M., Hayashi, T., Yamada, M., Wada, K., & Sekiguchi, M. (2020) · PLoS ONE · doi:10.1371/journal.pone.0230647 · Cited by 11
“Since dopaminergic neurotransmission from the VTA to the NAc is known to play an important role in emotional arousal and reward [38], we speculated that this pathway was activated after the ingestion of a diet high in ω-3 PUFAs to reduce FST-immobility.”
Background
Metadata
- Authors
- Ikemoto, S., Yang, C., & Tan, A.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Ikemoto, Satoshi
- Venue
- Behavioural Brain Research
- Publisher
- Elsevier BV
- Published
- 2015-09
- Volume
- 290
- Pages
- 17-31
- ISSN
- 0166-4328 (ISSN-L)
- PMC
- PMC4447603
- OpenAlex
- W2081845928
- Semantic Scholar
- bb06782b6fb20361735cf21f960fea754adbcf67
- Cited by
- 226
- References
- 255
- Citations by year
- 2026: 12 · 2025: 16 · 2024: 14 · 2023: 15 · 2022: 21 · 2021: 25 · 2020: 29 · 2019: 22 · 2018: 22 · 2017: 21 · 2016: 26 · 2015: 3
- FWCI
- 2.85
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Behavioural Brain Research (publishedVersion, cc-by)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute on Drug Abuse (ZIADA000575, ZIADA000439, ZIADA000550)
- 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
- dopamine, approach motivation, substantia nigra, ventral tegmental area, reward, aversion, thalamus, epithalamus, drugs of abuse, mood disorders
- MeSH terms
- Animals, Basal Ganglia, Motivation, Nerve Net, Reward, Dopaminergic Neurons
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