Electrical stimulation of reward sites in the ventral tegmental area increases dopamine transmission in the nucleus accumbens of the rat
Abstract
In vivo microdialysis with HPLC-ED was used to measure dopamine (DA), 3,4-dihydroxyphenylacetic acid (DOPAC), homovanillic acid (HVA) and 5-hydroxyindoleacetic acid (5-HIAA) in the nucleus accumbens of the rat, prior, during, and after 15-min periods of electrical brain stimulation at sites in the ventral tegmental area (VTA) that supported intracranial self-stimulation (ICSS). In the first experiment, both ICSS and yoked stimulation of the VTA evoked significant increases in extracellular concentrations of DA, its metabolites, and 5-HIAA. Comparable results from ICSS and yoked groups were interpreted as evidence that the rewarding properties of VTA stimulation were a causal factor in the elevated DA transmission in the nucleus accumbens, rather than intense operant behavior. Further evidence for this hypothesis came from a second set of data in which changes in extracellular DA levels during the measurement of rate/intensity functions for ICSS were positively correlated. 5-HIAA concentrations also increased during ICSS but these changes were not correlated with either ICSS rate or current intensity, suggesting that changes in serotonin metabolism were unlikely to subserve brain stimulation reward in the VTA. These results add to the growing body of evidence linking changes in extracellular DA in the mesolimbic DA system with both brain stimulation reward and the conditioned and unconditioned rewarding effects of biologically relevant stimuli.
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Electrical brain stimulation at the medial forebrain bundle/VTA is rewarding and triggers dopamine release in the ventral striatum and investigatory responses of sniffing.
“Electrical brain stimulation at the medial forebrain bundle/VTA is rewarding and triggers dopamine release in the ventral striatum (Fiorino et al., 1993; Garris et al., 1999; Cheer et al., 2005; Hernandez et al., 2006) and investigatory responses of sniffing (Clarke and Trowill, 1971; Ikemoto and Panksepp, 1994).”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Fiorino et al., 1993
Cites
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
From motivation to action: Functional interface between the limbic system and the motor system
MOGENSON, G., JONES, D., & YIM, C. (1980) · Progress in Neurobiology · doi:10.1016/0301-0082(80)90018-0 · Cited by 2,331 · see citing works
Microdialysis—Theory and application
Benveniste, H., & Hüttemeier, P. C. (1990) · Progress in Neurobiology · doi:10.1016/0301-0082(90)90027-e · Cited by 647 · see citing works
Herkenham, M. (1987) · Neuroscience · doi:10.1016/0306-4522(87)90268-5 · Cited by 520 · see citing works
Sexual behavior enhances central dopamine transmission in the male rat
Pfaus, J. G., Damsma, G., Nomikos, G. G., Wenkstern, D. G., Blaha, C. D., Phillips, A. G., & Fibiger, H. C. (1990) · Brain Research · doi:10.1016/0006-8993(90)91309-5 · Cited by 438 · see citing works
Self-citationWesterink, B. H. C., Damsma, G., Rollema, H., Vries, J. B. D., & Horn, A. S. (1987) · Life Sciences · doi:10.1016/0024-3205(87)90695-3 · Cited by 423 · see citing works
Zetterström, T., Sharp, T., Collin, A.-K., & Ungerstedt, U. (1988) · European Journal of Pharmacology · doi:10.1016/0014-2999(88)90110-0 · Cited by 378 · see citing works
Damsma, G., Pfaus, J. G., Wenkstern, D., Phillips, A. G., & al, E. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.1.181 · Cited by 370 · see citing works
Self-citationAmphetamine‐Induced Dopamine Release in the Rat Striatum: An In Vivo Microdialysis Study
Butcher, S. P., Fairbrother, I. S., Kelly, J. S., & Arbuthnott, G. W. (1988) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1988.tb02919.x · Cited by 289 · see citing works
Crow, T. J. (1973) · Psychological Medicine · doi:10.1017/s0033291700046353 · Cited by 220 · 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
Self-citationThe 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
Self-citationSexual behavior increases c-fos expression in the forebrain of the male rat
Robertson, G. S., Pfaus, J. G., Atkinson, L. J., Matsumura, H., Phillips, A. G., & Fibiger, H. C. (1991) · Brain Research · doi:10.1016/0006-8993(91)91477-i · Cited by 169 · see citing works
Self-citationGallistel, C. R., Gomita, Y., Yadin, E., & Campbell, K. J. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-05-01246.1985 · Cited by 119 · see citing works
Neurochemical correlates of brain-stimulation reward measured by ex vivo and in vivo analyses
Phillips, A. G., Blaha, C. D., & Fibiger, H. C. (1989) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(89)80017-x · Cited by 115 · see citing works
Self-citationEscape from Self-Produced Rates of Brain Stimulation
Steiner, S. S., Beer, B., & Shaffer, M. M. (1969) · Science · doi:10.1126/science.163.3862.90 · Cited by 100 · see citing works
Nakahara, D., Ozaki, N., Miura, Y., Miura, H., & Nagatsu, T. (1989) · Brain Research · doi:10.1016/0006-8993(89)91234-1 · Cited by 99 · see citing works
Nakahara, D., Fuchikami, K., Ozaki, N., Iwasaki, T., & Nagatsu, T. (1992) · Brain Research · doi:10.1016/0006-8993(92)90813-o · Cited by 63 · see citing works
Blaha, C. D., & Phillips, A. G. (1990) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(90)90050-p · Cited by 53 · see citing works
Self-citationRe-evaluation of the role of dopamine in intracranial self-stimulation using in vivo microdialysis
Miliaressis, E., Émond, C., & Merali, Z. (1991) · Behavioural Brain Research · doi:10.1016/s0166-4328(05)80095-6 · Cited by 52 · see citing works
Nakahara, D., Ozaki, N., Kapoor, V., & Nagatsu, T. (1989) · Neuroscience Letters · doi:10.1016/0304-3940(89)90343-1 · Cited by 47 · see citing works
Phillips, A. G., Coury, A., Fiorino, D. F., LePiane, F. G., Brown, E. E., & Fibiger, H. C. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb25968.x · Cited by 40 · see citing works
Self-citationHaloperidol blocks the conditioned place preferences induced by rewarding brain stimulation.
Ettenberg, A., & Duvauchelle, C. L. (1988) · Behavioral Neuroscience · doi:10.1037//0735-7044.102.5.687 · Cited by 31 · see citing works
Phillips, A. G., Jakubovič, A., & Fibiger, H. C. (1987) · Brain Research · doi:10.1016/0006-8993(87)91053-5 · Cited by 29 · see citing works
Self-citationResponse involvement in brain stimulation reward
Ettenberg, A., Laferrière, A., Milner, P. M., et al. (1981) · Physiology & Behavior · doi:10.1016/0031-9384(81)90236-5 · Cited by 18 · see citing works
The importance of subject control in reinforcing brain stimulation
Faircloth, K. P. (1974) · Learning and Motivation · doi:10.1016/0023-9690(74)90034-4 · Cited by 16 · see citing works
Subject control as a determinant of the reinforcing properties of intracranial stimulation☆
WAHKWANTSANG, & Stutz, R. M. (1984) · Physiology & Behavior · doi:10.1016/0031-9384(84)90197-5 · Cited by 11 · see citing works
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Ikemoto, S. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.004 · Cited by 1,477 · see citing works
Pharmacology and behavioral pharmacology of the mesocortical dopamine system
Tzschentke, T. M. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00033-2 · Cited by 481 · see citing works
Brain reward circuitry beyond the mesolimbic dopamine system: a neurobiological theory
Ikemoto, S. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.02.001 · Cited by 454 · see citing works
Adamantidis, A. R., Tsai, H.-C., Boutrel, B., Zhang, F., Stuber, G. D., Budygin, E. A., Tourino, C., Bonci, A., Deisseroth, K., & de Lecea, L. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2246-11.2011 · Cited by 357 · 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
Dynamic changes in nucleus accumbens dopamine efflux during the Coolidge effect in male rats
Fiorino, D. F., Coury, A., & Phillips, A. G. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-12-04849.1997 · Cited by 226 · see citing works
Self-citationZhu, J., & Reith, M. (2008) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/187152708786927877 · Cited by 140 · see citing works
Wenzel, J. M., Rauscher, N. A., Cheer, J. F., & Oleson, E. B. (2015) · ACS Chemical Neuroscience · doi:10.1021/cn500255p · Cited by 131 · see citing works
- Authors
- FIORINO, D., COURY, A., FIBIGER, H., & PHILLIPS, A.
- Affiliations
- University of British Columbia (CA)
- Corresponding author
- PHILLIPS, A
- ORCID
- FIORINO, D
- Venue
- Behavioural Brain Research
- Publisher
- Elsevier BV
- Published
- 1993-06-30
- Volume
- 55
- Issue
- 2
- Pages
- 131-141
- ISSN
- 0166-4328 (ISSN-L)
- OpenAlex
- W2076287600
- Cited by
- 131
- References
- 27
- Citations by year
- 2025: 3 · 2024: 1 · 2022: 2 · 2021: 6 · 2020: 3 · 2019: 3 · 2018: 1 · 2016: 2 · 2015: 5 · 2014: 3 · 2013: 2 · 2012: 3
- FWCI
- 1.80
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Behavioural Brain Research (publishedVersion)
- PubMed (publishedVersion)
- 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
- ventral tegmental area, nucleus accumbens, dopamine signaling, intracranial self-stimulation, electrical brain stimulation, reward, mesolimbic dopamine system, 5-hydroxyindoleacetic acid, serotonin metabolism, DOPAC, homovanillic acid, rate-intensity function
- MeSH terms
- Animals, Brain Mapping, Dominance, Cerebral, Dopamine, Electric Stimulation, Homovanillic Acid, Hydroxyindoleacetic Acid, Male, Motivation, Neural Pathways, Synaptic Transmission, Nucleus Accumbens, Reward, Self Stimulation, Serotonin, Tegmentum Mesencephali, 3,4-Dihydroxyphenylacetic Acid, Rats
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