Variations in extracellular levels of dopamine, noradrenaline, glutamate, and aspartate across the sleep–wake cycle in the medial prefrontal cortex and nucleus accumbens of freely moving rats
Abstract
We used intracerebral microdialysis coupled with electrophysiologic recordings to determine relative changes in the concentrations of several neurotransmitters in the medial prefrontal cortex and nucleus accumbens of freely moving rats during waking, slow‐wave sleep, and rapid eye movement (REM) sleep. The concentrations of noradrenaline, dopamine, glutamate, and aspartate in 2‐min dialysate samples were analyzed by capillary electrophoresis combined with laser‐induced fluorescence detection. Changes in glutamate and aspartate concentrations were found only in the nucleus accumbens, in which a decrease was obtained during both slow‐wave sleep and REM sleep compared to waking. A progressive reduction in the release of noradrenaline was observed from waking to REM sleep in both structures. In contrast, dopamine concentrations were higher during waking and REM sleep compared to that during slow‐wave sleep. The latter results demonstrate that contrary to the findings of earlier electrophysiologic studies carried out on ventral tegmental area dopaminergic neurons, changes in the release of dopamine in projection areas occur across the sleep–wake cycle. The elevated levels of dopamine during waking and REM sleep in the medial prefrontal cortex and the nucleus accumbens could result from changes during these two states in afferent modulation at the level of cell bodies or at the level of dopaminergic terminals. © 2005 Wiley‐Liss, Inc.
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There is some evidence that the increase in cholinergic activity during REM sleep is accompanied by increased dopaminergic activity originating from ventral tegmental, rather than striatal, areas which innervate nucleus accumbens and medial prefrontal cortex.
“There is some evidence that the increase in cholinergic activity during REM sleep is accompanied by an increased dopaminergic activity originating from ventral tegmental, rather than striatal, areas which innervate a network of further regions such as the nucleus accumbens and medial prefrontal cortex (724, 757).”
From About Sleep's Role in Memory (2013) · cites this paper as [724]
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
Ledent, C. A., Valverde, O., Cossu, G., Petitet, F., Aubert, J.-F., Beslot, F., Böhme, G. A., Impérato, A., Pedrazzini, T., Roques, B. P., et al. (1999) · Science · doi:10.1126/science.283.5400.401 · Cited by 3,612 · see citing works
Neurons containing hypocretin (orexin) project to multiple neuronal systems
Peyron, C., Tighe, D. K., van den Pol, A. N., de Lecea, L., Heller, H. C., Sutcliffe, J. G., & Kilduff, T. S. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-23-09996.1998 · Cited by 3,466 · see citing works
Lin, L., Faraco, J., Li, R., Kadotani, H., Rogers, W., Lin, X., Qiu, X., de Jong, P. J., Nishino, S., & Mignot, E. (1999) · Cell · doi:10.1016/s0092-8674(00)81965-0 · Cited by 2,613 · see citing works
Aston-Jones, G., & Bloom, F. (1981) · The Journal of Neuroscience · doi:10.1523/jneurosci.01-08-00876.1981 · Cited by 1,960 · see citing works
Regional cerebral blood flow throughout the sleep-wake cycle. An H2(15)O PET study
Braun, A. (1997) · Brain · doi:10.1093/brain/120.7.1173 · Cited by 1,268 · see citing works
Sleep Cycle Oscillation: Reciprocal Discharge by Two Brainstem Neuronal Groups
Hobson, J. A., McCarley, R. W., & Wyzinski, P. (1975) · Science · doi:10.1126/science.1094539 · Cited by 1,238 · see citing works
Functional neuroanatomy of human rapid-eye-movement sleep and dreaming
Maquet, P., Péters, J.-M., Aerts, J., Delfiore, G., Degueldre, C., Luxen, A., & Franck, G. (1996) · Nature · doi:10.1038/383163a0 · Cited by 1,168 · see citing works
On the significance of subterritories in the “accumbens” part of the rat ventral striatum
Zahm, D. S., & Brog, J. S. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90202-d · Cited by 1,040 · see citing works
Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens
Nicola, S. M., Surmeier, D. J., & Malenka, R. C. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.185 · Cited by 931 · see citing works
The cognitive neuroscience of sleep: neuronal systems, consciousness and learning
Hobson, J. A., & Pace-Schott, E. F. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn915 · Cited by 835 · see citing works
Gonon, F. G. (1988) · Neuroscience · doi:10.1016/0306-4522(88)90307-7 · Cited by 676 · see citing works
Dreaming and REM sleep are controlled by different brain mechanisms
Solms, M. (2000) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00003988 · Cited by 595 · see citing works
Nisell, M., Nomikos, G. G., & Svensson, T. H. (1994) · Synapse · doi:10.1002/syn.890160105 · Cited by 510 · see citing works
Forebrain activation in REM sleep: an FDG PET study
Nofzinger, E. A., Mintun, M. A., Wiseman, M., Kupfer, D. J., & Moore, R. Y. (1997) · Brain Research · doi:10.1016/s0006-8993(97)00807-x · Cited by 501 · see citing works
Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents
Condé, F., Maire-Lepoivre, E., Audinat, É., & Crépel, F. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903520407 · Cited by 494 · 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
Marrosu, F., Portas, C., Mascia, M. S., Casu, M. A., Fà, M., Giagheddu, M., Imperato, A., & Gessa, G. L. (1995) · Brain Research · doi:10.1016/0006-8993(94)01399-3 · Cited by 480 · see citing works
The hypocretin/orexin ligand–receptor system: implications for sleep and sleep disorders
Kilduff, T. S., & Peyron, C. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01594-0 · Cited by 438 · see citing works
Lorrain, D. S., Baccei, C. S., Bristow, L. J., Anderson, J. J., & Varney, M. A. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00652-8 · Cited by 432 · see citing works
Nicotinic effects on the firing pattern of midbrain dopamine neurons
GRENHOFF, J., ASTON‐JONES, G., & SVENSSON, T. H. (1986) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1986.tb07988.x · Cited by 399 · see citing works
Release of Hypocretin (Orexin) during Waking and Sleep States
Kiyashchenko, L. I., Mileykovskiy, B. Y., Maidment, N. T., Lam, H. A., Wu, M., John, J., Peever, J. H., & Siegel, J. M. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-13-05282.2002 · Cited by 337 · see citing works
Role and Origin of the GABAergic Innervation of Dorsal Raphe Serotonergic Neurons
Gervasoni, D., Peyron, C., Rampon, C., Barbagli, B., Chouvet, G., Urbain, N., Fort, P., & Luppi, P. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-11-04217.2000 · Cited by 298 · see citing works
Forster, G. L., & Blaha, C. D. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00250.x · Cited by 271 · see citing works
(1997) · Cited by 270 · see citing works
Miller, J. D., Farber, J., Gatz, P., Roffwarg, H. P., & German, D. C. (1983) · Brain Research · doi:10.1016/0006-8993(83)91101-0 · Cited by 269 · see citing works
Afferent modulation of dopamine neuron firing patterns
Kitai, S. T., Shepard, P. D., Callaway, J. C., & Scroggs, R. S. (1999) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)00040-9 · Cited by 234 · see citing works
Chergui, K., Suaud‐Chagny, M., & Gonon, F. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90465-0 · Cited by 229 · see citing works
Self-citationState-dependent release of acetylcholine in rat thalamus measured by in vivo microdialysis
Williams, J., Comisarow, J., Day, J., Fibiger, H., & Reiner, P. B. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-09-05236.1994 · Cited by 192 · see citing works
Trulson, M. E., & Preussler, D. W. (1984) · Experimental Neurology · doi:10.1016/s0014-4886(84)90105-5 · Cited by 162 · see citing works
Portas, C. M., Bjorvatn, B., Fagerland, S., Grønli, J., Mundal, V., Sørensen, E., & Ursin, R. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00438-7 · Cited by 161 · see citing works
Yonezawa, Y., Kuroki, T., Kawahara, T., Tashiro, N., & Uchimura, H. (1998) · European Journal of Pharmacology · doi:10.1016/s0014-2999(97)01435-0 · Cited by 133 · see citing works
Review Article Reciprocaldopamine-glutamatemodulation of release in the basalganglia
Morari, M., Marti, M., Sbrenna, S., Fuxé, K., Bianchi, C. L., & Beani, L. (1998) · Neurochemistry International · doi:10.1016/s0197-0186(98)00052-7 · Cited by 132 · see citing works
Maloney, K. J., Mainville, L., & Jones, B. E. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.01907.x · Cited by 122 · see citing works
Gronier, B., & Rasmussen, K. (1998) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0701850 · Cited by 107 · see citing works
Monoamines and sleep: microdialysis findings in pons and amygdala
Shouse, M. N., Staba, R. J., Saquib, S. F., & Farber, P. R. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02013-8 · Cited by 103 · see citing works
Bert, L., Robert, F., Denoroy, L., Stoppini, L., & Renaud, B. (1996) · Journal of Chromatography A · doi:10.1016/s0021-9673(96)00595-x · Cited by 87 · see citing works
Self-citationNeurophysiological support of consciousness during waking and sleep
Gottesmann, C. (1999) · Progress in Neurobiology · doi:10.1016/s0301-0082(99)00014-3 · Cited by 85 · see citing works
Self-citationOakman, S. A., Faris, P. L., Cozzari, C., & Hartman, B. K. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00307-3 · Cited by 79 · see citing works
Gronier, B., Perry, K. W., & Rasmussen, K. (2000) · Psychopharmacology · doi:10.1007/s002130050002 · Cited by 79 · see citing works
The neurochemistry of waking and sleeping mental activity: the disinhibition-dopamine hypothesis
GOTTESMANN, C. (2002) · Psychiatry and Clinical Neurosciences · doi:10.1046/j.1440-1819.2002.01022.x · Cited by 69 · see citing works
Self-citationParrot, S., Bert, L., Mouly‐Badina, L., et al. (2003) · Cellular and Molecular Neurobiology · doi:10.1023/a:1025009221285 · Cited by 64 · see citing works
Self-citationStudy of a GABA c receptor antagonist on sleep-waking behavior in rats
Arnaud, C., Gauthier, P., & Gottesmann, C. (2001) · Psychopharmacology · doi:10.1007/s002130000653 · Cited by 58 · see citing works
Self-citationBrain inhibitory mechanisms involved in basic and higher integrated sleep processes
Gottesmann, C. (2004) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.04.003 · Cited by 41 · see citing works
Self-citationNeuromodulation of the prefrontal cortex during sleep
Hilaire, Z. D. S., Orosco, M., Rouch, C., Python, A., & Nicolaı̈dis, S. (2000) · Neuroreport · doi:10.1097/00001756-200006050-00005 · Cited by 19 · see citing works
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Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
“There is some evidence that the increase in cholinergic activity during REM sleep is accompanied by an increased dopaminergic activity originating from ventral tegmental, rather than striatal, areas which innervate a network of further regions such as the nucleus accumbens and medial prefrontal cortex (724, 757).”
BackgroundControl of sleep and wakefulness
Brown, R. E., Basheer, R., McKenna, J. T., Strecker, R. E., & McCarley, R. W. (2012) · Physiological Reviews · doi:10.1152/physrev.00032.2011 · Cited by 1,477 · see citing works
VTA dopaminergic neurons regulate ethologically relevant sleep-wake behaviors
Eban-Rothschild, A., Rothschild, G., Giardino, W. J., Jones, J. R., & de Lecea, L. (2016) · Nature Neuroscience · doi:10.1038/nn.4377 · Cited by 583 · see citing works
Memory-enhancing properties of sleep depend on the oscillatory amplitude of norepinephrine
Kjaerby, C., Andersen, M., Hauglund, N., Untiet, V., Dall, C., Sigurdsson, B., Ding, F., Feng, J., Li, Y., Weikop, P., et al. (2022) · Nature Neuroscience · doi:10.1038/s41593-022-01102-9 · Cited by 306 · see citing works
Dopamine transporters govern diurnal variation in extracellular dopamine tone
Ferris, M. J., España, R. A., Locke, J. L., Konstantopoulos, J. K., Rose, J. H., Chen, R., & Jones, S. R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1407935111 · Cited by 192 · see citing works
Intrinsic organization of the anesthetized brain
Liang, Z., King, J., & Zhang, N. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.1020-12.2012 · Cited by 168 · see citing works
Extended wakefulness: compromised metabolics in and degeneration of locus ceruleus neurons
Zhang, J., Zhu, Y., Zhan, G., Fenik, P., Panossian, L., Wang, M. M., Reid, S., Lai, D., Davis, J. G., Baur, J. A., et al. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.5025-12.2014 · Cited by 171 · see citing works
Paradoxical somatodendritic decoupling supports cortical plasticity during REM sleep
Aime, M., Calcini, N., Borsa, M., Campelo, T., Rusterholz, T., Sattin, A., Fellin, T., & Adamantidis, A. (2022) · Science · doi:10.1126/science.abk2734 · Cited by 106 · see citing works
Disrupted sleep and circadian rhythms in schizophrenia and their interaction with dopamine signaling
Ashton, A., & Jagannath, A. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00636 · Cited by 106 · see citing works
Sleep Disturbances in Alzheimer’s and Parkinson’s Diseases
Rothman, S. M., & Mattson, M. P. (2012) · NeuroMolecular Medicine · doi:10.1007/s12017-012-8181-2 · Cited by 102 · see citing works
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Perogamvros, L., Dang-Vu, T. T., Desseilles, M., & Schwartz, S. (2013) · Frontiers in Psychology · doi:10.3389/fpsyg.2013.00474 · Cited by 77 · see citing works
“Therefore, it seems that emotional, salience and stress networks, subserved by the fear expression (amygdala, ACC), mesolimbic (VTA, NAcc, vmPFC) and extrahypothalamic (extended amygdala) systems respectively, may collaborate or be in opposition during dreaming, according to the emotion/behavior/cognition characterizi…”
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Menon, J. M. L., Nolten, C., Achterberg, E. J. M., Joosten, R. N. J. M. A., Dematteis, M., Feenstra, M. G. P., Drinkenburg, W. H. (., & Leenaars, C. H. C. (2019) · Journal of Circadian Rhythms · doi:10.5334/jcr.174 · Cited by 57 · see citing works
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Macedo, A. C., Balouch, S., & Tabet, N. (2017) · Journal of Alzheimer’s Disease · doi:10.3233/jad-161287 · Cited by 49 · see citing works
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De Gennaro, L., Lanteri, O., Piras, F., Scarpelli, S., Assogna, F., Ferrara, M., Caltagirone, C., & Spalletta, G. (2016) · Human Brain Mapping · doi:10.1002/hbm.23095 · Cited by 45 · see citing works
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LALOUX, C., DERAMBURE, P., HOUDAYER, E., JACQUESSON, J., BORDET, R., DESTÉE, A., & MONACA, C. (2008) · Journal of Sleep Research · doi:10.1111/j.1365-2869.2008.00625.x · Cited by 40 · see citing works
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Solms, M. (2011) · Handbook of Clinical Neurology · doi:10.1016/b978-0-444-52006-7.00034-4 · Cited by 36 · see citing works
Orzeł-Gryglewska, J., Matulewicz, P., & Jurkowlaniec, E. (2015) · Synapse · doi:10.1002/syn.21843 · Cited by 31 · see citing works
Pace-Schott, E. F. (2011) · Principles and Practice of Sleep Medicine · doi:10.1016/b978-1-4160-6645-3.00048-7 · Cited by 19 · see citing works
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Gottesmann, C. (2010) · International review of neurobiology · doi:10.1016/s0074-7742(10)92012-6 · Cited by 5 · see citing works
Self-citation
- Authors
- Léna, I., Parrot, S., Deschaux, O., Muffat‐Joly, S., Sauvinet, V., Renaud, B., Suaud‐Chagny, M. ‐., & Gottesmann, C.
- Affiliations
- Université Nice Sophia Antipolis (FR)
- Inserm (FR)
- Corresponding author
- Léna, I.
- Venue
- Journal of Neuroscience Research
- Publisher
- Wiley
- Published
- 2005-07-22
- Volume
- 81
- Issue
- 6
- Pages
- 891-899
- ISSN
- 0360-4012 (ISSN-L)
- 1097-4547
- OpenAlex
- W2062883133
- Cited by
- 322
- References
- 45
- Citations by year
- 2026: 7 · 2025: 9 · 2024: 10 · 2023: 16 · 2022: 14 · 2021: 19 · 2020: 19 · 2019: 18 · 2018: 18 · 2017: 18 · 2016: 25 · 2015: 13 · 2014: 14 · 2013: 19 · 2012: 16
- FWCI
- 7.41
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neuroscience Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- sleep-wake cycle, dopamine, norepinephrine, glutamate, aspartic acid, medial prefrontal cortex, nucleus accumbens, REM sleep, slow-wave sleep, neurotransmitter release, freely moving rats, microdialysis, capillary electrophoresis, dopaminergic terminals
- MeSH terms
- Animals, Aspartic Acid, Dopamine, Electrophysiology, Extracellular Space, Male, Norepinephrine, Nucleus Accumbens, Sleep, Sleep, REM, Wakefulness, Rats, Wistar, Polysomnography, Prefrontal Cortex, Microdialysis, Glutamic Acid, Electrophoresis, Capillary, Rats
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