Andino-Pavlovsky, V.; Souza, A.C.; Scheffer-Teixeira, R.; Tort, A.B.L.; Etchenique, R.; Ribeiro, S. "Dopamine modulates delta-gamma phase-amplitude coupling in the prefrontal cortex of behaving rats" (2017) Frontiers in Neural Circuits. 11
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Dopamine release and phase-amplitude cross-frequency coupling (CFC) have independently been implicated in prefrontal cortex (PFC) functioning. To causally investigate whether dopamine release affects phase-amplitude comodulation between different frequencies in local field potentials (LFP) recorded from the medial PFC (mPFC) of behaving rats, we used RuBiDopa, a light-sensitive caged compound that releases the neurotransmitter dopamine when irradiated with visible light. LFP power did not change in any frequency band after the application of light-uncaged dopamine, but significantly strengthened phase-amplitude comodulation between delta and gamma oscillations. Saline did not exert significant changes, while injections of dopamine and RuBiDopa produced a slow increase in comodulation for several minutes after the injection. The results show that dopamine release in the medial PFC shifts phase-amplitude comodulation from theta-gamma to delta-gamma. Although being preliminary results due to the limitation of the low number of animals present in this study, our findings suggest that dopamine-mediated modification of the frequencies involved in comodulation could be a mechanism by which this neurotransmitter regulates functioning in mPFC. © 2017 Andino-Pavlovsky, Souza, Scheffer-Teixeira, Tort, Etchenique and Ribeiro.


Documento: Artículo
Título:Dopamine modulates delta-gamma phase-amplitude coupling in the prefrontal cortex of behaving rats
Autor:Andino-Pavlovsky, V.; Souza, A.C.; Scheffer-Teixeira, R.; Tort, A.B.L.; Etchenique, R.; Ribeiro, S.
Filiación:Departamento de Química Inorganica, Analítica y Química Física, Instituto de Química Física de los Materiales, Medio Ambiente y Energía (INQUIMAE), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires, Argentina
Instituto do Cérebro, Federal University of Rio Grande do Norte, Natal, Brazil
Palabras clave:Comodulation; Delta-gamma coupling; Dopamine; LFP oscillation; Uncaging; dopamine; rubidopa; unclassified drug; 2,2' bipyridine; dichlorobis(2,2'-bipyridine)ruthenium; dopamine; organometallic compound; action potential amplitude; amplitude modulation; animal behavior; animal experiment; animal tissue; Article; brain function; controlled study; delta oscillation; dopamine release; electric potential; gamma oscillation; light irradiance; local field potential; male; medial prefrontal cortex; nonhuman; oscillation; rat; analogs and derivatives; animal; delta rhythm; drug effects; electroencephalography; gamma rhythm; metabolism; photostimulation; physiology; prefrontal cortex; procedures; REM sleep; spectroscopy; time factor; ultraviolet radiation; wakefulness; Wistar rat; 2,2'-Dipyridyl; Animals; Delta Rhythm; Dopamine; Electroencephalography; Gamma Rhythm; Male; Organometallic Compounds; Photic Stimulation; Prefrontal Cortex; Rats; Rats, Wistar; Sleep, REM; Spectrum Analysis; Time Factors; Ultraviolet Rays; Wakefulness
Título revista:Frontiers in Neural Circuits
Título revista abreviado:Front. Neural Circuits
CAS:dopamine, 51-61-6, 62-31-7; 2,2' bipyridine, 366-18-7; 2,2'-Dipyridyl; dichlorobis(2,2'-bipyridine)ruthenium; Dopamine; Organometallic Compounds


  • Araya, R., Andino-Pavlovsky, V., Yuste, R., Etchenique, R., Two-photon optical interrogation of individual dendritic spines with caged dopamine (2013) ACS Chem. Neurosci., 4, pp. 1163-1167
  • Axmacher, N., Henseler, M.M., Jensen, O., Weinreich, I., Elger, C.E., Fell, J., Cross-frequency coupling supports multi-item working memory in the human hippocampus (2010) Proc. Natl. Acad. Sci. U.S.A., 107, pp. 3228-3233
  • Bartos, M., Vida, I., Jonas, P., Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks (2007) Nat. Rev. Neurosci., 8, pp. 45-56
  • Benchenane, K., Peyrache, A., Khamassi, M., Tierney, P.L., Gioanni, Y., Battaglia, F.P., Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning (2010) Neuron, 66, pp. 921-936
  • Björklund, A., Dunnett, S.B., Dopamine neuron systems in the brain: An update (2007) Trends Neurosci, 30, pp. 194-202
  • Buzsaki, G., (2006) Rhythms of the Brain, , Oxford, UK: Oxford University Press
  • Buzsáki, G., Draguhn, A., Neuronal oscillations in cortical networks (2004) Science, 304, pp. 1926-1929
  • Canolty, R.T., Edwards, E., Dalal, S.S., Soltani, M., Nagarajan, S.S., Kirsch, H.E., High gamma power is phase-locked to theta oscillations in human neocortex (2006) Science, 313, pp. 1626-1628
  • Canolty, R.T., Knight, R.T., The functional role of cross-frequency coupling (2010) Trends Cogn. Sci., 14, pp. 506-515
  • Carr, D.B., Sesack, S.R., Hippocampal afferents to the rat prefrontal cortex: Synaptic targets and relation to dopamine terminals (1996) J. Comp. Neurol, 369, pp. 1-15
  • Chudasama, Y., Robbins, T.W., Dopaminergic modulation of visual attention and working memory in the rosent prefrontal cortex (2004) Neuropsychopharmacology, 29, pp. 1628-1636
  • Colgin, L.L., Moser, E.I., Gamma oscillations in the hippocampus (2010) Physiology, 25, pp. 319-329
  • Cragg, S.J., Rice, M.E., DAncing past the DAT at a DAsynapse (2004) Trends Neurosci, 27, pp. 270-277
  • Delorme, A., Makeig, S., EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis (2004) J. Neurosci. Methods, 134, pp. 9-21
  • Dzirasa, K., Ramsey, A.J., Takahashi, D.Y., Stapleton, J., Potes, J.M., Williams, J.K., Hyperdopaminergia and NMDA receptor hypofunction disrupt neural phase signaling (2009) J. Neurosci., 29, pp. 8215-8224
  • Ferreira, C.S., Marful, A., Staudigl, T., Bajo, T., Hanslmayr, S., Medial prefrontal theta oscillations track the time course of interference during selective memory retrieval (2014) J. Cogn. Neurosci., 26, pp. 777-791
  • Filevich, O., Salierno, M., Etchenique, R., A caged nicotine with nanosecond range kinetics and visible light sensitivity (2010) J. Inorg. Biochem., 104, pp. 1248-1251
  • Furth, K.E., Mastwal, S., Wang, K.H., Buonanno, A., Vullhorst, D., Dopamine, cognitive function, and gamma oscillations: Role of D4 receptors (2013) Front. Cell. Neurosci., 7, p. 102
  • Goto, Y., Otani, S., Grace, A.A., The Yin and Yang of dopamine release: A new perspective (2007) Neuropharmacology, 53, pp. 583-587
  • Gurden, H., Tassin, J.P., Jay, T.M., Integrity of the mesocortical dopaminergic system is necessary for complete expression of in vivo hippocampal–prefrontal cortex long-term potentiation (1999) Neuroscience, 94, pp. 1019-1027
  • Hasselmo, M.E., Bodelón, C., Wyble, B.P., A proposed function for hippocampal theta rhythm: Separate phases of encoding and retrieval enhance reversal of prior learning (2002) Neural Comput, 14, pp. 793-817
  • Hobson, J.A., Pace-Schott, E.F., The cognitive neuroscience of sleep: Neuronal systems, consciousness and learning (2002) Nat. Rev. Neurosci., 3, pp. 679-693
  • Jay, T.M., Burette, F., Laroche, S., Plasticity of the hippocampal-prefrontal cortex synapses (1996) J. Physiol. Paris, 90, pp. 361-366
  • Jay, T.M., Rocher, C., Hotte, M., Naudon, L., Gurden, H., Spedding, M., Plasticity at hippocampal to prefrontal cortex synapses is impaired by loss of dopamine and stress: Importance for psychiatric diseases (2004) Neurotox. Res., 6, pp. 233-244
  • Jones, M.W., Wilson, M.A., Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task (2005) Plos Biol, 3
  • Kaplan, R., Bush, D., Bonnefond, M., Bandettini, P.A., Barnes, G.R., Doeller, C.F., Medial prefrontal theta phase coupling during spatial memory retrieval (2014) Hippocampus, 24, pp. 656-665
  • Lisman, J.E., Jensen, O., The theta-gamma neural code (2013) Neuron, 77, pp. 1002-1016
  • Lopes-Dos-santos, V., Campi, J., Filevich, O., Ribeiro, S., Etchenique, R., In vivo photorelease of GABA in the mouse cortex (2011) Braz. J. Med. Biol. Res., 44, pp. 688-693
  • Louie, K., Wilson, M.A., Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep (2001) Neuron, 29, pp. 145-156
  • McBain, C.J., Fisahn, A., Interneurons unbound (2001) Nat. Rev. Neurosci., 2, pp. 11-23
  • Navailles, S., Guillem, K., Vouillac-Mendoza, C., Ahmed, S.H., Coordinated recruitment of cortical–subcortical circuits and ascending dopamine and serotonin neurons during inhibitory control of cocaine seeking in rats (2014) Cereb. Cortex, 25, pp. 3167-3181
  • Neve, K.A., Neve, R.L., Molecular biology of dopamine receptors (1997) The Dopamine Receptors, pp. 27-76. , K. A. Neve (Portland, OR: Springer)
  • Nyhus, E., Curran, T., Functional role of gamma and theta oscillations in episodic memory (2010) Neurosci. Biobehav. Rev., 34, pp. 1023-1035
  • O’Keefe, J., Place units in the hippocampus of the freely moving rat (1976) Exp. Neurol., 51, pp. 78-109
  • O’Neill, P.K., Gordon, J.A., Sigurdsson, T., Theta oscillations in the medial prefrontal cortex are modulated by spatial working memory and synchronize with the hippocampus through its ventral subregion (2013) J. Neurosci., 33, pp. 14211-14224
  • Onslow, A.C., Bogacz, R., Jones, M.W., Quantifying phase–amplitude coupling in neuronal network oscillations (2011) Prog. Biophys. Mol. Biol., 105, pp. 49-57
  • Pavlides, C., Winson, J., Influences of hippocampal place cell firing in the awake state on the activity of these cells during subsequent sleep episodes (1989) J. Neurosci., 9, pp. 2907-2918
  • Peters, Y., Barnhardt, N.E., O’Donnell, P., Prefrontal cortical up states are synchronized with ventral tegmental area activity (2004) Synapse, 52, pp. 143-152
  • Puig, M.V., Rose, J., Schmidt, R., Freund, N., Dopamine modulation of learning and memory in the prefrontal cortex: Insights from studies in primates, rodents, and birds (2014) Front. Neural Circuits, 8, p. 93
  • Rial Verde, E.M., Zayat, L., Etchenique, R., Yuste, R., Photorelease of GABA with visible light using an inorganic caging group (2008) Front. Neural Circuits, 2, p. 2
  • Richfield, E., Penney, J., Young, A., Anatomical and affinity state comparisons between dopamine D 1 and D 2 receptors in the rat central nervous system (1989) Neuroscience, 30, pp. 767-777
  • Rosen, Z.B., Cheung, S., Siegelbaum, S.A., Midbrain dopamine neurons bidirectionally regulate CA3-CA1 synaptic drive (2015) Nat. Neurosci., 18, pp. 1763-1771
  • Rubinstein, M., Cepeda, C., Hurst, R.S., Flores-Hernandez, J., Ariano, M.A., Falzone, T.L., Dopamine D4 receptor-deficient mice display cortical hyperexcitability (2001) J. Neurosci, 21, pp. 3756-3763
  • Salierno, M., Marceca, E., Peterka, D.S., Yuste, R., Etchenique, R., A fast ruthenium polypyridine cage complex photoreleases glutamate with visible or IR light in one and two photon regimes (2010) J. Inorg. Biochem., 104, pp. 418-422
  • Scheffer-Teixeira, R., Belchior, H., Caixeta, F.V., Souza, B.C., Ribeiro, S., Tort, A.B., Theta phase modulates multiple layer-specific oscillations in the CA1 region (2012) Cereb. Cortex, 22, pp. 2404-2414
  • Scheffzük, C., Kukushka, V.I., Vyssotski, A.L., Draguhn, A., Tort, A.B., Brankačk, J., Selective coupling between theta phase and neocortical fast gamma oscillations during REM-sleep in mice (2011) Plos ONE, 6
  • Schomburg, E.W., Fernández-Ruiz, A., Mizuseki, K., Berényi, A., Anastassiou, C.A., Koch, C., Theta phase segregation of input-specific gamma patterns in entorhinal-hippocampal networks (2014) Neuron, 84, pp. 470-485
  • Schweimer, J., Hauber, W., Dopamine D1 receptors in the anterior cingulate cortex regulate effort-based decision making (2006) Learn. Mem., 13, pp. 777-782
  • Seamans, J.K., Yang, C.R., The principal features and mechanisms of dopamine modulation in the prefrontal cortex (2004) Prog. Neurobiol, 74, pp. 1-58
  • Siapas, A.G., Wilson, M.A., Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep (1998) Neuron, 21, pp. 1123-1128
  • Sigurdsson, T., Stark, K.L., Karayiorgou, M., Gogos, J.A., Gordon, J.A., Impaired hippocampal–prefrontal synchrony in a genetic mouse model of schizophrenia (2010) Nature, 464, pp. 763-767
  • Tort, A.B., Komorowski, R.W., Manns, J.R., Kopell, N.J., Eichenbaum, H., Theta–gamma coupling increases during the learning of item– context associations (2009) Proc. Natl. Acad. Sci. U.S.A., 106, pp. 20942-20947
  • Tort, A.B., Kramer, M.A., Thorn, C., Gibson, D.J., Kubota, Y., Graybiel, A.M., Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task (2008) Proc. Natl. Acad. Sci. U.S.A., 105, pp. 20517-20522
  • Tort, A.B., Komorowski, R., Eichenbaum, H., Kopell, N., Measuring phase-amplitude coupling between neuronal oscillations of different frequencies (2010) J. Neurophysiol., 104, pp. 1195-1210
  • Tseng, K.Y., O’Donnell, P., Dopamine–glutamate interactions controlling prefrontal cortical pyramidal cell excitability involve multiple signaling mechanisms (2004) J. Neurosci, 24, pp. 5131-5139
  • Tye, K.M., Deisseroth, K., Optogenetic investigation of neural circuits underlying brain disease in animal models (2012) Nat. Rev. Neurosci., 13, pp. 251-266
  • Whishaw, I., Vanderwolf, C.H., Hippocampal EEG and behavior: Change in amplitude and frequency of RSA (theta rhythm) associated with spontaneous and learned movement patterns in rats and cats (1973) Behav. Biol., 8, pp. 461-484
  • Wierzynski, C.M., Lubenov, E.V., Gu, M., Siapas, A.G., State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep (2009) Neuron, 61, pp. 587-596
  • Winson, J., Patterns of hippocampal theta rhythm in the freely moving rat (1974) Electroencephalogr. Clin. Neurophysiol., 36, pp. 291-301
  • Xu, X., Zheng, C., An, L., Wang, R., Zhang, T., Effects of dopamine and serotonin systems on modulating neural oscillations in hippocampus-prefrontal cortex pathway in rats (2016) Brain Topogr, 29, pp. 539-551
  • Zhang, K., Guo, J.Z., Peng, Y., Xi, W., Guo, A., Dopamine-mushroom body circuit regulates saliency-based decision-making in Drosophila (2007) Science, 316, pp. 1901-1904
  • Zhang, X., Zhong, W., Brankačk, J., Weyer, S.W., Müller, U.C., Tort, A.B., Impaired theta-gamma coupling in APP-deficient mice (2016) Sci. Rep., 6, p. 21948
  • Zhong, P., Yan, Z., Distinct physiological effects of dopamine D4 receptors on prefrontal cortical pyramidal neurons and fast-spiking interneurons (2016) Cereb. Cortex, 26, pp. 180-191


---------- APA ----------
Andino-Pavlovsky, V., Souza, A.C., Scheffer-Teixeira, R., Tort, A.B.L., Etchenique, R. & Ribeiro, S. (2017) . Dopamine modulates delta-gamma phase-amplitude coupling in the prefrontal cortex of behaving rats. Frontiers in Neural Circuits, 11.
---------- CHICAGO ----------
Andino-Pavlovsky, V., Souza, A.C., Scheffer-Teixeira, R., Tort, A.B.L., Etchenique, R., Ribeiro, S. "Dopamine modulates delta-gamma phase-amplitude coupling in the prefrontal cortex of behaving rats" . Frontiers in Neural Circuits 11 (2017).
---------- MLA ----------
Andino-Pavlovsky, V., Souza, A.C., Scheffer-Teixeira, R., Tort, A.B.L., Etchenique, R., Ribeiro, S. "Dopamine modulates delta-gamma phase-amplitude coupling in the prefrontal cortex of behaving rats" . Frontiers in Neural Circuits, vol. 11, 2017.
---------- VANCOUVER ----------
Andino-Pavlovsky, V., Souza, A.C., Scheffer-Teixeira, R., Tort, A.B.L., Etchenique, R., Ribeiro, S. Dopamine modulates delta-gamma phase-amplitude coupling in the prefrontal cortex of behaving rats. Front. Neural Circuits. 2017;11.