DOI: 10.1523/jneurosci.3502-04.2004. Prefrontal Cortex Stimulation Induces 2-Arachidonoyl-Glycerol-Mediated Suppression of Excitation in Dopamine Neurons

Prefrontal Cortex Stimulation Induces 2-Arachidonoyl-Glycerol-Mediated Suppression of Excitation in Dopamine Neurons

10.1523/jneurosci.3502-04.2004

Crossref journal-article

Society for Neuroscience

The Journal of Neuroscience (393)

Abstract

Endocannabinoids form a novel class of retrograde messengers that modulate short- and long-term synaptic plasticity. Depolarization-induced suppression of excitation (DSE) and inhibition (DSI) are the best characterized transient forms of endocannabinoid-mediated synaptic modulation. Stimulation protocols consisting of long-lasting voltage steps to the postsynaptic cell are routinely used to evoke DSE-DSI. Little is known, however, about more physiological conditions under which these molecules are releasedin vitro. Moreover, the occurrencein vivoof such forms of endocannabinoid-mediated modulation is still controversial. Here we show that physiologically relevant patterns of synaptic activity induce a transient suppression of excitatory transmission onto dopamine neuronsin vitro. Accordingly,in vivoendocannabinoids depress the increase in firing and bursting activity evoked in dopamine neurons by prefrontal cortex stimulation. This phenomenon is selectively mediated by the endocannabinoid 2-arachidonoyl-glycerol (2-AG), which activates presynaptic cannabinoid type 1 receptors. 2-AG synthesis involves activation of metabotropic glutamate receptors and Ca2+mobilization from intracellular stores. These findings indicate that dopamine neurons release 2-AG to shape afferent activity and ultimately their own firing pattern. This novel endocannabinoid-mediated self-regulatory role of dopamine neurons may bear relevance in the pathogenesis of neuropsychiatric disorders such as schizophrenia and addiction.

Bibliography

Melis, M., Perra, S., Muntoni, A. L., Pillolla, G., Lutz, B., Marsicano, G., Di Marzo, V., Gessa, G. L., & Pistis, M. (2004). Prefrontal Cortex Stimulation Induces 2-Arachidonoyl-Glycerol-Mediated Suppression of Excitation in Dopamine Neurons. The Journal of Neuroscience, 24(47), 10707â10715.

Authors 9

Miriam Melis (first)
Simona Perra (additional)
Anna Lisa Muntoni (additional)
Giuliano Pillolla (additional)
Beat Lutz (additional)
Giovanni Marsicano (additional)
Vincenzo Di Marzo (additional)
Gian Luigi Gessa (additional)
Marco Pistis (additional)

References 82 Referenced 202

10.1016/S0301-0082(02)00080-1
10.1007/s002109900200
10.1016/S0028-3908(97)00014-2
10.1126/science.277.5329.1094
10.1046/j.1471-4159.1999.0722113.x
10.1006/bbrc.1999.0254
10.1046/j.1432-1327.2001.02072.x / Eur J Biochem (2001)
10.1083/jcb.200305129
10.1038/nn1126
10.1038/28393
10.1016/S0896-6273(03)00235-6
10.1016/0006-8993(85)90140-4
10.1038/sj.bjp.0705726
10.1038/372686a0
10.1016/S0166-2236(98)01283-1
10.1046/j.1471-4159.2000.0752434.x
10.1038/sj.npp.1300496
10.1038/27919
10.1152/jn.00351.2004
10.1016/S0014-2999(03)01295-0
10.1523/JNEUROSCI.0403-04.2004
10.1016/0006-8993(88)90606-3
10.1016/0306-4522(88)90307-7
10.1016/0306-4522(91)90196-U
10.1016/0306-4522(83)90135-5
10.1523/JNEUROSCI.04-11-02877.1984 / J Neurosci (1984)
10.1523/JNEUROSCI.09-10-03463.1989 / J Neurosci (1989)
10.1152/jn.1999.82.4.1974 / J Neurophysiol (1999)
10.1016/0006-8993(78)90654-6
10.1016/S0028-3908(02)00157-0
10.1016/S0009-3084(02)00149-4
10.1016/S0306-4522(01)00287-1
10.1111/j.1460-9568.2004.03293.x
10.1152/jn.01161.2002
10.1016/0006-8993(95)01406-3
10.1046/j.1471-4159.2001.00499.x
10.1073/pnas.96.24.14136
10.1016/S0079-6123(00)26028-7
10.1113/jphysiol.1992.sp019136 / J Physiol (Lond) (1992)
10.1016/0165-0173(93)90008-N
10.1016/S0306-4522(97)00654-4
10.1054/plef.2001.0351
{'key': '2023041303095425000_24.47.10707.43', 'first-page': '453', 'volume': '55', 'year': '1999', 'journal-title': 'Mol Pharmacol'} / Mol Pharmacol (1999)
10.1054/plef.2001.0342
10.1016/S0896-6273(01)00375-0
Marinelli S, Mercuri NB (2004) Cannabinoid and vanilloid receptors are activated by N-arachidonyl-dopamine in rat midbrain dopaminergic neurons. Paper presented at International Cannabinoid Research Society, 2004 Symposium on the Cannabinoids, Burlington, VT, June.
10.1038/nature00839
10.1038/346561a0
10.1016/0006-2952(95)00109-D
10.1523/JNEUROSCI.4503-03.2004
10.1523/JNEUROSCI.20-20-j0003.2000 / J Neurosci (2000)
10.1523/JNEUROSCI.23-01-00149.2003 / J Neurosci (2003)
10.1016/0304-3940(93)90641-W
10.1046/j.1460-9568.2002.01929.x
10.1016/S0006-2952(03)00109-6
10.1016/S0165-0173(97)00039-8
Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates. San Diego: Academic.
10.1073/pnas.96.10.5802
{'key': '2023041303095425000_24.47.10707.59', 'first-page': '707', 'volume': '76', 'year': '1997', 'journal-title': 'Neuroscience'} / Neuroscience (1997)
10.1073/pnas.122149199
10.1097/00001756-200108080-00051
10.1523/JNEUROSCI.5214-03.2004
10.1038/sj.bjp.0704297
10.1016/S0028-3908(99)00092-1
10.1152/jn.1998.80.1.1 / J Neurophysiol (1998)
10.1016/S0896-6273(02)00967-4
10.1111/j.1460-9568.1997.tb01352.x
10.1016/0091-3057(91)90382-C
10.1038/42015
10.1006/bbrc.1995.2437
10.1074/jbc.274.5.2794
10.1111/j.1748-1716.1989.tb08640.x
10.1523/JNEUROSCI.14-05-03005.1994 / J Neurosci (1994)
10.1002/(SICI)1098-2396(199603)22:3<195::AID-SYN1>3.0.CO;2-7
10.1007/BF01291780
10.1523/JNEUROSCI.21-24-j0003.2001 / J Neurosci (2001)
10.1073/pnas.96.21.12198
10.1146/annurev.ne.19.030196.002201
10.1046/j.1471-4159.2002.01005.x
10.1016/S0959-4388(96)80079-1
10.1073/pnas.0306707101
{'key': '2023041303095425000_24.47.10707.82', 'first-page': '313', 'volume': '269', 'year': '1994', 'journal-title': 'J Pharmacol Exp Ther'} / J Pharmacol Exp Ther (1994)

Dates

Type	When
Created	20 years, 9 months ago (Nov. 24, 2004, 6:03 p.m.)
Deposited	2 years, 4 months ago (April 13, 2023, 12:27 p.m.)
Indexed	1 week, 2 days ago (Aug. 27, 2025, 12:31 p.m.)
Issued	20 years, 9 months ago (Nov. 24, 2004)
Published	20 years, 9 months ago (Nov. 24, 2004)
Published Online	20 years, 9 months ago (Nov. 24, 2004)
Published Print	20 years, 9 months ago (Nov. 24, 2004)

Funders 0

None

BibTeX

@article{Melis_2004, title={Prefrontal Cortex Stimulation Induces 2-Arachidonoyl-Glycerol-Mediated Suppression of Excitation in Dopamine Neurons}, volume={24}, ISSN={1529-2401}, url={http://dx.doi.org/10.1523/jneurosci.3502-04.2004}, DOI={10.1523/jneurosci.3502-04.2004}, number={47}, journal={The Journal of Neuroscience}, publisher={Society for Neuroscience}, author={Melis, Miriam and Perra, Simona and Muntoni, Anna Lisa and Pillolla, Giuliano and Lutz, Beat and Marsicano, Giovanni and Di Marzo, Vincenzo and Gessa, Gian Luigi and Pistis, Marco}, year={2004}, month=nov, pages={10707–10715} }

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