Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.
Fast Synaptic Subcortical Control of Hippocampal Circuits
Viktor Varga,1,*,
Attila Losonczy,2,*,,
Boris V. Zemelman,2,*
Zsolt Borhegyi,1
Gábor Nyiri,1
Andor Domonkos,1
Balázs Hangya,1
Noémi Holderith,1
Jeffrey C. Magee,2
Tamás F. Freund1
Abstract:
Cortical information processing is under state-dependent controlof subcortical neuromodulatory systems. Although this modulatoryeffect is thought to be mediated mainly by slow nonsynapticmetabotropic receptors, other mechanisms, such as direct synaptictransmission, are possible. Yet, it is currently unknown ifany such form of subcortical control exists. Here, we presentdirect evidence of a strong, spatiotemporally precise excitatoryinput from an ascending neuromodulatory center. Selective stimulationof serotonergic median raphe neurons produced a rapid activationof hippocampal interneurons. At the network level, this subcorticaldrive was manifested as a pattern of effective disynaptic GABAergicinhibition that spread throughout the circuit. This form ofsubcortical network regulation should be incorporated into currentconcepts of normal and pathological cortical function.
1 Institute of Experimental Medicine, Budapest 1083, Hungary. 2 Howard Hughes Medical Institute, Janelia Farm Research Campus, Ashburn, VA 20147, USA.
* These authors contributed equally to this work.
Present address: Department of Neuroscience, Columbia University,New York, NY 10032, USA.
To whom correspondence should be addressed. E-mail: vargav{at}koki.hu (V.V.), losonczya{at}janelia.hhmi.org (A.L.)
The editors suggest the following Related Resources on Science sites:
In Science Signaling
EDITORS' CHOICE
Peter Stern (20 October 2009) Sci. Signal.2 (93), ec342.
[DOI: 10.1126/scisignal.293ec342] |Abstract »
THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
The Synchronous Activity of Lateral Habenular Neurons Is Essential for Regulating Hippocampal Theta Oscillation.
H. Aizawa, S. Yanagihara, M. Kobayashi, K. Niisato, T. Takekawa, R. Harukuni, T. J. McHugh, T. Fukai, Y. Isomura, and H. Okamoto (2013)
J. Neurosci.
33, 8909-8921
|Abstract »|Full Text »|PDF »
Mechanisms Generating Dual-Component Nicotinic EPSCs in Cortical Interneurons.
C. Bennett, S. Arroyo, D. Berns, and S. Hestrin (2012)
J. Neurosci.
32, 17287-17296
|Abstract »|Full Text »|PDF »
Direct Alteration of a Specific Inhibitory Circuit of the Hippocampus by Antidepressants.
P. Mendez, A. Pazienti, G. Szabo, and A. Bacci (2012)
J. Neurosci.
32, 16616-16628
|Abstract »|Full Text »|PDF »
The vesicular glutamate transporter VGLUT3 contributes to protection against neonatal hypoxic stress.
S. Miot, N. Voituron, A. Sterlin, E. Vigneault, L. Morel, B. Matrot, N. Ramanantsoa, B. Amilhon, O. Poirel, E. Lepicard, et al. (2012)
J. Physiol.
590, 5183-5198
|Abstract »|Full Text »|PDF »
Targeting brain serotonin synthesis: insights into neurodevelopmental disorders with long-term outcomes related to negative emotionality, aggression and antisocial behaviour.
K.-P. Lesch, N. Araragi, J. Waider, D. van den Hove, and L. Gutknecht (2012)
Phil Trans R Soc B
367, 2426-2443
|Abstract »|Full Text »|PDF »
Development of GABAergic inputs controls the contribution of maturing neurons to the adult hippocampal network.
Y. Li, J. B. Aimone, X. Xu, E. M. Callaway, and F. H. Gage (2012)
PNAS
109, 4290-4295
|Abstract »|Full Text »|PDF »
Sticking out of the crowd: the molecular identity and development of cholecystokinin-containing basket cells.
E. Keimpema, A. Straiker, K. Mackie, T. Harkany, and J. Hjerling-Leffler (2012)
J. Physiol.
590, 703-714
|Abstract »|Full Text »|PDF »
Vesicular and Plasma Membrane Transporters for Neurotransmitters.
R. D. Blakely and R. H. Edwards (2012)
Cold Spring Harb Perspect Biol
4, a005595
|Abstract »|Full Text »|PDF »
Co-transmission of dopamine and glutamate.
J. I. Broussard (2011)
J. Gen. Physiol.
139, 93-96
|Full Text »|PDF »
Terminal Field and Firing Selectivity of Cholecystokinin-Expressing Interneurons in the Hippocampal CA3 Area.
B. Lasztoczi, J. J. Tukker, P. Somogyi, and T. Klausberger (2011)
J. Neurosci.
31, 18073-18093
|Abstract »|Full Text »|PDF »
Cell-Type-Specific Modulation of Feedback Inhibition by Serotonin in the Hippocampus.
J. Winterer, A. V. Stempel, T. Dugladze, C. Foldy, N. Maziashvili, A. R. Zivkovic, J. Priller, I. Soltesz, T. Gloveli, and D. Schmitz (2011)
J. Neurosci.
31, 8464-8475
|Abstract »|Full Text »|PDF »
Modulation of hippocampal stratum lacunosum-moleculare microcircuits.
A Genetically Defined Morphologically and Functionally Unique Subset of 5-HT Neurons in the Mouse Raphe Nuclei.
V. Kiyasova, S. P. Fernandez, J. Laine, L. Stankovski, A. Muzerelle, S. Doly, and P. Gaspar (2011)
J. Neurosci.
31, 2756-2768
|Abstract »|Full Text »|PDF »
Channelrhodopsin as a tool to investigate synaptic transmission and plasticity.
P. Schoenenberger, Y.-P. Z. Scharer, and T. G. Oertner (2011)
Exp Physiol
96, 34-39
|Abstract »|Full Text »|PDF »
The Largest Group of Superficial Neocortical GABAergic Interneurons Expresses Ionotropic Serotonin Receptors.
S. Lee, J. Hjerling-Leffler, E. Zagha, G. Fishell, and B. Rudy (2010)
J. Neurosci.
30, 16796-16808
|Abstract »|Full Text »|PDF »
Two-photon single-cell optogenetic control of neuronal activity by sculpted light.
B. K. Andrasfalvy, B. V. Zemelman, J. Tang, and A. Vaziri (2010)
PNAS
107, 11981-11986
|Abstract »|Full Text »|PDF »