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PMID: 19396159 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Parvalbumin neurons and gamma rhythms enhance cortical circuit performance.

Nature ·Vol. 459 ·No. 7247 ·2009-06-04 ·Pages 698-702

Sohal VS, Zhang F, Yizhar O, Deisseroth K

Abstract

Synchronized oscillations and inhibitory interneurons have important and interconnected roles within cortical microcircuits. In particular, interneurons defined by the fast-spiking phenotype and expression of the calcium-binding protein parvalbumin have been suggested to be involved in gamma (30-80 Hz) oscillations, which are hypothesized to enhance information processing. However, because parvalbumin interneurons cannot be selectively controlled, definitive tests of their functional significance in gamma oscillations, and quantitative assessment of the impact of parvalbumin interneurons and gamma oscillations on cortical circuits, have been lacking despite potentially enormous significance (for example, abnormalities in parvalbumin interneurons may underlie altered gamma-frequency synchronization and cognition in schizophrenia and autism). Here we use a panel of optogenetic technologies in mice to selectively modulate multiple distinct circuit elements in neocortex, alone or in combination. We find that inhibiting parvalbumin interneurons suppresses gamma oscillations in vivo, whereas driving these interneurons (even by means of non-rhythmic principal cell activity) is sufficient to generate emergent gamma-frequency rhythmicity. Moreover, gamma-frequency modulation of excitatory input in turn was found to enhance signal transmission in neocortex by reducing circuit noise and amplifying circuit signals, including inputs to parvalbumin interneurons. As demonstrated here, optogenetics opens the door to a new kind of informational analysis of brain function, permitting quantitative delineation of the functional significance of individual elements in the emergent operation and function of intact neural circuitry.

MeSH Terms
Animals Cell Line Cerebral Cortex/physiology Cortical Synchronization Electrophysiology Evoked Potentials Interneurons/cytology,physiology Mice Neocortex/physiology Parvalbumins/physiology Periodicity Photic Stimulation Prefrontal Cortex/physiology Signal Transduction
Chemicals
Parvalbumins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Sohal Vikaas S
Department of Bioengineering, Stanford University, Stanford, California 94305, USA.
Zhang Feng
Yizhar Ofer
Deisseroth Karl
References (30)
30 references, click to expand
  1. An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology.
    J Neural Eng. 2007 Sep;4(3):S143-56 PMID: 17873414
  2. Correlation maps allow neuronal electrical properties to be predicted from single-cell gene expression profiles in rat neocortex.
    Cereb Cortex. 2004 Dec;14(12):1310-27 PMID: 15192011
  3. Intracellular correlates of hippocampal theta rhythm in identified pyramidal cells, granule cells, and basket cells.
    Hippocampus. 1995;5(1):78-90 PMID: 7787949
  4. Fast and slow contrast adaptation in retinal circuitry.
    Neuron. 2002 Dec 5;36(5):909-19 PMID: 12467594
  5. Interneuron Diversity series: Rhythm and mood in perisomatic inhibition.
    Trends Neurosci. 2003 Sep;26(9):489-95 PMID: 12948660
  6. Perception's shadow: long-distance synchronization of human brain activity.
    Nature. 1999 Feb 4;397(6718):430-3 PMID: 9989408
  7. High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice.
    Proc Natl Acad Sci U S A. 2007 May 8;104(19):8143-8 PMID: 17483470
  8. Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex.
    Neuroscience. 1998 Aug;85(3):677-701 PMID: 9639265
  9. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2.
    Neuron. 2007 Apr 19;54(2):205-18 PMID: 17442243
  10. Cellular and network mechanisms of rhythmic recurrent activity in neocortex.
    Nat Neurosci. 2000 Oct;3(10):1027-34 PMID: 11017176
  11. Gamma oscillations correlate with working memory load in humans.
    Cereb Cortex. 2003 Dec;13(12):1369-74 PMID: 14615302
  12. Inter- and intra-laminar connections of pyramidal cells in the neocortex.
    Neurosci Res. 2005 Oct;53(2):95-103 PMID: 16054257
  13. Reproducibility and variability in neural spike trains.
    Science. 1997 Mar 21;275(5307):1805-8 PMID: 9065407
  14. Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits.
    Science. 2006 Jan 13;311(5758):233-5 PMID: 16410524
  15. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation.
    Nature. 1995 Feb 16;373(6515):612-5 PMID: 7854418
  16. Targeting and readout strategies for fast optical neural control in vitro and in vivo.
    J Neurosci. 2007 Dec 26;27(52):14231-8 PMID: 18160630
  17. Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system.
    Nature. 2007 Nov 1;450(7166):56-62 PMID: 17972876
  18. Sequential structure of neocortical spontaneous activity in vivo.
    Proc Natl Acad Sci U S A. 2007 Jan 2;104(1):347-52 PMID: 17185420
  19. Integrator or coincidence detector? The role of the cortical neuron revisited.
    Trends Neurosci. 1996 Apr;19(4):130-7 PMID: 8658595
  20. In vivo labeling of parvalbumin-positive interneurons and analysis of electrical coupling in identified neurons.
    J Neurosci. 2002 Aug 15;22(16):7055-64 PMID: 12177202
  21. Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons.
    Nat Neurosci. 2000 Apr;3(4):366-71 PMID: 10725926
  22. Millisecond-timescale, genetically targeted optical control of neural activity.
    Nat Neurosci. 2005 Sep;8(9):1263-8 PMID: 16116447
  23. Excess of high frequency electroencephalogram oscillations in boys with autism.
    Biol Psychiatry. 2007 Nov 1;62(9):1022-9 PMID: 17543897
  24. Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior.
    Neuron. 2007 Feb 15;53(4):591-604 PMID: 17296559
  25. Modulation of neuronal interactions through neuronal synchronization.
    Science. 2007 Jun 15;316(5831):1609-12 PMID: 17569862
  26. The hierarchical development of monkey visual cortical regions as revealed by the maturation of parvalbumin-immunoreactive neurons.
    Brain Res Dev Brain Res. 1996 Oct 23;96(1-2):261-76 PMID: 8922688
  27. Modulation of oscillatory neuronal synchronization by selective visual attention.
    Science. 2001 Feb 23;291(5508):1560-3 PMID: 11222864
  28. Cortical inhibitory neurons and schizophrenia.
    Nat Rev Neurosci. 2005 Apr;6(4):312-24 PMID: 15803162
  29. Multimodal fast optical interrogation of neural circuitry.
    Nature. 2007 Apr 5;446(7136):633-9 PMID: 17410168
  30. Gating of human theta oscillations by a working memory task.
    J Neurosci. 2001 May 1;21(9):3175-83 PMID: 11312302
Article Info
Journal
Nature
Abbr.
Nature
ISSN
1476-4687
Published
2009-06-04
Epub
2009-00-26
Pages
698-702
Language
English
Region
England
NLM ID
0410462
PMCID
PMC3969859
Subset
IM
Grants
NINDS NIH HHS · F31 NS059160 · United States
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