Skip to content
naulon

No retraction, correction or concern found when last checked on Oct 31, 2026.

Parvalbumin and Somatostatin Interneurons Contribute to the Generation of Hippocampal Gamma Oscillations

Pantelis Antonoudiou, Yu Lin Tan, Georgina Kontou and 2 more

The Journal of Neuroscience · 2020 · CC BY-NC-SA

doi:10.1523/jneurosci.0261-20.2020

Abstract

γ-frequency oscillations (30-120 Hz) in cortical networks influence neuronal encoding and information transfer, and are disrupted in multiple brain disorders. While synaptic inhibition is important for synchronization across the γ-frequency range, the role of distinct interneuronal subtypes in slow (<60 Hz) and fast γ states remains unclear. Here, we used optogenetics to examine the involvement of parvalbumin-expressing (PV + ) and somatostatin-expressing (SST + ) interneurons in γ oscillations in the mouse hippocampal CA3 ex vivo , using animals of either sex. Disrupting either PV + or SST + interneuron activity, via either photoinhibition or photoexcitation, led to a decrease in the power of cholinergically induced slow γ oscillations. Furthermore, photoexcitation of SST + interneurons induced fast γ oscillations, which depended on both synaptic excitation and inhibition. Our findings support a critical role for both PV + and SST + interneurons in slow hippocampal γ oscillations, and further suggest that intense activation of SST + interneurons can enable the CA3 circuit to generate fast γ oscillations. SIGNIFICANCE STATEMENT The generation of hippocampal γ oscillations depends on synchronized inhibition provided by GABAergic interneurons. Parvalbumin-expressing (PV + ) interneurons are thought to play the key role in coordinating the spike timing of excitatory pyramidal neurons, but the role distinct inhibitory circuits in network synchronization remains unresolved. Here, we show, for the first time, that causal disruption of either PV + or somatostatin-expressing (SST + ) interneuron activity impairs the generation of slow γ oscillations in the ventral hippocampus ex vivo . We further show that SST + interneuron activation along with general network excitation is sufficient to generate high-frequency γ oscillations in the same preparation. These results affirm a crucial role for both PV + and SST + interneurons in hippocampal γ oscillation generation.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 90

  1. 1.
  2. 2.

    Akam T, Oren I, Mantoan L, Ferenczi E, Kullmann DM (2012 ) Oscillatory dynamics in the hippocampus support dentate gyrus–CA3 coupling. Nat Neurosci 15:763–768.

    Not in our library10.1038/nn.3081

  3. 3.

    Anastassiou CA, Perin R, Markram H, Koch C (2011 ) Ephaptic coupling of cortical neurons. Nat Neurosci 14:217–223.

    Not in our library10.1038/nn.2727

  4. 4.

    Andersen P, Bliss TV, Skrede KK (1971 ) Unit analysis of hippocampal population spikes. Exp Brain Res 13:208–221.

    Not in our library10.1007/bf00234086

  5. 5.

    Atallah BV, Scanziani M (2009 ) Instantaneous modulation of gamma oscillation frequency by balancing excitation with inhibition. Neuron 62:566–577.

    Not in our library10.1016/j.neuron.2009.04.027

  6. 6.

    Bartos M, Elgueta C (2012 ) Functional characteristics of parvalbumin- and cholecystokinin-expressing basket cells. J Physiol 590:669–681.

    Not in our library10.1113/jphysiol.2011.226175

  7. 7.

    Bartos M, Vida I, Jonas P (2007 ) Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 8:45–56.

    Not in our library10.1038/nrn2044

  8. 8.

    Basar-Eroglu C, Brand A, Hildebrandt H, Karolina Kedzior K, Mathes B, Schmiedt C (2007 ) Working memory related gamma oscillations in schizophrenia patients. Int J Psychophysiol 64:39–45.

    Not in our library10.1016/j.ijpsycho.2006.07.007

  9. 9.

    Bastos AM, Vezoli J, Fries P (2015 ) Communication through coherence with inter-areal delays. Curr Opin Neurobiol 31:173–180.

    Not in our library10.1016/j.conb.2014.11.001

  10. 10.

    Baude A, Bleasdale C, Dalezios Y, Somogyi P, Klausberger T (2007 ) Immunoreactivity for the GABAA receptor 1 subunit, somatostatin and connexin36 distinguishes axoaxonic, basket, and bistratified interneurons of the rat hippocampus. Cereb Cortex 17:2094–2107.

    Not in our library10.1093/cercor/bhl117

  11. 11.

    Beierlein M, Gibson JR, Connors BW (2000 ) A network of electrically coupled interneurons drives synchronized inhibitionin neocortex. Nat Neurosci 3:904–910.

    Not in our library10.1038/78809

  12. 12.

    Betterton RT, Broad LM, Tsaneva-Atanasova K, Mellor JR (2017 ) Acetylcholine modulates gamma frequency oscillations in the hippocampus by activation of muscarinic M1 receptors. Eur J Neurosci 45:1570–1585.

    Not in our library10.1111/ejn.13582

  13. 13.

    Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K (2005 ) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8:1263–1268.

    Not in our library10.1038/nn1525

  14. 14.

    Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G (1995 ) Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15:47–60.

    Not in our library10.1523/jneurosci.15-01-00047.1995

  15. 15.

    Burns SP, Xing D, Shapley RM (2011 ) Is gamma-band activity in the local field potential of V1 cortex a 'clock' or filtered noise? J Neurosci 31:9658–9664.

    Not in our library10.1523/jneurosci.0660-11.2011

  16. 16.

    Butler JL, Hay YA, Paulsen O (2018 ) Comparison of three gamma oscillations in the mouse entorhinal-hippocampal system. Eur J Neurosci 48:2795–2806.

    Not in our library10.1111/ejn.13831

  17. 17.

    Butler JL, Mendonça PR, Robinson HP, Paulsen O (2016 ) Intrinsic cornu ammonis area 1 theta-nested gamma oscillations induced by optogenetic theta frequency stimulation. J Neurosci 36:4155–4169.

    Not in our library10.1523/jneurosci.3150-15.2016

  18. 18.

    Butler JL, Paulsen O (2014 ) The hippocampal cacophony: multiple layers of communication. Neuron 84:251–253.

    Not in our library10.1016/j.neuron.2014.10.017

  19. 19.

    Buzsáki G (2002 ) Theta oscillations in the hippocampus. Neuron 33:325–340.

    Not in our library10.1016/s0896-6273(02)00586-x

  20. 20.

    Buzsáki G, Wang XJ (2012 ) Mechanisms of gamma oscillations. Annu Rev Neurosci 35:203–225.

    Not in our library10.1146/annurev-neuro-062111-150444

  21. 21.

    Cardin JA (2016 ) Snapshots of the brain in action: local circuit operations through the lens of γ oscillations. J Neurosci 36:10496–10504.

    Not in our library10.1523/jneurosci.1021-16.2016

  22. 22.

    Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI (2009 ) Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459:663–667.

    Not in our library10.1038/nature08002

  23. 23.

    Cattaneo S, Zaghi M, Maddalena R, Bedogni F, Sessa A, Taverna S (2019 ) Somatostatin-expressing interneurons co-release GABA and glutamate onto different postsynaptic targets in the striatum. bioRxiv 566984 DOI:.

    Not in our library10.1101/566984

  24. 24.

    Chen G, Zhang Y, Li X, Zhao X, Ye Q, Lin Y, Tao HW, Rasch MJ, Zhang X (2017 ) Distinct inhibitory circuits orchestrate cortical beta and gamma band oscillations. Neuron 96:1403–1418.e6.

    Not in our library10.1016/j.neuron.2017.11.033

  25. 25.

    Chow BY, Han X, Dobry AS, Qian X, Chuong AS, Li M, Henninger MA, Belfort GM, Lin Y, Monahan PE, Boyden ES (2010 ) High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature 463:98–102.

    Not in our library10.1038/nature08652

  26. 26.

    Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI (2009 ) Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462:353–357.

    Not in our library10.1038/nature08573

  27. 27.

    Craig MT, McBain CJ (2015 ) Fast gamma oscillations are generated intrinsically in CA1 without the involvement of fast-spiking basket cells. J Neurosci 35:3616–3624.

    Not in our library10.1523/jneurosci.4166-14.2015

  28. 28.

    Csicsvari J, Jamieson B, Wise KD, Buzsáki G (2003 ) Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311–322.

    Not in our library10.1016/s0896-6273(02)01169-8

  29. 29.

    Devalle F, Roxin A, Montbrió E (2017 ) Firing rate equations require a spike synchrony mechanism to correctly describe fast oscillations in inhibitory networks. PLoS Comput Biol 13:e1005881.

    Not in our library10.1371/journal.pcbi.1005881

  30. 30.

    El-Gaby M, Zhang Y, Wolf K, Schwiening CJ, Paulsen O, Shipton OA (2016 ) Archaerhodopsin selectively and reversibly silences synaptic transmission through altered pH. Cell Rep 16: 2259–2268.

    Not in our library10.1016/j.celrep.2016.07.057

  31. 31.

    Fee MS, Mitra PP, Kleinfeld D (1996 ) Automatic sorting of multiple unit neuronal signals in the presence of anisotropic and non-Gaussian variability. J Neurosci Methods 69:175–188.

    Not in our library10.1016/s0165-0270(96)00050-7

  32. 32.

    Ferenczi EA, Vierock J, Atsuta-Tsunoda K, Tsunoda SP, Ramakrishnan C, Gorini C, Thompson K, Lee SY, Berndt A, Perry C, Minniberger S, Vogt A, Mattis J, Prakash R, Delp S, Deisseroth K, Hegemann P (2016 ) Optogenetic approaches addressing extracellular modulation of neural excitability. Sci Rep 6:23947.

    Not in our library10.1038/srep23947

  33. 33.

    Fisahn A, Pike FG, Buhl EH, Paulsen O (1998 ) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394:186–189.

    Not in our library10.1038/28179

  34. 34.

    Fries P (2005 ) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 9:474–480.

    Not in our library10.1016/j.tics.2005.08.011

  35. 35.

    Fries P (2015 ) Rhythms for cognition: communication through coherence. Neuron 88:220–235.

    Not in our library10.1016/j.neuron.2015.09.034

  36. 36.

    Fries P, Reynolds JH, Rorie AE, Desimone R (2001 ) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291:1560–1563.

    Not in our library10.1126/science.1055465

  37. 37.

    Fuchs EC, Zivkovic AR, Cunningham MO, Middleton S, Lebeau FE, Bannerman DM, Rozov A, Whittington MA, Traub RD, Rawlins JN, Monyer H (2007 ) Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior. Neuron 53:591–604.

    Not in our library10.1016/j.neuron.2007.01.031

  38. 38.

    Gloveli T, Dugladze T, Saha S, Monyer H, Heinemann U, Traub RD, Whittington MA, Buhl EH (2005 ) Differential involvement of oriens/pyramidale interneurones in hippocampal network oscillations In vitro. J Physiol 562:131–147.

    Not in our library10.1113/jphysiol.2004.073007

  39. 39.

    Gulyás AI, Szabó GG, Ulbert I, Holderith N, Monyer H, Erdélyi F, Szabó G, Freund TF, Hájos N (2010 ) Parvalbumin-containing fast-spiking basket cells generate the field potential oscillations induced by cholinergic receptor activation in the hippocampus. J Neurosci 30:15134–15145.

    Not in our library10.1523/jneurosci.4104-10.2010

  40. 40.

    Hájos N, Pálhalmi J, Mann EO, Németh B, Paulsen O, Freund TF (2004 ) Spike timing of distinct types of GABAergic interneuron during hippocampal gamma oscillations in vitro. J Neurosci 24:9127–9137.

    Not in our library10.1523/jneurosci.2113-04.2004

  41. 41.

    Hájos N, Paulsen O (2009 ) Network mechanisms of gamma oscillations in the CA3 region of the hippocampus. Neural Netw 22:1113–1119.

    Not in our library10.1016/j.neunet.2009.07.024

  42. 42.

    Hakim R, Shamardani K, Adesnik H (2018 ) A neural circuit for gamma-band coherence across the retinotopic map in mouse visual cortex. Elife 7:e28569

    Not in our library10.7554/elife.28569

  43. 43.

    Hasenstaub A, Shu Y, Haider B, Kraushaar U, Duque A, McCormick DA (2005 ) Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 47:423–435.

    Not in our library10.1016/j.neuron.2005.06.016

  44. 44.
  45. 45.

    Herrmann CS, Demiralp T (2005 ) Human EEG gamma oscillations in neuropsychiatric disorders. Clin Neurophysiol 116:2719–2733.

    Not in our library10.1016/j.clinph.2005.07.007

  46. 46.

    Hofer SB, Ko H, Pichler B, Vogelstein J, Ros H, Zeng H, Lein E, Lesica NA, Mrsic-Flogel TD (2011 ) Differential connectivity and response dynamics of excitatory and inhibitory neurons in visual cortex. Nat Neurosci 14:1045–1052.

    Not in our library10.1038/nn.2876

  47. 47.

    Hu H, Gan J, Jonas P (2014 ) Interneurons: fast-spiking, parvalbumin+ GABAergic interneurons: from cellular design to microcircuit function. Science 345:1255263.

    Not in our library10.1126/science.1255263

  48. 48.

    Huang S, Uusisaari MY (2013 ) Physiological temperature during brain slicing enhances the quality of acute slice preparations. Frontiers in Cellular Neuroscience 7:48.

    Not in our library10.3389/fncel.2013.00048

  49. 49.

    Kim D, Jeong H, Lee J, Ghim JW, Her ES, Lee SH, Jung MW (2016 ) Distinct roles of parvalbumin- and somatostatin-expressing interneurons in working memory. Neuron 92:902–915.

    Not in our library10.1016/j.neuron.2016.09.023

  50. 50.

    Kohus Z, Káli S, Rovira-Esteban L, Schlingloff D, Papp O, Freund TF, Hájos N, Gulyás AI (2016 ) Properties and dynamics of inhibitory synaptic communication within the CA3 microcircuits of pyramidal cells and interneurons expressing parvalbumin or cholecystokinin. J Physiol 594:3745–3774.

    Not in our library10.1113/jp272231

  51. 51.

    Lasztóczi B, Klausberger T (2016 ) Hippocampal place cells couple to three different gamma oscillations during place field traversal. Neuron 91:34–40.

    Not in our library10.1016/j.neuron.2016.05.036

  52. 52.

    Leão RN, Mikulovic S, Leão KE, Munguba H, Gezelius H, Enjin A, Patra K, Eriksson A, Loew LM, Tort AB, Kullander K (2012 ) OLM interneurons differentially modulate CA3 and entorhinal inputs to hippocampal CA1 neurons. Nat Neurosci 15:1524–1530.

    Not in our library10.1038/nn.3235

  53. 53.

    Lovett-Barron M, Kaifosh P, Kheirbek MA, Danielson N, Zaremba JD, Reardon TR, Turi GF, Hen R, Zemelman BV, Losonczy A (2014 ) Dendritic inhibition in the hippocampus supports fear learning. Science 343:857–863.

    Not in our library10.1126/science.1247485

  54. 54.

    Lovett-Barron M, Turi GF, Kaifosh P, Lee PH, Bolze F, Sun XH, Nicoud JF, Zemelman BV, Sternson SM, Losonczy A (2012 ) Regulation of neuronal input transformations by tunable dendritic inhibition. Nat Neurosci 15:423–430.

    Not in our library10.1038/nn.3024

  55. 55.

    Ma Y, Hu H, Berrebi AS, Mathers PH, Agmon A (2006 ) Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J Neurosci 26:5069–5082.

    Not in our library10.1523/jneurosci.0661-06.2006

  56. 56.

    Mann EO, Radcliffe CA, Paulsen O (2005a ) Hippocampal gamma-frequency oscillations: from interneurones to pyramidal cells, and back. J Physiol 562:55–63.

    Not in our library10.1113/jphysiol.2004.078758

  57. 57.

    Mann EO, Suckling JM, Hajos N, Greenfield SA, Paulsen O (2005b ) Perisomatic feedback inhibition underlies cholinergically induced fast network oscillations in the rat hippocampus in vitro. Neuron 45:105–117.

    Not in our library10.1016/j.neuron.2004.12.016

  58. 58.

    Muller C, Remy S (2014 ) Dendritic inhibition mediated by O-LM and bistratified interneurons in the hippocampus. Front Synaptic Neurosci 6:23.

    Not in our library10.3389/fnsyn.2014.00023

  59. 59.

    Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P, Ollig D, Hegemann P, Bamberg E (2003 ) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci USA 100:13940–13945.

    Not in our library10.1073/pnas.1936192100

  60. 60.

    Octeau JC, Gangwani MR, Allam SL, Tran D, Huang S, Hoang-Trong TM, Golshani P, Rumbell TH, Kozloski JR, Khakh BS (2019 ) Transient, consequential increases in extracellular potassium ions accompany channelrhodopsin2 excitation. Cell Rep 27:2249–2261.e7.

    Not in our library10.1016/j.celrep.2019.04.078

  61. 61.

    Oren I, Hájos N, Paulsen O (2010 ) Identification of the current generator underlying cholinergically induced gamma frequency field potential oscillations in the hippocampal CA3 region. J Physiol 588:785–797.

    Not in our library10.1113/jphysiol.2009.180851

  62. 62.

    Oren I, Mann EO, Paulsen O, Hájos N (2006 ) Synaptic currents in anatomically identified CA3 neurons during hippocampal gamma oscillations in vitro. J Neurosci 26:9923–9934.

    Not in our library10.1523/jneurosci.1580-06.2006

  63. 63.

    Packer AM, Yuste R (2011 ) Dense, unspecific connectivity of neocortical parvalbumin-positive interneurons: a canonical microcircuit for inhibition? J Neurosci 31:13260–13271.

    Not in our library10.1523/jneurosci.3131-11.2011

  64. 64.

    Penttonen M, Kamondi A, Acsady L, Buzsaki G (1998 ) Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo. Eur J Neurosci 10:718–728.

    Not in our library10.1046/j.1460-9568.1998.00096.x

  65. 65.

    Pfeffer CK, Xue M, He M, Huang ZJ, Scanziani M (2013 ) Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat Neurosci 16:1068–1076.

    Not in our library10.1038/nn.3446

  66. 66.

    Pike FG, Goddard RS, Suckling JM, Ganter P, Kasthuri N, Paulsen O (2000 ) Distinct frequency preferences of different types of rat hippocampal neurones in response to oscillatory input currents. J Physiol 529:205–213.

    Not in our library10.1111/j.1469-7793.2000.00205.x

  67. 67.

    Pouille F, Scanziani M (2001 ) Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293:1159–1163.

    Not in our library10.1126/science.1060342

  68. 68.

    Quian Quiroga R (2009 ) What is the real shape of extracellular spikes? J Neurosci Methods 177:194–198.

    Not in our library10.1016/j.jneumeth.2008.09.033

  69. 69.

    Quian Quiroga R, Nadasdy Z, Ben-Shaul Y (2004 ) Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput 16: 1661–1687.

    Not in our library10.1162/089976604774201631

  70. 70.

    Ray S, Maunsell JH (2015 ) Do gamma oscillations play a role in cerebral cortex? Trends Cogn Sci 19:78–85.

    Not in our library10.1016/j.tics.2014.12.002

  71. 71.

    Royer S, Zemelman BV, Losonczy A, Kim J, Chance F, Magee JC, Buzsáki G (2012 ) Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat Neurosci 15:769–710.

    Not in our library10.1038/nn.3077

  72. 72.

    Savanthrapadian S, Meyer T, Elgueta C, Booker SA, Vida I, Bartos M (2014 ) Synaptic properties of SOM- and CCK-expressing cells in dentate gyrus interneuron networks. J Neurosci 34:8197–8209.

    Not in our library10.1523/jneurosci.5433-13.2014

  73. 73.

    Schomburg EW, Fernández-Ruiz A, Mizuseki K, Berényi A, Anastassiou CA, Koch C, Buzsáki G (2014 ) Theta phase segregation of input-specific gamma patterns in entorhinal-hippocampal networks. Neuron 84:470–485.

    Not in our library10.1016/j.neuron.2014.08.051

  74. 74.

    Sohal VS (2016 ) How close are we to understanding what (if anything) oscillations do in cortical circuits? J Neurosci 36:10489–10495.

    Not in our library10.1523/jneurosci.0990-16.2016

  75. 75.

    Sohal VS, Zhang F, Yizhar O, Deisseroth K (2009 ) Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459:698–702.

    Not in our library10.1038/nature07991

  76. 76.

    Somogyi P, Klausberger T (2005 ) Defined types of cortical interneurone structure space and spike timing in the hippocampus. J Physiol 562:9–26.

    Not in our library10.1113/jphysiol.2004.078915

  77. 77.

    Spellman T, Rigotti M, Ahmari SE, Fusi S, Gogos JA, Gordon JA (2015 ) Hippocampal–prefrontal input supports spatial encoding in working memory. Nature 522:309–314.

    Not in our library10.1038/nature14445

  78. 78.

    Sullivan D, Csicsvari J, Mizuseki K, Montgomery S, Diba K, Buzsáki G (2011 ) Relationships between hippocampal sharp waves, ripples, and fast gamma oscillation: influence of dentate and entorhinal cortical activity. J Neurosci 31:8605–8616.

    Not in our library10.1523/jneurosci.0294-11.2011

  79. 79.

    Taniguchi H, He M, Wu P, Kim S, Paik R, Sugino K, Kvitsiani D, Kvitsani D, Fu Y, Lu J, Lin Y, Miyoshi G, Shima Y, Fishell G, Nelson SB, Huang ZJ (2011 ) A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71:995–1013.

    Not in our library10.1016/j.neuron.2011.07.026

  80. 80.

    Tukker JJ, Fuentealba P, Hartwich K, Somogyi P, Klausberger PT (2007 ) Cell type-specific tuning of hippocampal interneuron firing during gamma oscillations. J Neurosci 27:8184–8189.

    Not in our library10.1523/jneurosci.1685-07.2007

  81. 81.

    Tukker JJ, Lasztóczi B, Katona L, Roberts JD, Pissadaki EK, Dalezios Y, Márton L, Zhang L, Klausberger T, Somogyi P (2013 ) Distinct dendritic arborization and in vivo firing patterns of parvalbumin-expressing basket cells in the hippocampal area CA3. J Neurosci 33:6809–6825.

    Not in our library10.1523/jneurosci.5052-12.2013

  82. 82.

    Uhlhaas PJ, Singer W (2010 ) Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci 11:100–113.

    Not in our library10.1038/nrn2774

  83. 83.

    Uhlhaas PJ, Singer W (2006 ) Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 52:155–168.

    Not in our library10.1016/j.neuron.2006.09.020

  84. 84.

    Urban-Ciecko J, Barth AL (2016 ) Somatostatin-expressing neurons in cortical networks. Nat Rev Neurosci 17:401–409.

    Not in our library10.1038/nrn.2016.53

  85. 85.

    Veit J, Hakim R, Jadi MP, Sejnowski TJ, Adesnik H (2017 ) Cortical gamma band synchronization through somatostatin interneurons. Nat Neurosci 20: 951–959.

    Not in our library10.1038/nn.4562

  86. 86.

    Whittington MA, Traub RD, Jefferys JG (1995 ) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373:612–615.

    Not in our library10.1038/373612a0

  87. 87.

    Wierenga C, Wadman W (2003 ) Functional relation between interneuron input and population activity in the rat hippocampal cornu ammonis 1 area. Neuroscience 118:1129–1139.

    Not in our library10.1016/s0306-4522(03)00060-5

  88. 88.

    Womelsdorf T, Everling S (2015 ) Long-range attention networks: circuit motifs underlying endogenously controlled stimulus selection. Trends Neurosci 38:682–700.

    Not in our library10.1016/j.tins.2015.08.009

  89. 89.

    Yamamoto J, Suh J, Takeuchi D, Tonegawa S (2014 ) Successful execution of working memory linked to synchronized high-frequency gamma oscillations. Cell 157:845–857.

    Not in our library10.1016/j.cell.2014.04.009

  90. 90.

    Zar JH (1999 ) 929 Biostatistical analysis, Ed 4 Englewood Cliffs, NJ: Prentice Hall.

    Not in our library

Cited by papers we hold 1

Reads

Read by people on this page

None yet.

Checked or read by AI through naulon

None yet.

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.

Are you an author?

Is this your paper?

Claim it to add your note and be paid when agents cite it. Free.