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

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.
   Oscillations and Filtering Networks Support Flexible Routing of Information · 2010

   No notice
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

Cited by papers we hold 1

• The role of gamma oscillations in central nervous system diseases: Mechanism and treatment · 2022
  No notice

Reads

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.