Skip to main content
Log in

Impact of gamma-oscillatory inhibition on the signal transmission of a cortical pyramidal neuron

  • Research Article
  • Published:
Cognitive Neurodynamics Aims and scope Submit manuscript

Abstract

Networks of synchronized fast-spiking interneurons are thought to be key elements in the generation of gamma (γ) oscillations (30–80 Hz) in the brain. We examined how such γ-oscillatory inhibition regulates the output of a cortical pyramidal cell. Specifically, we modeled a situation where a pyramidal cell receives inputs from γ-synchronized fast-spiking inhibitory interneurons. This model successfully reproduced several important aspects of a recent experimental result regarding the γ-inhibitory regulation of pyramidal cellular firing that is presumably associated with the sensation of whisker stimuli. Through an in-depth analysis of this model system, we show that there is an obvious rhythmic gating effect of the γ-oscillated interneuron networks on the pyramidal neuron’s signal transmission. This effect is further illustrated by the interactions of this interneuron network and the pyramidal neuron. Prominent power in the γ frequency range can emerge provided that there are appropriate delays on the excitatory connections and inhibitory synaptic conductance between interneurons. These results indicate that interactions between excitation and inhibition are critical for the modulation of coherence and oscillation frequency of network activities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, Geiger J, Jonas P (2002) Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc Natl Acad Sci USA 99(20):13222

    Article  PubMed  CAS  Google Scholar 

  • Bartos M, Vida I, Jonas P (2007) Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 8(1):45–56

    Article  PubMed  CAS  Google Scholar 

  • 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(1):47

    PubMed  CAS  Google Scholar 

  • Brunel N, Hakim V (1999) Fast global oscillations in networks of integrate-and-fire neurons with low firing rates. Neural Comput 11(7):1621–1671

    Article  PubMed  CAS  Google Scholar 

  • Brunel N, Wang X (2003) What determines the frequency of fast network oscillations with irregular neural discharges? I. synaptic dynamics and excitation-inhibition balance. J Neurophysiol 90(1):415

    Article  PubMed  Google Scholar 

  • Burchell T, Faulkner H, Whittington M (1998) Gamma frequency oscillations gate temporally coded afferent inputs in the rat hippocampal slice. Neurosci Lett 255(3):151–154

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Engel A, Singer W (2001) Temporal binding and the neural correlates of sensory awareness. Trends Cogn Sci 5(1):16–25

    Article  PubMed  Google Scholar 

  • Ferezou I, Bolea S, Petersen C (2006) Visualizing the cortical representation of whisker touch: voltage-sensitive dye imaging in freely moving mice. Neuron 50(4):617–629

    Article  PubMed  CAS  Google Scholar 

  • Fries P (2009) Neuronal gamma-band synchronization as a fundamental process in cortical computation. Ann Rev Neurosci 32(1):209–224

    Article  PubMed  CAS  Google Scholar 

  • Gouwens N, Zeberg H, Tsumoto K, Tateno T, Aihara K, Robinson H (2010) Synchronization of firing in cortical fast-spiking interneurons at gamma frequencies: a phase-resetting analysis. PLoS Comput Biol 6(9):e1000951

    Article  PubMed  Google Scholar 

  • Hajos N, Palhalmi J, Mann E, Nemeth B, Paulsen O, Freund T (2004) Spike timing of distinct types of GABAergic interneuron during hippocampal gamma oscillations in vitro. J Neurosci 24(41):9127

    Article  PubMed  CAS  Google Scholar 

  • Hines M, Carnevale N (1997) The NEURON simulation environment. Neural Comput 9(6):1179–1209

    Article  PubMed  CAS  Google Scholar 

  • Knoblich U, Siegle J, Pritchett D, Moore C (2010) What do we gain from gamma? Local dynamic gain modulation drives enhanced efficacy and efficiency of signal transmission. Front Human Neurosci 4. Article 185

  • Maex R, De Schutter E (2003) Resonant synchronization in heterogeneous networks of inhibitory neurons. J Neurosci 23(33):10503

    PubMed  CAS  Google Scholar 

  • Morita K, Kalra R, Aihara K, Robinson H (2008) Recurrent synaptic input and the timing of gamma-frequency-modulated firing of pyramidal cells during neocortical “UP” states. J Neurosci 28(8):1871

    Article  CAS  Google Scholar 

  • Pospischil M, Toledo-Rodriguez M, Monier C, Piwkowska Z, Bal T, Frégnac Y, Markram H, Destexhe A (2008) Minimal Hodgkin–Huxley type models for different classes of cortical and thalamic neurons. Biol Cybern 99(4):427–441

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Tateno T, Robinson H (2009) Integration of broadband conductance input in rat somatosensory cortical inhibitory interneurons: an inhibition-controlled switch between intrinsic and input-driven spiking in fast-spiking cells. J Neurophysiol 101(2):1056

    Article  PubMed  CAS  Google Scholar 

  • Tateno T, Harsch A, Robinson H (2004) Threshold firing frequency-current relationships of neurons in rat somatosensory cortex: type 1 and type 2 dynamics. J Neurophysiol 92(4):2283–2294

    Article  CAS  Google Scholar 

  • Tiesinga P, José J (2000) Robust gamma oscillations in networks of inhibitory hippocampal interneurons. Netw: Comput Neural Syst 11(1):1–23

    Article  CAS  Google Scholar 

  • Tiesinga P, Sejnowski T (2010) Mechanisms for phase shifting in cortical networks and their role in communication through coherence. Front Human Neurosci 4. Article 196

  • Tiesinga P, Fellous J, Salinas E, José J, Sejnowski T (2004) Inhibitory synchrony as a mechanism for attentional gain modulation. J Physiol Paris 98(4-6):296–314

    Article  Google Scholar 

  • Traub R, Jefferys J, Whittington M (1997) Simulation of gamma rhythms in networks of interneurons and pyramidal cells. J Comput Neurosci 4(2):141–150

    Article  PubMed  CAS  Google Scholar 

  • Traub R, Bibbig A, Fisahn A, LeBeau F, Whittington M, Buhl E (2000) A model of gamma-frequency network oscillations induced in the rat CA3 region by carbachol in vitro. Eur J Neurosci 12(11):4093–4106

    Article  PubMed  CAS  Google Scholar 

  • Traub R, Kopell N, Bibbig A, Buhl E, LeBeau F, Whittington M (2001) Gap junctions between interneuron dendrites can enhance synchrony of gamma oscillations in distributed networks. J Neurosci 21(23):9478

    PubMed  CAS  Google Scholar 

  • Vida I, Bartos M, Jonas P (2006) Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates. Neuron 49(1):107–117

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Buzsaki G (1996) Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci 16(20):6402

    PubMed  CAS  Google Scholar 

  • Whittington M, Traub R, Jefferys J (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373(6515):612–615

    Article  PubMed  CAS  Google Scholar 

  • Zhu J, Connors B (1999) Intrinsic firing patterns and whisker-evoked synaptic responses of neurons in the rat barrel cortex. J Neurophysiol 81(3):1171

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was funded by a Hong Kong University Grants Council Grant Competitive Earmarked Research Grant (CERG) number PolyU 5279/08E. K. Morita is supported by KAKENHI 21700366 and 20246026 from MEXT. H. Robinson is supported by a grant from the EC Framework Programme 7 (No. 12788) and the Daiwa Anglo-Japanese Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiumin Li.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, X., Morita, K., Robinson, H.P.C. et al. Impact of gamma-oscillatory inhibition on the signal transmission of a cortical pyramidal neuron. Cogn Neurodyn 5, 241–251 (2011). https://doi.org/10.1007/s11571-011-9169-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11571-011-9169-6

Keywords

Navigation