Synchronization of firing in cortical fast-spiking interneurons at gamma frequencies: A phase-resetting analysis

PLoS Computational Biology

Volumn 6, Issue 9, 2010, Pages

  Gouwens, Nathan W ^a,b   Zeberg, Hugo ^a,c   Tsumoto, Kunichika ^d,e   Tateno, Takashi ^d,f   Aihara, Kazuyuki ^d,e   Robinson, Hugh P C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b HARVARD MEDICAL SCHOOL   (United States)

^c KAROLINSKA INSTITUTE   (Sweden)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e INSTITUTE OF INDUSTRIAL SCIENCE   (Japan)

^f OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

NEURONS; PIECEWISE LINEAR TECHNIQUES;

CHEMICAL SYNAPSE; ELECTRICAL SYNAPSIS; FAST SPIKING; FAST SPIKING CELLS; GABAERGIC; GAMMA OSCILLATIONS; GAP-JUNCTIONS; PHASE RESETTING; SPIKING NEURONES; SYNAPTIC INTERACTIONS;

SYNCHRONIZATION;

4 AMINOBUTYRIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; ELECTRIC FIELD; ELECTRICAL SYNAPSE; GABAERGIC TRANSMISSION; GAMMA RADIATION; INTERNEURON; NEOCORTEX; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CONDUCTION; NONHUMAN; OSCILLATION; PRESYNAPTIC NERVE; RAT; SOMATOSENSORY CORTEX; SPIKE WAVE; STOCHASTIC MODEL;

EID: 78049432650     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000951     Document Type: Article

References (50)

1. Buszaki G, Draguhn A (2004) Neuronal oscillations in cortical networks. Science 304: 1926-1929.
2. Singer W (1999) Neuronal synchrony: a versatile code for the definition of relations? Neuron 24: 49-65.
3. 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.
4. Whittington MA, Traub RD, Jefferys JG (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373: 612-615.
5. Whittington MA, Stanford IM, Colling SB, Jefferys JG, Traub RD (1997) Spatiotemporal patterns of gamma frequency oscillations tetanically induced in the rat hippocampal slice. J Physiol 502(Pt 3): 591-607.
6. Cardin JA, Carlen M, Meletis K, Knoblich U, Zhang F, et al. (2009) Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459: 663-667.
7. Hasenstaub A, Shu Y, Haider B, Kraushaar U, Duque A, et al. (2005) Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 47: 423-435.
8. Morita K, Kalra R, Aihara K, Robinson HPC (2008) Recurrent Synaptic Input and the Timing of Gamma-Frequency-Modulated Firing of Pyramidal Cells during Neocortical ''UP'' States. J Neurosci 28: 1871-1881.
9. Lytton WW, Sejnowski TJ (1991) Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons. J Neurophysiol 66: 1059-1079.
10. Vida I, Bartos M, Jonas P (2006) Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates. Neuron 49: 107-117.
11. White JA, Chow CC, Ritt J, Solo-Trevino C, Kopell N (1998) Synchronization and oscillatory dynamics in heterogeneous, mutually inhibited neurons. J Comput Neurosci 5: 5-16.
12. Galarreta M, Hestrin S (1999) A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402: 72-75.
13. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402: 75-79.
14. Tamas G, Buhl EH, Lorinz A, Somogyi P (2000) Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat Neurosci 3: 366-371.
15. Bacci A, Huguenard JR (2006) Enhancement of spike-timing precision by autaptic transmission in neocortical inhibitory interneurons. Neuron 49: 118-130.
16. Tateno T, Harsch A, Robinson HP (2004) Threshold firing frequency-current relationships of neurons in rat somatosensory cortex: type 1 and type 2 dynamics. J Neurophysiol 92: 2283-2294.
17. Tateno T, Robinson HPC (2008) 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: 1056-1072.
18. Traub RD (2001) Gap junctions between interneuron dendrites can enhance synchrony of gamma oscillations in distributed networks. J Neurosci 21: 9478-9486.
19. Bartos M (2002) Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc Natl Acad Sci U S A 99: 13222-13227.
20. Kopell N, Ermentrout GB (2004) Chemical and electrical synapses perform complementary roles in the synchronization of interneuronal networks. Proc Natl Acad Sci U S A 101: 15482-15487.
21. Rinzel JM, Ermentrout GB (1998) Analysis of neuronal excitability. In: CK, Segev I, eds. Methods in Neuronal Modelling. Cambridge MA: MIT Press.
22. Pikovsky A, Rosenblum M, Kurths J (2001) Synchronization: a universal concept in nonlinear sciences. Cambridge: Cambridge University Press.
23. Kawaguchi Y, Kubota Y (1993) Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70: 387-396.
24. Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7: 476-486.
25. Robinson HPC, Kawai N (1993) Injection of digitally synthesized synaptic conductance transients to measure the integrative properties of neurons. J Neurosci Methods 49: 157-165.
26. Sharp AA, O'Neil MB, Abbott LF, Marder E (1993) Dynamic clamp: computergenerated conductances in real neurons. J Neurophysiol 69: 992-995.
27. Amitai Y, Gibson JR, Beierlein M, Patrick SL, Ho AM, et al. (2002) The spatial dimensions of electrically coupled networks of interneurons in the neocortex. J Neurosci 22: 4142-4152.
28. Galarreta M, Hestrin S (2001) Electrical synapses between GABA-releasing interneurons. Nature Rev Neurosci 2: 425-433.
29. Martina M, Royer S, Pare D (2001) Cell-type-specific GABA responses and chloride homeostasis in the cortex and amygdala. J Neurophysiol 86: 2887-2895.
30. Gulledge AT, Stuart GJ (2003) Excitatory actions of GABA in the cortex. Neuron 37: 299-309.
31. Di Bernardo M, Budd CJ, Champneys AR (2001) Grazing and border-collision in piecewise-smooth systems: a unified analytical framework. Phys Rev Lett 86: 2553-2556.
32. Inoue J, Doi S, Kumagai S (2001) Numerical analysis of spectra of the Frobenius-Perron operator of a noisy one-dimensional mapping: Toward a theory of stochastic bifurcations. Phys Rev E Stat Nonlin Soft Matter Phys 64: 056219.
33. Ermentrout GB, Kopell N (1991) Multiple pulse interactions and averaging in systems of coupled neural oscillators. J Math Biology 29: 195-217.
34. Reyes AD, Fetz EE (1993) Two modes of interspike interval shortening by brief transient depolarizations in cat neocortical neurons. J Neurophysiol 69: 1661-1672.
35. Stoop R, Schindler K, Bunimovich LA (2000) When pyramidal neurons lock, when they respond chaotically, and when they like to synchronize. Neurosci Res 36: 81-91.
36. Netoff TI, Banks MI, Dorval AD, Acker CD, Haas JS, et al. (2005) Synchronization in hybrid neuronal networks of the hippocampal formation. J Neurophysiol 93: 1197-1208.
37. Mancilla JG, Lewis TJ, Pinto DJ, Rinzel J, Connors BW (2007) Synchronization of electrically coupled pairs of inhibitory interneurons in neocortex. J Neurosci 27: 2058-2073.
38. Hu H, Martina M, Jonas P (2009) Dendritic mechanisms underlying rapid synaptic activation of fast-spiking hippocampal interneurons. Science 327: 52-58.
39. Martina M, Vida I, Jonas P (2000) Distal initiation and active propagation of action potentials in interneuron dendrites. Science 287: 295-300.
40. Galarreta M, Hestrin S (2002) Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex. Proc Natl Acad Sci U S A 99: 12438-12443.
41. Erisir A, Lau D, Rudy B, Leonard CS (1999) Function of specific K(+) channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 82: 2476-2489.
42. Gutkin BS, Ermentrout GB, Reyes AD (2005) Phase-response curves give the responses of neurons to transient inputs. J Neurophysiol 94: 1623-1635.
43. Ermentrout B, Wechselberger M (2009) Canards, clusters and synchronization in a weakly coupled interneuron model. SIAM J Applied Dynamical Systems 8: 253-278.
44. Tateno T, Robinson HP (2007) Phase resetting curves and oscillatory stability in interneurons of rat somatosensory cortex. Biophys J 92: 683-695.
45. Yoshimura Y, Callaway EM (2005) Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity. Nat Neurosci 8: 1552-1559.
46. Bennett MV, Zukin RS (2004) Electrical coupling and neuronal synchronization in the Mammalian brain. Neuron 41: 495-511.
47. Holt GR, Softky WR, Koch C, Douglas RJ (1996) Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. J Neurophysiol 75: 1806-1814.
48. Destexhe A, Bal T, eds (2009) Dynamic-Clamp: From Principles to Applications: Springer.
49. Robinson HPC (1998) Analog circuits for injecting time-varying linear and nonlinear (NMDA-type) conductances into neurons. J Physiol 518P: 9-10.
50. Robinson HPC (2008) A scriptable DSP-based system for dynamic conductance injection. J Neurosci Methods 169: 271-281.