Cell type-specific control of neuronal responsiveness by gamma-band oscillatory inhibition

Journal of Neuroscience

Volumn 30, Issue 6, 2010, Pages 2150-2159

  Otte, Stephani ^a,b   Hasenstaub, Andrea ^a   Callaway, Edward M ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN SLICE; CELL TYPE; CORTICAL SYNCHRONIZATION; GAMMA BAND OSCILLATORY INHIBITION; HYPERPOLARIZATION; MODULATION; MOUSE; NERVE CELL INHIBITION; NERVE CELL NETWORK; NERVE CONDUCTION; NERVOUS SYSTEM PARAMETERS; NONHUMAN; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE; WHOLE CELL;

ACTION POTENTIALS; ANIMALS; CELL MEMBRANE; CEREBRAL CORTEX; INTERNEURONS; MICE; MICE, TRANSGENIC; MODELS, NEUROLOGICAL; NERVE NET; NEURONS; PATCH-CLAMP TECHNIQUES; PERIODICITY; PYRAMIDAL CELLS;

EID: 76649107649     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4818-09.2010     Document Type: Article

References (71)

1. Bartos M, Vida I, Frotscher M, Geiger JR, Jonas P (2001) Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. J Neurosci 21:2687-2698.
2. Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, Geiger JR, Jonas P (2002) Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc Natl Acad Sci U S A 99:13222-13227.
3. Bartos M, Vida I, Jonas P (2007) Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 8:45-56.
4. Başar E, Güntekin B (2008) A review of brain oscillations in cognitive disorders and the role of neurotransmitters. Brain Res 1235:172-193.
5. Blitzer RD, Wong T, Nouranifar R, Landau EM (1994) The cholinergic inhibition of afterhyperpolarization in rat hippocampus is independent of cAMP-dependent protein kinase. Brain Res 646:312-314.
6. Buschman TJ, Miller EK (2007) Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315:1860-1862.
7. Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, Berger MS, Barbaro NM, Knight RT (2006) High gamma power is phase-locked to theta oscillations in human neocortex. Science 313:1626-1628.
8. Cardin JA, Palmer LA, Contreras D (2008) Cellular mechanisms underlying stimulus-dependent gain modulation in primary visual cortex neurons in vivo. Neuron 59:150-160.
9. Cardin JA, Carlen 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.
10. Chattopadhyaya B, Di Cristo G, Higashiyama H, Knott GW, Kuhlman SJ, Welker E, Huang ZJ (2004) Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 24:9598-9611.
11. Csicsvari J, Jamieson B, Wise KD, Buzsáki G (2003) Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37:311-322.
12. Cunningham MO, Whittington MA, Bibbig A, Roopun A, LeBeau FE, Vogt A, Monyer H, Buhl EH, Traub RD (2004) A role for fast rhythmic bursting neurons in cortical gamma oscillations in vitro. Proc Natl Acad Sci U S A 101:7152-7157.
13. Dorval AD, Christini DJ, White JA (2001) Real-Time Linux dynamic clamp: a fast and flexible way to construct virtual ion channels in living cells. Ann Biomed Eng 29:897-907.
14. + channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 82:2476-2489.
15. Fanselow EE, Richardson KA, Connors BW (2008) Selective, state-dependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex. J Neurophysiol 100:2640-2652.
16. Fellous JM, Sejnowski TJ (2000) Cholinergic induction of oscillations in the hippocampal slice in the slow (0.5-2 Hz), theta (5-12 Hz), and gamma (35-70 Hz) bands. Hippocampus 10:187-197.
17. Fellous JM, Houweling AR, Modi RH, Rao RP, Tiesinga PH, Sejnowski TJ (2001) Frequency dependence of spike timing reliability in cortical pyramidal cells and interneurons. J Neurophysiol 85:1782-1787.
18. 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.
19. Fisahn A, Contractor A, Traub RD, Buhl EH, Heinemann SF, McBain CJ (2004) Distinct roles for the kainate receptor subunits GluR5 and GluR6 in kainate-induced hippocampal gamma oscillations. J Neurosci 24:9658-9668.
20. Freeman WJ, Holmes MD, Burke BC, Vanhatalo S (2003) Spatial spectra of scalp EEG and EMG from awake humans. Clin Neurophysiol 114: 1053-1068.
21. Freund TF (2003) Interneuron diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci 26:489-495.
22. Fries P (2009) Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci 32:209-224.
23. Fries P, Neuenschwander S, Engel AK, Goebel R, Singer W (2001) Rapid feature selective neuronal synchronization through correlated latency shifting. Nat Neurosci 4:194-200.
24. Fries P, Nikolić D, Singer W (2007) The gamma cycle. Trends Neurosci 30:309-316.
25. Galarreta M, Hestrin S (2001) Electrical synapses between GABA-releasing interneurons. Nat Rev Neurosci 2:425-433.
26. 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.
27. Galarreta M, Erdélyi F, Szabó G, Hestrin S (2004) Electrical coupling among irregular-spiking GABAergic interneurons expressing cannabinoid receptors. J Neurosci 24:9770-9778.
28. Haider B, McCormick DA (2009) Rapid neocortical dynamics: cellular and network mechanisms. Neuron 62:171-189.
29. Haider B, Duque A, Hasenstaub AR, McCormick DA (2006) Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J Neurosci 26:4535-4545.
30. Hájos N, Katona I, Naiem SS, MacKie K, Ledent C, Mody I, Freund TF (2000) Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur J Neurosci 12:3239-3249.
31. Halabisky B, Shen F, Huguenard JR, Prince DA (2006) Electrophysiological classification of somatostatin-positive interneurons in mouse sensorimotor cortex. J Neurophysiol 96:834-845.
32. 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.
33. Herrmann CS, Demiralp T (2005) Human EEG gamma oscillations in neuropsychiatric disorders. Clin Neurophysiol 116:2719-2733.
34. Higgs MH, Slee SJ, Spain WJ (2006) Diversity of gain modulation by noise in neocortical neurons: regulation by the slow afterhyperpolarization conductance. J Neurosci 26:8787-8799.
35. Hutcheon B, Yarom Y (2000) Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci 23:216-222.
36. Jensen O, Kaiser J, Lachaux JP (2007) Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci 30: 317-324.
37. Kasper EM, Lübke J, Larkman AU, Blakemore C (1994) Pyramidal neurons in layer 5 of the rat visual cortex. III. Differential maturation of axon targeting, dendritic morphology, and electrophysiological properties. J Comp Neurol 339:495-518.
38. Kawaguchi Y (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13:4908-4923.
39. Kawaguchi Y, Kubota Y (1998) Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neuroscience 85:677-701.
40. Klausberger T, Magill PJ, Marton LF, Roberts JD, Cobden PM, Buzsaki G, Somogyi P (2003) Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421:844-848.
41. Lakatos P, Shah AS, Knuth KH, Ulbert I, Karmos G, Schroeder CE (2005) An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. J Neurophysiol 94:1904-1911.
42. Lakatos P, Karmos G, Mehta AD, Ulbert I, Schroeder CE (2008) Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 320:110-113.
43. López-Bendito G, Sturgess K, Erdélyi F, Szabó G, Molnár Z, Paulsen O (2004) Preferential origin and layer destination of GAD65-GFP cortical interneurons. Cereb Cortex 14:1122-1133.
44. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807.
45. McCormick DA (1992) Neurotransmitter actions in the thalamus and cerebral cortex. J Clin Neurophysiol 9:212-223.
46. McCormick DA, Pape HC, Williamson A (1991) Actions of norepinephrine in the cerebral cortex and thalamus: implications for function of the central noradrenergic system. Prog Brain Res 88:293-305.
47. McLelland D, PaulsenO (2009) Neuronal oscillations and the rate-to-phase transform: mechanism, model and mutual information. J Physiol 587: 769-785.
48. Miles R, Tó th K, Gulyá s AI, Há jos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815-823.
49. Nicoll RA (1988) The coupling of neurotransmitter receptors to ion channels in the brain. Science 241:545-551.
50. Oliva AA Jr, Jiang M, Lam T, Smith KL, Swann JW (2000) Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci 20:3354-3368.
51. Papp E, Leinekugel X, Henze DA, Lee J, Buzsáki G (2001) The apical shaft of CA1 pyramidal cells is under GABAergic interneuronal control. Neuroscience 102:715-721.
52. Paré D, Shink E, Gaudreau H, Destexhe A, Lang EJ (1998) Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons in vivo. J Neurophysiol 79:1450-1460.
53. +current sIAHP by a phosphatase-kinase balance under basal conditions in rat CA1 pyramidal neurons. J Neurophysiol 79:3252-3256.
54. Prescott SA, Sejnowski TJ (2008) Spike-rate coding and spike-time coding are affected oppositely by different adaptation mechanisms. J Neurosci 28:13649-13661.
55. Rodriguez R, Kallenbach U, Singer W, Munk MH (2004) Short- and longterm effects of cholinergic modulation on gamma oscillations and response synchronization in the visual cortex. J Neurosci 24:10369-10378.
56. Sah P, Faber ES (2002) Channels underlying neuronal calcium-activated potassium currents. Prog Neurobiol 66:345-353.
57. Schreiber S, Fellous JM, Tiesinga P, Sejnowski TJ (2004) Influence of ionic conductances on spike timing reliability of cortical neurons for suprathreshold rhythmic inputs. J Neurophysiol 91:194-205.
58. Shu Y, Hasenstaub A, McCormick DA (2003) Turning on and off recurrent balanced cortical activity. Nature 423:288-293.
59. Sohal VS, Zhang F, Yizhar O, Deisseroth K (2009) Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459:698-702.
60. Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85:1969-1985.
61. Szabadics J, Lorincz A, Tamás G (2001) Beta and gamma frequency synchronization by dendritic GABAergic synapses and gap junctions in a network of cortical interneurons. J Neurosci 21:5824-5831.
62. Tamás G, Buhl EH, Lörincz A, Somogyi P (2000) Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat Neurosci 3:366-371.
63. Tamás G, Buhl EH, Lörincz A, Somogyi P (2004) Input and frequency-specific entrainment of postsynaptic firing by IPSPs of perisomatic or dendritic origin. Eur J Neurosci 20:2681-2690.
64. Tiesinga PH, Fellous JM, Salinas E, José JV, Sejnowski TJ (2004) Inhibitory synchrony as a mechanism for attentional gain modulation. J Physiol Paris 98:296-314.
65. +channels underlying the slow afterhyperpolarization in enteric afterhyperpolarization-generating myenteric neurons: role of calcium and phosphorylation. Clin Exp Pharmacol Physiol 29:935-943.
66. Wang Z, McCormickDA (1993) Control of firing mode of corticotectal and corticopontine layer V burst-generating neurons by norepinephrine, acetylcholine, and 1S,3R-ACPD. J Neurosci 13:2199-2216.
67. Whittington MA, Traub RD, Jefferys JG (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373:612-615.
68. Womelsdorf T, Fries P (2006) Neuronal coherence during selective attentional processing and sensory-motor integration. J Physiol Paris 100: 182-193.
69. Womelsdorf T, Fries P, Mitra PP, Desimone R (2006) Gamma-band synchronization in visual cortex predicts speed of change detection. Nature 439:733-736.
70. Xu X, Callaway EM (2009) Laminar specificity of functional input to distinct types of inhibitory cortical neurons. J Neurosci 29:70-85.
71. Xu X, Roby KD, CallawayEM (2006) Mouse cortical inhibitory neuron type that coexpresses somatostatin and calretinin. J Comp Neurol 499:144-160.