Cortical balance of excitation and inhibition is regulated by the rate of synaptic activity

Journal of Neuroscience

Volumn 33, Issue 36, 2013, Pages 14359-14368

  Taub, Aryeh H ^a   Katz, Yonatan ^a   Lampl, Ilan ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

6, 7 DINITRO 2, 3 QUINOXALINEDIONE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; BRAIN DEPTH STIMULATION; BRAIN ELECTROPHYSIOLOGY; CELL TRANSFER; EXCITATORY POSTSYNAPTIC POTENTIAL; INHIBITORY POSTSYNAPTIC POTENTIAL; NERVE CELL INHIBITION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; RAT; SYNAPSE;

ANESTHESIA, GENERAL; ANESTHETICS, GENERAL; ANIMALS; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; INHIBITORY POSTSYNAPTIC POTENTIALS; NEURONS; RATS; RATS, WISTAR; SOMATOSENSORY CORTEX;

EID: 84883320270     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1748-13.2013     Document Type: Article

References (50)

1. Alitto HJ, Dan Y (2012) Cell-type-specific modulation of neocortical activity by basal forebrain input. Front Syst Neurosci 6:79. CrossRef Medline
2. Alkire MT, McReynolds JR, Hahn EL, Trivedi AN (2007) Thalamic microinjection of nicotine reverses sevoflurane-induced loss of righting reflex in the rat. Anesthesiology 107:264-272. CrossRef Medline
3. Antkowiak B (2002) In vitro networks: cortical mechanisms of anaesthetic action. Br J Anaesth 89:102-111. CrossRef Medline
4. Atallah BV, Bruns W, Carandini M, Scanziani M (2012) Parvalbuminexpressing interneurons linearly transform cortical responses to visual stimuli. Neuron 73:159-170. CrossRef Medline
5. Barthó P, Hirase H, Monconduit L, Zugaro M, Harris KD, Buzsáki G (2004) Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J Neurophysiol 92:600-608. CrossRef Medline
6. Beierlein M, Gibson JR, Connors BW (2003) Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90:2987-3000. CrossRef Medline
7. Bereshpolova Y, Stoelzel CR, Zhuang J, Amitai Y, Alonso JM, Swadlow HA (2011) Getting drowsy? Alert/nonalert transitions and visual thalamocortical network dynamics. J Neurosci 31:17480-17487. CrossRef Medline
8. Castro-Alamancos MA (2004) Absence of rapid sensory adaptation in neocortex during information processing states. Neuron 41:455-464. CrossRef Medline
9. Constantinople CM, BrunoRM (2011) Effects and mechanisms of wakefulness on local cortical networks. Neuron 69:1061-1068. CrossRef Medline
10. De Weese MR, Zador AM (2006) Non-Gaussian membrane potential dynamics imply sparse, synchronous activity in auditory cortex. J Neurosci 26:12206-12218. CrossRef Medline
11. Franks NP, Zecharia AY (2011) Sleep and general anesthesia. Can J Anaesth 58:139-148. CrossRef Medline
12. Friedberg MH, Lee SM, Ebner FF (1999) Modulation of receptive field properties of thalamic somatosensory neurons by the depth of anesthesia. J Neurophysiol 81:2243-2252. Medline
13. Gabernet L, Jadhav SP, Feldman DE, Carandini M, ScanzianiM (2005) Somatosensory integration controlled by dynamic thalamocortical feedforward inhibition. Neuron 48:315-327. CrossRef Medline
14. Gentet LJ, Avermann M, Matyas F, Staiger JF, Petersen CC (2010) Membrane potential dynamics of GABAergic neurons in the barrel cortex of behaving mice. Neuron 65:422-435. CrossRef Medline
15. Goard M, Dan Y (2009) Basal forebrain activation enhances cortical coding of natural scenes. Nat Neurosci 12:1444-1449. CrossRef Medline
16. González-Burgos G, Krimer LS, Povysheva NV, Barrionuevo G, Lewis DA (2005) Functional properties of fast spiking interneurons and their synaptic connections with pyramidal cells in primate dorsolateral prefrontal cortex. J Neurophysiol 93:942-953. Medline
17. Haider B, Häusser M, Carandini M (2013) Inhibition dominates sensory responses in the awake cortex. Nature 493:97-100. CrossRef Medline
18. Heiss JE, Katz Y, Ganmor E, Lampl I (2008) Shift in the balance between excitation and inhibition during sensory adaptation of S1 neurons. J Neurosci 28:13320-13330. CrossRef Medline
19. Hirata A, Castro-Alamancos MA (2010) Neocortex network activation and deactivation states controlled by the thalamus. J Neurophysiol 103:1147-1157. CrossRef Medline
20. Hromádka T, Deweese MR, Zador AM (2008) Sparse representation of sounds in the unanesthetized auditory cortex. PLoS Biol 6:e16. CrossRef Medline
21. Isaacson JS, Scanziani M (2011) How inhibition shapes cortical activity. Neuron 72:231-243. CrossRef Medline
22. Jameson LC, Sloan TB (2006) Using EEG to monitor anesthesia drug effects during surgery. J Clin Monit Comput 20:445-472. CrossRef Medline
23. Katz Y, Heiss JE, Lampl I (2006) Cross-whisker adaptation of neurons in the rat barrel cortex. J Neurosci 26:13363-13372. CrossRef Medline
24. Katz Y, Okun M, Lampl I (2012) Trial-to-trial correlation between thalamic sensory response and global EEG activity. Eur J Neurosci 35:826-837. CrossRef Medline
25. Keifer JC, Baghdoyan HA, Lydic R (1996) Pontine cholinergic mechanisms modulate the cortical electroencephalographic spindles of halothane anesthesia. Anesthesiology 84:945-954. CrossRef Medline
26. Litvak V, Sompolinsky H, Segev I, Abeles M (2003) On the transmission of rate code in long feedforward networks with excitatory-inhibitory balance. J Neurosci 23:3006-3015. Medline
27. Liu BH, Li YT, Ma WP, Pan CJ, Zhang LI, TaoHW (2011) Broad inhibition sharpens orientation selectivity by expanding input dynamic range in mouse simple cells. Neuron 71:542-554. CrossRef Medline
28. Mahon S, Deniau JM, Charpier S (2001) Relationship between EEG potentials and intracellular activity of striatal and cortico-striatal neurons: an in vivo study under different anesthetics. Cereb Cortex 11:360-373. CrossRef Medline
29. 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. CrossRef Medline
30. Müller CP, Pum ME, Amato D, Schüttler J, Huston JP, SilvaMA (2011) The in vivo neurochemistry of the brain during general anesthesia. J Neurochem 119:419-446. CrossRef Medline
31. Nishikawa K, MacIver MB (2000) Membrane and synaptic actions of halo-thane on rat hippocampal pyramidal neurons and inhibitory interneurons. J Neurosci 20:5915-5923. Medline
32. Okun M, Lampl I (2008) Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities. Nat Neurosci 11: 535-537. CrossRef Medline
33. Okun M, Naim A, Lampl I (2010) The subthreshold relation between cortical local field potential and neuronal firing unveiled by intracellular recordings in awake rats. J Neurosci 30:4440-4448. CrossRef Medline
34. Peña JL, Pérez-Perera L, Bouvier M, Velluti RA (1999) Sleep and wakefulness modulation of the neuronal firing in the auditory cortex of the guinea pig. Brain Res 816:463-470. CrossRef Medline
35. Poulet JF, Petersen CC (2008) Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 454:881-885. CrossRef Medline
36. Poulet JF, Fernandez LM, Crochet S, Petersen CC (2012) Thalamic control of cortical states. Nat Neurosci 15:370-372. CrossRef Medline
37. Priebe NJ, Ferster D (2006) Mechanisms underlying cross-orientation suppression in cat visual cortex. Nat Neurosci 9:552-561. CrossRef Medline
38. Rampil IJ (1998) A primer for EEG signal processing in anesthesia. Anesthesiology 89:980-1002. CrossRef Medline
39. Ries CR, Puil E (1999) Mechanism of anesthesia revealed by shunting actions of isoflurane on thalamocortical neurons. J Neurophysiol 81:1795-1801. Medline
40. Sakata S, Harris KD (2012) Laminar-dependent effects of cortical state on auditory cortical spontaneous activity. Front Neural Circuits 6:109. CrossRef Medline
41. + channel is a molecular substrate for neuronal effects of inhalation anesthetics. J Neurosci 20:6347-6354. Medline
42. Steriade M, McCormick DA, Sejnowski TJ (1993) Thalamocortical oscillations in the sleeping and aroused brain. Science 262:679-685. CrossRef Medline
43. Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85:1969-1985. Medline
44. Stoelzel CR, Bereshpolova Y, Swadlow HA (2009) Stability of thalamocortical synaptic transmission across awake brain states. J Neurosci 29:6851-6859. CrossRef Medline
45. Tahvildari B, Wölfel M, Duque A, McCormick DA (2012) Selective functional interactions between excitatory and inhibitory cortical neurons and differential contribution to persistent activity of the slow oscillation. J Neurosci 32:12165-12179. CrossRef Medline
46. Troyer TW, Krukowski AE, Priebe NJ, Miller KD (1998) Contrast-invariant orientation tuning in cat visual cortex: thalamocortical input tuning and correlation-based intracortical connectivity. J Neurosci 18:5908-5927. Medline
47. Tsodyks MV, Skaggs WE, Sejnowski TJ, McNaughton BL (1997) Paradoxical effects of external modulation of inhibitory interneurons. J Neurosci 17:4382-4388. Medline
48. van Vreeswijk C, Sompolinsky H (1996) Chaos in neuronal networks with balanced excitatory and inhibitory activity. Science 274:1724-1726. CrossRef Medline
49. Vijayan S, Hale GJ, Moore CI, Brown EN, Wilson M (2010) Activity in the barrel cortex during active behavior and sleep. J Neurophysiol 103:2074-2084. CrossRef Medline
50. Wehr M, ZadorAM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442-446. CrossRef Medline