Activity-dependent mismatch between axo-axonic synapses and the axon initial segment controls neuronal output

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 31, 2015, Pages 9757-9762

  Wefelmeyer, Winnie ^a   Cattaert, Daniel ^b   Burrone, Juan ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Axon initial segment; Chandelier cells; Homeostatic plasticity; Intrinsic plasticity; Optogenetics

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; CHANNELRHODOPSIN 2; RHODOPSIN; UNCLASSIFIED DRUG; CHANNELRHODOPSIN 2, RAT; VESICULAR INHIBITORY AMINO ACID TRANSPORTER;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AXON INITIAL SEGMENT; BRAIN SLICE; CONTROLLED STUDY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; INTERNEURON; MALE; MATHEMATICAL MODEL; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NERVE FIBER; NONHUMAN; OPTOGENETICS; PERINATAL PERIOD; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPSE; ANIMAL; BIOLOGICAL MODEL; CHANNEL GATING; DOWN REGULATION; HIPPOCAMPUS; LIGHT; METABOLISM; PHYSIOLOGY; RADIATION RESPONSE; SPRAGUE DAWLEY RAT; TRANSGENIC MOUSE;

RATTUS;

ACTION POTENTIALS; ANIMALS; AXONS; DOWN-REGULATION; HIPPOCAMPUS; ION CHANNEL GATING; LIGHT; MALE; MICE, TRANSGENIC; MODELS, NEUROLOGICAL; OPTOGENETICS; PYRAMIDAL CELLS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; RHODOPSIN; SYNAPSES; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 84938613444     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1502902112     Document Type: Article

References (43)

1. Debanne D, Campanac E, Bialowas A, Carlier E, Alcaraz G (2011) Axon physiology. Physiol Rev 91(2):555-602.
2. Bender KJ, Trussell LO (2012) The physiology of the axon initial segment. Annu Rev Neurosci 35:249-265.
3. Yoshimura T, Rasband MN (2014) Axon initial segments: Diverse and dynamic neuronal compartments. Curr Opin Neurobiol 27:96-102.
4. Grubb MS, et al. (2011) Short- and long-term plasticity at the axon initial segment. J Neurosci 31(45):16049-16055.
5. Grubb MS, Burrone J (2010) Building and maintaining the axon initial segment. Curr Opin Neurobiol 20(4):481-488.
6. Inan M, Anderson SA (2014) The chandelier cell, form and function. Curr Opin Neurobiol 26:142-148.
7. Somogyi P, Freund TF, Cowey A (1982) The axo-axonic interneuron in the cerebral cortex of the rat, cat and monkey. Neuroscience 7(11):2577-2607.
8. Somogyi P, Nunzi MG, Gorio A, Smith AD (1983) A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells. Brain Res 259(1):137-142.
9. Taniguchi H, Lu J, Huang ZJ (2013) The spatial and temporal origin of chandelier cells in mouse neocortex. Science 339(6115):70-74.
10. Zitman FM, et al. (2014) Dentate gyrus local circuit is implicated in learning under stress-A role for neurofascin. Mol Neurobiol, 10.1007/s12035-014-9044-7.
11. Viney TJ, et al. (2013) Network state-dependent inhibition of identified hippocampal CA3 axo-axonic cells in vivo. Nat Neurosci 16(12):1802-1811.
12. Molnár G, et al. (2008) Complex events initiated by individual spikes in the human cerebral cortex. PLoS Biol 6(9):e222.
13. Dugladze T, Schmitz D, Whittington MA, Vida I, Gloveli T (2012) Segregation of axonal and somatic activity during fast network oscillations. Science 336(6087): 1458-1461.
14. Woodruff AR, Anderson SA, Yuste R (2010) The enigmatic function of chandelier cells. Front Neurosci 4:201.
15. Woodruff AR, et al. (2011) State-dependent function of neocortical chandelier cells. J Neurosci 31(49):17872-17886.
16. Evans MD, et al. (2013) Calcineurin signaling mediates activity-dependent relocation of the axon initial segment. J Neurosci 33(16):6950-6963.
17. Grubb MS, Burrone J (2010) Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability. Nature 465(7301):1070-1074.
18. Kuba H, Oichi Y, Ohmori H (2010) Presynaptic activity regulates Na(+) channel distribution at the axon initial segment. Nature 465(7301):1075-1078.
19. Muir J, Kittler JT (2014) Plasticity of GABAA receptor diffusion dynamics at the axon initial segment. Front Cell Neurosci 8:151.
20. Chand AN, Galliano E, Chesters RA, Grubb MS (2015) A distinct subtype of dopaminergic interneuron displays inverted structural plasticity at the axon initial segment. J Neurosci 35(4):1573-1590.
21. Somogyi P (1977) A specific 'axo-axonal' interneuron in the visual cortex of the rat. Brain Res 136(2):345-350.
22. Nusser Z, Sieghart W, Benke D, Fritschy JM, Somogyi P (1996) Differential synaptic localization of two major gamma-aminobutyric acid type A receptor alpha subunits on hippocampal pyramidal cells. Proc Natl Acad Sci USA 93(21):11939-11944.
23. Inan M, et al. (2013) Dense and overlapping innervation of pyramidal neurons by chandelier cells. J Neurosci 33(5):1907-1914.
24. King AN, Manning CF, Trimmer JS (2014) A unique ion channel clustering domain on the axon initial segment of mammalian neurons. J Comp Neurol 522(11):2594-2608.
25. Thome C, et al. (2014) Axon-carrying dendrites convey privileged synaptic input in hippocampal neurons. Neuron 83(6):1418-1430.
26. Stell BM, Mody I (2002) Receptors with different affinities mediate phasic and tonic GABA(A) conductances in hippocampal neurons. J Neurosci 22(10):RC223.
27. Semyanov A (2003) Cell type specificity of GABA(A) receptor mediated signaling in the hippocampus. Curr Drug Targets CNS Neurol Disord 2(4):240-247.
28. Wlodarczyk AI, et al. (2013) GABA-independent GABAA receptor openings maintain tonic currents. J Neurosci 33(9):3905-3914.
29. Royeck M, et al. (2008) Role of axonal NaV1.6 sodium channels in action potential initiation of CA1 pyramidal neurons. J Neurophysiol 100(4):2361-2380.
30. Misonou H, et al. (2006) Bidirectional activity-dependent regulation of neuronal ion channel phosphorylation. J Neurosci 26(52):13505-13514.
31. Misonou H, Trimmer JS (2004) Determinants of voltage-gated potassium channel surface expression and localization in Mammalian neurons. Crit Rev Biochem Mol Biol 39(3):125-145.
32. Tseng WC, Jenkins PM, Tanaka M, Mooney R, Bennett V (2015) Giant ankyrin-G stabilizes somatodendritic GABAergic synapses through opposing endocytosis of GABAA receptors. Proc Natl Acad Sci USA 112(4):1214-1219.
33. Karmarkar UR, Buonomano DV (2006) Different forms of homeostatic plasticity are engaged with distinct temporal profiles. Eur J Neurosci 23(6):1575-1584.
34. Maffei A, Nataraj K, Nelson SB, Turrigiano GG (2006) Potentiation of cortical inhibition by visual deprivation. Nature 443(7107):81-84.
35. Hartman KN, Pal SK, Burrone J, Murthy VN (2006) Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons. Nat Neurosci 9(5):642-649.
36. Sayin U, Osting S, Hagen J, Rutecki P, Sutula T (2003) Spontaneous seizures and loss of axo-axonic and axo-somatic inhibition induced by repeated brief seizures in kindled rats. J Neurosci 23(7):2759-2768.
37. Dinocourt C, Petanjek Z, Freund TF, Ben-Ari Y, Esclapez M (2003) Loss of interneurons innervating pyramidal cell dendrites and axon initial segments in the CA1 region of the hippocampus following pilocarpine-induced seizures. J Comp Neurol 459(4): 407-425.
38. Kress GJ, Dowling MJ, Meeks JP, Mennerick S (2008) High threshold, proximal initiation, and slow conduction velocity of action potentials in dentate granule neuron mossy fibers. J Neurophysiol 100(1):281-291.
39. Meeks JP, Mennerick S (2007) Action potential initiation and propagation in CA3 pyramidal axons. J Neurophysiol 97(5):3460-3472.
40. Schmidt-Hieber C, Jonas P, Bischofberger J (2008) Action potential initiation and propagation in hippocampal mossy fibre axons. J Physiol 586(7):1849-1857.
41. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37(2):173-182.
42. Madisen L, et al. (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13(1):133-140.
43. Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9(6):1179-1209.