A distinct subtype of dopaminergic interneuron displays inverted structural plasticity at the axon initial segment

Journal of Neuroscience

Volumn 35, Issue 4, 2015, Pages 1573-1590

  Chand, Annisa N ^a   Galliano, Elisa ^a   Chesters, Robert A ^a   Grubb, Matthew S ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Axon initial segment; Dopamine; Interneuron; Olfactory bulb; Plasticity

Indexed keywords

ANKYRIN; CALCINEURIN; CALCIUM CHANNEL L TYPE; CELL ADHESION MOLECULE; CYCLIN DEPENDENT KINASE 5; NEUROFASCIN; NIFEDIPINE; ROSCOVITINE; SODIUM CHANNEL; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG; PHOTOPROTEIN; SODIUM CHANNEL BLOCKING AGENT; TETRODOTOXIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AXON INITIAL SEGMENT; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; CURRENT CLAMP TECHNIQUE; DOPAMINERGIC ACTIVITY; ELECTROPHYSIOLOGICAL PROCEDURES; IMAGE ANALYSIS; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; MOUSE; NERVE CELL PLASTICITY; NERVE FIBER; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; ANIMAL; ANIMAL EMBRYO; C57BL MOUSE; CELL CULTURE; CLASSIFICATION; CYTOLOGY; DOPAMINERGIC NERVE CELL; DRUG EFFECTS; FEMALE; GENETICS; MALE; METABOLISM; NEWBORN; PHYSIOLOGY; TRANSGENIC MOUSE; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; AXONS; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE 5; DOPAMINERGIC NEURONS; EMBRYO, MAMMALIAN; FEMALE; LUMINESCENT PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONAL PLASTICITY; OLFACTORY BULB; RATS; RATS, WISTAR; SODIUM CHANNEL BLOCKERS; TETRODOTOXIN; TYROSINE 3-MONOOXYGENASE;

EID: 84921903236     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3515-14.2015     Document Type: Article

References (93)

1. Adam Y, Mizrahi A (2011) Long-term imaging reveals dynamic changes in the neuronal composition of the glomerular layer. J Neurosci 31:7967–7973.CrossRef Medline
2. Akritas MG (1990) The rank transform method in some two-factor designs. J Am Stat Assoc 85:73–78. CrossRef
3. Baalman KL, Cotton RJ, Rasband SN, Rasband MN (2013) Blast wave exposure impairs memory and decreases axon initial segment length. J Neurotrauma 30:741–751.CrossRef Medline
4. Baker H (1986) Species differences in the distribution of substance P and tyrosine hydroxylase immunoreactivity in the olfactory bulb. J Comp Neurol 252:206–226. CrossRef Medline
5. Baker H, Kawano T, Margolis FL, Joh TH (1983) Transneuronal regulation of tyrosine hydroxylase expression in olfactory bulb of mouse and rat. J Neurosci 3:69–78. Medline
6. Banerjee K, Akiba Y, Baker H, Cave JW (2013) Epigenetic control of neurotransmitter expression in olfactory bulb interneurons. Int J Dev Neurosci 31:415–423. CrossRef Medline
7. Baranauskas G, David Y, Fleidervish IA (2013) Spatial mismatch between the Na+flux and spike initiation in axon initial segment. Proc Natl Acad Sci U S A 110:4051–4056. CrossRef Mesdline
8. Bastien-Dionne PO, David LS, Parent A, Saghatelyan A (2010) Role of sensory activity on chemospecific populations of interneurons in the adult olfactory bulb. J Comp Neurol 518:1847–1861. CrossRef Medline
9. Bean BP (2007) The action potential in mammalian central neurons. Nat Rev Neurosci 8:451–465. CrossRef Medline
10. Bender KJ, Trussell LO (2012) The physiology of the axon initial segment. Annu Rev Neurosci 35:249–265. CrossRef Medline
11. Borisovska M, Bensen AL, Chong G, Westbrook GL (2013) Distinct modes of dopamine and GABA release in a dual transmitter neuron. J Neurosci 33:1790–1796. CrossRef Medline
12. Buffington SA, Rasband MN (2011) The axon initial segment in nervous system disease and injury. Eur J Neurosci 34:1609–1619. CrossRef Medline
13. Cave JW, Akiba Y, Banerjee K, Bhosle S, Berlin R, Baker H (2010) Differential regulation of dopaminergic gene expression by Er81. J Neurosci 30: 4717–4724. CrossRef Medline
14. Chen JL, Lin WC, Cha JW, So PT, Kubota Y, Nedivi E (2011) Structural basis for the role of inhibition in facilitating adult brain plasticity. Nat Neurosci 14:587–594. CrossRef Medline
15. Cigola E, Volpe BT, Lee JW, Franzen L, Baker H (1998) Tyrosine hydroxylase expression in primary cultures of olfactory bulb: role of L-type calcium channels. J Neurosci 18:7638–7649. Medline
16. Clark BD, Goldberg EM, Rudy B (2009) Electrogenic tuning of the axon initial segment. Neuroscientist 15:651–668. CrossRef Medline
17. Coombs JS, Curtis DR, Eccles JC (1957) The generation of impulses in motoneurones. J Physiol 139:232–249. Medline
18. Ennis M, Zhou FM, Ciombor KJ, Aroniadou-Anderjaska V, Hayar A, Borrelli E, Zimmer LA, Margolis F, Shipley MT (2001) Dopamine D2 receptormediated presynaptic inhibition of olfactory nerve terminals. J Neurophysiol 86:2986–2997. Medline
19. Evans MD, Sammons RP, Lebron S, Dumitrescu AS, Watkins TBK, Uebele VN, Renger JJ, Grubb MS (2013) Calcineurin signaling mediates activity-dependent relocation of the axon initial segment. J Neurosci 33: 6950–6963. CrossRef Medline
20. Eyal G, Mansvelder HD, de Kock CPJ, Segev I (2014) Dendrites impact the encoding capabilities of the axon. J Neurosci 34:8063–8071. CrossRef Medline
21. Frias CP, Wierenga CJ (2013) Activity-dependent adaptations in inhibitory axons. Front Cell Neurosci 7:219. CrossRef Medline
22. Garrido JJ, Giraud P, Carlier E, Fernandes F, Moussif A, Fache MP, Debanne D, Dargent B (2003) A targeting motif involved in sodium channel clustering at the axonal initial segment. Science 300:2091–2094. CrossRef Medline
23. Grace AA, Bunney BS (1983) Intracellular and extracellular electrophysiology of nigral dopaminergic neurons–2. Action potential generating mechanisms and morphological correlates. Neuroscience 10:317–331. CrossRef Medline
24. Grubb MS, Burrone J (2010a) Building and maintaining the axon initial segment. Curr Opin Neurobiol 20:481–488. CrossRef Medline
25. Grubb MS, Burrone J (2010b) Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability. Nature 465:1070–1074. CrossRef Medline
26. Grubb MS, Shu Y, Kuba H, Rasband MN, Wimmer VC, Bender KJ (2011) Short- and long-term plasticity at the axon initial segment. J Neurosci 31:16049–16055. CrossRef Medline
27. Gründemann J, Häusser M (2010) Neuroscience: A plastic axonal hotspot. Nature 465:1022–1023. CrossRef Medline
28. Halász N, Johansson O, Hökfelt T, Ljungdahl A, Goldstein M (1981) Immunohistochemical identification of two types of dopamine neuron in the rat olfactory bulb as seen by serial sectioning. J Neurocytol 10:251–259. CrossRef Medline
29. Hartman KN, Pal SK, Burrone J, Murthy VN (2006) Activity-dependent regulation of inhibitory synaptic transmission in hippocampal neurons. Nat Neurosci 9:642–649. CrossRef Medline
30. Harty RC, Kim TH, Thomas EA, Cardamone L, Jones NC, Petrou S, Wimmer VC (2013) Axon initial segment structural plasticity in animal models of genetic and acquired epilepsy. Epilepsy Res 105:272–279. CrossRef Medline
31. Häusser M, Stuart G, Racca C, Sakmann B (1995) Axonal initiation and active dendritic propagation of action potentials in substantia nigra neurons. Neuron 15:637–647. CrossRef Medline
32. Hedstrom KL, Ogawa Y, Rasband MN (2008) AnkyrinG is required for maintenance of the axon initial segment and neuronal polarity. J Cell Biol 183:635–640. CrossRef Medline
33. Henny P, Brown MTC, Northrop A, Faunes M, Ungless MA, Magill PJ, Bolam JP (2012) Structural correlates of heterogeneous in vivo activity of midbrain dopaminergic neurons. Nat Neurosci 15:613–619. CrossRef Medline
34. Hoogland PV, Huisman E (1999) Tyrosine hydroxylase immunoreactivestructures in the aged human olfactory bulb and olfactory peduncle. J Chem Neuroanat 17:153–161. CrossRef Medline
35. Hsia AY, Vincent JD, Lledo PM (1999) Dopamine depresses synaptic inputs into the olfactory bulb. J Neurophysiol 82:1082–1085. Medline
36. Jenerick H (1963) Phase plane trajectories of the muscle spike potential. Biophys J 3:363–377. CrossRef Medline
37. Kaphzan H, Buffington SA, Jung JI, Rasband MN, Klann E (2011) Alterations in intrinsic membrane properties and the axon initial segment in a mouse model of Angelman syndrome. J Neurosci 31:17637–17648. CrossRef Medline
38. Kaphzan H, Buffington SA, Ramaraj AB, Lingrel JB, Rasband MN, Santini E, Klann E (2013) Genetic reduction of the _1 subunit of Na/K-ATPase corrects multiple hippocampal phenotypes in Angelman syndrome. Cell Rep 4:405–412. CrossRef Medline
39. Keck T, Mrsic-Flogel TD, Vaz Afonso M, Eysel UT, Bonhoeffer T, Hübener M (2008) Massive restructuring of neuronal circuits during functional reorganization of adult visual cortex. Nat Neurosci 11:1162–1167. CrossRef Medline
40. Keck T, Scheuss V, Jacobsen RI, Wierenga CJ, Eysel UT, Bonhoeffer T, Hübener M (2011) Loss of sensory input causes rapid structural changes of inhibitory neurons in adult mouse visual cortex. Neuron 71:869–882. CrossRef Medline
41. Khaliq ZM, Raman IM (2006) Relative contributions of axonal and somatic Na channels to action potential initiation in cerebellar Purkinje neurons. J Neurosci 26:1935–1944. CrossRef Medline
42. Kilman V, van Rossum MCW, Turrigiano GG (2002) Activity deprivation reduces miniature IPSC amplitude by decreasing the number of postsynaptic GABAA receptors clustered at neocortical synapses. J Neurosci 22: 1328–1337. Medline
43. Kiyokage E, Pan YZ, Shao Z, Kobayashi K, Szabo G, Yanagawa Y, Obata K, Okano H, Toida K, Puche AC, Shipley MT (2010) Molecular identity of periglomerular and short axon cells. J Neurosci 30:1185–1196. CrossRef Medline
44. Klausberger T, Somogyi P (2008) Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321:53–57. CrossRef Medline
45. Kole MHP, Stuart GJ (2012) Signal processing in the axon initial segment. Neuron 73:235–247. CrossRef Medline
46. Kosaka T, Kosaka K (2009) Two types of tyrosine hydroxylase positive GABAergic juxtaglomerular neurons in the mouse main olfactory bulb are different in their time of origin. Neurosci Res 64:436–441. CrossRef Medline
47. Kosaka T, Kosaka K (2011) “Interneurons” in the olfactory bulb revisited. Neurosci Res 69:93–99. CrossRef Medline
48. Kosaka T, Komada M, Kosaka K (2008) Sodium channel cluster, betaIVspectrin and ankyrinG positive “hot spots” on dendritic segments of parvalbumin-containing neurons and some other neurons in the mouse and rat main olfactory bulbs. Neurosci Res 62:176–186. CrossRef Medline
49. Kuba H, Ishii TM, Ohmori H (2006) Axonal site of spike initiation enhances auditory coincidence detection. Nature 444:1069–1072. CrossRef Medline
50. Kuba H, Oichi Y, Ohmori H (2010) Presynaptic activity regulates Na(+) channel distribution at the axon initial segment. Nature 465:1075–1078.CrossRef Medline
51. Kuba H, Adachi R, Ohmori H (2014) Activity-dependent and activityindependent development of the axon initial segment. J Neurosci 34: 3443–3453. CrossRef Medline
52. Lammel S, Lim BK, Malenka RC (2014) Reward and aversion in a heterogeneous midbrain dopamine system. Neuropharmacology 76:351–359. CrossRef Medline
53. Lee TS, Kaku T, Takebayashi S, Uchino T, Miyamoto S, Hadama T, Perez- Reyes E, Ono K (2006) Actions of mibefradil, efonidipine and nifedipine block of recombinant T- and L-type Ca channels with distinct inhibitory mechanisms. Pharmacology 78:11–20. CrossRef Medline
54. Lemaillet G, Walker B, Lambert S (2003) Identification of a conserved ankyrin-binding motif in the family of sodium channel alpha subunits. J Biol Chem 278:27333–27339. CrossRef Medline
55. Lindeberg J, Usoskin D, Bengtsson H, Gustafsson A, Kylberg A, Söderström S, Ebendal T (2004) Transgenic expression of Cre recombinase from the tyrosine hydroxylase locus. Genesis 40:67–73. CrossRef Medline
56. Liu S, Plachez C, Shao Z, Puche A, Shipley MT (2013) Olfactory bulb short axon cell release of GABA and dopamine produces a temporally biphasic inhibition-excitation response in external tufted cells. J Neurosci 33: 2916–2926. CrossRef Medline
57. Livneh Y, Feinstein N, Klein M, Mizrahi A (2009) Sensory input enhances synaptogenesis of adult-born neurons. J Neurosci 29:86–97. CrossRef Medline
58. Lledo PM, Alonso M, Grubb MS (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7:179–193. CrossRef Medline
59. Lorincz A, Nusser Z (2008) Cell-type-dependent molecular composition of the axon initial segment. J Neurosci 28:14329–14340. CrossRef Medline
60. MacAskill AF, Kittler JT (2010) Control of mitochondrial transport and localization in neurons. Trends Cell Biol 20:102–112. CrossRef Medline
61. Maher BJ, Westbrook GL (2008) Co-transmission of dopamine and GABA in periglomerular cells. J Neurophysiol 99:1559–1564. CrossRef Medline
62. Marik SA, Yamahachi H, McManus JNJ, Szabo G, Gilbert CD (2010) Axonal dynamics of excitatory and inhibitory neurons in somatosensory cortex. PLoS Biol 8:e1000395. CrossRef Medline
63. McGann JP (2013) Presynaptic inhibition of olfactory sensory neurons: new mechanisms and potential functions. Chem Senses 38:459–474. CrossRef Medline
64. McGann JP, Pírez N, Gainey MA, Muratore C, Elias AS, Wachowiak M (2005) Odorant representations are modulated by intra- but not interglomerular presynaptic inhibition of olfactory sensory neurons. Neuron 48:1039–1053. CrossRef Medline
65. Mizrahi A (2007) Dendritic development and plasticity of adult-born neurons in the mouse olfactory bulb. Nat Neurosci 10:444–452. Medline
66. Mizrahi A, Katz LC (2003) Dendritic stability in the adult olfactory bulb. Nat Neurosci 6:1201–1207. CrossRef Medline
67. Muir J, Kittler JT (2014) Plasticity ofGABAAreceptor diffusion dynamics at the axon initial segment. Front Cell Neurosci 8:151. Medline
68. O’Leary T, van Rossum MCW, Wyllie DJA (2010) Homeostasis of intrinsic excitability in hippocampal neurones: dynamics and mechanism of the response to chronic depolarization. J Physiol 588:157–170. CrossRef Medline
69. Panzanelli P, Fritschy JM, Yanagawa Y, Obata K, Sassoé-Pognetto M (2007) GABAergic phenotype of periglomerular cells in the rodent olfactory bulb. J Comp Neurol 502:990–1002. CrossRef Medline
70. Parrish-Aungst S, Kiyokage E, Szabo G, Yanagawa Y, Shipley MT, Puche AC (2011) Sensory experience selectively regulates transmitter synthesis enzymes in interglomerular circuits. Brain Res 1382:70–76. CrossRef Medline
71. Pignatelli A, Kobayashi K, Okano H, Belluzzi O (2005) Functional properties of dopaminergic neurones in the mouse olfactory bulb. J Physiol 564:501–514. CrossRef Medline
72. Pignatelli A, Ackman JB, Vigetti D, Beltrami AP, Zucchini S, Belluzzi O (2009) A potential reservoir of immature dopaminergic replacement neurons in the adult mammalian olfactory bulb. Pflugers Arch 457:899–915. CrossRef Medline
73. Puopolo M, Bean BP, Raviola E (2005) Spontaneous activity of isolated dopaminergic periglomerular cells of the main olfactory bulb. J Neurophysiol 94:3618–3627. CrossRef Medline
74. RasbandMN (2010) The axon initial segment and the maintenance of neuronal polarity. Nat Rev Neurosci 11:552–562. CrossRef Medline
75. Roeper J (2013) Dissecting the diversity of midbrain dopamine neurons. Trends Neurosci 36:336–342. CrossRef Medline
76. Saghatelyan A, Roux P, Migliore M, Rochefort C, Desmaisons D, Charneau P, Shepherd GM, Lledo PM (2005) Activity-dependent adjustments of the inhibitory network in the olfactory bulb following early postnatal deprivation. Neuron 46:103–116. CrossRef Medline
77. Sawada M, Kaneko N, Inada H, Wake H, Kato Y, Yanagawa Y, Kobayashi K, Nemoto T, Nabekura J, Sawamoto K (2011) Sensory input regulates spatial and subtype-specific patterns of neuronal turnover in the adult olfactory bulb. J Neurosci 31:11587–11596. CrossRef Medline
78. Serguera C, Triaca V, Kelly-Barrett J, Banchaabouchi MA, Minichiello L (2008) Increased dopamine after mating impairs olfaction and prevents odor interference with pregnancy. Nat Neurosci 11:949–956. CrossRef Medline
79. Shepherd GM (2004) The synaptic organization of the brain. Oxfordm UK: Oxford UP.
80. Shu Y, Duque A, Yu Y, Haider B, McCormick DA (2007) Properties of action-potential initiation in neocortical pyramidal cells: evidence fromwhole cell axon recordings. J Neurophysiol 97:746–760. CrossRef Medline
81. Smith RL, Baker H, Kolstad K, Spencer DD, Greer CA (1991) Localization of tyrosine hydroxylase and olfactory marker protein immunoreactivities in the human and macaque olfactory bulb. Brain Res 548:140–148. CrossRef Medline
82. Song AH, Wang D, Chen G, Li Y, Luo J, Duan S, Poo MM (2009) A selective filter for cytoplasmic transport at the axon initial segment. Cell 136:1148–1160. CrossRef Medline
83. Trombley PQ, Westbrook GL (1990) Excitatory synaptic transmission in cultures of rat olfactory bulb. J Neurophysiol 64:598–606. Medline
84. Trunova S, Baek B, Giniger E (2011) Cdk5 regulates the size of an axon initial segment-like compartment in mushroom body neurons of the Drosophila central brain. J Neurosci 31:10451–10462. CrossRef Medline
85. Tucker KR, Huertas MA, Horn JP, Canavier CC, Levitan ES (2012) Pacemaker rate and depolarization block in nigral dopamine neurons: a somatic sodium channel balancing act. J Neurosci 32:14519–14531. CrossRef Medline
86. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391:892–896. CrossRef Medline
87. Vest RS, Davies KD, O’Leary H, Port JD, Bayer KU (2007) Dual mechanism of a natural CaMKII inhibitor. Mol Biol Cell 18:5024–5033. CrossRef Medline
88. Wang L, Wang H, Yu L, Chen Y (2011) Role of axonal sodium-channel band in neuronal excitability. Phys Rev E Stat Nonlin Soft Matter Phys 84: 052901. CrossRef Medline
89. Wei CJ, Linster C, Cleland TA (2006) Dopamine D(2) receptor activation modulates perceived odor intensity. Behav Neurosci 120:393–400. CrossRef Medline
90. Whitesell JD, Sorensen KA, Jarvie BC, Hentges ST, Schoppa NE (2013) Interglomerular lateral inhibition targeted on external tufted cells in the olfactory bulb. J Neurosci 33:1552–1563. CrossRef Medline
91. Yamahachi H, Marik SA, McManus JNJ, Denk W, Gilbert CD (2009) Rapid axonal sprouting and pruning accompany functional reorganization in primary visual cortex. Neuron 64:719–729. CrossRef Medline
92. Zhou D, Lambert S, Malen PL, Carpenter S, Boland LM, Bennett V (1998) AnkyrinG is required for clustering of voltage-gated Na channels at axon initial segments and for normal action potential firing. J Cell Biol 143: 1295–1304. CrossRef Medline
93. Zonta B, Desmazieres A, Rinaldi A, Tait S, Sherman DL, Nolan MF, Brophy PJ (2011) A critical role for Neurofascin in regulating action potential initiation through maintenance of the axon initial segment. Neuron 69:945–956. CrossRef Medline