Dendritic Ca2+ responses in neonatal lateral superior olive neurons elicited by glycinergic/GABAergic synapses and action potentials

Neuroscience

Volumn 154, Issue 1, 2008, Pages 338-345

  Kullmann, P H M ^a   Kandler, K ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b University of Pittsburgh School of Medicine   (United States)

Author keywords

action potential; auditory; back propagation; confocal imaging; dendritic spikes; development

Indexed keywords

CALCIUM ION; TETRODOTOXIN; 4 AMINOBUTYRIC ACID; CALCIUM; GLYCINE; LOCAL ANESTHETIC AGENT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CALCIUM CELL LEVEL; CALCIUM METABOLISM; CELLULAR DISTRIBUTION; CONCENTRATION (PARAMETERS); CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DENDRITE; EVOKED AUDITORY RESPONSE; GABAERGIC SYSTEM; INHIBITION KINETICS; MOLECULAR IMAGING; MOUSE; NERVE POTENTIAL; NEUROBIOLOGY; NEUROCHEMISTRY; NEWBORN; NONHUMAN; PERCEPTIVE THRESHOLD; PRIORITY JOURNAL; RAT; SUPERIOR OLIVARY NUCLEUS; SYNAPSE; SYNAPTIC POTENTIAL; WAVEFORM; ACTION POTENTIAL; ANIMAL; C57BL MOUSE; CONFOCAL MICROSCOPY; CYTOLOGY; DRUG EFFECT; ELECTROSTIMULATION; IN VITRO STUDY; METABOLISM; METHODOLOGY; NERVE CELL; NERVE TRACT; OLIVARY NUCLEUS; PATCH CLAMP; PHYSIOLOGY; PONS; RADIATION EXPOSURE; RADIATION RESPONSE; SPRAGUE DAWLEY RAT;

ACTION POTENTIALS; ANESTHETICS, LOCAL; ANIMALS; ANIMALS, NEWBORN; CALCIUM; DENDRITES; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; GAMMA-AMINOBUTYRIC ACID; GLYCINE; MICE; MICE, INBRED C57BL; MICROSCOPY, CONFOCAL; NEURAL PATHWAYS; NEURONS; OLIVARY NUCLEUS; PATCH-CLAMP TECHNIQUES; PONS; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; TETRODOTOXIN;

EID: 44749086493     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.02.026     Document Type: Article

References (49)

1. Balakrishnan V., Becker M., Löhrke S., Nothwang H.G., Güresir E., and Friauf E. Expression and function of chloride transporters during development of inhibitory neurotransmission in the auditory brainstem. J Neurosci 23 (2003) 4134-4145
2. Bi G., and Poo M. Synaptic modification by correlated activity: Hebb's postulate revisited. Annu Rev Neurosci 24 (2001) 139-166
3. Blaesse P., Guillemin I., Schindler J., Schweizer M., Delpire E., Khiroug L., Friauf E., and Nothwang H.G. Oligomerization of KCC2 correlates with development of inhibitory neurotransmission. J Neurosci 26 (2006) 10407-10419
4. Boudreau J.C., and Tsuchitani C. Binaural interaction in the cat superior olive S segment. J Neurophysiol 31 (1968) 442-454
5. Caird D., and Klinke R. Processing of binaural stimuli by cat superior olivary complex neurons. Exp Brain Res 52 (1983) 385-399
6. Cant N.B., and Casseday J.H. Projections from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei. J Comp Neurol 247 (1986) 457-476
7. Doucet J.R., and Ryugo D.K. Axonal pathways to the lateral superior olive labeled with biotinylated dextran amine injections in the dorsal cochlear nucleus of rats. J Comp Neurol 461 (2003) 452-465
8. Ehrlich I., Lohrke S., and Friauf E. Shift from depolarizing to hyperpolarizing glycine action in rat auditory neurones is due to age-dependent Cl- regulation. J Physiol 520 Pt 1 (1999) 121-137
9. Gillespie D.C., Kim G., and Kandler K. Inhibitory synapses in the developing auditory system are glutamatergic. Nat Neurosci 8 (2005) 332-338
10. Glendenning K.K., Hutson K.A., Nudo R.J., and Masterton R.B. Acoustic chiasm II: Anatomical basis of binaurality in the lateral superior olive of the cat. J Comp Neurol 232 (1985) 261-285
11. Goldberg J.H., Lacefield C.O., and Yuste R. Global dendritic calcium spikes in mouse layer 5 low threshold spiking interneurones: implications for control of pyramidal cell bursting. J Physiol 558 (2004) 465-478
12. Henkel C.K., and Gabriele M.L. Organization of the disynaptic pathway from the anteroventral cochlear nucleus to the lateral superior olivary nucleus in the ferret. Anat Embryol (Berl) 199 (1999) 149-160
13. Kakazu Y., Akaike N., Komiyama S., and Nabekura J. Regulation of intracellular chloride by cotransporters in developing lateral superior olive neurons. J Neurosci 19 (1999) 2843-2851
14. Kandler K. Activity-dependent organization of inhibitory circuits: lessons from the auditory system. Curr Opin Neurobiol 14 (2004) 96-104
15. Kandler K., and Friauf E. Pre- and postnatal development of efferent connections of the cochlear nucleus in the rat. J Comp Neurol 328 (1993) 161-184
16. Kandler K., and Friauf E. Development of glycinergic and glutamatergic synaptic transmission in the auditory brainstem of perinatal rats. J Neurosci 15 (1995) 6890-6904
17. Kim G., and Kandler K. Elimination and strengthening of glycinergic/GABAergic connections during tonotopic map formation. Nat Neurosci 6 (2003) 282-290
18. Kotak V.C., Korada S., Schwartz I.R., and Sanes D.H. A developmental shift from GABAergic to glycinergic transmission in the central auditory system. J Neurosci 18 (1998) 4646-4655
19. Kotak V.C., and Sanes D.H. Deafferentation weakens excitatory synapses in the developing central auditory system. Eur J Neurosci 9 (1997) 2340-2347
20. Kotak V.C., and Sanes D.H. Long-lasting inhibitory synaptic depression is age- and calcium-dependent. J Neurosci 20 (2000) 5820-5826
21. Kullmann P.H., Ene F.A., and Kandler K. Glycinergic and GABAergic calcium responses in the developing lateral superior olive. Eur J Neurosci 15 (2002) 1093-1104
22. Kullmann P.H., and Kandler K. Glycinergic/GABAergic synapses in the lateral superior olive are excitatory in neonatal C57Bl/6J mice. Brain Res Dev Brain Res 131 (2001) 143-147
23. Kuwabara N., and Zook J.M. Classification of the principal cells of the medial nucleus of the trapezoid body. J Comp Neurol 314 (1991) 707-720
24. Lohmann C., Finski A., and Bonhoeffer T. Local calcium transients regulate the spontaneous motility of dendritic filopodia. Nat Neurosci 8 (2005) 305-312
25. LoTurco J.J., Owens D.F., Heath M.J., Davis M.B., and Kriegstein A.R. GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15 (1995) 1287-1298
26. Magee J., Hoffman D., Colbert C., and Johnston D. Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons [review]. Annu Rev Physiol 60 (1998) 327-346
27. Markram H., Helm P.J., and Sakmann B. Dendritic calcium transients evoked by single back-propagating action potentials in rat neocortical pyramidal neurons. J Physiol (Lond) 485 (1995) 1-20
28. 2+ transients evoked by action potentials in rat dorsal cochlear nucleus pyramidal and cartwheel neurons. J Neurophysiol 89 (2003) 2225-2237
29. Nabekura J., Katsurabayashi S., Kakazu Y., Shibata S., Matsubara A., Jinno S., Mizoguchi Y., Sasaki A., and Ishibashi H. Developmental switch from GABA to glycine release in single central synaptic terminals. Nat Neurosci 7 (2004) 17-23
30. 2+ elevating to depressing. J Neurosci 15 (1995) 5065-5077
31. Regehr W.G., and Tank D.W. Calcium concentration dynamics produced by synaptic activation of CA1 hippocampal pyramidal cells. J Neurosci 12 (1992) 4202-4223
32. Rietzel H.J., and Friauf E. Neuron types in the rat lateral superior olive and developmental changes in the complexity of their dendritic arbors. J Comp Neurol 390 (1998) 20-40
33. Rozsa B., Zelles T., Vizi E.S., and Lendvai B. Distance-dependent scaling of calcium transients evoked by backpropagating spikes and synaptic activity in dendrites of hippocampal interneurons. J Neurosci 24 (2004) 661-670
34. Sanes D.H., and Friauf E. Development and influence of inhibition in the lateral superior olivary nucleus. Hear Res 147 (2000) 46-58
35. Sanes D.H., Markowitz S., Bernstein J., and Wardlow J. The influence of inhibitory afferents on the development of postsynaptic dendritic arbors. J Comp Neurol 321 (1992) 637-644
36. Sanes D.H., and Rubel E.W. The ontogeny of inhibition and excitation in the gerbil lateral superior olive. J Neurosci 8 (1988) 682-700
37. Sanes D.H., Song J., and Tyson J. Refinement of dendritic arbors along the tonotopic axis of the gerbil lateral superior olive. Dev Brain Res 67 (1992) 47-55
38. Sanes D.H., and Siverls V. Development and specificity of inhibitory terminal arborizations in the central nervous system. J Neurobiol 8 (1991) 837-854
39. Sanes D.H., and Takacs C. Activity-dependent refinement of inhibitory connections. Eur J Neurosci 5 (1993) 570-574
40. Scott L.L., Hage T.A., and Golding N.L. Weak action potential backpropagation is associated with high-frequency axonal firing capability in principal neurons of the gerbil medial superior olive. J Physiol 583 (2007) 647-661
41. Sjostrom P.J., and Nelson S.B. Spike timing, calcium signals and synaptic plasticity. Curr Opin Neurobiol 12 (2002) 305-314
42. Smith P.H., Joris P.X., Carney L.H., and Yin T.C. Projections of physiologically characterized globular bushy cell axons from the cochlear nucleus of the cat. J Comp Neurol 304 (1991) 387-407
43. Spangler K.M., Warr W.B., and Henkel C.K. The projections of principal cells of the medial nucleus of the trapezoid body in the cat. J Comp Neurol 238 (1985) 249-262
44. Svoboda K., Denk W., Kleinfeld D., and Tank D.W. In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385 (1997) 161-165
45. Thompson A.M., and Thompson G.C. Efferent projections from posteroventral cochlear nucleus to lateral superior olive in guinea pig. Brain Res 421 (1987) 382-386
46. Tollin D.J. The lateral superior olive: a functional role in sound source localization. Neuroscientist 9 (2003) 127-143
47. Warr W.B. Fiber degeneration following lesions in the multipolar and globular cell areas in the ventral cochlear nucleus of the cat. Brain Res 40 (1972) 247-270
48. Yuste R., and Denk W. Dendritic spines as basic functional units of neuronal integration. Nature 375 (1995) 682-684
49. 2+ accumulations in dendrites of neocortical pyramidal neurons: an apical band and evidence for two functional compartments. Neuron 13 (1994) 23-43