Spines slow down dendritic chloride diffusion and affect short-term ionic plasticity of GABAergic inhibition

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Mohapatra, Namrata ^a   Tønnesen, Jan ^c,e   Vlachos, Andreas ^a   Kuner, Thomas ^d   Deller, Thomas ^a   Nägerl, U Valentin ^c,e   Santamaria, Fidel ^b   Jedlicka, Peter ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

^c CNRS   (France)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; CHLORIDE;

ANIMAL; BIOLOGICAL MODEL; BIOLOGY; BRAIN; DENDRITE; DENDRITIC SPINE; HUMAN; METABOLISM; PHYSIOLOGY; PROCEDURES; SYNAPTIC TRANSMISSION;

ANIMALS; BRAIN; CHLORIDES; COMPUTATIONAL BIOLOGY; DENDRITES; DENDRITIC SPINES; GAMMA-AMINOBUTYRIC ACID; HUMANS; MODELS, NEUROLOGICAL; SYNAPTIC TRANSMISSION;

EID: 84962576101     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep23196     Document Type: Article

References (60)

1. De Koninck, Y. Altered chloride homeostasis in neurological disorders: a new target. Curr. Opin. Pharmacol. 7, 93-99 (2007).
2. Fiumelli, H., Woodin, M. A. Role of activity-dependent regulation of neuronal chloride homeostasis in development. Curr. Opin. Neurobiol. 17, 81-86 (2007).
3. Blaesse, P., Airaksinen, M. S., Rivera, C., Kaila, K. Cation-Chloride Cotransporters and Neuronal Function. Neuron 61, 820-838 (2009).
4. Kaila, K., Price, T. J., Payne, J. A., Puskarjov, M., Voipio, J. Cation-chloride cotransporters in neuronal development, plasticity and disease. Nat Rev Neurosci 15, 637-654 (2014).
5. Santamaria, F., Wils, S., De Schutter, E., Augustine, G. J. Anomalous Diffusion in Purkinje Cell Dendrites Caused by Spines. Neuron 52, 635-648 (2006).
6. Santamaria, F., Wils, S., De Schutter, E., Augustine, G. J. The diffusional properties of dendrites depend on the density of dendritic spines. Eur. J. Neurosci. 34, 561-568 (2011).
7. Biess, A., Korkotian, E., Holcman, D. Barriers to diffusion in dendrites and estimation of calcium spread following synaptic inputs. PLoS Comput. Biol. 7, e1002182, doi: 10.1371/journal.pcbi.1002182 (2011).
8. Qian, N., Sejnowski, T. J. An electro-diffusion model for computing membrane potentials and ionic concentrations in branching dendrites, spines and axons. Biol. Cybern. 62, 1-15 (1989).
9. Qian, N., Sejnowski, T. J. When is an inhibitory synapse effective? Proc. Natl. Acad. Sci. USA 87, 8145-8149 (1990).
10. Kuner, T., Augustine, G. J. A genetically encoded ratiometric indicator for chloride: capturing chloride transients in cultured hippocampal neurons. Neuron 27, 447-459 (2000).
11. Duebel, J. et al. Two-photon imaging reveals somatodendritic chloride gradient in retinal ON-type bipolar cells expressing the biosensor clomeleon. Neuron 49, 81-94 (2006).
12. Berglund, K. et al. Imaging synaptic inhibition throughout the brain via genetically targeted Clomeleon. Brain Cell Biol. 36, 101-118 (2008).
13. Arosio, D., Ratto, G. M. Twenty years of fluorescence imaging of intracellular Chloride. Front. Cell. Neurosci. 8, doi: 10.3389/fncel.2014.00258 (2014).
14. Raimondo, J. V. et al. A genetically-encoded chloride and pH sensor for dissociating ion dynamics in the nervous system. Front. Cell. Neurosci. 7, 202, doi: 10.3389/fncel.2013.00202 (2013).
15. Jedlicka, P., Deller, T., Gutkin, B. S., Backus, K. H. Activity-dependent intracellular chloride accumulation and diffusion controls GABA A receptor-mediated synaptic transmission. Hippocampus 21, 885-898 (2011).
16. Doyon, N. et al. Efficacy of synaptic inhibition depends on multiple, dynamically interacting mechanisms implicated in chloride homeostasis. Plos Comput. Biol. 7, e1002149, doi: 10.1371/journal.pcbi.1002149 (2011).
17. Lewin, N., Aksay, E., Clancy, C. E. Computational Modeling Reveals Dendritic Origins of GABAA-Mediated Excitation in CA1 Pyramidal Neurons. Plos One 7, e47250, doi: 10.1371/journal.pone.0047250 (2012).
18. Bormann, J., Hamill, O. P., Sakmann, B. Mechanism of anion permeation through channels gated by glycine and gammaaminobutyric acid in mouse cultured spinal neurones. J. Physiol. 385, 243-286 (1987).
19. Kaila, K., Voipio, J. Postsynaptic fall in intracellular pH induced by GABA-activated bicarbonate conductance. Nature 330, 163-165 (1987).
20. Kaila, K., Pasternack, M., Saarikoski, J., Voipio, J. Influence of GABA-gated bicarbonate conductance on potential, current and intracellular chloride in crayfish muscle fibres. J. Physiol. 416, 161-181 (1989).
21. Staley, K. J., Soldo, B. L., Proctor, W. R. Ionic mechanisms of neuronal excitation by inhibitory GABAA receptors. Science 269, 977-981 (1995).
22. Staley, K. J., Proctor, W. R. Modulation of mammalian dendritic GABA(A) receptor function by the kinetics of Cl? and HCO3? transport. J. Physiol. 519, 693-712 (1999).
23. Backus, K. H., Deitmer, J. W., Friauf, E. Glycine-activated currents are changed by coincident membrane depolarization in developing rat auditory brainstem neurones. J. Physiol. 507, 783-794 (1998).
24. Jedli?ka, P., Backus, K. H. Inhibitory transmission, activity-dependent ionic changes and neuronal network oscillations. Physiol. Res. 55, 139-149 (2006).
25. Wright, R., Raimondo, J. V., Akerman, C. J. Spatial and temporal dynamics in the ionic driving force for GABA(A) receptors. Neural Plast. 2011, 728395, doi: 10.1155/2011/728395 (2011).
26. Raimondo, J. V., Markram, H., Akerman, C. J. Short-term ionic plasticity at GABAergic synapses. Front. Synaptic Neurosci. 4, 5, doi: 10.3389/fnsyn.2012.00005 (2012).
27. Mohapatra, N., Deans, H. T., Santamaria, F., Jedlicka, P. Modeling ion concentrations. In Encyclopedia of Computational Neuroscience (eds Jaeger, D., Jung, R.) 1-6 (Springer New York) doi: 10.1007/978-1-4614-7320-6-239-2 (2014).
28. Hepburn, I., Chen, W., Wils, S., De Schutter, E. STEPS: efficient simulation of stochastic reaction-diffusion models in realistic morphologies. BMC Syst. Biol. 6, 36, doi: 10.1186/1752-0509-6-36 (2012).
29. Chen, W., De Schutter, E. Python-based geometry preparation and simulation visualization toolkits for STEPS. Front. Neuroinform. 8, 37, doi: 10.3389/fninf.2014.00037 (2014).
30. Holcman, D., Schuss, Z. Diffusion laws in dendritic spines. J. Math. Neurosci. 1, 10, doi: 10.1186/2190-8567-1-10 (2011).
31. Tonnesen, J., Katona, G., Rózsa, B., Nägerl, U. V. Spine neck plasticity regulates compartmentalization of synapses. Nat. Neurosci. 17, 678-85 (2014).
32. Tonnesen, J., Nägerl, U. V. Two-color STED imaging of synapses in living brain slices. Methods Mol. Biol. 950, 65-80 (2013).
33. Trommald, M., Hulleberg, G. Dimensions and density of dendritic spines from rat dentate granule cells based on reconstructions from serial electron micrographs. J. Comp. Neurol. 377, 15-28 (1997).
34. Kleinhans, C., Kafitz, K. W., Rose, C. R. Diffusion of sodium signals in spiny dendrites. Poster T7-10A presented at 11th Göttingen Meeting of the German Neuroscience Society:35th Göttingen Neurobiology Conference, Göttingen. Neuroforum: Springer. (2015).
35. Hrabetová, S., Hrabe, J., Nicholson, C. Dead-space microdomains hinder extracellular diffusion in rat neocortex during ischemia. J. Neurosci. 23, 8351-8359 (2003).
36. Syková, E., Nicholson, C. Diffusion in brain extracellular space. Physiol. Rev. 88, 1277-1340 (2008).
37. Jedlicka, P., Vlachos, A., Schwarzacher, S. W., Deller, T. A role for the spine apparatus in LTP and spatial learning. Behav. Brain Res. 192, 12-19 (2008).
38. Glykys, J. et al. Local impermeant anions establish the neuronal chloride concentration. Science 343, 670-5 (2014).
39. Luhmann, H. J., Kirischuk, S., Kilb, W. Comment on 'Local impermeant anions establish the neuronal chloride concentration'. Science 345, 1130, doi: 10.1126/science.1255337 (2014).
40. Voipio, J. et al. Comment on 'Local impermeant anions establish the neuronal chloride concentration'. Science 345, 1130, doi: 10.1126/science.1252978 (2014).
41. Holcman, D., Yuste, R. The new nanophysiology: regulation of ionic flow in neuronal subcompartments. Nat. Rev. Neurosci. 16, 685-692, doi: 10.1038/nrn4022 (2015).
42. Govindarajan, A., Israely, I., Huang, S. Y., Tonegawa, S. The Dendritic Branch Is the Preferred Integrative Unit for Protein Synthesis-Dependent LTP. Neuron 69, 132-146 (2011).
43. Huberfeld, G. et al. Perturbed chloride homeostasis and GABAergic signaling in human temporal lobe epilepsy. J. Neurosci. 27, 9866-9873 (2007).
44. Tornberg, J., Voikar, V., Savilahti, H., Rauvala, H., Airaksinen, M. S. Behavioural phenotypes of hypomorphic KCC2-deficient mice. Eur. J. Neurosci. 21, 1327-1337 (2005).
45. MacKenzie, G., Maguire, J. Chronic stress shifts the GABA reversal potential in the hippocampus and increases seizure susceptibility. Epilepsy Res. 109, 13-27 (2015).
46. Kalkman, H. O. Alterations in the expression of neuronal chloride transporters may contribute to schizophrenia. Prog. Neuro-Psychopharmacology Biol. Psychiatry 35, 410-414, doi: 10.1016/j.pnpbp.2011.01.004 (2011).
47. Lamsa, K., Taira, T. Use-Dependent Shift From Inhibitory to Excitatory GABAA Receptor Action in SP-O Interneurons in the Rat Hippocampal CA3 Area. J. Neurophysiol. 90, 1983-1995 (2003).
48. Gulyás, A. I., Sík, A., Payne, J. A., Kaila, K., Freund, T. F. The KCl cotransporter, KCC2, is highly expressed in the vicinity of excitatory synapses in the rat hippocampus. Eur. J. Neurosci. 13, 2205-2217 (2001).
49. Fiumelli, H. et al. An Ion Transport-Independent Role for the Cation-Chloride Cotransporter KCC2 in Dendritic Spinogenesis In Vivo. Cereb. Cortex 23, 378-388 (2013).
50. Hines, M. L., Carnevale, N. T. Expanding NEURON's repertoire of mechanisms with NMODL. Neural Comput. 12, 995-1007 (2000).
51. Megias, M., Emri, Z., Freund, T. F., Gulyas, A. I. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102, 527-540 (2001).
52. Kaila, K. Ionic basis of GABAA receptor channel function in the nervous system. Prog. Neurobiol. 42, 489-537 (1994).
53. Santhakumar, V., Aradi, I., Soltesz, I. Role of mossy fiber sprouting and mossy cell loss in hyperexcitability: a network model of the dentate gyrus incorporating cell types and axonal topography. J. Neurophysiol. 93, 437-53 (2005).
54. Schmidt-Hieber, C., Jonas, P., Bischofberger, J. Subthreshold dendritic signal processing and coincidence detection in dentate gyrus granule cells. J. Neurosci. 27, 8430-8441 (2007).
55. Golding, N. L., Mickus, T. J., Katz, Y., Kath, W. L., Spruston, N. Factors mediating powerful voltage attenuation along CA1 pyramidal neuron dendrites. J. Physiol. 568, 69-82 (2005).
56. Lenz, M. et al. Repetitive magnetic stimulation induces plasticity of excitatory postsynapses on proximal dendrites of cultured mouse CA1 pyramidal neurons. Brain Struct. Funct. 220, 3323-3337, doi: 10.1007/s00429-014-0859-9 (2014).
57. Tonnesen, J., Nadrigny, F., Willig, K. I., Wedlich-Söldner, R., Nägerl, U. V. Two-color STED microscopy of living synapses using a single laser-beam pair. Biophys. J. 101, 2545-2552 (2011).
58. Schmid, B., Schindelin, J., Cardona, A., Longair, M., Heisenberg, M. A high-level 3D visualization API for Java and ImageJ. BMC Bioinformatics 11, 274, doi: 10.1186/1471-2105-11-274 (2010).
59. Schmidt-Hieber, C., Bischofberger, J. Fast sodium channel gating supports localized and efficient axonal action potential initiation. J. Neurosci. 30, 10233-10242 (2010).
60. Vuksic, M. et al. 3D-reconstruction and functional properties of GFP-positive and GFP-negative granule cells in the fascia dentata of the Thy1-GFP mouse. Hippocampus 18, 364-375 (2008).