Extrasynaptic glutamate receptor activation as cellular bases for dynamic range compression in pyramidal neurons

Frontiers in Physiology

Volumn 3 AUG, Issue , 2012, Pages

  Oikonomou, Katerina D ^a   Short, Shaina M ^a   Rich, Matthew T ^a   Antic, Srdjan D ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Dendritic spike; Prefrontal cortex; Pyramidal neuron; Synaptic integration; Voltage sensitive dye

Indexed keywords

EID: 84866492697     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00334     Document Type: Article

References (78)

1. Acker, C. D., and Antic, S. D. (2009). Quantitative assessment of the distributions of membrane conductances involved in action potential backpropagation along Basal dendrites. J. Neurophysiol. 101, 1524-1541.
2. Antic, S., Major, G., and Zecevic, D. (1999). Fast optical recordings of membrane potential changes from dendrites of pyramidal neurons. J. Neurophysiol. 82, 1615-1621.
3. Antic, S. D. (2003). Action potentials in basal and oblique dendrites of rat neocortical pyramidal neurons. J. Physiol. (Lond.) 550, 35-50.
4. Antic, S. D., Acker, C. D., Zhou, W. L., Moore, A. R., and Milojkovic, B. A. (2007). The role of dendrites in the maintenance of the UP state, in Mechanisms of Spontaneous Active States in the Neocortex, ed. I. Tim-ofeev (Kerala: Research Signpost), 45-72.
5. Antic, S. D., Zhou, W. L., Moore, A. R., Short, S. M., and Ikonomu, K. D. (2010). The decade of the dendritic NMDA spike. J. Neurosci. Res. 88, 2991-3001.
6. Ariav, G., Polsky, A., and Schiller, J. (2003). Submillisecond precision of the input-output transformation function mediated by fast sodium dendritic spikes in basal dendrites of CA1 pyramidal neurons. J. Neurosci. 23, 7750-7758.
7. Asztely, F., Erdemli, G., and Kullmann, D. M. (1997). Extrasynaptic gluta-mate spillover in the hippocampus: dependence on temperature and the role of active glutamate uptake. Neuron 18, 281-293.
8. Ballesteros-Yanez, I., Benavides-Piccione, R., Elston, G. N., Yuste, R., and DeFelipe, J. (2006). Density and morphology of dendritic spines in mouse neocortex. Neuroscience 138, 403-409.
9. Bekkers, J. M. (2000). Properties of voltage-gated potassium currents innucleated patches from large layer 5 cortical pyramidal neurons of the rat. J. Physiol. 3, 593-609
10. Benavides-Piccione, R., Hamzei-Sichani, F., Ballesteros-Yanez, I., DeFelipe, J., and Yuste, R. (2006). Dendritic size of pyramidal neurons differs among mouse cortical regions. Cereb. Cortex 16, 990-1001.
11. Benucci, A., Verschure, P. F., and Konig, P. (2004). Two-state membrane potential fluctuations driven by weak pairwise correlations. Neural Comput. 16, 2351-2378.
12. Branchereau, P., Van Bockstaele, E. J., Chan, J., and Pickel, V. M. (1996). Pyramidal neurons in rat prefrontal cortex show a complex synaptic response to single electrical stimulation of the locus coeruleus region: evidence for antidromic activation and GABAergic inhibition using in vivo intracellular recording and electron microscopy. Synapse 22, 313-331.
13. Branco, T., and Hausser, M. (2011). Synaptic integration gradients in single cortical pyramidal cell den-drites. Neuron 69, 885-892.
14. Cai, X., Liang, C. W., Muralidharan, S., Kao, J. P., Tang, C. M., and Thompson, S. M. (2004). Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron 44, 351-364.
15. Campbell, S., and Hablitz, J. J. (2005). Modification of epileptiform discharges in neocortical neurons following glutamate uptake inhibition. Epilepsia 46(SUPPL. 5), 129-133.
16. Cash, S., and Yuste, R. (1999). Linear summation of excitatory inputs by CA1 pyramidal neurons. Neuron 22, 383-394.
17. Chalifoux,J.R.,and Carter,A.G. (2011). Glutamate spillover promotes the generation of NMDA spikes. J. Neu-rosci. 31, 16435-16446.
18. Clatworthy, P. L., Chirimuuta, M., Lau-ritzen, J. S., and Tolhurst, D. J.(2003). Coding of the contrasts in natural images by populations of neurons in primary visual cortex (V1). Vision Res. 43, 1983-2001.
19. Contreras, D., Durmuller, N., and Ste-riade, M. (1997). Plateau potentials in cat neocortical association cells in vivo: synaptic control of dendritic excitability. Eur. J. Neurosci. 9, 2588-2595.
20. Cowan, R. L., and Wilson, C. J. (1994). Spontaneous firing patterns and axonal projections of single corti-costriatal neurons in the rat medial agranular cortex. J. Neurophysiol. 71, 17-32.
21. De-Miguel, F. F., and Fuxe, K. (2012). Extrasynaptic neurotransmission as a way of modulating neuronal functions. Front. Physiol. 3:16. doi:10.3389/fphys.2012.00016
22. Dodt, H. U., Frick, A., Kampe, K., and Zieglgansberger, W. (1998). NMDA and AMPA receptors on neocorti-cal neurons are differentially distributed. Eur. J. Neurosci. 10, 3351-3357.
23. Elston, G. N. (2003). Cortex, cognition and the cell: new insights into the pyramidal neuron and pre-frontal function. Cereb. Cortex 13, 1124-1138.
24. Enoki, R., Kiuchi,T., Koizumi,A., Sasaki, G., Kudo, Y., and Miyakawa, H. (2004). NMDA receptor-mediated depolarizing after-potentials in the basal dendrites of CA1 pyramidal neurons. Neurosci. Res. 48, 325-333.
25. Gasparini, S., Migliore, M., and Magee, J. C. (2004). On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. J. Neurosci. 24, 11046-11056.
26. Geisler, W. S., and Albrecht, D. G. (1995). Bayesian analysis of identification performance in monkey visual cortex: nonlinear mechanisms and stimulus certainty. Vision Res. 35, 2723-2730.
27. Harris, A. Z., and Pettit, D. L. (2007). Extrasynaptic and synaptic NMDA receptors form stable and uniform pools in rat hippocampal slices. J. Physiol. (Lond.) 584, 509-519.
28. Herman, M. A., Nahir, B., and Jahr, C. E. (2011). Distribution of extracellular glutamate in the neuropil of hippocampus. PLoS ONE 6, e26501. doi:10.1371/journal.pone.0026501
29. Hodgkin,A.L.,and Huxley,A.F. (1952). A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. (Lond.) 117, 500-544.
30. Holthoff, K., Kovalchuk, Y., Yuste, R., and Konnerth, A. (2004). Single-shock LTD by local dendritic spikes in pyramidal neurons of mouse visual cortex. J. Physiol. (Lond.) 560, 27-36.
31. Jia, H., Rochefort, N. L., Chen, X., and Konnerth, A. (2010). Dendritic organization of sensory input to cortical neurons in vivo. Nature 464, 1307-1312.
32. Jourdain, P., Bergersen, L. H., Bhaukau-rally, K., Bezzi, P., Santello, M., Domercq, M., Matute, C., Tonello, F., Gundersen, V., and Volterra, (2007). Glutamate exocytosis from astrocytes controls synap- tic strength. Nat. Neurosci. 10, 331-339.
33. Kampa, B. M., and Stuart, G. J. (2006). Calcium spikes in basal dendrites of layer 5 pyramidal neurons during action potential bursts. J. Neurosci. 26, 7424-7432.
34. Katona, G., Kaszas, A., Turi, G. F., Hajos, N., Tamas, G., Vizi, E. S., and Rozsa, (2011). Roller Coaster Scanning reveals spontaneous triggering of dendritic spikes in CA1 interneu- rons. Proc. Natl. Acad. Sci. U.S.A. 108, 2148-2153.
35. Kleindienst, T., Winnubst, J., Roth-Alpermann, C., Bonhoeffer, T., and Lohmann, C. (2011). Activity-dependent clustering of functional synaptic inputs on developing hip-pocampal dendrites. Neuron 72, 1012-1024.
36. Korngreen, A., and Sakmann,B. (2000). Voltage-gated K+ channels in layer 5 neocortical pyramidal neurones from young rats: subtypes and gradients. J. Physiol. 3, 621-639.
37. Kullmann, D. M., Min, M. Y., Asztely, F., and Rusakov, D. A. (1999). Extracellular glutamate diffusion determines the occupancy of gluta-mate receptors at CA1 synapses in the hippocampus. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354, 395-402.
38. Kurashige, H., and Cateau, H. (2011). Dendritic slow dynamics enables localized cortical activity to switch between mobile and immobile modes with noisy background input. PLoS ONE 6, e24007. doi:10.1371/journal.pone.0024007
39. Larkman, A. U. (1991). Dendritic morphology of pyramidal neurones of the visual cortex of the rat: III. Spine distributions. J. Comp. Neurol. 306, 332-343.
40. Larkum, M. E., and Nevian, T. (2008). Synaptic clustering by dendritic signalling mechanisms. Curr. Opin. Neurobiol. 18, 321-331.
41. Larkum, M. E., Nevian, T., Sandler, M., Polsky, A., and Schiller, J. (2009). Synaptic integration in tuft den-dritesof layer 5pyramidal neurons: a new unifying principle. Science 325, 756-760.
42. Lewis, B. L., and O'Donnell, P. (2000). Ventral tegmental area afferents to the prefrontal cortex maintain membrane potential 'up' states in pyramidal neurons via D(1) dopamine receptors. Cereb. Cortex 10, 1168-1175.
43. London,M.,andSegev,I. (2001).Synap-tic scaling in vitro and in vivo. Nat. Neurosci. 4, 853-855.
44. Losonczy, A., Makara, J. K., and Magee, J. C. (2008). Compartmentalized dendritic plasticity and input feature storage in neurons. Nature 452, 436-441.
45. Magee, J. C. (2011). Observations on clustered synaptic plasticity and highly structured input patterns. Neuron 72, 887-888.
46. Major, G., Polsky, A., Denk, W., Schiller, J., and Tank, D. W. (2008). Spatiotemporally graded NMDA spike/plateau potentials in basal dendrites of neocortical pyramidal neurons. J. Neurophysiol. 99, 2584-2601.
47. Mayer, M. L., Westbrook, G. L., and Guthrie, P. B. (1984). Voltage-dependent block by Mg2+ of NMDAresponsesinspinalcord neurones. Nature 309, 261-263.
48. Milojkovic, B. A., Radojicic, M. S., and Antic, S. D. (2005a). A strict correlation between dendritic and somatic plateau depolarizations in the rat prefrontal cortex pyramidal neurons. J. Neurosci. 25, 3940-3951.
49. Milojkovic, B. A., Wuskell, J. P., Loew, L. M., and Antic, S. D. (2005b). Initia-tionof sodium spikeletsinbasal den-drites of neocortical pyramidal neurons. J. Membr. Biol. 208, 155-169.
50. Milojkovic, B. A., Radojicic, M. S., Goldman-Rakic, P. S., and Antic, S. D. (2004). Burst generation in rat pyramidal neurones byregenera-tive potentials elicited in a restricted part of the basilar dendritic tree. J. Physiol. (Lond.) 558, 193-211.
51. Milojkovic, B. A., Zhou, W. L., and Antic, S. D. (2007). Voltage and calcium transients in basal dendrites of the rat prefrontal cortex. J. Physiol. (Lond.) 585, 447-468.
52. Min, R., and Nevian, T. (2012). Astro-cyte signaling controls spike timing-dependent depression at neocortical synapses.Nat. Neurosci.15, 746-753.
53. Moore, A. R., Zhou, W. L., Potapenko, E. S., Kim, E. J., and Antic, S. D. (2011). Brief dopaminergic stimulations produce transient physiological changes in prefrontal pyramidal neurons. Brain Res. 1370, 1-15.
54. Morita, K. (2008). Possible role of dendritic compartmentalization in the spatial working memory circuit. J. Neurosci. 28, 7699-7724.
55. Nimchinsky, E. A., Yasuda, R., Oert-ner, T. G., and Svoboda, K. (2004). The number of glutamate receptors opened by synaptic stimulation in single hippocampal spines. J. Neu-rosci. 24, 2054-2064.
56. Nizami, L. (2005). Dynamic range relations for auditory primary afferents. Hear. Res. 208, 26-46.
57. Nowak, L., Bregestovski, P., Ascher, P., Herbet, A., and Prochiantz, A. (1984). Magnesium gatesglutamate-activated channels in mouse central neurones. Nature 307, 462-465.
58. Oakley, J. C., Schwindt, P. C., and Crill, W. E. (2001). Dendritic calcium spikes in layer 5 pyramidal neurons amplify and limit transmission of ligand-gated dendritic current to soma. J. Neurophysiol. 86, 514-527.
59. Parpura, V., Basarsky, T. A., Liu, F., Jef-tinija, K., Jeftinija, S., and Haydon, P. G. (1994). Glutamate-mediated astrocyte-neuron signalling. Nature 369, 744-747.
60. Persi, E., Hansel, D., Nowak, L., Barone, P., and van Vreeswijk, C. (2011). Power-law input-outputtransfer functions explain the contrast-response and tuning properties of neurons in visual cortex. PLoS Comput. Biol. 7, e1001078. doi:10.1371/journal.pcbi.1001078
61. Poirazi, P., Brannon, T., and Mel, B. W. (2003). Pyramidal neuron as two-layer neural network. Neuron 37, 989-999.
62. Polsky,A., Mel, B., and Schiller,J. (2009). Encoding and decoding bursts by NMDA spikes in basal dendrites of layer 5 pyramidal neurons. J. Neu-rosci. 29, 11891-11903.
63. Polsky, A., Mel, B. W., and Schiller, J. (2004). Computational subunits in thin dendrites of pyramidal cells. Nat. Neurosci. 7, 621-627.
64. Remy, S., Csicsvari, J., and Beck, H. (2009). Activity-dependent control of neuronal output by local and global dendritic spike attenuation. Neuron 61, 906-916.
65. Rhodes, P. (2006). The properties and implications of NMDA spikes in neocortical pyramidal cells. J. Neu-rosci. 26, 6704-6715.
66. Schaefer, A. T., Helmstaedter, M., Schmitt, A. C., Bar-Yehuda, D., Almog, M., Ben-Porat, H., Sak-mann, B., and Korngreen,A. (2007). Dendritic voltage-gated K+ conductance gradient in pyramidal neurones of neocortical layer 5B from rats. J. Physiol. (Lond.) 579, 737-752.
67. Schiller, J., Helmchen, F., and Sakmann, B. (1995). Spatial profile of dendritic calcium transients evoked by action potentials in rat neocortical pyramidal neurones. J. Physiol. 487, 583-600.
68. Schiller, J., Major, G., Koester, H. J., and Schiller, Y. (2000). NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 404, 285-289.
69. Suzuki, T., Kodama, S., Hoshino, C., Izumi, T., and Miyakawa, H. (2008). A plateau potential mediated by the activation of extrasynaptic NMDA receptors in rat hippocampal CA1 pyramidal neurons. Eur. J. Neurosci. 28, 521-534.
70. Swadlow, H. A., and Hicks, T. P. (1997). Subthreshold receptive fields and baseline excitability of silent S1 callosal neurons in awake rabbits: contributions of AMPA/kainate and NMDA receptors. Exp. Brain Res. 115, 403-409.
71. Timofeev, I., Grenier, F., and Steriade, M. (2001). Disfacilitation and active inhibition in the neocortex during the natural sleep-wake cycle: an intracellular study. Proc. Natl. Acad. Sci. U.S.A. 98, 1924-1929.
72. Tovar, K. R., and Westbrook, G. L. (1999). The incorporation of NMDA receptors withadistinct sub-unit composition at nascent hip-pocampal synapses in vitro. J. Neu-rosci. 19, 4180-4188.
73. Varga, Z.,Jia,H., Sakmann, B.,and Kon-nerth, A. (2011). Dendritic coding of multiple sensory inputs in single cortical neurons in vivo. Proc. Natl. Acad. Sci. U.S.A. 108, 15420-15425.
74. Waters, J., and Helmchen, F. (2004). Boosting of action potential back-propagation by neocortical network activity in vivo. J. Neurosci. 24, 11127-11136.
75. Wei, D. S., Mei, Y. A., Bagal, A., Kao, J. P., Thompson, S. M., and Tang, C. M. (2001). Compartmentalized and binary behavior of terminal dendritesinhippocampal pyramidal neurons. Science 293, 2272-2275.
76. Wilson, C. J., and Kawaguchi,Y. (1996). The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J. Neurosci. 16, 2397-2410.
77. Yasuda, R., Sabatini, B. L., and Svo-boda,K. (2003). Plasticity of calcium channels in dendritic spines. Nat. Neurosci. 6, 948-955.
78. Zhou, W. L., Yan, P., Wuskell, J. P., Loew, L. M., and Antic, S. D. (2008). Dynamics of action potential back-propagation in basal dendrites of prefrontal cortical pyramidal neurons. Eur. J. Neurosci. 27, 1-14.