Spike-timing control by dendritic plateau potentials in the presence of synaptic barrages

Frontiers in Computational Neuroscience

Volumn 8, Issue August, 2014, Pages

  Shai, Adam S ^a,b   Koch, Christof ^b   Anastassiou, Costas A ^b  

^a California Institute of Technology   (United States)

^b ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

Author keywords

Dendrites; Inhibition; Non linear dendrites; Plateau potentials; Spike timing

Indexed keywords

DENDRITES (METALLOGRAPHY); DEPOLARIZATION; ENZYME INHIBITION;

ELECTRICAL POTENTIAL; MODEL-BASED OPC; NON LINEAR; PLATEAU POTENTIALS; PYRAMIDAL NEURON; REALISTIC MODEL; SPIKE TIMING; SYNAPTIC INPUT;

DAMS;

CONDUCTANCE; DENDRITE; MODEL; SPIKE; SYNAPSE;

EID: 84979776568     PISSN: None     EISSN: 16625188     Source Type: Journal    
DOI: 10.3389/fncom.2014.00089     Document Type: Article

References (46)

1. 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. doi: 10.1002/jnr.22444
2. Ascoli, G. A., Alonso-Nanclares, L., Anderson, S. A., Barrionuevo, G., Benavides-Piccione, R., Burkhalter, A., et al. (2008). Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9, 557-568. doi: 10.1038/nrn2402
3. Burgess, N., Barry, C., and O'Keefe, J. (2007). An oscillatory interference model of grid cell firing. Hippocampus 17, 801-812. doi: 10.1002/hipo.20327
4. Buzsaki, G. (2010). Neural syntax: cell assemblies, synapsembles, and readers. Neuron 68, 362-385. doi: 10.1016/j.neuron.2010.09.023
5. Carnevale, N. T., and Hines, M. L. (2006). The NEURON Book. Cambridge: Cambridge University Press.
6. Cutsuridis, V., and Taxidis, J. (2013). Deciphering the role of CA1 inhibitory circuits in sharp wave-ripple complexes. Front. Syst. Neurosci. 7:13. doi: 10.3389/fnsys.2013.00013
7. Freund, T. F., and Buzsáki, G. (1996). Interneurons of the hippocampus. Hippocampus 6, 347-470.
8. Gidon, A., and Segev, I. (2012). Principles governing the operation of synaptic inhibition in dendrites. Neuron 75, 330-341. doi: 10.1016/j.neuron.2012.05.015
9. Hay, E., Hill, S., Schurmann, F., Markram, H., and Segev, I. (2011). Models of neocortical layer 5b pyramidal cells capturing a wide range of dendritic and perisomatic active properties. PLoS Comput. Biol. 7:e1002107. doi: 10.1371/journal.pcbi.1002107
10. Jadi, M., Polsky, A., Schiller, J., and Mel, B. W. (2012). Location-dependent effects of inhibition on local spiking in pyramidal neuron dendrites. PLoS Comput. Biol. 8:e1002550. doi: 10.1371/journal.pcbi.1002550
11. Jarsky, T., Roxin, A., Kath, W. L., and Spruston, N. (2005). Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nat. Neurosci. 8, 1667-1676. doi: 10.1038/nn1599
12. Kamondi, A., Acsady, L., Wang, X. J., and Buzsaki, G. (1998). Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus 8, 244-261.
13. Klausberger, T., and Somogyi, P. (2008). Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321, 53-57. doi: 10.1126/science.1149381
14. Koch, C. (1999). Biophysics of Computation, Information Processing in Single Neurons. New York, NY: Oxford University Press.
15. Larkum, M. E., Kaiser, K. M., and Sakmann, B. (1999). Calcium electrogenesis in distal apical dendrites of layer 5 pyramidal cells at a critical frequency of back-propagating action potentials. Proc. Natl. Acad. Sci. U.S.A. 96, 14600-14604. doi: 10.1073/pnas.96.25.14600
16. Larkum, M. E., Nevian, T., Sandler, M., Polsky, A., and Schiller, J. (2009). Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: a new unifying principle. Science 325, 756-760. doi: 10.1126/science.1171958
17. Larkum, M. E., Senn, W., and Luscher, H. R. (2004). Top-down dendritic input increases the gain of layer 5 pyramidal neurons. Cereb. Cortex 14, 1059-1070. doi: 10.1093/cercor/bhh065
18. Larkum, M. E., Waters, J., Sakmann, B., and Helmchen, F. (2007). Dendritic spikes in apical dendrites of neocortical layer 2/3 pyramidal neurons. J. Neurosci. 27, 8999-9008. doi: 10.1523/JNEUROSCI.1717-07.2007
19. Magee, J., Hoffman, D., Colbert, C., and Johnston, D. (1998). Electrical and calcium signaling in dendrites of hippocampal pyramidal neurons. Annu. Rev. Physiol. 60, 327-346. doi: 10.1146/annurev.physiol.60.1.327
20. Mainen, Z. F., and Sejnowski, T. J. (1996). Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382, 363-366. doi: 10.1038/382363a0
21. Markram, H., and Sakmann, B. (1994). Calcium transients in dendrites of neocortical neurons evoked by single subthreshold excitatory postsynaptic potentials via low-voltage-activated calcium channels. Proc. Natl. Acad. Sci. U.S.A. 91, 5207-5211. doi: 10.1073/pnas.91.11.5207
22. Marsalek, P., Koch, C., and Maunsell, J. (1997). On the relationship between synaptic input and spike output jitter in individual neurons. Proc. Natl. Acad. Sci. U.S.A. 94, 735-740. doi: 10.1073/pnas.94.2.735
23. Mel, B. (1992a). “The clusteron: toward a simple abstraction for a complex neuron,” in Advances in Neural Information Processing 4, eds J. E. Moody, S. J. Hanson, and R. P. Lippmann (Burlington, MA: Morgan-Kaufmann Publishers), 35-42.
24. Mel, B. W. (1992b). Nmda-based pattern-discrimination in a modeled cortical neuron. Neural Comput. 4, 502-517. doi: 10.1162/neco.1992.4.4.502
25. Metz, A. E., Spruston, N., and Martina, M. (2007). Dendritic D-type potassium currents inhibit the spike after depolarization in rat hippocampal CA1 pyramidal neurons. J. Physiol. 581, 175-187. doi: 10.1113/jphysiol.2006.127068
26. 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. 585, 447-468. doi: 10.1113/jphysiol.2007.142315
27. Mizuseki, K., Sirota, A., Pastalkova, E., and Buzsaki, G. (2009). Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 64, 267-280. doi: 10.1016/j.neuron.2009.08.037
28. Murayama, M., Perez-Garci, E., Nevian, T., Bock, T., Senn, W., and Larkum, M. E. (2009). Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature 457, 1137-1141. doi: 10.1038/nature07663
29. O'Keefe, J., and Recce, M. L. (1993). Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317-330. doi: 10.1002/hipo.450030307
30. Palmer, L. M., Schulz, J. M., Murphy, S. C., Ledergerber, D., Murayama, M., and Larkum, M. E. (2012). The cellular basis of GABA(B)-mediated interhemispheric inhibition. Science 335, 989-993. doi: 10.1126/science.1217276
31. Palmer, L. M., Shai, A. S., Reeve, J. E., Anderson, H. L., Paulsen, O., and Larkum, M. E. (2014). NMDA spikes enhance action potential generation during sensory input. Nat. Neurosci. 17, 383-390. doi: 10.1038/nn.3646
32. Papoutsi, A., Kastellakis, G., Psarrou, M., Anastasakis, S., and Poirazi, P. (2014). Coding and decoding with dendrites. J. Physiol. Paris. 108, 18-27. doi: 10.1016/j.jphysparis.2013.05.003
33. Pare, D., Shink, E., Gaudreau, H., Destexhe, A., and Lang, E. J. (1998). Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons In vivo. J. Neurophysiol. 79, 1450-1460.
34. Perez-Garci, E., Larkum, M. E., and Nevian, T. (2013). Inhibition of dendritic Ca2+ spikes by GABAB receptors in cortical pyramidal neurons is mediated by a direct Gi/o-beta-subunit interaction with Cav1 channels. J. Physiol. 591, 1599-1612. doi: 10.1113/jphysiol.2012.245464
35. Pinsky, P. F., and Rinzel, J. (1994). Intrinsic and network rhythmogenesis in a reduced Traub model for CA3 neurons. J. Comput. Neurosci. 1, 39-60. doi: 10.1007/BF00962717
36. Poirazi, P., Brannon, T., and Mel, B. (2003a). Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell. Neuron 37, 977-987. doi: 10.1016/S0896-6273(03)00148-X
37. Poirazi, P., Brannon, T., and Mel, B. (2003b). Pyramidal neuron as two-layer neural network. Neuron 37, 989-999. doi: 10.1016/S0896-6273(03)00149-1
38. Polsky, A., Mel, B. W., and Schiller, J. (2004). Computational subunits in thin dendrites of pyramidal cells. Nat. Neurosci. 7, 621-627. doi: 10.1038/nn1253
39. Pouille, F., and Scanziani, M. (2001). Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293, 1159-1163. doi: 10.1126/science.1060342
40. Remme, M. W., Lengyel, M., and Gutkin, B. S. (2010). Democracy-independence trade-off in oscillating dendrites and its implications for grid cells. Neuron 66, 429-437. doi: 10.1016/j.neuron.2010.04.027
41. Royer, S., Zemelman, B. V., Losonczy, A., Kim, J., Chance, F., Magee, J. C., et al. (2012). Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat. Neurosci. 15, 769-775. doi: 10.1038/nn.3077
42. Schiller, J., Schiller, Y., Stuart, G., and Sakmann, B. (1997). Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J. Physiol. 505, 605-616. doi: 10.1111/j.1469-7793.1997.605ba.x
43. Seamans, J. K., Gorelova, N. A., and Yang, C. R. (1997). Contributions of voltage-gated Ca2+ channels in the proximal versus distal dendrites to synaptic integration in prefrontal cortical neurons. J. Neurosci. 17, 5936-5948.
44. Su, H., Alroy, G., Kirson, E. D., and Yaari, Y. (2001). Extracellular calcium modulates persistent sodium current-dependent burst-firing in hippocampal pyramidal neurons. J. Neurosci. 21, 4173-4182.
45. Taxidis, J., Mizuseki, K., Mason, R., and Owen, M. R. (2013). Influence of slow oscillation on hippocampal activity and ripples through cortico-hippocampal synaptic interactions, analyzed by a cortical-CA3-CA1 network model. Front. Comput. Neurosci. 7:3. doi: 10.3389/fncom.2013.00003
46. Williams, S. R., and Stuart, G. J. (1999). Mechanisms and consequences of action potential burst firing in rat neocortical pyramidal neurons. J. Physiol. 521 Pt 2, 467-482. doi: 10.1111/j.1469-7793.1999.00467.x