Dendritic Na+ spikes enable cortical input to drive action potential output from hippocampal CA2 pyramidal neurons

eLife

Volumn 3, Issue November, 2014, Pages 1-24

  Sun, Qian ^a   Srinivas, Kalyan V ^a   Sotayo, Alaba ^a   Siegelbaum, Steven A ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ARTICLE; BIOLOGY; BRAIN ELECTROPHYSIOLOGY; COMPUTER SIMULATION; DENDRITIC SPINE; DEPOLARIZATION; ELECTRIC POTENTIAL; ELECTROSTIMULATION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPUS; IMMUNOCYTOCHEMISTRY; PYRAMIDAL NERVE CELL;

EID: 84936120895     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.04551     Document Type: Article

References (61)

1. Ariav G, Polsky A, Schiller J. 2003. Submillisecond precision of the input-output transformation function mediated by fast sodium dendritic spikes in basal dendrites of CA1 pyramidal neurons. The Journal of Neuroscience 23:7750-7758.
2. Bartesaghi R, Gessi T. 2004. Parallel activation of field CA2 and dentate gyrus by synaptically elicited perforant path volleys. Hippocampus 14:948-963. doi: 10.1002/hipo.20011.
3. Bartesaghi R, Migliore M, Gessi T. 2006. Input-output relations in the entorhinal cortex-dentate-hippocampal system: evidence for a non-linear transfer of signals. Neuroscience 142:247-265. doi: 10.1016/j.neuroscience.2006.06.001.
4. Burgalossi A, Herfst L, von Heimendahl M, Forste H, Haskic K, Schmidt M, Brecht M. 2011. Microcircuits of functionally identified neurons in the rat medial entorhinal cortex. Neuron 70:773-786. doi: 10.1016/j. neuron.2011.04.003.
5. Caruana DA, Alexander GM, Dudek SM. 2012. New insights into the regulation of synaptic plasticity from an unexpected place: hippocampal area CA2. Learning & Memory 19:391-400. doi: 10.1101/lm.025304.111.
6. Chen WR, Midtgaard J, Shepherd GM. 1997. Forward and backward propagation of dendritic impulses and their synaptic control in mitral cells. Science 278:463-467. doi: 10.1126/science.278.5337.463.
7. Chevaleyre V, Siegelbaum SA. 2010. Strong CA2 pyramidal neuron synapses define a powerful disynaptic cortico-hippocampal loop. Neuron 66:560-572. doi: 10.1016/j.neuron.2010.04.013.
8. Cui Z, Gerfen CR, Young WS III. 2013. Hypothalamic and other connections with dorsal CA2 area of the mouse hippocampus. The Journal of Comparative Neurology 521:1844-1866. doi: 10.1002/cne.23263.
9. De Vito LM, Konigsberg R, Lykken C, Sauvage M, Young WS III, Eichenbaum H. 2009. Vasopressin 1b receptor knock-out impairs memory for temporal order. The Journal of Neuroscience 29:2676-2683. doi: 10.1523/ JNEUROSCI.5488-08.2009.
10. Fino E, Yuste R. 2011. Dense inhibitory connectivity in neocortex. Neuron 69:1188-1203. doi: 10.1016/j. neuron.2011.02.025.
11. Gasparini S, Magee JC. 2006. State-dependent dendritic computation in hippocampal CA1 pyramidal neurons. The Journal of Neuroscience 26:2088-2100. doi: 10.1523/JNEUROSCI.4428-05.2006.
12. Gasparini S, Migliore M, Magee JC. 2004. On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. The Journal of Neuroscience 24:11046-11056. doi: 10.1523/JNEUROSCI.2520-04.2004.
13. Golding NL, Spruston N. 1998. Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 21:1189-1200. doi: 10.1016/S0896-6273(00)80635-2.
14. Golding NL, Staff NP, Spruston N. 2002. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418:326-331. doi: 10.1038/nature00854.
15. Hausser M, Spruston N, Stuart GJ. 2000. Diversity and dynamics of dendritic signaling. Science 290:739-744. doi: 10.1126/science.290.5492.739.
16. Hines ML, Carnevale NT. 1997. The NEURON simulation environment. Neural Computation 9:1179-1209. doi: 10.1162/neco.1997.9.6.1179.
17. Hitti FL, Siegelbaum SA. 2014. The hippocampal CA2 region is essential for social memory. Nature 508:88-92. doi: 10.1038/nature13028.
18. Hoffman DA, Magee JC, Colbert CM, Johnston D. 1997. K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387:869-875. doi: 10.1038/42571.
19. Ishizuka N, Cowan WM, Amaral DG. 1995. A quantitative analysis of the dendritic organization of pyramidal cells in the rat hippocampus. The Journal of Comparative Neurology 362:17-45. doi: 10.1002/ cne.903620103.
20. Jarsky T, Roxin A, Kath WL, Spruston N. 2005. Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons. Nature Neuroscience 8:1667-1676. doi: 10.1038/nn1599.
21. Johnston D, Magee JC, Colbert CM, Cristie BR. 1996. Active properties of neuronal dendrites. Annual Review of Neuroscience 19:165-186. doi: 10.1146/annurev.ne.19.030196.001121.
22. Johnston D, Narayanan R. 2008. Active dendrites: colorful wings of the mysterious butterflies. Trends in Neurosciences 31:309-316. doi: 10.1016/j.tins.2008.03.004.
23. Jones MW, McHugh TJ. 2011. Updating hippocampal representations: CA2 joins the circuit. Trends in Neurosciences 34:526-535. doi: 10.1016/j.tins.2011.07.007.
24. Kamondi A, Acsady L, Buzsaki G. 1998. Dendritic spikes are enhanced by cooperative network activity in the intact hippocampus. The Journal of Neuroscience 18:3919-3928.
25. Kim S, Guzman SJ, Hu H, Jonas P. 2012. Active dendrites support efficient initiation of dendritic spikes in hippocampal CA3 pyramidal neurons. Nature Neuroscience 15:600-606. doi: 10.1038/nn.3060.
26. Kohara K, Pignatelli M, Rivest AJ, Jung HY, Kitamura T, Suh J, Frank D, Kajikawa K, Mise N, Obata Y, Wickersham IR, Tonegawa S. 2014. Cell type-specific genetic and optogenetic tools reveal hippocampal CA2 circuits. Nature Neuroscience 17:269-279. doi: 10.1038/nn.3614.
27. Larkum ME, Nevian T, Sandler M, Polsky A, 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.
28. Larkum ME, Waters J, Sakmann B, Helmchen F. 2007. Dendritic spikes in apical dendrites of neocortical layer 2/3 pyramidal neurons. The Journal of Neuroscience 27:8999-9008. doi: 10.1523/JNEUROSCI.1717-07.2007.
29. Larkum ME, Zhu JJ, Sakmann B. 1999. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398:338-341. doi: 10.1038/18686.
30. Lavzin M, Rapoport S, Polsky A, Garion L, Schiller J. 2012. Nonlinear dendritic processing determines angular tuning of barrel cortex neurons in vivo. Nature 490:397-401. doi: 10.1038/nature11451.
31. Lee SE, Simons SB, Heldt SA, Zhao M, Schroeder JP, Vellano CP, Cowan DP, Ramineni S, Yates CK, Feng Y, Smith Y, Sweatt JD, Weinshenker D, Ressler KJ, Dudek SM, Hepler JR. 2010. RGS14 is a natural suppressor of both synaptic plasticity in CA2 neurons and hippocampal-based learning and memory. Proceedings of the National Academy of Sciences of USA 107:16994-16998. doi: 10.1073/pnas.1005362107.
32. Llinas R, Nicholson C, Freeman JA, Hillman DE. 1968. Dendritic spikes and their inhibition in alligator Purkinje cells. Science 160:1132-1135. doi: 10.1126/science.160.3832.1132.
33. London M, Hausser M. 2005. Dendritic computation. Annual Review of Neuroscience 28:503-532. doi: 10.1146/ annurev.neuro.28.061604.135703.
34. Losonczy A, Magee JC. 2006. Integrative properties of radial oblique dendrites in hippocampal CA1 pyramidal neurons. Neuron 50:291-307. doi: 10.1016/j.neuron.2006.03.016.
35. Losonczy A, Makara JK, Magee JC. 2008. Compartmentalized dendritic plasticity and input feature storage in neurons. Nature 452:436-441. doi: 10.1038/nature06725.
36. Magee JC. 1998. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. The Journal of Neuroscience 18:7613-7624.
37. Major G, Larkum ME, Schiller J. 2013. Active properties of neocortical pyramidal neuron dendrites. Annual Review of Neuroscience 36:1-24. doi: 10.1146/annurev-neuro-062111-150343.
38. Martina M, Vida I, Jonas P. 2000. Distal initiation and active propagation of action potentials in interneuron dendrites. Science 287:295-300. doi: 10.1126/science.287.5451.295.
39. Muller C, Beck H, Coulter D, Remy S. 2012. Inhibitory control of linear and supralinear dendritic excitation in CA1 pyramidal neurons. Neuron 75:851-864. doi: 10.1016/j.neuron.2012.06.025.
40. Nevian T, Larkum ME, Polsky A, Schiller J. 2007. Properties of basal dendrites of layer 5 pyramidal neurons: a direct patch-clamp recording study. Nature Neuroscience 10:206-214. doi: 10.1038/nn1826.
41. Pagani JH, Zhao M, Cui Z, Williams Avram SK, Caruana DA, Dudek SM, Young WS. 2014. Role of the vasopressin 1b receptor in rodent aggressive behavior and synaptic plasticity in hippocampal area CA2. Molecular Psychiatry doi: 10.1038/mp.2014.47.
42. Remy S, Csicsvari J, Beck H. 2009. Activity-dependent control of neuronal output by local and global dendritic spike attenuation. Neuron 61:906-916. doi: 10.1016/j.neuron.2009.01.032.
43. Remy S, Spruston N. 2007. Dendritic spikes induce single-burst long-term potentiation. Proceedings of the National Academy of Sciences of USA 104:17192-17197. doi: 10.1073/pnas.0707919104.
44. Santoro B, Wainger BJ, Siegelbaum SA. 2004. Regulation of HCN channel surface expression by a novel C-terminal protein-protein interaction. The Journal of Neuroscience 24:10750-10762. doi: 10.1523/ JNEUROSCI.3300-04.2004.
45. Schiller J, Major G, Koester HJ, Schiller Y. 2000. NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 404:285-289. doi: 10.1038/35005094.
46. Schiller J, Schiller Y, Stuart G, Sakmann B. 1997. Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. The Journal of Physiology 505:605-616. doi: 10.1111/j.1469-7793.1997.605ba.x.
47. Simons SB, Escobedo Y, Yasuda R, Dudek SM. 2009. Regional differences in hippocampal calcium handling provide a cellular mechanism for limiting plasticity. Proceedings of the National Academy of Sciences of USA 106:14080-14084. doi: 10.1073/pnas.0904775106.
48. Smith SL, Smith IT, Branco T, Hausser M. 2013. Dendritic spikes enhance stimulus selectivity in cortical neurons in vivo. Nature 503:115-120. doi: 10.1038/nature12600.
49. Spruston N. 2008. Pyramidal neurons: dendritic structure and synaptic integration. Nature Reviews Neuroscience 9:206-221. doi: 10.1038/nrn2286.
50. Stevenson EL, Caldwell HK. 2014. Lesions to the CA2 region of the hippocampus impair social memory in mice. The European Journal of Neuroscience 40:3294-3301.
51. Stuart G, Schiller J, Sakmann B. 1997a. Action potential initiation and propagation in rat neocortical pyramidal neurons. The Journal of Physiology 505:617-632. doi: 10.1111/j.1469-7793.1997.617ba.x.
52. Stuart G, Spruston N, Sakmann B, Hausser M. 1997b. Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends in Neurosciences 20:125-131. doi: 10.1016/S0166-2236(96)10075-8.
53. Stuart GJ, Sakmann B. 1994. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367:69-72. doi: 10.1038/367069a0.
54. Tamamaki N, Nojyo Y. 1993. Projection of the entorhinal layer II neurons in the rat as revealed by intracellular pressure-injection of neurobiotin. Hippocampus 3:471-480. doi: 10.1002/hipo.450030408.
55. Turner RW, Meyers DE, Richardson TL, Barker JL. 1991. The site for initiation of action potential discharge over the somatodendritic axis of rat hippocampal CA1 pyramidal neurons. The Journal of Neuroscience 11:2270-2280.
56. Vetter P, Roth A, Hausser M. 2001. Propagation of action potentials in dendrites depends on dendritic morphology. Journal of Neurophysiology 85:926-937.
57. Waters J, Larkum M, Sakmann B, Helmchen F. 2003. Supralinear Ca2+ influx into dendritic tufts of layer 2/3 neocortical pyramidal neurons in vitro and in vivo. The Journal of Neuroscience 23:8558-8567.
58. Williams SR, Stuart GJ. 2002. Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons. Science 295:1907-1910. doi: 10.1126/science.1067903.
59. Witter MP. 2007. The perforant path: projections from the entorhinal cortex to the dentate gyrus. Progress in Brain Research 163:43-61. doi: 10.1016/S0079-6123(07)63003-9.
60. Wong RK, Prince DA, Basbaum AI. 1979. Intradendritic recordings from hippocampal neurons. Proceedings of the National Academy of Sciences of USA 76:986-990. doi: 10.1073/pnas.76.2.986.
61. Zhao M, Choi YS, Obrietan K, Dudek SM. 2007. Synaptic plasticity (and the lack thereof) in hippocampal CA2 neurons. The Journal of Neuroscience 27:12025-12032. doi: 10.1523/JNEUROSCI.4094-07.2007.