Unique membrane properties and enhanced signal processing in human neocortical neurons

eLife

Volumn 5, Issue OCTOBER2016, 2016, Pages

  Eyal, Guy ^a   Verhoog, Matthijs B ^b   Testa Silva, Guilherme ^b   Deitcher, Yair ^a   Lodder, Johannes C ^b   Benavides Piccione, Ruth ^c,d   Morales, Juan ^e   Defelipe, Javier ^c,d   de Kock, Christiaan P J ^b   Mansvelder, Huibert D ^b   Segev, Idan ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c INSTITUTO CAJAL   (Spain)

^d UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

^e UNIVERSIDAD POLITÉCNICA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AXON; BRAIN CELL; DENDRITE; HUMAN; IN VITRO STUDY; MEMBRANE; NEOCORTEX; PYRAMIDAL NERVE CELL; SIGNAL PROCESSING; SPIKE; SYNAPSE; TEMPORAL CORTEX; THEORETICAL MODEL; ACTION POTENTIAL; ADULT; ANIMAL; BIOLOGICAL MODEL; CELL MEMBRANE; CYTOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; MALE; MICROTOMY; MIDDLE AGED; MOUSE; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; TEMPORAL LOBE; ULTRASTRUCTURE; VERY ELDERLY;

ACTION POTENTIALS; ADULT; AGED, 80 AND OVER; ANIMALS; AXONS; CELL MEMBRANE; DENDRITES; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; HUMANS; MALE; MICE; MICROTOMY; MIDDLE AGED; MODELS, NEUROLOGICAL; NEOCORTEX; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; TEMPORAL LOBE;

EID: 84994753130     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.16553     Document Type: Article

References (61)

1. Agmon-Snir H, Segev I. 1993. Signal delay and input synchronization in passive dendritic structures. Journal of Neurophysiology 70:2066–2085. PMID: 8294970
2. Benavides-Piccione R, Fernaud-Espinosa I, Robles V, Yuste R, DeFelipe J. 2013. Age-based comparison of human dendritic spine structure using complete three-dimensional reconstructions. Cerebral Cortex 23:1798–1810. doi: 10.1093/cercor/bhs154, PMID: 22710613
3. Bozek K, Wei Y, Yan Z, Liu X, Xiong J, Sugimoto M, Tomita M, P ä äbo S, Sherwood CC, Hof PR, Ely JJ, Li Y, Steinhauser D, Willmitzer L, Giavalisco P, Khaitovich P. 2015. Organization and evolution of brain lipidome revealed by large-scale analysis of human, chimpanzee, macaque, and mouse tissues. Neuron 85:695–702.doi: 10.1016/j.neuron.2015.01.003, PMID: 25661180
4. Brodmann K. 2007. Brodmann’s: Localisation in the Cerebral Cortex. Springer Science & Business Media. Cajal RS. 1995. Histology of the Nervous System of Man and Vertebrates. USA: Oxford University Press.
5. Carnevale NT, Hines ML. 2006. The Neuron Book. Cambridge University Press. doi: 10.1017/CBO9780511541612
6. Chan RB, Oliveira TG, Cortes EP, Honig LS, Duff KE, Small SA, Wenk MR, Shui G, Di Paolo G. 2012. Comparative lipidomic analysis of mouse and human brain with Alzheimer disease. Journal of Biological Chemistry 287: 2678–2688. doi: 10.1074/jbc.M111.274142, PMID: 22134919
7. Chevli R, Fitch CD. 1982. The antimalarial drug mefloquine binds to membrane phospholipids. Antimicrobial Agents and Chemotherapy 21:581–586. doi: 10.1128/AAC.21.4.581
8. Cole KS. 1968. Membranes, Ions, and Impulses: A Chapter of Classical Biophysics. Univ of California Press.
9. de Kock CP, Burnashev N, Lodder JC, Mansvelder HD, Brussaard AB. 2004. NMDA receptors induce somatodendritic secretion in hypothalamic neurones of lactating female rats. Journal of Physiology 561:53–64. doi: 10.1113/jphysiol.2004.069005, PMID: 15459239
10. DeFelipe J, Alonso-Nanclares L, Arellano JI. 2002. Microstructure of the neocortex: comparative aspects. Journal of Neurocytology 31:299–316. doi: 10.1023/A:1024130211265, PMID: 12815249
11. DeFelipe J. 2011. The evolution of the brain, the human nature of cortical circuits, and intellectual creativity. Frontiers in Neuroanatomy 5:p.29. doi: 10.3389/fnana.2011.00029
12. Elston GN, Benavides-Piccione R, DeFelipe J. 2001. The pyramidal cell in cognition: a comparative study in human and monkey. Journal of Neuroscience 21:RC163. PMID: 11511694
13. Eyal G, Mansvelder HD, de Kock CP, Segev I. 2014. Dendrites impact the encoding capabilities of the axon. Journal of Neuroscience 34:8063–8071. doi: 10.1523/JNEUROSCI.5431-13.2014, PMID: 24920612
14. Feldman ML, Peters A. 1979. A technique for estimating total spine numbers on Golgi-impregnated dendrites. The Journal of Comparative Neurology 188:527–542. doi: 10.1002/cne.901880403, PMID: 93115
15. Gentet LJ, Stuart GJ, Clements JD. 2000. Direct measurement of specific membrane capacitance in neurons. Biophysical Journal 79:314–320. doi: 10.1016/S0006-3495(00)76293-X, PMID: 10866957
16. Golding NL, Mickus TJ, Katz Y, Kath WL, Spruston N. 2005. Factors mediating powerful voltage attenuation along CA1 pyramidal neuron dendrites. The Journal of Physiology 568:69–82. doi: 10.1113/jphysiol.2005.
17. 086793, PMID: 16002454
18. Golgi C. 1906. The neuron doctrine: theory and facts. Nobel Lecture 1921:190–217.
19. Harnett MT, Magee JC, Williams SR. 2015. Distribution and function of HCN channels in the apical dendritic tuft of neocortical pyramidal neurons. Journal of Neuroscience 35:1024–1037. doi: 10.1523/JNEUROSCI.2813-14.2015, PMID: 25609619
20. Hay E, Hill S, Schü rmann F, Markram H, Segev I. 2011. Models of neocortical layer 5b pyramidal cells capturing a wide range of dendritic and perisomatic active properties. PLoS Computational Biology 7:e1002107. doi: 10.1371/journal.pcbi.1002107, PMID: 21829333
21. Herculano-Houzel S, Mota B, Wong P, Kaas JH. 2010. Connectivity-driven white matter scaling and folding in primate cerebral cortex. PNAS 107:19008–19013. doi: 10.1073/pnas.1012590107
22. Hodgkin AL, Huxley AF, Katz B. 1952. Measurement of current-voltage relations in the membrane of the giant axon of Loligo. Journal of Physiology 116:424–448. doi: 10.1113/jphysiol.1952.sp004716, PMID: 14946712
23. Jack JJB, Noble D, Tsien RW. 1975. Electric Current Flow in Excitable Cells. Clarendon Press Oxford.
24. Jacobs B, Schall M, Prather M, Kapler E, Driscoll L, Baca S, Jacobs J, Ford K, Wainwright M, Treml M. 2001. Regional dendritic and spine variation in human cerebral cortex: a quantitative golgi study. Cerebral Cortex 11: 558–571. doi: 10.1093/cercor/11.6.558, PMID: 11375917
25. Jahr CE, Stevens CF. 1990. Voltage dependence of NMDA-activated macroscopic conductances predicted by single-channel kinetics. Journal of Neuroscience 10:3178–3182. PMID: 1697902
26. Kole MH, Hallermann S, Stuart GJ. 2006. Single Ih channels in pyramidal neuron dendrites: properties, distribution, and impact on action potential output. Journal of Neuroscience 26:1677–1687. doi: 10.1523/JNEUROSCI.3664-05.2006, PMID: 16467515
27. Kö hling R, Avoli M. 2006. Methodological approaches to exploring epileptic disorders in the human brain in vitro. Journal of Neuroscience Methods 155:1–19. doi: 10.1016/j.jneumeth.2006.04.009, PMID: 16753220
28. 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, PMID: 19661433
29. Lecompte MF, Gaibelet G, Lebrun C, TercéF, Collet X, Orlowski S. 2015. Cholesterol and sphingomyelin- containing model condensed lipid monolayers: Heterogeneities involving ordered microdomains assessed by two cholesterol derivatives. Langmuir 31:11921–11931. doi: 10.1021/acs.langmuir.5b02646, PMID: 26466013
30. London M, H ä usser M. 2005. Dendritic computation. Annual Review of Neuroscience 28:503–532. doi: 10.1146/annurev.neuro.28.061604.135703, PMID: 16033324
31. Lorensen WE, Cline HE. 1987. Marching cubes: a high resolution 3D surface construction algorithm. In: ACM Siggraph Computer Graphics. p 163–169.
32. Magee JC. 1998. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. Journal of Neuroscience 18:7613–7624. PMID: 9742133
33. Mainen ZF, Sejnowski TJ. 1996. Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382:363–366. doi: 10.1038/382363a0, PMID: 8684467
34. Major G, Evans JD, Jack JJB. 1993. Solutions for transients in arbitrarily branching cables. Biophysical Journal 65: 450–468. doi: 10.1016/S0006-3495(93)81038-5
35. Major G, Larkman AU, Jonas P, Sakmann B, Jack JJ. 1994. Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices. Journal of Neuroscience 14:4613–4638. PMID: 8046439
36. Markram H, Muller E, Ramaswamy S, Reimann MW, Abdellah M, Sanchez CA, Ailamaki A, Alonso-Nanclares L, Antille N, Arsever S, Kahou GA, Berger TK, Bilgili A, Buncic N, Chalimourda A, Chindemi G, Courcol JD, Delalondre F, Delattre V, Druckmann S, et al. 2015. Reconstruction and simulation of neocortical microcircuitry. Cell 163:456–492. doi: 10.1016/j.cell.2015.09.029, PMID: 26451489
37. Mass ey FJ. 1951. The kolmogorov-smirnov test for goodness of fit. Journal of the American StatisticalAssociation 46:68–78. doi: 10.1080/01621459.1951.10500769
38. Mohan H, Verhoog MB, Doreswamy KK, Eyal G, Aardse R, Lodder BN, Goriounova NA, Asamoah B, B Brakspear AB, Groot C, van der Sluis S, Testa-Silva G, Obermayer J, Boudewijns ZS, Narayanan RT, Baayen JC, Segev I, Mansvelder HD, de Kock CP. 2015. Dendritic and axonal architecture of individual pyramidal neurons across layers of adult human neocortex. Cerebral Cortex 25:4839–4853. doi: 10.1093/cercor/bhv188, PMID: 26318661
39. Moschetta A, Xu F, Hagey LR, van Berge-Henegouwen GP, van Erpecum KJ, Brouwers JF, Cohen JC, Bierman M, Hobbs HH, Steinbach JH, Hofmann AF. 2005. A phylogenetic survey of biliary lipids in vertebrates. Journal of Lipid Research 46:2221–2232. doi: 10.1194/jlr.M500178-JLR200, PMID: 16061950
40. Norenberg A, Hu H, Vida I, Bartos M, Jonas P. 2010. Distinct nonuniform cable properties optimize rapid and efficient activation of fast-spiking GABAergic interneurons. PNAS 107:894–899. doi: 10.1073/pnas.0910716107
41. Palmer LM, Shai AS, Reeve JE, Anderson HL, Paulsen O, Larkum ME. 2014. NMDA spikes enhance action potential generation during sensory input. Nature Neuroscience 17:383–390. doi: 10.1038/nn.3646, PMID: 24487231
42. Poirazi P, Mel BW. 2001. Impact of active dendrites and structural plasticity on the memory capacity of neural tissue. Neuron 29:779–796. doi: 10.1016/S0896-6273(01)00252-5, PMID: 11301036
43. Rall W, Burke RE, Holmes WR, Jack JJ, Redman SJ, Segev I. 1992. Matching dendritic neuron models to experimental data. Physiological Reviews 72:S159–186. PMID: 1438585
44. Rapp M, Yarom Y, Segev I. 1992. The impact of parallel fiber background activity on the cable properties of cerebellar Purkinje cells. Neural Computation 4:518–533. doi: 10.1162/neco.1992.4.4.518
45. Rhodes P. 2006. The properties and implications of NMDA spikes in neocortical pyramidal cells. Journal of Neuroscience 26:6704–6715. doi: 10.1523/JNEUROSCI.3791-05.2006, PMID: 16793878
46. Roth A, H ä usser M. 2001. Compartmental models of rat cerebellar Purkinje cells based on simultaneous somatic and dendritic patch-clamp recordings. Journal of Physiology 535:445–472. doi: 10.1111/j.1469-7793.2001.00445.x, PMID: 11533136
47. Rumbell TH, Draguljić D, Yadav A, Hof PR, Luebke JI, Weaver CM. 2016. Automated evolutionary optimization of ion channel conductances and kinetics in models of young and aged rhesus monkey pyramidal neurons. Journal of Computational Neuroscience 41:65–90. doi: 10.1007/s10827-016-0605-9, PMID: 27106692
48. Sarid L, Bruno R, Sakmann B, Segev I, Feldmeyer D. 2007. Modeling a layer 4-to-layer 2/3 module of a single column in rat neocortex: interweaving in vitro and in vivo experimental observations. PNAS 104:16353–16358. doi: 10.1073/pnas.0707853104
49. Sarid L, Feldmeyer D, Gidon A, Sakmann B, Segev I. 2015. Contribution of intracolumnar layer 2/3-to-layer 2/3 excitatory connections in shaping the response to whisker deflection in rat barrel cortex. Cerebral Cortex 25: 849–858. doi: 10.1093/cercor/bht268, PMID: 24165834
50. Schwartzkroin PA, Prince DA. 1978. Cellular and field potential properties of epileptogenic hippocampal slices. Brain Research 147:117–130. doi: 10.1016/0006-8993(78)90776-X, PMID: 656907
51. Segev I, London M. 2000. Untangling dendrites with quantitative models. Science 290:744–750. doi: 10.1126/science.290.5492.744, PMID: 11052930
52. Segev I, Rall W. 1988. Computational study of an excitable dendritic spine. Journal of Neurophysiology 60:499–523. PMID: 2459320
53. Stuart G, Spruston N. 1998. Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. Journal of Neuroscience 18:3501–3510. PMID: 9570781
54. Stuart GJ, Sakmann B. 1994. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367:69–72. doi: 10.1038/367069a0, PMID: 8107777
55. Szabadics J, Varga C, Molná r G, Oláh S, BarzóP, Tamá s G. 2006. Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 311:233–235. doi: 10.1126/science.1121325, PMID: 16410524
56. Szoboszlay M, Lorincz A, Lanore F, Vervaeke K, Silver RA, Nusser Z. 2016. Functional properties of dendritic gap junctions in cerebellar golgi cells. Neuron 90:1043–1056. doi: 10.1016/j.neuron.2016.03.029, PMID: 27133465
57. Testa-Silva G, Verhoog MB, Goriounova NA, Loebel A, Hjorth J, Baayen JC, de Kock CP, Mansvelder HD. 2010. Human synapses show a wide temporal window for spike-timing-dependent plasticity. Frontiers in Synaptic Neuroscience 2:12. doi: 10.3389/fnsyn.2010.00012, PMID: 21423498
58. Testa-Silva G, Verhoog MB, Linaro D, de Kock CP, Baayen JC, Meredith RM, De Zeeuw CI, Giugliano M, Mansvelder HD. 2014. High bandwidth synaptic communication and frequency tracking in human neocortex. PLoS Biology 12:e1002007. doi: 10.1371/journal.pbio.1002007, PMID: 25422947
59. Thurbon D, Lü scher HR, Hofstetter T, Redman SJ. 1998. Passive electrical properties of ventral horn neurons in rat spinal cord slices. Journal of Neurophysiology 79:2485–2502. PMID: 9582222
60. Verhoog MB, Goriounova NA, Obermayer J, Stroeder J, Hjorth JJ, Testa-Silva G, Baayen JC, de Kock CP, Meredith RM, Mansvelder HD. 2013. Mechanisms underlying the rules for associative plasticity at adult human neocortical synapses. Journal of Neuroscience 33:17197–17208. doi: 10.1523/JNEUROSCI.3158-13.2013, PMID: 24155324
61. Watson KK, Jones TK, Allman JM. 2006. Dendritic architecture of the von economo neurons. Neuroscience 141: 1107–1112. doi: 10.1016/j.neuroscience.2006.04.084, PMID: 16797136