Enhanced Dendritic Compartmentalization in Human Cortical Neurons

Overview

Journal Cell

Publisher Cell Press

Specialty Cell Biology

Date 2018 Oct 20

PMID 30340039

Citations 119

Authors

Lou Beaulieu-Laroche

Enrique H S Toloza

Marie-Sophie van der Goes

Mathieu Lafourcade

Derrick Barnagian

Ziv M Williams

Emad N Eskandar

Matthew P Frosch

Sydney S Cash

Mark T Harnett

Affiliations

Soon will be listed here.

Abstract

The biophysical features of neurons shape information processing in the brain. Cortical neurons are larger in humans than in other species, but it is unclear how their size affects synaptic integration. Here, we perform direct electrical recordings from human dendrites and report enhanced electrical compartmentalization in layer 5 pyramidal neurons. Compared to rat dendrites, distal human dendrites provide limited excitation to the soma, even in the presence of dendritic spikes. Human somas also exhibit less bursting due to reduced recruitment of dendritic electrogenesis. Finally, we find that decreased ion channel densities result in higher input resistance and underlie the lower coupling of human dendrites. We conclude that the increased length of human neurons alters their input-output properties, which will impact cortical computation. VIDEO ABSTRACT.

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References

Larkum M, Zhu J . Signaling of layer 1 and whisker-evoked Ca2+ and Na+ action potentials in distal and terminal dendrites of rat neocortical pyramidal neurons in vitro and in vivo. J Neurosci. 2002; 22(16):6991-7005. PMC: 6757874. DOI: 20026717. View

Gentet L, Stuart G, Clements J . Direct measurement of specific membrane capacitance in neurons. Biophys J. 2000; 79(1):314-20. PMC: 1300935. DOI: 10.1016/S0006-3495(00)76293-X. View

Tran-Van-Minh A, Abrahamsson T, Cathala L, DiGregorio D . Differential Dendritic Integration of Synaptic Potentials and Calcium in Cerebellar Interneurons. Neuron. 2016; 91(4):837-850. DOI: 10.1016/j.neuron.2016.07.029. View

Williams S, Stuart G . Site independence of EPSP time course is mediated by dendritic I(h) in neocortical pyramidal neurons. J Neurophysiol. 2000; 83(5):3177-82. DOI: 10.1152/jn.2000.83.5.3177. View

Cichon J, Gan W . Branch-specific dendritic Ca(2+) spikes cause persistent synaptic plasticity. Nature. 2015; 520(7546):180-5. PMC: 4476301. DOI: 10.1038/nature14251. View

Atkinson S, Williams S . Postnatal development of dendritic synaptic integration in rat neocortical pyramidal neurons. J Neurophysiol. 2009; 102(2):735-51. PMC: 2724330. DOI: 10.1152/jn.00083.2009. View

Mainen Z, Sejnowski T . Influence of dendritic structure on firing pattern in model neocortical neurons. Nature. 1996; 382(6589):363-6. DOI: 10.1038/382363a0. View

Hattox A, Nelson S . Layer V neurons in mouse cortex projecting to different targets have distinct physiological properties. J Neurophysiol. 2007; 98(6):3330-40. DOI: 10.1152/jn.00397.2007. View

Hay E, Hill S, Schurmann F, Markram H, Segev I . Models of neocortical layer 5b pyramidal cells capturing a wide range of dendritic and perisomatic active properties. PLoS Comput Biol. 2011; 7(7):e1002107. PMC: 3145650. DOI: 10.1371/journal.pcbi.1002107. View

10.

Williams S . Spatial compartmentalization and functional impact of conductance in pyramidal neurons. Nat Neurosci. 2004; 7(9):961-7. DOI: 10.1038/nn1305. View

11.

Zeng H, Shen E, Hohmann J, Oh S, Bernard A, Royall J . Large-scale cellular-resolution gene profiling in human neocortex reveals species-specific molecular signatures. Cell. 2012; 149(2):483-96. PMC: 3328777. DOI: 10.1016/j.cell.2012.02.052. View

12.

Schiller J, Major G, KOESTER H, Schiller Y . NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature. 2000; 404(6775):285-9. DOI: 10.1038/35005094. View

13.

Spruston N, Jaffe D, Williams S, Johnston D . Voltage- and space-clamp errors associated with the measurement of electrotonically remote synaptic events. J Neurophysiol. 1993; 70(2):781-802. DOI: 10.1152/jn.1993.70.2.781. View

14.

DeFelipe J, Alonso-Nanclares L, Arellano J . Microstructure of the neocortex: comparative aspects. J Neurocytol. 2003; 31(3-5):299-316. DOI: 10.1023/a:1024130211265. View

15.

Spruston N . Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci. 2008; 9(3):206-21. DOI: 10.1038/nrn2286. View

16.

Verhoog M, Goriounova N, Obermayer J, Stroeder J, Hjorth J, Testa-Silva G . Mechanisms underlying the rules for associative plasticity at adult human neocortical synapses. J Neurosci. 2013; 33(43):17197-208. PMC: 6618441. DOI: 10.1523/JNEUROSCI.3158-13.2013. View

17.

Williams S, Stuart G . Mechanisms and consequences of action potential burst firing in rat neocortical pyramidal neurons. J Physiol. 1999; 521 Pt 2:467-82. PMC: 2269673. DOI: 10.1111/j.1469-7793.1999.00467.x. View

18.

Tran-Van-Minh A, Caze R, Abrahamsson T, Cathala L, Gutkin B, DiGregorio D . Contribution of sublinear and supralinear dendritic integration to neuronal computations. Front Cell Neurosci. 2015; 9:67. PMC: 4371705. DOI: 10.3389/fncel.2015.00067. View

19.

Hausser M, Mel B . Dendrites: bug or feature?. Curr Opin Neurobiol. 2003; 13(3):372-83. DOI: 10.1016/s0959-4388(03)00075-8. View

20.

Vaidya S, Johnston D . Temporal synchrony and gamma-to-theta power conversion in the dendrites of CA1 pyramidal neurons. Nat Neurosci. 2013; 16(12):1812-20. PMC: 3958963. DOI: 10.1038/nn.3562. View