Dendritic and Axonal Architecture of Individual Pyramidal Neurons across Layers of Adult Human Neocortex

被引:161
作者
Mohan, Hemanth [1 ]
Verhoog, Matthijs B. [1 ]
Doreswamy, Keerthi K. [1 ]
Eyal, Guy [2 ,3 ]
Aardse, Romy [1 ]
Lodder, Brendan N. [1 ]
Goriounova, Natalia A. [1 ]
Asamoah, Boateng [1 ]
Brakspear, A. B. Clementine B. [1 ]
Groot, Colin [1 ]
van der Sluis, Sophie [4 ]
Testa-Silva, Guilherme [1 ]
Obermayer, Joshua [1 ]
Boudewijns, Zimbo S. R. M. [1 ]
Narayanan, Rajeevan T. [1 ]
Baayen, Johannes C. [5 ]
Segev, Idan [2 ,3 ]
Mansvelder, Huibert D. [1 ]
de Kock, Christiaan P. J. [1 ]
机构
[1] Vrije Univ Amsterdam, Ctr Neurogen & Cognit Res, Dept Integrat Neurophysiol, NL-1081 HV Amsterdam, Netherlands
[2] Hebrew Univ Jerusalem, Dept Neurobiol, IL-91904 Jerusalem, Israel
[3] Hebrew Univ Jerusalem, Edmond & Lily Safra Ctr Brain Sci, IL-91904 Jerusalem, Israel
[4] Vrije Univ Amsterdam Med Ctr, Dept Clin Genet, Sect Complex Trait Genet, Ctr Neurogen & Cognit Res, Amsterdam, Netherlands
[5] Vrije Univ Amsterdam Med Ctr, Dept Neurosurg, NL-1081 HV Amsterdam, Netherlands
关键词
HUMAN CEREBRAL-CORTEX; QUANTITATIVE-ANALYSIS; SYNAPTIC INTEGRATION; CALRETININ NEURONS; PREFRONTAL CORTEX; SPINY STELLATE; CELLS; MORPHOLOGY; BRAIN; EVOLUTION;
D O I
10.1093/cercor/bhv188
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
The size and shape of dendrites and axons are strong determinants of neuronal information processing. Our knowledge on neuronal structure and function is primarily based on brains of laboratory animals. Whether it translates to human is not known since quantitative data on "full" human neuronal morphologies are lacking. Here, we obtained human brain tissue during resection surgery and reconstructed basal and apical dendrites and axons of individual neurons across all cortical layers in temporal cortex (Brodmann area 21). Importantly, morphologies did not correlate to etiology, disease severity, or disease duration. Next, we show that human L(ayer) 2 and L3 pyramidal neurons have 3-fold larger dendritic length and increased branch complexity with longer segments compared with temporal cortex neurons from macaque and mouse. Unsupervised cluster analysis classified 88% of human L2 and L3 neurons into human-specific clusters distinct from mouse and macaque neurons. Computational modeling of passive electrical properties to assess the functional impact of large dendrites indicates stronger signal attenuation of electrical inputs compared with mouse. We thus provide a quantitative analysis of "full" human neuron morphologies and present direct evidence that human neurons are not "scaled-up" versions of rodent or macaque neurons, but have unique structural and functional properties.
引用
收藏
页码:4839 / 4853
页数:15
相关论文
共 71 条
[1]   A solution to dependency: using multilevel analysis to accommodate nested data [J].
Aarts, Emmeke ;
Verhage, Matthijs ;
Veenvliet, Jesse V. ;
Dolan, Conor V. ;
van der Sluis, Sophie .
NATURE NEUROSCIENCE, 2014, 17 (04) :491-496
[2]   The Morphology of Supragranular Pyramidal Neurons in the Human Insular Cortex: A Quantitative Golgi Study [J].
Anderson, Kaeley ;
Bones, Brian ;
Robinson, Brooks ;
Hass, Charles ;
Lee, Hyowon ;
Ford, Kevin ;
Roberts, Tomi-Ann ;
Jacobs, Bob .
CEREBRAL CORTEX, 2009, 19 (09) :2131-2144
[3]   Glutamatergic Nonpyramidal Neurons From Neocortical Layer VI and Their Comparison With Pyramidal and Spiny Stellate Neurons [J].
Andjelic, Sofija ;
Gallopin, Thierry ;
Cauli, Bruno ;
Hill, Elisa L. ;
Roux, Lisa ;
Badr, Sammy ;
Hu, Emilie ;
Tamas, Gabor ;
Lambolez, Bertrand .
JOURNAL OF NEUROPHYSIOLOGY, 2009, 101 (02) :641-654
[4]   Organization and development of corticocortical associative neurons expressing the orphan nuclear receptor Nurr1 [J].
Arimatsu, Y ;
Ishida, M ;
Kaneko, T ;
Ichinose, S ;
Omori, A .
JOURNAL OF COMPARATIVE NEUROLOGY, 2003, 466 (02) :180-196
[5]   Mobilizing the base of neuroscience data: the case of neuronal morphologies [J].
Ascoli, GA .
NATURE REVIEWS NEUROSCIENCE, 2006, 7 (04) :318-324
[6]   Targeted dendrotomy reveals active and passive contributions of the dendritic tree to synaptic integration and neuronal output [J].
Bekkers, John M. ;
Haeusser, Michael .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2007, 104 (27) :11447-11452
[7]   Dendritic Morphology of Pyramidal Neurons in the Chimpanzee Neocortex: Regional Specializations and Comparison to Humans [J].
Bianchi, Serena ;
Stimpson, Cheryl D. ;
Bauernfeind, Amy L. ;
Schapiro, Steven J. ;
Baze, Wallace B. ;
McArthur, Mark J. ;
Bronson, Ellen ;
Hopkins, William D. ;
Semendeferi, Katerina ;
Jacobs, Bob ;
Hof, Patrick R. ;
Sherwood, Chet C. .
CEREBRAL CORTEX, 2013, 23 (10) :2429-2436
[8]   Translaminar Inhibitory Cells Recruited by Layer 6 Corticothalamic Neurons Suppress Visual Cortex [J].
Bortone, Dante S. ;
Olsen, Shawn R. ;
Scanziani, Massimo .
NEURON, 2014, 82 (02) :474-485
[9]  
Braak H., 1980, ARCHITECTONICS HUMAN, DOI DOI 10.1007/978-3-642-81522-5
[10]   Sensory Experience Alters Specific Branches of Individual Corticocortical Axons during Development [J].
Bruno, Randy M. ;
Hahn, Thomas T. G. ;
Wallace, Damian J. ;
de Kock, Christiaan P. J. ;
Sakmann, Bert .
JOURNAL OF NEUROSCIENCE, 2009, 29 (10) :3172-3181