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

H. Mohan, M.B. Verhoog, K.K. Doreswamy, G. Eyal, R. Aardse, B.N. Lodder, N.A. Goriounova, B. Asamoah, A.B. Brakspear, C. Groot, S. van der Sluis, G. Testa-Silva, J.M.G. Obermayer, Z.S.R.M. Boudewijns, R.T. Narayanan, J.C. Baayen, I Segev, H.D. Mansvelder, C.P.J. de Kock

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

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.
Original languageEnglish
Pages (from-to)4839-4853
JournalCerebral Cortex
Volume25
Issue number12
DOIs
Publication statusPublished - 2015

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Pyramidal Cells
Neocortex
Neurons
Macaca
Dendrites
Temporal Lobe
Axons
Brain
Laboratory Animals
Automatic Data Processing
Cluster Analysis
Rodentia

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Mohan, H. ; Verhoog, M.B. ; Doreswamy, K.K. ; Eyal, G. ; Aardse, R. ; Lodder, B.N. ; Goriounova, N.A. ; Asamoah, B. ; Brakspear, A.B. ; Groot, C. ; van der Sluis, S. ; Testa-Silva, G. ; Obermayer, J.M.G. ; Boudewijns, Z.S.R.M. ; Narayanan, R.T. ; Baayen, J.C. ; Segev, I ; Mansvelder, H.D. ; de Kock, C.P.J. / Dendritic and Axonal Architecture of Individual Pyramidal Neurons across Layers of Adult Human Neocortex. In: Cerebral Cortex. 2015 ; Vol. 25, No. 12. pp. 4839-4853.
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abstract = "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.",
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Mohan, H, Verhoog, MB, Doreswamy, KK, Eyal, G, Aardse, R, Lodder, BN, Goriounova, NA, Asamoah, B, Brakspear, AB, Groot, C, van der Sluis, S, Testa-Silva, G, Obermayer, JMG, Boudewijns, ZSRM, Narayanan, RT, Baayen, JC, Segev, I, Mansvelder, HD & de Kock, CPJ 2015, 'Dendritic and Axonal Architecture of Individual Pyramidal Neurons across Layers of Adult Human Neocortex.' Cerebral Cortex, vol. 25, no. 12, pp. 4839-4853. https://doi.org/10.1093/cercor/bhv188

Dendritic and Axonal Architecture of Individual Pyramidal Neurons across Layers of Adult Human Neocortex. / Mohan, H.; Verhoog, M.B.; Doreswamy, K.K.; Eyal, G.; Aardse, R.; Lodder, B.N.; Goriounova, N.A.; Asamoah, B.; Brakspear, A.B.; Groot, C.; van der Sluis, S.; Testa-Silva, G.; Obermayer, J.M.G.; Boudewijns, Z.S.R.M.; Narayanan, R.T.; Baayen, J.C.; Segev, I; Mansvelder, H.D.; de Kock, C.P.J.

In: Cerebral Cortex, Vol. 25, No. 12, 2015, p. 4839-4853.

Research output: Contribution to JournalArticleAcademicpeer-review

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T1 - Dendritic and Axonal Architecture of Individual Pyramidal Neurons across Layers of Adult Human Neocortex.

AU - Mohan, H.

AU - Verhoog, M.B.

AU - Doreswamy, K.K.

AU - Eyal, G.

AU - Aardse, R.

AU - Lodder, B.N.

AU - Goriounova, N.A.

AU - Asamoah, B.

AU - Brakspear, A.B.

AU - Groot, C.

AU - van der Sluis, S.

AU - Testa-Silva, G.

AU - Obermayer, J.M.G.

AU - Boudewijns, Z.S.R.M.

AU - Narayanan, R.T.

AU - Baayen, J.C.

AU - Segev, I

AU - Mansvelder, H.D.

AU - de Kock, C.P.J.

PY - 2015

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N2 - 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.

AB - 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.

U2 - 10.1093/cercor/bhv188

DO - 10.1093/cercor/bhv188

M3 - Article

VL - 25

SP - 4839

EP - 4853

JO - Cerebral Cortex

JF - Cerebral Cortex

SN - 1047-3211

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ER -