Non-canonical role for Lpar1-EGFP subplate neurons in early postnatal mouse somatosensory cortex

Filippo Ghezzi; Andre Marques-Smith; Paul G Anastasiades; Daniel Lyngholm; Cristiana Vagnoni; Alexandra Rowett; Gokul Parameswaran; Anna Hoerder-Suabedissen; Yasushi Nakagawa; Zoltan Molnar; Simon J B Butt

doi:10.7554/eLife.60810

Non-canonical role for Lpar1-EGFP subplate neurons in early postnatal mouse somatosensory cortex

Filippo Ghezzi, Andre Marques-Smith, Paul G Anastasiades, Daniel Lyngholm, Cristiana Vagnoni, Alexandra Rowett, Gokul Parameswaran, Anna Hoerder-Suabedissen, Yasushi Nakagawa, Zoltan Molnar, Simon J B Butt^*

^*Corresponding author for this work

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Abstract

Subplate neurons (SPNs) are thought to play a role in nascent sensory processing in neocortex. To better understand how heterogeneity within this population relates to emergent function, we investigated the synaptic connectivity of Lpar1-EGFP SPNs through the first postnatal week in whisker somatosensory cortex (S1BF). These SPNs comprise of two morphological subtypes: fusiform SPNs with local axons and pyramidal SPNs with axons that extend through the marginal zone. The former receive translaminar synaptic input up until the emergence of the whisker barrels, a timepoint coincident with significant cell death. In contrast, pyramidal SPNs receive local input from the subplate at early ages but then – during the later time window – acquire input from overlying cortex. Combined electrical and optogenetic activation of thalamic afferents identified that Lpar1-EGFP SPNs receive sparse thalamic innervation. These data reveal components of the postnatal network that interpret sparse thalamic input to direct the emergent columnar structure of S1BF.

Original language	English
Article number	e60810
Number of pages	24
Journal	eLife
Volume	10
DOIs	https://doi.org/10.7554/eLife.60810
Publication status	Published - 12 Jul 2021

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Funding Information:
Research in the Butt lab that contributed to this work was funded by the Medical Research Council (MRC)(MR/K004387/1), Biotechnology and Biological Sciences Research Council (BB/P003796/1), Human Frontiers Science Program Organisation (CDA0023/2008 C), and Brain and Behavior Research Foundation (Narsad; ref 19079). Studentships awarded to FG and AM-S were funded by the Wellcome Trust; PGA was funded by an Imperial College London studentship; CV was funded by an MRC studentship. Funding for equipment came from the Wellcome Trust (089286/Z/09/Z) and OUP John Fell Fund (AV6721-C8000). Work in the Molnár laboratory related to early cortical circuit formation was funded by the MRC (G00900901, MR/N026039/1), Royal Society, and Anatomical Society.

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© Ghezzi et al.

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title = "Non-canonical role for Lpar1-EGFP subplate neurons in early postnatal mouse somatosensory cortex",

abstract = "Subplate neurons (SPNs) are thought to play a role in nascent sensory processing in neocortex. To better understand how heterogeneity within this population relates to emergent function, we investigated the synaptic connectivity of Lpar1-EGFP SPNs through the first postnatal week in whisker somatosensory cortex (S1BF). These SPNs comprise of two morphological subtypes: fusiform SPNs with local axons and pyramidal SPNs with axons that extend through the marginal zone. The former receive translaminar synaptic input up until the emergence of the whisker barrels, a timepoint coincident with significant cell death. In contrast, pyramidal SPNs receive local input from the subplate at early ages but then – during the later time window – acquire input from overlying cortex. Combined electrical and optogenetic activation of thalamic afferents identified that Lpar1-EGFP SPNs receive sparse thalamic innervation. These data reveal components of the postnatal network that interpret sparse thalamic input to direct the emergent columnar structure of S1BF.",

author = "Filippo Ghezzi and Andre Marques-Smith and Anastasiades, {Paul G} and Daniel Lyngholm and Cristiana Vagnoni and Alexandra Rowett and Gokul Parameswaran and Anna Hoerder-Suabedissen and Yasushi Nakagawa and Zoltan Molnar and Butt, {Simon J B}",

note = "Funding Information: Research in the Butt lab that contributed to this work was funded by the Medical Research Council (MRC)(MR/K004387/1), Biotechnology and Biological Sciences Research Council (BB/P003796/1), Human Frontiers Science Program Organisation (CDA0023/2008 C), and Brain and Behavior Research Foundation (Narsad; ref 19079). Studentships awarded to FG and AM-S were funded by the Wellcome Trust; PGA was funded by an Imperial College London studentship; CV was funded by an MRC studentship. Funding for equipment came from the Wellcome Trust (089286/Z/09/Z) and OUP John Fell Fund (AV6721-C8000). Work in the Moln{\'a}r laboratory related to early cortical circuit formation was funded by the MRC (G00900901, MR/N026039/1), Royal Society, and Anatomical Society. Publisher Copyright: {\textcopyright} Ghezzi et al.",

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AU - Ghezzi, Filippo

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AU - Anastasiades, Paul G

AU - Lyngholm, Daniel

AU - Vagnoni, Cristiana

AU - Rowett, Alexandra

AU - Parameswaran, Gokul

AU - Hoerder-Suabedissen, Anna

AU - Nakagawa, Yasushi

AU - Molnar, Zoltan

AU - Butt, Simon J B

N1 - Funding Information: Research in the Butt lab that contributed to this work was funded by the Medical Research Council (MRC)(MR/K004387/1), Biotechnology and Biological Sciences Research Council (BB/P003796/1), Human Frontiers Science Program Organisation (CDA0023/2008 C), and Brain and Behavior Research Foundation (Narsad; ref 19079). Studentships awarded to FG and AM-S were funded by the Wellcome Trust; PGA was funded by an Imperial College London studentship; CV was funded by an MRC studentship. Funding for equipment came from the Wellcome Trust (089286/Z/09/Z) and OUP John Fell Fund (AV6721-C8000). Work in the Molnár laboratory related to early cortical circuit formation was funded by the MRC (G00900901, MR/N026039/1), Royal Society, and Anatomical Society. Publisher Copyright: © Ghezzi et al.

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N2 - Subplate neurons (SPNs) are thought to play a role in nascent sensory processing in neocortex. To better understand how heterogeneity within this population relates to emergent function, we investigated the synaptic connectivity of Lpar1-EGFP SPNs through the first postnatal week in whisker somatosensory cortex (S1BF). These SPNs comprise of two morphological subtypes: fusiform SPNs with local axons and pyramidal SPNs with axons that extend through the marginal zone. The former receive translaminar synaptic input up until the emergence of the whisker barrels, a timepoint coincident with significant cell death. In contrast, pyramidal SPNs receive local input from the subplate at early ages but then – during the later time window – acquire input from overlying cortex. Combined electrical and optogenetic activation of thalamic afferents identified that Lpar1-EGFP SPNs receive sparse thalamic innervation. These data reveal components of the postnatal network that interpret sparse thalamic input to direct the emergent columnar structure of S1BF.

AB - Subplate neurons (SPNs) are thought to play a role in nascent sensory processing in neocortex. To better understand how heterogeneity within this population relates to emergent function, we investigated the synaptic connectivity of Lpar1-EGFP SPNs through the first postnatal week in whisker somatosensory cortex (S1BF). These SPNs comprise of two morphological subtypes: fusiform SPNs with local axons and pyramidal SPNs with axons that extend through the marginal zone. The former receive translaminar synaptic input up until the emergence of the whisker barrels, a timepoint coincident with significant cell death. In contrast, pyramidal SPNs receive local input from the subplate at early ages but then – during the later time window – acquire input from overlying cortex. Combined electrical and optogenetic activation of thalamic afferents identified that Lpar1-EGFP SPNs receive sparse thalamic innervation. These data reveal components of the postnatal network that interpret sparse thalamic input to direct the emergent columnar structure of S1BF.

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DO - 10.7554/eLife.60810

M3 - Article (Academic Journal)

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SN - 2050-084X

VL - 10

JO - eLife

JF - eLife

M1 - e60810

ER -

Non-canonical role for Lpar1-EGFP subplate neurons in early postnatal mouse somatosensory cortex

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