Bottom-up inputs are required for establishment of top-down connectivity onto cortical layer 1 neurogliaform cells.

Leena Ali Ibrahim; Shuhan Huang; Marian Fernandez-Otero; Mia Sherer; Yanjie Qiu; Spurti Vemuri; Qing Xu; Robert Machold; Gabrielle Pouchelon; Bernardo Rudy; Gord Fishell

doi:10.1016/j.neuron.2021.08.004

Bottom-up inputs are required for establishment of top-down connectivity onto cortical layer 1 neurogliaform cells.

Leena Ali Ibrahim, Shuhan Huang, Marian Fernandez-Otero, Mia Sherer, Yanjie Qiu, Spurti Vemuri, Qing Xu, Robert Machold, Gabrielle Pouchelon, Bernardo Rudy, Gord Fishell

King Abdullah University of Science and Technology

Research output: Contribution to journal › Article › peer-review

24 Scopus citations

Abstract

Higher-order projections to sensory cortical areas converge on layer 1 (L1), the primary site for integration of top-down information via the apical dendrites of pyramidal neurons and L1 GABAergic interneurons. Here we investigated the contribution of early thalamic inputs onto L1 interneurons for establishment of top-down connectivity in the primary visual cortex. We find that bottom-up thalamic inputs predominate during L1 development and preferentially target neurogliaform cells. We show that these projections are critical for the subsequent strengthening of top-down inputs from the anterior cingulate cortex onto L1 neurogliaform cells. Sensory deprivation or selective removal of thalamic afferents blocked this phenomenon. Although early activation of the anterior cingulate cortex resulted in premature strengthening of these top-down afferents, this was dependent on thalamic inputs. Our results demonstrate that proper establishment of top-down connectivity in the visual cortex depends critically on bottom-up inputs from the thalamus during postnatal development.

Original language	English (US)
Journal	Neuron
DOIs	https://doi.org/10.1016/j.neuron.2021.08.004
State	Published - Sep 3 2021

Bibliographical note

KAUST Repository Item: Exported on 2021-09-06
Acknowledgements: We thank Dr. Anne Takesian and Dr. Chinfei Chen for their valuable comments on the manuscript. We also thank Dr. Shruti Muralidhar for proofreading the manuscript. We thank Dr. Tim Burbridge for demonstrating retinal injections. This work was supported by a Goldenson Foundation grant (FY18) and a Hearst Foundation grant (FY19) (to L.A.I.), grants from the National Institutes of Health (NIH) (MH071679, NS08297, NS074972, and MH095147 to G.F. and P01NS074972, R01NS107257, and R01NS110079 to B.R.), as well as support from the Simons Foundation (SFARI to G.F.).

ASJC Scopus subject areas

General Neuroscience

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10.1016/j.neuron.2021.08.004

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title = "Bottom-up inputs are required for establishment of top-down connectivity onto cortical layer 1 neurogliaform cells.",

abstract = "Higher-order projections to sensory cortical areas converge on layer 1 (L1), the primary site for integration of top-down information via the apical dendrites of pyramidal neurons and L1 GABAergic interneurons. Here we investigated the contribution of early thalamic inputs onto L1 interneurons for establishment of top-down connectivity in the primary visual cortex. We find that bottom-up thalamic inputs predominate during L1 development and preferentially target neurogliaform cells. We show that these projections are critical for the subsequent strengthening of top-down inputs from the anterior cingulate cortex onto L1 neurogliaform cells. Sensory deprivation or selective removal of thalamic afferents blocked this phenomenon. Although early activation of the anterior cingulate cortex resulted in premature strengthening of these top-down afferents, this was dependent on thalamic inputs. Our results demonstrate that proper establishment of top-down connectivity in the visual cortex depends critically on bottom-up inputs from the thalamus during postnatal development.",

author = "Ibrahim, {Leena Ali} and Shuhan Huang and Marian Fernandez-Otero and Mia Sherer and Yanjie Qiu and Spurti Vemuri and Qing Xu and Robert Machold and Gabrielle Pouchelon and Bernardo Rudy and Gord Fishell",

note = "KAUST Repository Item: Exported on 2021-09-06 Acknowledgements: We thank Dr. Anne Takesian and Dr. Chinfei Chen for their valuable comments on the manuscript. We also thank Dr. Shruti Muralidhar for proofreading the manuscript. We thank Dr. Tim Burbridge for demonstrating retinal injections. This work was supported by a Goldenson Foundation grant (FY18) and a Hearst Foundation grant (FY19) (to L.A.I.), grants from the National Institutes of Health (NIH) (MH071679, NS08297, NS074972, and MH095147 to G.F. and P01NS074972, R01NS107257, and R01NS110079 to B.R.), as well as support from the Simons Foundation (SFARI to G.F.).",

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AU - Ibrahim, Leena Ali

AU - Huang, Shuhan

AU - Fernandez-Otero, Marian

AU - Sherer, Mia

AU - Qiu, Yanjie

AU - Vemuri, Spurti

AU - Xu, Qing

AU - Machold, Robert

AU - Pouchelon, Gabrielle

AU - Rudy, Bernardo

AU - Fishell, Gord

N1 - KAUST Repository Item: Exported on 2021-09-06 Acknowledgements: We thank Dr. Anne Takesian and Dr. Chinfei Chen for their valuable comments on the manuscript. We also thank Dr. Shruti Muralidhar for proofreading the manuscript. We thank Dr. Tim Burbridge for demonstrating retinal injections. This work was supported by a Goldenson Foundation grant (FY18) and a Hearst Foundation grant (FY19) (to L.A.I.), grants from the National Institutes of Health (NIH) (MH071679, NS08297, NS074972, and MH095147 to G.F. and P01NS074972, R01NS107257, and R01NS110079 to B.R.), as well as support from the Simons Foundation (SFARI to G.F.).

PY - 2021/9/3

Y1 - 2021/9/3

N2 - Higher-order projections to sensory cortical areas converge on layer 1 (L1), the primary site for integration of top-down information via the apical dendrites of pyramidal neurons and L1 GABAergic interneurons. Here we investigated the contribution of early thalamic inputs onto L1 interneurons for establishment of top-down connectivity in the primary visual cortex. We find that bottom-up thalamic inputs predominate during L1 development and preferentially target neurogliaform cells. We show that these projections are critical for the subsequent strengthening of top-down inputs from the anterior cingulate cortex onto L1 neurogliaform cells. Sensory deprivation or selective removal of thalamic afferents blocked this phenomenon. Although early activation of the anterior cingulate cortex resulted in premature strengthening of these top-down afferents, this was dependent on thalamic inputs. Our results demonstrate that proper establishment of top-down connectivity in the visual cortex depends critically on bottom-up inputs from the thalamus during postnatal development.

AB - Higher-order projections to sensory cortical areas converge on layer 1 (L1), the primary site for integration of top-down information via the apical dendrites of pyramidal neurons and L1 GABAergic interneurons. Here we investigated the contribution of early thalamic inputs onto L1 interneurons for establishment of top-down connectivity in the primary visual cortex. We find that bottom-up thalamic inputs predominate during L1 development and preferentially target neurogliaform cells. We show that these projections are critical for the subsequent strengthening of top-down inputs from the anterior cingulate cortex onto L1 neurogliaform cells. Sensory deprivation or selective removal of thalamic afferents blocked this phenomenon. Although early activation of the anterior cingulate cortex resulted in premature strengthening of these top-down afferents, this was dependent on thalamic inputs. Our results demonstrate that proper establishment of top-down connectivity in the visual cortex depends critically on bottom-up inputs from the thalamus during postnatal development.

UR - http://hdl.handle.net/10754/670921

UR - https://linkinghub.elsevier.com/retrieve/pii/S0896627321005791

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DO - 10.1016/j.neuron.2021.08.004

M3 - Article

C2 - 34478630

SN - 0896-6273

JO - Neuron

JF - Neuron

ER -

Bottom-up inputs are required for establishment of top-down connectivity onto cortical layer 1 neurogliaform cells.

Abstract

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