Axonal connections between S1 barrel, M1, and S2 cortex in the newborn mouse

The development of functionally interconnected networks between primary (S1), secondary somatosensory (S2), and motor (M1) cortical areas requires coherent neuronal activity via corticocortical projections. However, the anatomical substrate of functional connections between S1 and M1 or S2 during ea...

Full description

Bibliographic Details
Main Authors: Levente Gellért, Heiko J. Luhmann, Werner Kilb
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-01-01
Series:Frontiers in Neuroanatomy
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnana.2023.1105998/full
_version_ 1797943920977510400
author Levente Gellért
Heiko J. Luhmann
Werner Kilb
author_facet Levente Gellért
Heiko J. Luhmann
Werner Kilb
author_sort Levente Gellért
collection DOAJ
description The development of functionally interconnected networks between primary (S1), secondary somatosensory (S2), and motor (M1) cortical areas requires coherent neuronal activity via corticocortical projections. However, the anatomical substrate of functional connections between S1 and M1 or S2 during early development remains elusive. In the present study, we used ex vivo carbocyanine dye (DiI) tracing in paraformaldehyde-fixed newborn mouse brain to investigate axonal projections of neurons in different layers of S1 barrel field (S1Bf), M1, and S2 toward the subplate (SP), a hub layer for sensory information transfer in the immature cortex. In addition, we performed extracellular recordings in neocortical slices to unravel the functional connectivity between these areas. Our experiments demonstrate that already at P0 neurons from the cortical plate (CP), layer 5/6 (L5/6), and the SP of both M1 and S2 send projections through the SP of S1Bf. Reciprocally, neurons from CP to SP of S1Bf send projections through the SP of M1 and S2. Electrophysiological recordings with multi-electrode arrays in cortical slices revealed weak, but functional synaptic connections between SP and L5/6 within and between S1 and M1. An even lower functional connectivity was observed between S1 and S2. In summary, our findings demonstrate that functional connections between SP and upper cortical layers are not confined to the same cortical area, but corticocortical connection between adjacent cortical areas exist already at the day of birth. Hereby, SP can integrate early cortical activity of M1, S1, and S2 and shape the development of sensorimotor integration at an early stage.
first_indexed 2024-04-10T20:31:45Z
format Article
id doaj.art-703837bdd2754352a52652e80cde218d
institution Directory Open Access Journal
issn 1662-5129
language English
last_indexed 2024-04-10T20:31:45Z
publishDate 2023-01-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Neuroanatomy
spelling doaj.art-703837bdd2754352a52652e80cde218d2023-01-25T05:36:15ZengFrontiers Media S.A.Frontiers in Neuroanatomy1662-51292023-01-011710.3389/fnana.2023.11059981105998Axonal connections between S1 barrel, M1, and S2 cortex in the newborn mouseLevente GellértHeiko J. LuhmannWerner KilbThe development of functionally interconnected networks between primary (S1), secondary somatosensory (S2), and motor (M1) cortical areas requires coherent neuronal activity via corticocortical projections. However, the anatomical substrate of functional connections between S1 and M1 or S2 during early development remains elusive. In the present study, we used ex vivo carbocyanine dye (DiI) tracing in paraformaldehyde-fixed newborn mouse brain to investigate axonal projections of neurons in different layers of S1 barrel field (S1Bf), M1, and S2 toward the subplate (SP), a hub layer for sensory information transfer in the immature cortex. In addition, we performed extracellular recordings in neocortical slices to unravel the functional connectivity between these areas. Our experiments demonstrate that already at P0 neurons from the cortical plate (CP), layer 5/6 (L5/6), and the SP of both M1 and S2 send projections through the SP of S1Bf. Reciprocally, neurons from CP to SP of S1Bf send projections through the SP of M1 and S2. Electrophysiological recordings with multi-electrode arrays in cortical slices revealed weak, but functional synaptic connections between SP and L5/6 within and between S1 and M1. An even lower functional connectivity was observed between S1 and S2. In summary, our findings demonstrate that functional connections between SP and upper cortical layers are not confined to the same cortical area, but corticocortical connection between adjacent cortical areas exist already at the day of birth. Hereby, SP can integrate early cortical activity of M1, S1, and S2 and shape the development of sensorimotor integration at an early stage.https://www.frontiersin.org/articles/10.3389/fnana.2023.1105998/fullcortical developmentnewborn mousesubplatesensorimotor integrationbarrel fieldmotor cortex
spellingShingle Levente Gellért
Heiko J. Luhmann
Werner Kilb
Axonal connections between S1 barrel, M1, and S2 cortex in the newborn mouse
Frontiers in Neuroanatomy
cortical development
newborn mouse
subplate
sensorimotor integration
barrel field
motor cortex
title Axonal connections between S1 barrel, M1, and S2 cortex in the newborn mouse
title_full Axonal connections between S1 barrel, M1, and S2 cortex in the newborn mouse
title_fullStr Axonal connections between S1 barrel, M1, and S2 cortex in the newborn mouse
title_full_unstemmed Axonal connections between S1 barrel, M1, and S2 cortex in the newborn mouse
title_short Axonal connections between S1 barrel, M1, and S2 cortex in the newborn mouse
title_sort axonal connections between s1 barrel m1 and s2 cortex in the newborn mouse
topic cortical development
newborn mouse
subplate
sensorimotor integration
barrel field
motor cortex
url https://www.frontiersin.org/articles/10.3389/fnana.2023.1105998/full
work_keys_str_mv AT leventegellert axonalconnectionsbetweens1barrelm1ands2cortexinthenewbornmouse
AT heikojluhmann axonalconnectionsbetweens1barrelm1ands2cortexinthenewbornmouse
AT wernerkilb axonalconnectionsbetweens1barrelm1ands2cortexinthenewbornmouse