Sexual differences in neuronal and synaptic properties across subregions of the mouse insular cortex

Abstract Background The insular cortex (IC) plays a pivotal role in processing interoceptive and emotional information, offering insights into sex differences in behavior and cognition. The IC comprises two distinct subregions: the anterior insular cortex (aIC), that processes emotional and social s...

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Main Authors: Daniela Iezzi, Alba Cáceres-Rodríguez, Benjamin Strauss, Pascale Chavis, Olivier J. Manzoni
Format: Article
Language:English
Published: BMC 2024-04-01
Series:Biology of Sex Differences
Subjects:
Online Access:https://doi.org/10.1186/s13293-024-00593-4
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author Daniela Iezzi
Alba Cáceres-Rodríguez
Benjamin Strauss
Pascale Chavis
Olivier J. Manzoni
author_facet Daniela Iezzi
Alba Cáceres-Rodríguez
Benjamin Strauss
Pascale Chavis
Olivier J. Manzoni
author_sort Daniela Iezzi
collection DOAJ
description Abstract Background The insular cortex (IC) plays a pivotal role in processing interoceptive and emotional information, offering insights into sex differences in behavior and cognition. The IC comprises two distinct subregions: the anterior insular cortex (aIC), that processes emotional and social signals, and the posterior insular cortex (pIC), specialized in interoception and perception of pain. Pyramidal projection neurons within the IC integrate multimodal sensory inputs, influencing behavior and cognition. Despite previous research focusing on neuronal connectivity and transcriptomics, there has been a gap in understanding pyramidal neurons characteristics across subregions and between sexes. Methods Adult male and female C57Bl/6J mice were sacrificed and tissue containing the IC was collected for ex vivo slice electrophysiology recordings that examined baseline sex differences in synaptic plasticity and transmission within aIC and pIC subregions. Results Clear differences emerged between aIC and pIC neurons in both males and females: aIC neurons exhibited distinctive features such as larger size, increased hyperpolarization, and a higher rheobase compared to their pIC counterparts. Furthermore, we observed variations in neuronal excitability linked to sex, with male pIC neurons displaying a greater level of excitability than their female counterparts. We also identified region-specific differences in excitatory and inhibitory synaptic activity and the balance between excitation and inhibition in both male and female mice. Adult females demonstrated greater synaptic strength and maximum response in the aIC compared to the pIC. Lastly, synaptic long-term potentiation occurred in both subregions in males but was specific to the aIC in females. Conclusions We conclude that there are sex differences in synaptic plasticity and excitatory transmission in IC subregions, and that distinct properties of IC pyramidal neurons between sexes could contribute to differences in behavior and cognition between males and females.
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spelling doaj.art-752740cb745d4250b300389c8298ef262024-04-07T11:06:11ZengBMCBiology of Sex Differences2042-64102024-04-0115112110.1186/s13293-024-00593-4Sexual differences in neuronal and synaptic properties across subregions of the mouse insular cortexDaniela Iezzi0Alba Cáceres-Rodríguez1Benjamin Strauss2Pascale Chavis3Olivier J. Manzoni4INMED, INSERM U1249INMED, INSERM U1249INMED, INSERM U1249INMED, INSERM U1249INMED, INSERM U1249Abstract Background The insular cortex (IC) plays a pivotal role in processing interoceptive and emotional information, offering insights into sex differences in behavior and cognition. The IC comprises two distinct subregions: the anterior insular cortex (aIC), that processes emotional and social signals, and the posterior insular cortex (pIC), specialized in interoception and perception of pain. Pyramidal projection neurons within the IC integrate multimodal sensory inputs, influencing behavior and cognition. Despite previous research focusing on neuronal connectivity and transcriptomics, there has been a gap in understanding pyramidal neurons characteristics across subregions and between sexes. Methods Adult male and female C57Bl/6J mice were sacrificed and tissue containing the IC was collected for ex vivo slice electrophysiology recordings that examined baseline sex differences in synaptic plasticity and transmission within aIC and pIC subregions. Results Clear differences emerged between aIC and pIC neurons in both males and females: aIC neurons exhibited distinctive features such as larger size, increased hyperpolarization, and a higher rheobase compared to their pIC counterparts. Furthermore, we observed variations in neuronal excitability linked to sex, with male pIC neurons displaying a greater level of excitability than their female counterparts. We also identified region-specific differences in excitatory and inhibitory synaptic activity and the balance between excitation and inhibition in both male and female mice. Adult females demonstrated greater synaptic strength and maximum response in the aIC compared to the pIC. Lastly, synaptic long-term potentiation occurred in both subregions in males but was specific to the aIC in females. Conclusions We conclude that there are sex differences in synaptic plasticity and excitatory transmission in IC subregions, and that distinct properties of IC pyramidal neurons between sexes could contribute to differences in behavior and cognition between males and females.https://doi.org/10.1186/s13293-024-00593-4SexInsular cortexPyramidal neurons
spellingShingle Daniela Iezzi
Alba Cáceres-Rodríguez
Benjamin Strauss
Pascale Chavis
Olivier J. Manzoni
Sexual differences in neuronal and synaptic properties across subregions of the mouse insular cortex
Biology of Sex Differences
Sex
Insular cortex
Pyramidal neurons
title Sexual differences in neuronal and synaptic properties across subregions of the mouse insular cortex
title_full Sexual differences in neuronal and synaptic properties across subregions of the mouse insular cortex
title_fullStr Sexual differences in neuronal and synaptic properties across subregions of the mouse insular cortex
title_full_unstemmed Sexual differences in neuronal and synaptic properties across subregions of the mouse insular cortex
title_short Sexual differences in neuronal and synaptic properties across subregions of the mouse insular cortex
title_sort sexual differences in neuronal and synaptic properties across subregions of the mouse insular cortex
topic Sex
Insular cortex
Pyramidal neurons
url https://doi.org/10.1186/s13293-024-00593-4
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