Comparison of the Upper Marginal Neurons of Cortical Layer 2 with Layer 2/3 Pyramidal Neurons in Mouse Temporal Cortex
Layer 2/3 (L2/3) excitatory neurons in the neocortex make major contributions to corticocortical connections and therefore function to integrate information across cortical areas and hemispheres. Recent evidence suggests that excitatory neurons in L2/3 can have different properties. Sparse evidence...
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doaj-707292b500364210aca55c2aebd9c0e12020-11-25T00:59:06ZengFrontiers Media S.A.Frontiers in Neuroanatomy1662-51292017-12-011110.3389/fnana.2017.00115316067Comparison of the Upper Marginal Neurons of Cortical Layer 2 with Layer 2/3 Pyramidal Neurons in Mouse Temporal CortexHuan Luo0Huan Luo1Kayoko Hasegawa2Mingsheng Liu3Wen-Jie Song4Wen-Jie Song5Department of Sensory and Cognitive Physiology, Graduate School of Medical Sciences, Kumamoto University, Kumamoto, JapanProgram for Leading Graduate Schools HIGO Program, Kumamoto University, Kumamoto, JapanDepartment of Sensory and Cognitive Physiology, Graduate School of Medical Sciences, Kumamoto University, Kumamoto, JapanDepartment of Neurology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences, Beijing, ChinaDepartment of Sensory and Cognitive Physiology, Graduate School of Medical Sciences, Kumamoto University, Kumamoto, JapanProgram for Leading Graduate Schools HIGO Program, Kumamoto University, Kumamoto, JapanLayer 2/3 (L2/3) excitatory neurons in the neocortex make major contributions to corticocortical connections and therefore function to integrate information across cortical areas and hemispheres. Recent evidence suggests that excitatory neurons in L2/3 can have different properties. Sparse evidence from previous studies suggests that L2 neurons located at the border between L1 and L2 (referred to as L2 marginal neurons, L2MNs), have a morphology distinct from a typical pyramidal neuron. However, whether the membrane properties and input/output properties of L2MNs are different from those of typical pyramidal neurons in L2/3 is unknown. Here we addressed these questions in a slice preparation of mouse temporal cortex. We found that L2MNs were homogeneous in intrinsic membrane properties but appeared diverse in morphology. In agreement with previous studies, L2MNs either had oblique apical dendrites or had no obvious apical dendrites. The tufts of both apical and basal dendrites of these neurons invaded L1 extensively. All L2MNs showed a regular firing pattern with moderate adaptation. Compared with typical L2/3 pyramidal neurons that showed regular spiking (RS) activity (neurons), L2MNs showed a higher firing rate, larger sag ratio, and higher input resistance. No difference in the amplitude of excitatory and inhibitory postsynaptic potentials (EPSPs and IPSPs, respectively), evoked by stimulation of L1, was found between the two types of neurons, but the IPSPs in L2MNs had a slower time course than those in L2/3 RS cells. In paired recordings, unitary EPSPs showed no significant differences between synapses formed by L2MNs and those formed by L2/3 RS neurons. However, short-term synaptic depression (STSD) examined with a L2MN as the presynaptic neuron was greater when another L2MN was the postsynaptic neuron than when a L2/3 RS neuron was the postsynaptic neuron. The distinct morphological features of L2MNs found here have developmental implications, and the differences in electrophysiological properties between L2MNs and other L2/3 pyramidal neurons suggest that they play different functional roles in cortical networks.http://journal.frontiersin.org/article/10.3389/fnana.2017.00115/fullneuronal morphologyregular spikingintrinsic propertiessynaptic depressioncortex anatomy |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Huan Luo Huan Luo Kayoko Hasegawa Mingsheng Liu Wen-Jie Song Wen-Jie Song |
spellingShingle |
Huan Luo Huan Luo Kayoko Hasegawa Mingsheng Liu Wen-Jie Song Wen-Jie Song Comparison of the Upper Marginal Neurons of Cortical Layer 2 with Layer 2/3 Pyramidal Neurons in Mouse Temporal Cortex Frontiers in Neuroanatomy neuronal morphology regular spiking intrinsic properties synaptic depression cortex anatomy |
author_facet |
Huan Luo Huan Luo Kayoko Hasegawa Mingsheng Liu Wen-Jie Song Wen-Jie Song |
author_sort |
Huan Luo |
title |
Comparison of the Upper Marginal Neurons of Cortical Layer 2 with Layer 2/3 Pyramidal Neurons in Mouse Temporal Cortex |
title_short |
Comparison of the Upper Marginal Neurons of Cortical Layer 2 with Layer 2/3 Pyramidal Neurons in Mouse Temporal Cortex |
title_full |
Comparison of the Upper Marginal Neurons of Cortical Layer 2 with Layer 2/3 Pyramidal Neurons in Mouse Temporal Cortex |
title_fullStr |
Comparison of the Upper Marginal Neurons of Cortical Layer 2 with Layer 2/3 Pyramidal Neurons in Mouse Temporal Cortex |
title_full_unstemmed |
Comparison of the Upper Marginal Neurons of Cortical Layer 2 with Layer 2/3 Pyramidal Neurons in Mouse Temporal Cortex |
title_sort |
comparison of the upper marginal neurons of cortical layer 2 with layer 2/3 pyramidal neurons in mouse temporal cortex |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Neuroanatomy |
issn |
1662-5129 |
publishDate |
2017-12-01 |
description |
Layer 2/3 (L2/3) excitatory neurons in the neocortex make major contributions to corticocortical connections and therefore function to integrate information across cortical areas and hemispheres. Recent evidence suggests that excitatory neurons in L2/3 can have different properties. Sparse evidence from previous studies suggests that L2 neurons located at the border between L1 and L2 (referred to as L2 marginal neurons, L2MNs), have a morphology distinct from a typical pyramidal neuron. However, whether the membrane properties and input/output properties of L2MNs are different from those of typical pyramidal neurons in L2/3 is unknown. Here we addressed these questions in a slice preparation of mouse temporal cortex. We found that L2MNs were homogeneous in intrinsic membrane properties but appeared diverse in morphology. In agreement with previous studies, L2MNs either had oblique apical dendrites or had no obvious apical dendrites. The tufts of both apical and basal dendrites of these neurons invaded L1 extensively. All L2MNs showed a regular firing pattern with moderate adaptation. Compared with typical L2/3 pyramidal neurons that showed regular spiking (RS) activity (neurons), L2MNs showed a higher firing rate, larger sag ratio, and higher input resistance. No difference in the amplitude of excitatory and inhibitory postsynaptic potentials (EPSPs and IPSPs, respectively), evoked by stimulation of L1, was found between the two types of neurons, but the IPSPs in L2MNs had a slower time course than those in L2/3 RS cells. In paired recordings, unitary EPSPs showed no significant differences between synapses formed by L2MNs and those formed by L2/3 RS neurons. However, short-term synaptic depression (STSD) examined with a L2MN as the presynaptic neuron was greater when another L2MN was the postsynaptic neuron than when a L2/3 RS neuron was the postsynaptic neuron. The distinct morphological features of L2MNs found here have developmental implications, and the differences in electrophysiological properties between L2MNs and other L2/3 pyramidal neurons suggest that they play different functional roles in cortical networks. |
topic |
neuronal morphology regular spiking intrinsic properties synaptic depression cortex anatomy |
url |
http://journal.frontiersin.org/article/10.3389/fnana.2017.00115/full |
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