The Protracted Maturation of Associative Layer IIIC Pyramidal Neurons in the Human Prefrontal Cortex During Childhood: A Major Role in Cognitive Development and Selective Alteration in Autism
The human specific cognitive shift starts around the age of 2 years with the onset of self-awareness, and continues with extraordinary increase in cognitive capacities during early childhood. Diffuse changes in functional connectivity in children aged 2–6 years indicate an increase in the capacity o...
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Frontiers Media S.A.
2019-03-01
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| Series: | Frontiers in Psychiatry |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fpsyt.2019.00122/full |
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| author | Zdravko Petanjek Zdravko Petanjek Zdravko Petanjek Dora Sedmak Dora Sedmak Dora Sedmak Domagoj Džaja Domagoj Džaja Domagoj Džaja Ana Hladnik Ana Hladnik Ana Hladnik Mladen Roko Rašin Nataša Jovanov-Milosevic Nataša Jovanov-Milosevic Nataša Jovanov-Milosevic |
| author_facet | Zdravko Petanjek Zdravko Petanjek Zdravko Petanjek Dora Sedmak Dora Sedmak Dora Sedmak Domagoj Džaja Domagoj Džaja Domagoj Džaja Ana Hladnik Ana Hladnik Ana Hladnik Mladen Roko Rašin Nataša Jovanov-Milosevic Nataša Jovanov-Milosevic Nataša Jovanov-Milosevic |
| author_sort | Zdravko Petanjek |
| collection | DOAJ |
| description | The human specific cognitive shift starts around the age of 2 years with the onset of self-awareness, and continues with extraordinary increase in cognitive capacities during early childhood. Diffuse changes in functional connectivity in children aged 2–6 years indicate an increase in the capacity of cortical network. Interestingly, structural network complexity does not increase during this time and, thus, it is likely to be induced by selective maturation of a specific neuronal subclass. Here, we provide an overview of a subclass of cortico-cortical neurons, the associative layer IIIC pyramids of the human prefrontal cortex. Their local axonal collaterals are in control of the prefrontal cortico-cortical output, while their long projections modulate inter-areal processing. In this way, layer IIIC pyramids are the major integrative element of cortical processing, and changes in their connectivity patterns will affect global cortical functioning. Layer IIIC neurons have a unique pattern of dendritic maturation. In contrast to other classes of principal neurons, they undergo an additional phase of extensive dendritic growth during early childhood, and show characteristic molecular changes. Taken together, circuits associated with layer IIIC neurons have the most protracted period of developmental plasticity. This unique feature is advanced but also provides a window of opportunity for pathological events to disrupt normal formation of cognitive circuits involving layer IIIC neurons. In this manuscript, we discuss how disrupted dendritic and axonal maturation of layer IIIC neurons may lead into global cortical disconnectivity, affecting development of complex communication and social abilities. We also propose a model that developmentally dictated incorporation of layer IIIC neurons into maturing cortico-cortical circuits between 2 to 6 years will reveal a previous (perinatal) lesion affecting other classes of principal neurons. This “disclosure” of pre-existing functionally silent lesions of other neuronal classes induced by development of layer IIIC associative neurons, or their direct alteration, could be found in different forms of autism spectrum disorders. Understanding the gene-environment interaction in shaping cognitive microcircuitries may be fundamental for developing rehabilitation and prevention strategies in autism spectrum and other cognitive disorders. |
| first_indexed | 2024-12-22T19:50:44Z |
| format | Article |
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| institution | Directory Open Access Journal |
| issn | 1664-0640 |
| language | English |
| last_indexed | 2024-12-22T19:50:44Z |
| publishDate | 2019-03-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Psychiatry |
| spelling | doaj.art-ae6a59455358475f92473186eb0245ac2022-12-21T18:14:34ZengFrontiers Media S.A.Frontiers in Psychiatry1664-06402019-03-011010.3389/fpsyt.2019.00122411601The Protracted Maturation of Associative Layer IIIC Pyramidal Neurons in the Human Prefrontal Cortex During Childhood: A Major Role in Cognitive Development and Selective Alteration in AutismZdravko Petanjek0Zdravko Petanjek1Zdravko Petanjek2Dora Sedmak3Dora Sedmak4Dora Sedmak5Domagoj Džaja6Domagoj Džaja7Domagoj Džaja8Ana Hladnik9Ana Hladnik10Ana Hladnik11Mladen Roko Rašin12Nataša Jovanov-Milosevic13Nataša Jovanov-Milosevic14Nataša Jovanov-Milosevic15Department of Anatomy and Clinical Anatomy, School of Medicine, University of Zagreb, Zagreb, CroatiaDepartment of Neuroscience, Croatian Institute for Brain Research, School of Medicine, University of Zagreb, Zagreb, CroatiaCenter of Excellence for Basic, Clinical and Translational Neuroscience, School of Medicine, University of Zagreb, Zagreb, CroatiaDepartment of Anatomy and Clinical Anatomy, School of Medicine, University of Zagreb, Zagreb, CroatiaDepartment of Neuroscience, Croatian Institute for Brain Research, School of Medicine, University of Zagreb, Zagreb, CroatiaCenter of Excellence for Basic, Clinical and Translational Neuroscience, School of Medicine, University of Zagreb, Zagreb, CroatiaDepartment of Anatomy and Clinical Anatomy, School of Medicine, University of Zagreb, Zagreb, CroatiaDepartment of Neuroscience, Croatian Institute for Brain Research, School of Medicine, University of Zagreb, Zagreb, CroatiaCenter of Excellence for Basic, Clinical and Translational Neuroscience, School of Medicine, University of Zagreb, Zagreb, CroatiaDepartment of Anatomy and Clinical Anatomy, School of Medicine, University of Zagreb, Zagreb, CroatiaDepartment of Neuroscience, Croatian Institute for Brain Research, School of Medicine, University of Zagreb, Zagreb, CroatiaCenter of Excellence for Basic, Clinical and Translational Neuroscience, School of Medicine, University of Zagreb, Zagreb, CroatiaDepartment of Neuroscience and Cell Biology, Rutgers University, Robert Wood Johnson Medical School, Piscataway, NJ, United StatesDepartment of Neuroscience, Croatian Institute for Brain Research, School of Medicine, University of Zagreb, Zagreb, CroatiaCenter of Excellence for Basic, Clinical and Translational Neuroscience, School of Medicine, University of Zagreb, Zagreb, CroatiaDepartment of Medical Biology, School of Medicine, University of Zagreb, Zagreb, CroatiaThe human specific cognitive shift starts around the age of 2 years with the onset of self-awareness, and continues with extraordinary increase in cognitive capacities during early childhood. Diffuse changes in functional connectivity in children aged 2–6 years indicate an increase in the capacity of cortical network. Interestingly, structural network complexity does not increase during this time and, thus, it is likely to be induced by selective maturation of a specific neuronal subclass. Here, we provide an overview of a subclass of cortico-cortical neurons, the associative layer IIIC pyramids of the human prefrontal cortex. Their local axonal collaterals are in control of the prefrontal cortico-cortical output, while their long projections modulate inter-areal processing. In this way, layer IIIC pyramids are the major integrative element of cortical processing, and changes in their connectivity patterns will affect global cortical functioning. Layer IIIC neurons have a unique pattern of dendritic maturation. In contrast to other classes of principal neurons, they undergo an additional phase of extensive dendritic growth during early childhood, and show characteristic molecular changes. Taken together, circuits associated with layer IIIC neurons have the most protracted period of developmental plasticity. This unique feature is advanced but also provides a window of opportunity for pathological events to disrupt normal formation of cognitive circuits involving layer IIIC neurons. In this manuscript, we discuss how disrupted dendritic and axonal maturation of layer IIIC neurons may lead into global cortical disconnectivity, affecting development of complex communication and social abilities. We also propose a model that developmentally dictated incorporation of layer IIIC neurons into maturing cortico-cortical circuits between 2 to 6 years will reveal a previous (perinatal) lesion affecting other classes of principal neurons. This “disclosure” of pre-existing functionally silent lesions of other neuronal classes induced by development of layer IIIC associative neurons, or their direct alteration, could be found in different forms of autism spectrum disorders. Understanding the gene-environment interaction in shaping cognitive microcircuitries may be fundamental for developing rehabilitation and prevention strategies in autism spectrum and other cognitive disorders.https://www.frontiersin.org/article/10.3389/fpsyt.2019.00122/fullcerebral cortextheory of mindcortico-cortical neuronsdendritic developmentschizophreniaexcitatory transmission |
| spellingShingle | Zdravko Petanjek Zdravko Petanjek Zdravko Petanjek Dora Sedmak Dora Sedmak Dora Sedmak Domagoj Džaja Domagoj Džaja Domagoj Džaja Ana Hladnik Ana Hladnik Ana Hladnik Mladen Roko Rašin Nataša Jovanov-Milosevic Nataša Jovanov-Milosevic Nataša Jovanov-Milosevic The Protracted Maturation of Associative Layer IIIC Pyramidal Neurons in the Human Prefrontal Cortex During Childhood: A Major Role in Cognitive Development and Selective Alteration in Autism Frontiers in Psychiatry cerebral cortex theory of mind cortico-cortical neurons dendritic development schizophrenia excitatory transmission |
| title | The Protracted Maturation of Associative Layer IIIC Pyramidal Neurons in the Human Prefrontal Cortex During Childhood: A Major Role in Cognitive Development and Selective Alteration in Autism |
| title_full | The Protracted Maturation of Associative Layer IIIC Pyramidal Neurons in the Human Prefrontal Cortex During Childhood: A Major Role in Cognitive Development and Selective Alteration in Autism |
| title_fullStr | The Protracted Maturation of Associative Layer IIIC Pyramidal Neurons in the Human Prefrontal Cortex During Childhood: A Major Role in Cognitive Development and Selective Alteration in Autism |
| title_full_unstemmed | The Protracted Maturation of Associative Layer IIIC Pyramidal Neurons in the Human Prefrontal Cortex During Childhood: A Major Role in Cognitive Development and Selective Alteration in Autism |
| title_short | The Protracted Maturation of Associative Layer IIIC Pyramidal Neurons in the Human Prefrontal Cortex During Childhood: A Major Role in Cognitive Development and Selective Alteration in Autism |
| title_sort | protracted maturation of associative layer iiic pyramidal neurons in the human prefrontal cortex during childhood a major role in cognitive development and selective alteration in autism |
| topic | cerebral cortex theory of mind cortico-cortical neurons dendritic development schizophrenia excitatory transmission |
| url | https://www.frontiersin.org/article/10.3389/fpsyt.2019.00122/full |
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