Cortical hierarchy, dual counterstream architecture and the importance of top-down generative networks
Hierarchy is a major organizational principle of the cortex and underscores modern computational theories of cortical function. The local microcircuit amplifies long-distance inter-areal input, which show distance-dependent changes in their laminar profiles. Statistical modeling of these changes in...
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doaj-3a882e0becb64654a32ef3c72d2493d02020-12-17T04:47:15ZengElsevierNeuroImage1095-95722021-01-01225117479Cortical hierarchy, dual counterstream architecture and the importance of top-down generative networksJulien Vezoli0Loïc Magrou1Rainer Goebel2Xiao-Jing Wang3Kenneth Knoblauch4Martin Vinck5Henry Kennedy6Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, 60528 Frankfurt, GermanyUniv Lyon, Université Claude Bernard Lyon 1, Inserm, Stem Cell and Brain Research Institute U1208, 69500 Bron, FranceFaculty of Psychology and Neuroscience, Department of Cognitive Neuroscience, Maastricht University, P.O. Box 616, 6200 MD, Maastricht, the NetherlandsCenter for Neural Science, New York University (NYU), New York, NY 10003, USAUniv Lyon, Université Claude Bernard Lyon 1, Inserm, Stem Cell and Brain Research Institute U1208, 69500 Bron, FranceErnst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, 60528 Frankfurt, Germany; Corresponding author.Univ Lyon, Université Claude Bernard Lyon 1, Inserm, Stem Cell and Brain Research Institute U1208, 69500 Bron, France; Institute of Neuroscience, State Key Laboratory of Neuroscience, Chinese Academy of Sciences (CAS) Key Laboratory of Primate Neurobiology, CAS, Shanghai 200031, China; Corresponding author at: Univ Lyon, Université Claude Bernard Lyon 1, Inserm, Stem Cell and Brain Research Institute U1208, 69500 Bron, France.Hierarchy is a major organizational principle of the cortex and underscores modern computational theories of cortical function. The local microcircuit amplifies long-distance inter-areal input, which show distance-dependent changes in their laminar profiles. Statistical modeling of these changes in laminar profiles demonstrates that inputs from multiple hierarchical levels to their target areas show remarkable consistency, allowing the construction of a cortical hierarchy based on a principle of hierarchical distance. The statistical modeling that is applied to structure can also be applied to laminar differences in the oscillatory coherence between areas thereby determining a functional hierarchy of the cortex. Close examination of the anatomy of inter-areal connectivity reveals a dual counterstream architecture with well-defined distance-dependent feedback and feedforward pathways in both the supra- and infragranular layers, suggesting a multiplicity of feedback pathways with well-defined functional properties. These findings are consistent with feedback connections providing a generative network involved in a wide range of cognitive functions. A dynamical model constrained by connectivity data sheds insight into the experimentally observed signatures of frequency-dependent Granger causality for feedforward versus feedback signaling. Concerted experiments capitalizing on recent technical advances and combining tract-tracing, high-resolution fMRI, optogenetics and mathematical modeling hold the promise of a much improved understanding of lamina-constrained mechanisms of neural computation and cognition. However, because inter-areal interactions involve cortical layers that have been the target of important evolutionary changes in the primate lineage, these investigations will need to include human and non-human primate comparisons.http://www.sciencedirect.com/science/article/pii/S1053811920309642Non-human primateHumanBrainElectrophysiologyAnatomyModeling |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Julien Vezoli Loïc Magrou Rainer Goebel Xiao-Jing Wang Kenneth Knoblauch Martin Vinck Henry Kennedy |
spellingShingle |
Julien Vezoli Loïc Magrou Rainer Goebel Xiao-Jing Wang Kenneth Knoblauch Martin Vinck Henry Kennedy Cortical hierarchy, dual counterstream architecture and the importance of top-down generative networks NeuroImage Non-human primate Human Brain Electrophysiology Anatomy Modeling |
author_facet |
Julien Vezoli Loïc Magrou Rainer Goebel Xiao-Jing Wang Kenneth Knoblauch Martin Vinck Henry Kennedy |
author_sort |
Julien Vezoli |
title |
Cortical hierarchy, dual counterstream architecture and the importance of top-down generative networks |
title_short |
Cortical hierarchy, dual counterstream architecture and the importance of top-down generative networks |
title_full |
Cortical hierarchy, dual counterstream architecture and the importance of top-down generative networks |
title_fullStr |
Cortical hierarchy, dual counterstream architecture and the importance of top-down generative networks |
title_full_unstemmed |
Cortical hierarchy, dual counterstream architecture and the importance of top-down generative networks |
title_sort |
cortical hierarchy, dual counterstream architecture and the importance of top-down generative networks |
publisher |
Elsevier |
series |
NeuroImage |
issn |
1095-9572 |
publishDate |
2021-01-01 |
description |
Hierarchy is a major organizational principle of the cortex and underscores modern computational theories of cortical function. The local microcircuit amplifies long-distance inter-areal input, which show distance-dependent changes in their laminar profiles. Statistical modeling of these changes in laminar profiles demonstrates that inputs from multiple hierarchical levels to their target areas show remarkable consistency, allowing the construction of a cortical hierarchy based on a principle of hierarchical distance. The statistical modeling that is applied to structure can also be applied to laminar differences in the oscillatory coherence between areas thereby determining a functional hierarchy of the cortex. Close examination of the anatomy of inter-areal connectivity reveals a dual counterstream architecture with well-defined distance-dependent feedback and feedforward pathways in both the supra- and infragranular layers, suggesting a multiplicity of feedback pathways with well-defined functional properties. These findings are consistent with feedback connections providing a generative network involved in a wide range of cognitive functions. A dynamical model constrained by connectivity data sheds insight into the experimentally observed signatures of frequency-dependent Granger causality for feedforward versus feedback signaling. Concerted experiments capitalizing on recent technical advances and combining tract-tracing, high-resolution fMRI, optogenetics and mathematical modeling hold the promise of a much improved understanding of lamina-constrained mechanisms of neural computation and cognition. However, because inter-areal interactions involve cortical layers that have been the target of important evolutionary changes in the primate lineage, these investigations will need to include human and non-human primate comparisons. |
topic |
Non-human primate Human Brain Electrophysiology Anatomy Modeling |
url |
http://www.sciencedirect.com/science/article/pii/S1053811920309642 |
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