The ventral pathway of the human brain: A continuous association tract system

The brain hemispheres can be divided into an upper dorsal and a lower ventral system. Each system consists of distinct cortical regions connected via long association tracts. The tracts cross the central sulcus or the limen insulae to connect the frontal lobe with the posterior brain. The dorsal str...

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Main Authors: Cornelius Weiller, Marco Reisert, Ivo Peto, Jürgen Hennig, Nikos Makris, Michael Petrides, Michel Rijntjes, Karl Egger
Format: Article
Language:English
Published: Elsevier 2021-07-01
Series:NeuroImage
Subjects:
UF
ECF
Online Access:http://www.sciencedirect.com/science/article/pii/S1053811921002548
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language English
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author Cornelius Weiller
Marco Reisert
Ivo Peto
Jürgen Hennig
Nikos Makris
Michael Petrides
Michel Rijntjes
Karl Egger
spellingShingle Cornelius Weiller
Marco Reisert
Ivo Peto
Jürgen Hennig
Nikos Makris
Michael Petrides
Michel Rijntjes
Karl Egger
The ventral pathway of the human brain: A continuous association tract system
NeuroImage
Ventral pathway
Extreme capsule
Heteromodal cortex
IFOF
UF
ECF
author_facet Cornelius Weiller
Marco Reisert
Ivo Peto
Jürgen Hennig
Nikos Makris
Michael Petrides
Michel Rijntjes
Karl Egger
author_sort Cornelius Weiller
title The ventral pathway of the human brain: A continuous association tract system
title_short The ventral pathway of the human brain: A continuous association tract system
title_full The ventral pathway of the human brain: A continuous association tract system
title_fullStr The ventral pathway of the human brain: A continuous association tract system
title_full_unstemmed The ventral pathway of the human brain: A continuous association tract system
title_sort ventral pathway of the human brain: a continuous association tract system
publisher Elsevier
series NeuroImage
issn 1095-9572
publishDate 2021-07-01
description The brain hemispheres can be divided into an upper dorsal and a lower ventral system. Each system consists of distinct cortical regions connected via long association tracts. The tracts cross the central sulcus or the limen insulae to connect the frontal lobe with the posterior brain. The dorsal stream is associated with sensorimotor mapping. The ventral stream serves structural analysis and semantics in different domains, as visual, acoustic or space processing. How does the prefrontal cortex, regarded as the platform for the highest level of integration, incorporate information from these different domains? In the current view, the ventral pathway consists of several separate tracts, related to different modalities. Originally the assumption was that the ventral path is a continuum, covering all modalities. The latter would imply a very different anatomical basis for cognitive and clinical models of processing. To further define the ventral connections, we used cutting-edge in vivo global tractography on high-resolution diffusion tensor imaging (DTI) data from 100 normal subjects from the human connectome project and ex vivo preparation of fiber bundles in the extreme capsule of 8 humans using the Klingler technique. Our data showed that ventral stream tracts, traversing through the extreme capsule, form a continuous band of fibers that fan out anteriorly to the prefrontal cortex, and posteriorly to temporal, occipital and parietal cortical regions. Introduction of additional volumes of interest in temporal and occipital lobes differentiated between the inferior fronto-occipital fascicle (IFOF) and uncinate fascicle (UF). Unequivocally, in both experiments, in all subjects a connection between the inferior frontal and middle-to-posterior temporal cortical region, otherwise known as the temporo-frontal extreme capsule fascicle (ECF) from nonhuman primate brain-tracing experiments was identified. In the human brain, this tract connects the language domains of “Broca's area” and “Wernicke's area”. The differentiation in the three tracts, IFOF, UF and ECF seems arbitrary, all three pass through the extreme capsule. Our data show that the ventral pathway represents a continuum. The three tracts merge seamlessly and streamlines showed considerable overlap in their anterior and posterior course. Terminal maps identified prefrontal cortex in the frontal lobe and association cortex in temporal, occipital and parietal lobes as streamline endings. This anatomical substrate potentially facilitates the prefrontal cortex to integrate information across different domains and modalities.
topic Ventral pathway
Extreme capsule
Heteromodal cortex
IFOF
UF
ECF
url http://www.sciencedirect.com/science/article/pii/S1053811921002548
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spelling doaj-218d4278e91143be8e8c06076ebc0f5c2021-05-26T04:25:11ZengElsevierNeuroImage1095-95722021-07-01234117977The ventral pathway of the human brain: A continuous association tract systemCornelius Weiller0Marco Reisert1Ivo Peto2Jürgen Hennig3Nikos Makris4Michael Petrides5Michel Rijntjes6Karl Egger7Department of Neurology and Clinical Neuroscience, Faculty of Medicine, University of Freiburg, Breisacher Str. 64, 79106 Freiburg, Germany; Corresponding author.Department of Medical Physics, Faculty of Medicine, University of Freiburg, Freiburg, GermanyDepartment of Neuroradiology, Faculty of Medicine, University of Freiburg, Freiburg, Germany; Department of Neurosurgery and Brain Repair, University of South Florida, Morsani College of Medicine, Tampa, FL, USADepartment of Medical Physics, Faculty of Medicine, University of Freiburg, Freiburg, GermanyCenter for Morphometric Analysis, Department of Psychiatry and Neurology, A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital and Psychiatric Neuroimaging Laboratory, Brigham and Women's Hospital, Harvard Medical School, Boston, MA, United States; Department of Anatomy and Neurobiology, Boston University School of Medicine, Boston, MA, United StatesDepartment of Neurology and Neurosurgery, McGill University, Montreal, Quebec, CanadaDepartment of Neurology and Clinical Neuroscience, Faculty of Medicine, University of Freiburg, Breisacher Str. 64, 79106 Freiburg, GermanyDepartment of Neuroradiology, Faculty of Medicine, University of Freiburg, Freiburg, GermanyThe brain hemispheres can be divided into an upper dorsal and a lower ventral system. Each system consists of distinct cortical regions connected via long association tracts. The tracts cross the central sulcus or the limen insulae to connect the frontal lobe with the posterior brain. The dorsal stream is associated with sensorimotor mapping. The ventral stream serves structural analysis and semantics in different domains, as visual, acoustic or space processing. How does the prefrontal cortex, regarded as the platform for the highest level of integration, incorporate information from these different domains? In the current view, the ventral pathway consists of several separate tracts, related to different modalities. Originally the assumption was that the ventral path is a continuum, covering all modalities. The latter would imply a very different anatomical basis for cognitive and clinical models of processing. To further define the ventral connections, we used cutting-edge in vivo global tractography on high-resolution diffusion tensor imaging (DTI) data from 100 normal subjects from the human connectome project and ex vivo preparation of fiber bundles in the extreme capsule of 8 humans using the Klingler technique. Our data showed that ventral stream tracts, traversing through the extreme capsule, form a continuous band of fibers that fan out anteriorly to the prefrontal cortex, and posteriorly to temporal, occipital and parietal cortical regions. Introduction of additional volumes of interest in temporal and occipital lobes differentiated between the inferior fronto-occipital fascicle (IFOF) and uncinate fascicle (UF). Unequivocally, in both experiments, in all subjects a connection between the inferior frontal and middle-to-posterior temporal cortical region, otherwise known as the temporo-frontal extreme capsule fascicle (ECF) from nonhuman primate brain-tracing experiments was identified. In the human brain, this tract connects the language domains of “Broca's area” and “Wernicke's area”. The differentiation in the three tracts, IFOF, UF and ECF seems arbitrary, all three pass through the extreme capsule. Our data show that the ventral pathway represents a continuum. The three tracts merge seamlessly and streamlines showed considerable overlap in their anterior and posterior course. Terminal maps identified prefrontal cortex in the frontal lobe and association cortex in temporal, occipital and parietal lobes as streamline endings. This anatomical substrate potentially facilitates the prefrontal cortex to integrate information across different domains and modalities.http://www.sciencedirect.com/science/article/pii/S1053811921002548Ventral pathwayExtreme capsuleHeteromodal cortexIFOFUFECF