Fiber anatomy of dorsal and ventral language streams
Highlights
► MR data and fiber dissection studies show anatomically defined fiber tracts composing ventral and dorsal language streams. ► The major fiber tract of the dorsal stream is the arcuate fasciculus. ► The major tract of the ventral stream is the inferior fronto-occipital fasciculus. ► There are considerable differences in fiber architecture between the monkey and the human brain. ► Polarized light imaging reproduces the described fiber architecture of these pathways with higher detail.
Introduction
The classical concept of anatomical language circuitry has been the connection between the temporal sensory region (Wernicke’s area) and the frontal motor region (Broca’s area) via the arcuate fasciculus (e.g. Geschwind, 1970) – this model has dominated the anatomical comprehension of language over decades (Catani & Mesulam, 2008). However, modern concepts describe the classical dorsal pathway along the arcuate fascicle/superior longitudinal fasciculus that is activated during repetition and a second ventral pathway via the extreme capsule which is activated during auditory comprehension (Saur et al., 2008). Therefore, the concept of a dorsal stream for the integration of sensory percept and internal models and a ventral stream for meaning has been proposed as the backbone language related network (Weiller, Bormann, Saur, Musso, & Rijntjes, 2011).
Although the arcuate fasciculus as the major fiber tract of the dorsal stream is well established, the anatomical existence of a ventral stream fiber tract running via the extreme/external capsule is still a matter of debate. Recent concepts of dorsal and ventral streams of language networks are mainly based on MR data and uncertainty arises if these results are based on real existing anatomical structures or if these may simply be caused by artifacts based on magnification problems of diffusion MRI such as the crossing and kissing fibers problem.
However, white matter architecture and structural connectivity of language related networks in the human brain clearly form the backbone for modern language models (Berthier et al., 2012, Friederici, 2009). Therefore, this review aims at a literature analysis of the anatomical description of structural fiber systems of the white matter related to language-sensitive areas (especially the arcuate fasciculus (AF), extreme (EmC) and external capsules (EC), the inferior fronto-occipital fasciculus (IFOF), and others) in the human and the monkey brain.
Table 1 shows the fiber tracts and the abbreviations used here. The term ‘fasciculus’ is generally used as a description of an anatomically defined, larger fiber tract or fiber bundle in the brain, while ‘extreme capsule’ and ‘external capsule’ are topographical descriptions of white matter with the extreme capsule (EmC) being located between insula and claustrum and external capsule (EC) being located between claustrum and putamen. Terms like ‘stream’ or ‘pathway’ are used mainly in functional imaging studies depicting information flow and are not clearly defined anatomical terms.
A pubmed inquiry, therefore, was performed to search for the following anatomical terms (date: 01-02-2012): ‘arcuate fasciculus’ with 194 hits, ‘inferior fronto occipital fasciculus’ with 105 hits, ‘external capsule brain’ with 466 hits, ‘extreme capsule brain’ with 70 hits. All abstracts were analyzed regarding anatomical information about fiber anatomy possibly contained. These papers were collected and build the basis of this review. In addition, several historical publications were sighted regarding the anatomical description of these fiber tracts. In addition, we present own case studies using macroscopical dissection and polarized light imaging (PLI) of the human brain.
Section snippets
Historical aspects
Recently, the history of the concept of dorsal and ventral routes for speech production was intensively reviewed by Weiller et al. (2011). It is very interesting, that nerve fiber architecture of the ventral stream was seriously discussed in former times, based on observations of Meynert (1866) and especially Wernicke (1874), but then was rejected and lost.
The anatomical substrate of the dorsal pathway of speech production is well known and accepted. The arcuate fasciculus and the superior
Monkey brain
Anatomical tract tracing is a method, which can detect connections between cortical regions in high detail (Axer, 2011). The tracer is injected into a specific brain region and is actively transported via the axons into connected brain areas (tract tracing). The process is dependent on active axonal transport mechanisms and can therefore only be used in experimental settings in the living animal. Radioactive labeled amino acids are transported anterogradely along the axon, and this method has
Discussion and conclusions
In summary, there are several pathways anatomically detectable, which constitute connections between language-related areas and may therefore be functionally important in language tasks (Fig. 3, Fig. 4). The major fiber tract of the dorsal stream is the AF and the major tract of the ventral stream is the IFOF.
However, the assignment of a specific function to a distinct fiber tract is rather critical. Generally speaking, white matter fiber tracts represent reciprocal connections between
Acknowledgments
This work was partly funded by the German Research Counsil (DFG, Deutsche Forschungsgemeinschaft; Grant No. Ax 20/3-1) and the German Federal Ministry of Education and Research (BMBF, Grant No. 01GW0740).
References (96)
- et al.
A novel approach to the human connectome: Ultra-high resolution mapping of fiber tracts in the brain
NeuroImage
(2011) - et al.
A 3D fiber model of the human brainstem
Computerized Medical Imaging and Graphics
(2002) - et al.
Arcuate fasciculus variability and repetition: The left sometimes can be right
Cortex
(2012) - et al.
Virtual in vivo interactive dissection of white matter fasciculi in the human brain
NeuroImage
(2002) - et al.
The arcuate fasciculus and the disconnection theme in language and aphasia: History and current state
Cortex
(2008) The anatomo-functional connectivity of language revisited. New insights provided by electrostimulation and tractography
Neuropsychologia
(2008)Pathways to language: Fiber tracts in the human brain
Trends in Cognitive Sciences
(2009)- et al.
MR connectomics: Principles and challenges
Journal of Neuroscience Methods
(2010) The functional neuroanatomy of language
Physics of Life Reviews
(2009)- et al.
Towards a functional neuroanatomy of speech perception
Trends in Cognitive Sciences
(2000)
Dorsal and ventral streams: A framework for understanding aspects of the functional anatomy of language
Cognition
The anatomical location of the arcuate fasciculus in the human brain: A diffusion tensor tractography study
Brain Research Bulletin
Horizontal portion of arcuate fasciculus fibers track to pars opercularis, not pars triangularis, in right and left hemispheres: A DTI study
NeuroImage
Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data
Cortex
Lateralization of ventral and dorsal auditory-language pathways in the human brain
NeuroImage
Combining functional and anatomical connectivity reveals brain networks for auditory language comprehension
NeuroImage
White matter asymmetry in healthy individuals: A diffusion tensor imaging study using tract-based spatial statistics
Neuroscience
Monkey to human comparative anatomy of the frontal lobe association tracts
Cortex
Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography
NeuroImage
Diffusion tensor spectroscopy and imaging of the arcuate fasciculus
NeuroImage
Fiber density asymmetry of the arcuate fasciculus in relation to functional hemispheric language lateralization in both right- and left-handed healthy subjects: A combined fMRI and DTI study
NeuroImage
How the ventral pathway got lost: And what its recovery might mean
Brain and Language
Syntactic processing depends on dorsal language tracts
Neuron
The cortical connectivity of the prefrontal cortex in the monkey brain
Cortex
Connectivity-based parcellation of Broca’s Area
Cerebral Cortex
Imaging of Wallerian degeneration in the brain
Current Medical Imaging Reviews
Microstructural analysis of human white matter architecture using polarized light imaging: Views from neuroanatomy
Frontiers in Neuroinformatics
Visualization of nerve fiber orientation in gross histological sections of the human brain
Microscopy Research and Technique
Invasive methods for tracing white matter architecture
Neuroanatomical prerequisites for language functions in the maturing brain
Cerebral Cortex
Vom Baue und Leben des Gehirns und Rückenmarks
Perisylvian language networks of the human brain
Annals of Neurology
Das Nervensystem des Menschen
Quantitative investigation of connections of the prefrontal cortex in the human and macaque using probabilistic diffusion tractography
The Journal of Neuroscience
A new association fiber tract in the cerebrum with remarks on the fiber tract dissection method of studying the brain
Journal of Comparative Neurology and Psychology
Anatomie des centres nerveux
Structural asymmetries in the infant language and sensori-motor networks
Cerebral Cortex
Intraoperative mapping of the subcortical language pathways using direct stimulations. An anatomo-functional study
Brain
Is the left uncinate fasciculus essential for language? A cerebral stimulation study
Journal of Neurology
Topography of the uncinate fascicle and adjacent temporal fiber tracts
Acta Neurochirurgica
Relationships between essential cortical language sites and subcortical pathways
Journal of Neurosurgery
The claustrum and its projection system in the human brain: A microsurgical and tractographic anatomical study
Journal of Neurosurgery
Dissociating the human language pathways with high angular resolution diffusion fiber tractography
The Journal of Neuroscience
The organization of language and the brain
Science
Perisylvian white matter connectivity in the human right hemisphere
BMC Neuroscience
DTI tractography of the human brain’s language pathways
Cerebral Cortex
The gross and minute anatomy of the central nervous system
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