Chapter 10 - White-matter pathways for speech and language processing
Introduction
The white-matter fiber bundles in the brain play a crucial role in the transmission of information between different regions. These fiber bundles are composed of millions of axons that are surrounded by myelin, which is essential for fast transmission of electrical impulses (Wake et al., 2011).
The relevance of white-matter fiber bundles for speech perception and speech production was first recognized in the late 19th century, when they were proposed to form possible connections between the different language centers (Wernicke, 1874). In his model, Wernicke (1874) proposed a speech production center (based on the work of Broca, 1861), a sensory language center, and a connection between the centers supporting their interaction. Broca's area in the inferior frontal cortex and Wernicke's area in the superior temporal cortex as the classical language areas are subparts of temporofrontal language network that also support higher-language function processes such as grammatical assignment and attribution of meaning (Vigneau et al., 2006, Hickok and Poeppel, 2007, Friederici, 2011).
The connections between the classic language regions that have been identified over the past decades are multifold. Initially, two broad processing streams connecting temporal and frontal areas were proposed: a ventral stream supporting sound-to-meaning mapping and a dorsal stream subserving sound-to-motor mapping (Hickok and Poeppel, 2000, Rauschecker and Scott, 2009).
In recent years, new imaging techniques, such as diffusion-weighted magnetic resonance imaging (dMRI), also called diffusion tensor imaging (DTI), allow white-matter fiber bundles to be tracked in vivo in the human brain (Mori and Zijl, 2002). DTI can provide information about the internal fibrous structure based on the measure of water diffusion. Since water will diffuse more rapidly in the direction aligned with the internal structure, the principal direction of the diffusion tensor can be used to infer white-matter connectivity in the brain. Often DTI is used to identify the different fiber tracts in the human brain (Behrens et al., 2003, Catani and Thiebaut de Schotten, 2008, Berthier et al., 2012). This approach is primarily structure-based and independent from function, but once identified, the role of those tracts that connect brain areas known to be involved in particular processes, e.g., language, are discussed (Catani et al., 2005, Makris and Pandya, 2009). This approach only allows very indirect conclusions about a particular fiber tract's function.
A second approach is called a function-based approach. It combines functional MRI (fMRI) and dMRI, and thereby allows specification of a given fiber tract's function, indirectly, in a two-step approach. In a first step, particular brain regions relevant for a specific language task are identified in a functional experiment by fMRI, and then in a second step these regions are used as seed regions from which a tractogram is calculated (Friederici et al., 2006, Saur et al., 2008). The resulting fiber tract is taken to transmit information relevant for the particular function investigated by the fMRI, although it is not always certain whether the tracing originates only from the seed region or also from adjacent parts. Within this function-based tractography approach, two methodologies can be applied: probabilistic and deterministic tracking. The probabilistic approach takes one seed point, which is neurofunctionally defined, as the starting point of tractography (Friederici et al., 2006). The deterministic approach takes two regions that are activated simultaneously as a function of a particular task and calculates the fiber tract between these (Saur et al., 2008).
The most direct test of a particular fiber tract's function, however, is to investigate language performance in patients with lesions in the white-matter fiber tracts (Galantucci et al., 2011, Papoutsi et al., 2011, Turken and Dronkers, 2011, Wilson et al., 2011), or to correlate language performance with the degree of myelination of particular fiber tracts in the developing brain (Brauer et al., 2011).
Based on these approaches different white-matter pathways that are relevant for auditory language processing have been identified. Most generally the long-range fiber bundles which connect the frontal cortex (including the classic language region of Broca's area and premotor cortex (PMC)) and the temporal cortex (including the classic language region of Wernicke's area and the auditory cortex) can be classified into two anatomic pathways, i.e., the dorsal and the ventral pathway. Each of the pathways consists of more than one fiber bundle. Below we will specify the different subparts of the dorsal and ventral pathways, both structurally and functionally. Note that, in addition to these long-range connections between the frontal and the temporal cortex, there are a number of short-range connections within the frontal cortex and the temporal cortex. Here we will only describe those that have been considered as relevant for speech and language.
Section snippets
The language-relevant brain regions
White-matter pathways that are relevant for speech and language can be defined neuroanatomically by their different target regions. Interestingly, these target regions often differ in their function (Friederici, 2002, Vigneau et al., 2006, Price, 2010), but moreover, with respect to their cytoarchitectonic structure (Brodmann, 1909, Amunts and Zilles, 2012) and their receptorarchitectonic structure (Zilles and Amunts, 2009, Amunts et al., 2010). Moreover, the different regions can be
The language pathways
Language regions in the frontal cortex and in the temporal cortex are neuroanatomically connected by both dorsally located and ventrally located long-range fiber tracts known as the dorsal and the ventral pathways.
Conclusions
The white-matter fiber tracts connecting the language-relevant regions in the frontal and temporal cortices can be classified into dorsal and ventral pathways. Each pathway consists of more than one major fiber tract. Within the ventral pathway one tract connects BA 45/47 with the STG and MTG and the other tract connects the orbitofrontal cortex with the anterior temporal cortex. The former ventral tract supports semantic processes, while the function of the latter is still debated. Within the
References (88)
- et al.
Architecture and organizational principles of Broca's region
Trends Cognit Sci
(2012) - et al.
Arcuate fasciculus variability and repetition: the left sometimes can be right
Cortex
(2012) - et al.
Conduction aphasia, sensory-motor integration, and phonological short-term memory – an aggregate analysis of lesion and fMRI data
Brain Lang
(2011) - et al.
Task-dependent and task-independent neurovascular responses to syntactic processing
Cortex
(2008) - et al.
The arcuate fascicle and the disconnection theme in language and aphasia: history and current state
Cortex
(2008) - et al.
A diffusion tensor imaging tractography atlas for virtual in vivo dissections
Cortex
(2008) Towards a neural basis of auditory sentence processing
Trends Cogn Sci
(2002)- et al.
The language network
Curr Opin Neurobiol
(2013) - et al.
Auditory language comprehension: an event-related fMRI study on the processing of syntactic and lexical information
Brain Lang
(2000) Connections for auditory language in the human brain
Brain Lang
(2013)
The battle for Broca's region
Trends Cogn Sci
Age-related changes in working memory during sentence comprehension: an fMRI study
Neuroimage
Domain-specific distribution of working memory processes along human prefrontal and parietal cortices: a functional magnetic resonance imaging study
Neurosci Lett
On Broca, brain, and binding: a new framework
Trends Cogn Sci
Towards a functional neuroanatomy of speech perception
Trends Cogn Sci
Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language
Cognition
Linking ordering in Broca's area to storage in left temporo-parietal regions: The case of sentence processing
Neuroimage
Is left fronto-temporal connectivity essential for syntax? Effective connectivity, tractography and performance in left-hemisphere damaged patients
Neuroimage
Left TPJ activity in verbal working memory: implications for storage- and sensory-specific models of short term memory
Neuroimage
Combining functional and anatomical connectivity reveals brain networks for auditor language comprehension
Neuroimage
Monkey to human comparative anatomy of the frontal lobe association tracts
Cortex
Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing
Neuroimage
Syntactic processing depends on dorsal language tracts
Neuron
Broca's region: novel organizational principles and multiple receptor mapping
PLoS Biol
Connectivity-based parcellation of Broca's area
Cereb Cortex
Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging
Nat Neurosci
Functional MRI of language: new approaches to understanding the cortical organization of semantic processing
Annu Rev Neurosci
Neuroanatomical prerequisites for language functions in the maturing brain
Cereb Cortex
Remarques sur le siège de la faculté du langage articulé, suivies d’une observation d’aphémie (parte de la parole)
Bull Soc Anat Paris
Beiträge zur histologischen Lokalisation der Grosshirnrinde. VI Die Cortexgliederung des Menschen
J Psychol Neurol
The search for the phonological store: from loop to convolution
J Cogn Neurosci
Modality-specific frontal and parietal areas for auditory and visual spatial localization in humans
Nat Neurosci
Perisylvian language networks of the human brain
Ann Neurol
Temporal lobe regions engaged during normal speech comprehension
Brain
Phoneme and word recognition in the auditory ventral stream
Proc Natl Acad Sci U S A
Dissociating the human language pathways with high angular resolution diffusion fiber tractography
J Neurosci
Dissociating the human language pathways with high angular resolution diffusion fiber tractography
J Neurosci
The brain basis of language processing: From structure to function
Physiol Rev
The role of left inferior frontal and superior temporal cortex in sentence comprehension: localizing syntactic and semantic processes
Cereb Cortex
The brain differentiates human and non-human grammars: Functional localization and structural connectivity
Proc Natl Acad Sci U S A
Disentangling syntax and intelligibility in auditory language comprehension
Hum Brain Mapp
White matter damage in primary progressive aphasias: a diffusion tensor tractography study
Brain
The constraints functional neuroimaging places on classical models of auditory word processing
J Cogn Neurosci
Functional organization of the neural language system: dorsal and ventral pathways are critical for syntax
Cereb Cortex
Cited by (85)
Syntactic process in people with Parkinson's disease
2023, Revista de Logopedia, Foniatria y AudiologiaCognitive outcome and its neural correlates after cardiorespiratory arrest in childhood
2024, Developmental ScienceDegeneracy in the neurological model of auditory speech repetition
2023, Communications BiologyFetal temporal sulcus depth asymmetry has prognostic value for language development
2023, Communications Biology