Elsevier

Cortex

Volume 44, Issue 8, September 2008, Pages 953-961
Cortex

Special issue: Original article
The arcuate fasciculus and the disconnection theme in language and aphasia: History and current state

https://doi.org/10.1016/j.cortex.2008.04.002Get rights and content

Abstract

Few themes have been more central to neurological models of aphasia than the disconnection paradigm and the role of the arcuate fasciculus. Introduced by luminaries of 19th Century neurology and resurrected by the charismatic work of Norman Geschwind, the disconnection theme has triggered spectacular advances of modern understanding of language and aphasia. But the disconnection paradigm had alternate fortunes, ranging from irrational exuberance to benign neglect, and its followers have not always shared the same view on its functional consequences and anatomical correlates. Our goal in this paper is, first, to survey the 19th Century roots of the connectionist approach to aphasia and, second, to describe emerging imaging technologies based on diffusion tensor imaging (DTI) that promise to consolidate and expand the disconnection approach to language and its disorders.

Introduction

Language is an exceedingly complex faculty that allows us to encode, elaborate and communicate thoughts and experiences through the mediation of arbitrary symbols known as words. The coherent function of the language network and its interactions with other neurocognitive networks depend on an orderly set of interconnections. Much of current understanding of language-related pathways is based on the pioneering work of 19th Century neuroanatomists, such as Reil, Burdach, Meynert, Wernicke, Dejerine. In the 1960s, in a series of influential papers, Geschwind crystallized those early anatomical findings adding new insights into brain connectivity as derived from anatomical, physiological and neuronographic studies both in animals and humans (Geschwind, 1965, Geschwind, 1970, Geschwind and Levitsky, 1968).

The neuroanatomy of the human brain that Geschwind relied on was based principally on hand dissection of fixed specimens and the tracing of degeneration in sections stained for myelin. Recent developments in magnetic resonance imaging have introduced new methods, based on diffusion tensor imaging (DTI) tractography (see also Jones, 2008, Catani and Thiebaut de Schotten, 2008) that can reconstruct white matter pathways in the living human brain. The resultant influx of information on human connectional anatomy is likely to modernize the disconnection approach to behavioural neurology and to reinvigorate models of cognition based on distributed large-scale networks (Catani and Mesulam, 2008, this issue). An overview of these trends, and of their historical contexts, with a special focus on the arcuate fasciculus and language, constitutes the subject matter of this paper.

Section snippets

Disconnection accounts of language disorders

The term disconnection is generally used to indicate classical syndromes where lesions to white matter connections lead to dysfunction of higher cognitive abilities (Catani and Ffytche, 2005, Mesulam, 2005). The term became popular in the second half of the 19th Century following Wernicke's (1874) description of the disconnection syndrome that was to become the prototype for all others – conduction aphasia. Wernicke, like his predecessor Theodore Meynert, conceived the brain as a mosaic of

The anatomy of the arcuate fasciculus

Reil, 1812, Reil et al., 1809 was the first to identify, almost two Centuries ago, a group of fibres running deeply into the white matter of the temporal, parietal and frontal regions located around the Sylvian fissure of each hemisphere (Fig. 4). In 1822 Burdach (1819–1826) described in detail this system of perisylivan fibres and named it the Fasciculus Arcuatus (Arcuate fasciculus), for the arching shape of its longest fibres. Subsequently, Dejerine (1895) confirmed the findings of the

Recent contribution from DTI tractography

Although the existence of the arcuate fasciculus has been confirmed in several post-mortem studies in humans, these methods (e.g., blunt dissections, axonal staining of degenerating axons, etc.) have not shed much light on the detailed anatomy of the relevant fibres. More powerful methods have been used to trace homologous axonal pathways in the monkey but the absence of language in non-human primates raises doubts on the possibility of translating connectional anatomy of putative language

Beyond the arcuate fasciculus: the ventral pathways

The arcuate fasciculus belongs to the core perisylvian circuitry underlying language. Functional imaging experiments and clinicopathological observations of a language-based neurodegenerative syndrome known as primary progressive aphasia (PPA) have been expanding the boundaries of this core circuitry (for a recent review see Mesulam, 2007). One of the most interesting developments has been the demonstration that areas in the medial, inferior and anterior temporal cortices, traditionally

Additional directions for DTI and tractography

As illustrated in Fig. 8, information on the anatomy of connections can potentially help to resolve dilemmas posed by cases that superficially appear to defy established neurocognitive models. For example, the site of maximal lesion overlap for a specific syndrome may extend into axonal pathways that interconnect a different set of remote areas, raising the possibility that the critical factor is not necessarily the destruction in the cortical area of overlap but a disconnection of the two

Concluding remarks and future directions

In this review we have tried to highlight the merits of the hodological (pathway-based) approach to behavioural neurology and its modern pursuit with DTI tractography as applied to language and the arcuate fasciculus. We realize, of course, that mapping symptoms onto single tracts is subjected to the same criticisms directed to narrow cortical localizationism, that our knowledge of human white matter anatomy is still very limited, and that giant strides are needed to reach the level of pathway

Acknowledgements

MC is funded by the Medical Research Council (UK), the AIMS network MM is funded by the National Institute of Deafness and Communication Disorders (DC008552), National Institute on Aging (AG13854).

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