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 areas containing ‘memory images’ related to motor acts (localized in primary motor areas) and sensory experiences (localized in primary visual, somesthestic, auditory, olfactory and gustatory areas). He also assumed that higher cognitive functions, in contrast to movements and perceptions, are not localized in specific regions but emerge from associative connections linking areas where images of motor and sensory memories reside. On the basis of this ‘general principle’, Wernicke (1874)
elaborated the first network model of language (): ‘...the first frontal gyrus
[third frontal circonvolution according to modern nomenclature], which has motor function, acts as center for motor imagery; the first temporal gyrus, which is sensory in nature, may be regarded as the centre of acoustic images; the fibrae propriae, converging into the insular cortex, form the mediating arc reflex.’ He argued that ‘aphasia may be caused by any disruption of this pathway, the clinical picture, however, may vary considerably and is related to the specific segment of the pathway involved.’ According to Wernicke, the ‘production of spontaneous movement, that is, the consciously formulated word, would be brought about by the rearousal of the motor image through the associated memory image of the sound.’ Spontaneous speech, in his opinion, resulted from the interaction of distant cortical areas. Consequently, he interpreted the characteristic paraphasic speech of patients with conduction aphasia as the expression of the inability of temporal regions to monitor Broca's area speech output through subinsular connections. Wernicke's model was the forerunner of current network models of cognition. His greatest merit was to anchor his ideas into the clinical–anatomical correlation method, where he coupled a careful description of the behavioural disturbances of his patients to the anatomical findings from post-mortem dissections. With him aphasiology became a discipline intimately concerned with the connectional anatomy of the human brain.
Carl Wernicke (1848−1905) and his representation of the language network from his 1874 MD thesis.
In France, the associationist theories were popularized by Charcot who brought Wernicke's ideas to his medical trainees during his ‘leçons du Mardi’ at the Salpetriere (Gelfand, 1999
). However, it was Jules Dejerine who formulated the most elegant contribution of French neurology to the disconnection paradigm. He beautifully explained the occurrence of reading difficulties (i.e., pure alexia) in a patient with otherwise normal writing ability using a pure disconnection mechanism, which he was able to demonstrate with post-mortem dissections (Epelbaum et al., 2008
, this issue).
Shortly after Wernicke's description of conduction aphasia, Lichtheim (1885)
extended the disconnection paradigm to give a comprehensive account of different aphasic syndromes. He hypothesized that Broca's and Wernicke's areas are interconnected to an hypothetical “concept center” (not anatomically localized) and added to Wernicke's nomenclature two other forms of aphasia, i.e., transcortical sensory and transcortical motor aphasia, that he interpreted as resulting from the disconnection of the concept center from the motor and auditory language centers, respectively (). In transcortical sensory aphasia, heard words cannot reach the thought center leading to impairment in understanding words, in transcortical motor aphasia thoughts cannot be verbalised due to impaired transfer of inputs from the thought center to Broca's area.
Ludwig Lichtheim (1845−1928) and his representation of the language network from his 1885 Brain paper.
Lichtheim translated Wernicke's ideas into simple and intuitive diagrams that became standard references for clinicians. However, Lichtheim also introduced hypothetical centers and connections backed by little supportive evidence. His diagrams served the purpose of fitting a theoretical framework that best explained clinical empirical observations without a necessary anatomical correspondence. These diagrams promoted a mechanical view of brain function where connections represented ‘transferring devices’ between stores of specialized information localized in individual cortical areas. This approach to brain function generated a wave of criticisms and the clinico-anatomical correlation method came under attack by many prominent investigators including Hughling Jackson, Von Monakow, Henry Head, Karl Lashley and Kurt Goldstein (for a review see Finger, 1994
In many respects these authors brought forward important criticisms that are still valid in modern neuroscience. First, they warned that localization of symptoms and localization of function were not identical. For example, for John Hughlings Jackson, there was no doubt that verbal fluency is more likely to be affected by damage to the left hemisphere than the right hemisphere. Jackson had difficulty, however, with the belief that observable symptoms specified the locations of special centers for the affected functions. He argued that it was entirely possible that some symptoms could be due to secondary effects of the damage on other regions of the brain, a distant ‘hodological effect’ according to more recent terminology (Catani and ffytche, 2005
; Catani, 2007
). He also believed that lesions were more useful for finding out what the remaining unaffected parts of the brain did without the benefit of the damaged area than what the damaged area did when it was part of the intact brain (Finger, 1994
This dialectic between the localizationists and their opponents lasted for several decades, until the work of Norman Geschwind in the 1960s. Geschwind brought new credibility to the localizationist approach by re-interpreting the functional role of connections and specialized cortical areas according to evidence arising from the new neuroscience of the 20th Century. He also extended the disconnection paradigm beyond white matter lesions to lesions of association cortex. In Geschwind's (1965)
model, even a lesion confined to association cortex could cause a disconnection syndrome, little distinction being made between such lesions and those restricted to white matter tracts (see also Glickstein and Berlucchi, 2008
, this issue). He argued that ‘lesions of association cortex, if extensive enough, act to disconnect primary receptive or motor areas from other regions of the cortex in the same or in the opposite hemisphere.... Thus a ‘disconnexion lesion’ will be a large lesion either of association cortex or of the white matter leading from this association cortex’ (Geschwind, 1965
Based on this broader view, Geschwind reappraised conduction aphasia as a disconnection syndrome resulting either from a lesion of the white matter connections or of the perisylvian cortex, the latter acting as relay station between Wernicke's and Broca's areas. In Geschwind's view, Wernicke's aphasia could also be conceptualized as a disconnection syndrome (). He argued for ‘the importance of the angular gyrus in acting as a region involved in corss-modal associations, particularly in cross-association between either vision, or touch and hearing. If the angular gyrus is important in the process of associating a heard name to a seen or felt object, it is probably also important for associations in the reverse direction. A name passes through Wernicke's area, then via the angular gyrus arouses associations in the other parts of the brain’ (Geschwind, 1965
). Wernicke's aphasia could then result either from a lesion of Wernicke's area or of its connections to the angular gyrus. But Geschwind admitted that his intuitions, pending experimental anatomical evidence, were to be regarded as ‘speculative’.
Norman Geschwind (1926−1984) and his representation of the language network from his 1970 Science paper.
With the advent of new information arising from structural and functional imaging, it appeared that parts of the Geschwind–Wernicke model represented an over-simplification. Kempler et al. (1988)
, for example, showed that lesions to the arcuate fasciculus were associated with hypometabolism in Wernicke's and Broca's areas only in 50% of the patients, the remaining showing hypometabolism only in Wernicke's area. Furthermore, the Geschwind–Wernicke model predicted that lesions at any point along the course of the arcuate fasciculus result in an identical aphasia. Yet, clinically, this emerged not to be the case with conduction aphasias forming a heterogeneous group ranging from “Broca-like” to “Wernicke-like” deficits (Levine and Calvanio, 1982
). These studies began to raise questions concerning the validity of existing neurocognitive formulations of language.
The dilemma that aphasiologists in specific, and behavioural neurologists in general, had to face stemmed principally from the lack of sufficient information on human neuroanatomy (see also Catani and Mesulam, 2008
, this issue). In contrast to the giant strides made in unravelling the connectivity of the monkey brain, the details of connection pathways in the human brain remained stuck in the methodology of the 19th Century. In a scientific commentary in Nature Crick and Jones (1993)
voiced these concerns to the scientific community: “to interpret the activity of the living human brains, their anatomy must be know in detail.” They urged the “development of new techniques since most of the methods used in the monkeys cannot be used on humans.” A year later, in 1994, Basser et al. (1994)
published their seminal paper where they describe for the first time DTI.
DTI, coupled to tractography, offers a non-invasive technique that reconstructs white matter trajectories in the living human brain (see also Jones, 2008
, this issue; Catani and Thiebaut de Schotten, 2008
, this issue). By measuring the diffusivity of water along different directions and by tracing a pathway of least hindrance to diffusion, DTI tractography can visualise continuous pathways as inferred from the movement of water molecules subjected to a magnetic gradient (Basser et al., 2000
; Le Bihan, 2003
). Tractography findings are not necessarily equivalent to data obtained from post-mortem dissections. Nevertheless, tractography results are likely to reflect highly reproducible features of the human brain anatomy (Catani et al., 2002
; Wakana et al., 2004
), and tractography-based dissections currently represent the only way to study the connectional anatomy of language pathways in living subjects. As will be shown below, the anatomy of the arcuate fasciculus is one question that has been addressed very fruitfully by DTI tractography.