Elsevier

Brain and Language

Volume 85, Issue 3, June 2003, Pages 357-368
Brain and Language

A fMRI study of word retrieval in aphasia

https://doi.org/10.1016/S0093-934X(02)00561-8Get rights and content

Abstract

The neural mechanisms underlying recovery of cognitive functions are incompletely understood. Aim of this study was to assess, using functional magnetic resonance (fMRI), the pattern of brain activity during covert word retrieval to letter and semantic cues in five aphasic patients after stroke, in order to assess the modifications of brain function which may be related to recovery. Four out of five patients had undergone language recovery, according to standard testing, after at least 6 months of rehabilitation. The cerebral activation of each patient was evaluated and compared with the activation pattern of normal controls studied with the same fMRI paradigm. In the patients, the pattern of brain activation was influenced by the site and extent of the lesion, by the degree of recovery of language, as reflected by task performance outside the scanner, and by task requirements. In the case of word retrieval to letter cues, a good performance was directly related to the activation in Broca’s area, or in the right-sided homologue. On the other hand, in the case of semantic fluency, the relationship between performance level and activation was less clear-cut, because of extensive recruitment of frontal areas in patients with defective performance. These findings suggest that the performance in letter fluency is dependent on the integrity of the left inferior frontal cortex, with the participation of the homologous right hemispheric region when the left inferior frontal cortex is entirely of partially damaged. Semantic fluency, which engages the distributed network of semantic memory, is also associated with more extensive patterns of cerebral activation, which however appear to reflect retrieval effort rather than retrieval success.

Introduction

The neurological mechanisms responsible for the recovery of aphasia due to acute vascular damage of the language-dominant hemisphere are largely unknown. In the early phase after a stroke, the functional impairment of brain networks not directly affected by the lesion (diaschisis), both in perilesional and contralateral brain areas, might contribute to the global severity of language impairment (Perani, Vallar, Cappa, Messa, & Fazio, 1987; Vallar et al., 1988). The recovery of these “distant effects” has been suggested to play a role in the “early,” partial recuperation stage, which takes place in many aphasic patients, in the weeks and months immediately following the stroke (Cappa et al., 1997).

Although recovery may be observed also many years after a stroke, the following stages of aphasia are usually characterised by a slower recovery rate, which has been suggested to be related to functional re-organisation. The hypothesis of a “take-over” of function by homotopic areas in the right hemisphere as the mechanism underlying aphasia recovery goes back to the last century (Gowers, 1895). On the basis of the results of positron emission tomography activation studies (Weiller et al., 1995), a functional re-organisation, involving in particular the regions homotopic to the language areas in the contralateral hemisphere, has been suggested to be responsible for long-term recovery. However, other recent neuroimaging investigations have reported more complex patterns of activation in recovered patients. In particular, several studies have indicated that the reactivation of ipsilateral, perilesional areas is often associated with good recovery (Belin et al., 1996; Cao, Vikingstad, George, Johnson, & Welch, 1999; Heiss, Kessler, Thiel, Ghaemi, & Karbe, 1999; Hund-Georgiadis, Lex, Morris, & von Cramon, 2000; Rosen et al., 2000; Warburton, Price, Swinburn, & Wise, 1999). Besides performance level, another crucial determinant to be considered to interpret the pattern of activation in aphasia is the type of task. As suggested by Gold and Kertesz (2000), it is plausible that tasks, which are known to involve the right hemisphere in normal controls, may be associated with more extensive right-sided activation in aphasics. These typically include semantic comprehension tasks, rather than speech production and word generation. Even within relatively simple tasks, modifications of the linguistic requirements may change the cognitive strategy and result in different pattern of cerebral reorganisation.

In the present study, we took advantage of the well-known difference in word retrieval to letter and to semantic cues. Different component processes are involved in the two tasks. In particular, letter fluency has been suggested to place greater demand on “frontal” strategic processes, while semantic fluency is more dependent from semantic memory, in which the temporal lobe plays a crucial role. There is both behavioral (Martin, Wiggs, Lalonde, & Mack, 1994) and imaging (Mummery, Patterson, Hodges, & Wise, 1996; Paulesu et al., 1997) evidence to support this claim. The two tasks can thus be considered as “probes” for two partially independent networks, involving different brain regions, which may have different potential for reorganisation. Here, we report the anatomo-functional correlates of cued lexical retrieval in five aphasic patients, who showed different degrees of recovery in the late stage of stroke after rehabilitation therapy. The patterns of brain activation were assessed with functional Magnetic Resonance (fMRI) during verbal fluency tasks.

Section snippets

Methods

The experimental protocol was approved by the local hospital Ethics Committee, and all the subjects signed the informed consent.

Normal subjects

Table 3, Table 4 report the results of the simple main effects of the phonemic and semantic verbal fluency tasks compared to the time-matched rest condition. For normal controls the pattern of activation was comparable to the one reported in the previous paper (see Paulesu et al., 1997). In particular, we found a selective activation of the left frontal operculum (Ba 44) during phonemic fluency and a larger activation of the retrosplenial cortex in the semantic fluency.

More in detail, during

Discussion

In agreement with previous findings (Poline, Vandenberghe, Holmes, Friston, & Frackowiak, 1996), in normal subjects phonemic and semantic fluency were associated with prevalent left prefrontal cortex activation. Some areas of task-specific activation were also present. In particular, the opercular portion of Broca’s area (Ba 44) and the basal ganglia and thalamus were engaged by phonemic fluency, whereas the left middle temporal gyrus (Ba 21) and the retrosplenial cortex/cuneus were activated

Acknowledgements

This study was partially supported by the V European Program for the project Connectivity in language rehabilitation in stroke in Europe (LSDE).

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