Elsevier

Cognitive Brain Research

Volume 7, Issue 3, January 1999, Pages 285-294
Cognitive Brain Research

Research report
Dynamic pattern of brain activation during sequencing of word strings evaluated by fMRI

https://doi.org/10.1016/S0926-6410(98)00031-7Get rights and content

Abstract

An impaired ability to recite highly automated word strings (e.g., the names of the months of the year) in reverse order concomitant with preserved production of the conventional sequence has been considered a salient sign of frontal lobe dysfunction. Using functional magnetic resonance imaging (fMRI), the spatial and temporal pattern of brain activation during covert performance of these tasks was evaluated in healthy subjects. As compared to the response obtained during forward recitation, re-sequencing of the word string yielded additional activation of the bilateral middle and inferior frontal gyri, the posterior parietal cortex and the left anterior cingulate gyrus. The prefrontal responses are in accordance with the clinical findings referred to. However, the set of activated areas, as a whole, presumably reflects contribution of the various components of the working memory system to the sequencing of word strings. During successive periods of task administration, subjects showed a linear increase of production speed. Analysis of corresponding dynamic changes of regional hemodynamic responses revealed a significant increase at the level of the left inferior parietal cortex and a decrease within the mesial aspect of the left superior frontal gyrus. Presumably, the former finding reflects increasing demands on the phonological short-term memory store, due to faster updating of its content under increased word production rate. Decreasing activation within the superior frontal gyrus might indicate contribution of this area to the initiation of the cognitive processes subserving the sequencing of verbal items. These findings demonstrate the capability of fMRI as a powerful tool for the analysis of dynamic brain activation.

Introduction

A critical role in the temporal organization of behavior 12, 13and serial aspects of speech processing [17]has been attributed to the frontal lobes. Accordingly, dysfunction of the prefrontal cortex of either hemisphere may compromise the ability to reverse the serial order of verbal items stored in short-term memory, e.g., backward production of sets of digits [3], or re-sequencing of highly automated word strings, such as the days of the week or the months of the year 4, 21. Furthermore, the latter task contributes to the differentiation of patients suffering from damage to the frontal lobes from those with non-frontal lesions and normal controls with satisfactory sensitivity and specificity 7, 8, 43. In order to identify the respective underlying foci of prefrontal activation in healthy subjects, the temporal and spatial pattern of brain activation during covert performance of reverse order recitation was compared to production of the conventional sequence. Since both tasks require covert production of identical verbal items, they should not differ with respect to their demands on the speech motor system. Thus, comparison of the respective activation patterns can be expected to display the cortical areas subserving the sequencing process required to reorganize the temporal order of words. Multiple periods of task administration were performed, in order to evaluate the changes of brain activation in the temporal domain due to automatisation processes. The learning function observed at the behavioral level was used as a reference to identify regions that show corresponding dynamic effects in their hemodynamic responses across successive activation periods.

Section snippets

Materials and methods

Eighteen right-handed subjects (10 males, eight females, age: 19–36 years) without a history of neurological or psychiatric diseases volunteered in the study. Informed consent was obtained according to the Declaration of Helsinki. The Ethical Committee of the University of Tübingen had approved the investigation. Handedness was determined using the Edinburgh Inventory [28]. Subjects performed the following tasks—in a balanced order—as fast as possible across the whole length of each activation

Results

(a) The sequential interperiod activation pattern showed, under both conditions, bilateral responses of the posterior part of the superior temporal gyrus (STG) with higher amplitudes on the left side in the first image after providing the verbal instructions (Fig. 1). In addition, both tasks yielded activation of the supplementary motor area (SMA) and the anterior cingulate gyrus (ACG). During FORWARD, the ACG response was restricted to the first temporal segment of the activation periods,

Discussion

Activation of bilateral mesial and dorsolateral prefrontal areas during REVERSE is in good accordance with clinical findings indicating this test to be sensitive to lesions of the prefrontral cortex 7, 8, 21, 43. However, hemodynamic responses were not restricted to these regions but extended to the inferior and superior parietal lobules. Therefore, the assumption that the reversal task exclusively depends on an elementary cognitive operation—housed at a specific prefrontal location—cannot be

Acknowledgements

This study was supported by the German Research Foundation (SFB 307-B10, Ackermann/Daum) and the `Forschungsprogramm des Tübinger Universitätsklinikums' (fortüne nr. 327).

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