Elsevier

NeuroImage

Volume 20, Issue 2, October 2003, Pages 693-712
NeuroImage

Regular article
Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies

https://doi.org/10.1016/S1053-8119(03)00343-4Get rights and content

Abstract

Numerous studies concerned with cerebral structures underlying word reading have been published during the last decade. A few controversies, however, together with methodological or theoretical discrepancies between laboratories, still contribute to blurring the overall view of advances effected in neuroimaging. Carried out within the dual route of reading framework, the aim of this metanalysis was to provide an objective picture of these advances. To achieve this, we used an automated analysis method based on the inventory of activation peaks issued from word or pseudoword reading contrasts of 35 published neuroimaging studies. A first result of this metanalysis was that no cluster of activations has been found more recruited by word than pseudoword reading, implying that the first steps of word access may be common to word and word-like stimuli and would take place within a left occipitotemporal region (previously referred to as the Visual Word Form Area—VWFA) situated in the ventral route, at the junction between inferior temporal and fusiform gyri. The results also indicated the existence of brain regions predominantly involved in one of the two routes to access word. The graphophonological conversion seems indeed to rely on left lateralized brain structures such as superior temporal areas, supramarginal gyrus, and the opercular part of the inferior frontal gyrus, these last two regions reflecting a greater load in working memory during such an access. The lexicosemantic route is thought to arise from the coactivation of the VWFA and semantic areas. These semantic areas would encompass a basal inferior temporal area, the posterior part of the middle temporal gyrus, and the triangular part of inferior frontal gyrus. These results confirm the suitability of the dual route framework to account for activations observed in nonpathological subjects while they read.

Introduction

Despite the large number of neuroimaging studies interested in unraveling brain organization sustaining reading, acquiring a clear picture of cerebral areas involved in visual word access and the specific cognitive processes thought to take place in these regions remains quite a tricky enterprise. The difficulty of such a task arises from many combined elements that contribute to mask the picture one can get by simply looking at the results that are already published.

A first element is the lack of explicit definition of the theoretical framework in which studies are undertaken. This is of prime importance in the interpretation of activation results, since theoretical concepts and the suspected necessary cognitive processes may vary from one study to another. Models of dual route theory provide a framework commonly used in studies of reading. This theory develops the view that word reading can be achieved through two distinct routes, relying on discrete processes (Fig. 1). The graphophonological route, also called indirect route, requires visual words to be transformed into their auditory counterparts, thanks to the application of grapheme-to-phoneme correspondences. The pronunciation of words being available, subjects can then access their meanings. These grapheme-to-phoneme correspondences are however more or less univocal according to the language considered and its degree of transparency: while the same group of letters will invariably lead to the same pronunciation in Spanish, some letter combinations in English will be read alouddifferently, depending on the word in which they are used (e.g., “int” like in “pint” or “mint”). To read correctly those words that do not follow the most usual spelling-to-sound rules, it is necessary to engage another route, called direct or lexicosemantic route. This route relies on the direct association between the visual forms of words (in much the same way as images) and their meanings. This association is thought to build progressively when subjects repetitively meet words, and the direct route is therefore used when subjects read frequent or orthographically irregular words (in which case the association has to be learned, since grapheme-to-phoneme correspondences (GPC) application cannot lead to the proper pronunciation). Learned word forms are then supposed to be stored in a visual word form system, also called orthographical lexicon, whose size and composition would depend on the subject's reading experience. The dual route model originates from the observation of patients that, following brain injury, relied exclusively on one of the two routes for reading. Surface dyslexia, characterized by the impairment of the lexicosemantic route and reading by the graphophonological route, typically leads to regularization errors (e.g., reading “pint” to rhyme with “mint”), homophones confusions (e.g., understand “pear” after reading “pair”), or to accept pseudowords homophones as real words (they accept “rite” as a correct word for “right”). The opposite syndrome, phonological dyslexia, leaves the direct route as the only possible access to written words meanings and leads to difficulties in reading words for which no form–meaning association had previously been established (infrequent words, pseudowords, new names, and also grammatical words, which are devoid of invariant meanings). Despite a general agreement on the processes involved in the two routes, some theoretical variations nevertheless subsist in the conception of the first stages of word access. We developed a conception of dual route models stating the existence of a visual word form system dedicated to the direct route only, which is concordant with the view of some authors Morton, et al., 1980, Coltheart et al., 1993. A concurrent view posits that the visual word form system would be common to both routes and that information would then be relayed to the most appropriate route for the word read (Warrington and Shallice, 1980). According to this latest view, the visual word form system would therefore process not only known words as a whole, but also other infralexical stimuli such as graphemes, syllables, or morphemes. Warrington and Shallice indeed considered that this system would play a role in the “parsing of letter strings into ordered familiar units and the visual categorization of these units” (Warrington and Shallice, 1980, p. 109). According to this view, when a word is presented, its visual grasping could be effected in different ways, depending on the experience of the reader. If this word has been previously seen a sufficient number of times, it may be globally recognized as a prelearned word form (as in the case of an access through the direct, lexicosemantic route). If this is not the case, the reader may then begin to segment the word into sublexical parts, corresponding either to letter combinations he has visually learned because they occur often in his language (such as the unit “tion” that is to be found in many English words) or to simple graphemes (that sometimes need several letters to be considered as a single unit, as with the grapheme “ch”). The main difference thus arises from the fact that this later view would not predict the existence of a specialization for the visual processing of known words, as is done with the concept of “written word lexicon,” but rather a specialization for alphabetical stimuli.

Despite these last theoretical variations on the first processing stages, we decided to insert this metanalysis in the framework of the dual route model of word reading. This model first emerged from cognitive neuropsychological observations of brain-damaged patients (taking therefore cerebral constraints into account), and it has found some support in experimental psychology in normal readers (Coltheart and Rastle, 1994). Additionally, we assisted very recently to a burst of neuroimaging experiments reporting the involvement of different brain areas depending on the specific route thought to underlie word access Herbster et al., 1997, Rumsey et al., 1997, Fiez, 1997, Simos et al., 2002, even though some controversies remain as to the nature of the processes undertaken in some brain regions. It is of prime importance to state that this article does not aim at assessing the appropriateness of this model in comparison to others such as connectionist models, but rather to see how it can accommodate to neuroimaging results.

Besides the possible discrepancies stated above and introduced by theoretical frameworks, differences in sensitivity may also arise out of methodological or technical variations from one laboratory to another, leading to a reduced set of activated regions which can drive authors to neglect the roles of other brain areas. More importantly, the use of varying anatomical labels among studies may also contribute to complicate a general overview of the literature, since it can induce readers to conclude that different brain areas are implicated despite activations that are congruent in terms of spatial coordinates.

The goal of this metanalysis was to clarify results published in the reading literature and to determine (a) whether there exists a system dedicated to the processing of visual word form as postulated by the dual route models, and (b) whether neuroimaging results support the possibility of two distinct routes for accessing words. To answer these questions, we performed an analysis that was as observer independent as possible, based on the core exploitation of coordinates related to cognitive contrasts obtained in 35 different neuroimaging studies. This analysis relied on the use of an automated spatial segregation of activation peaks coordinates, coupled with an automated anatomical labeling of the spatially congruent activations in the Montreal Neurological Institute stereotactic space (Tzourio-Mazoyer et al., 2002).

Section snippets

Raw data

The raw data of this metanalysis was constituted by activation peak coordinates reported in 35 neuroimaging studies (using PET and fMRI exclusively, see Table 1) and obtained in contrasts, implying the reading of words or pseudowords. Only studies ranging from years of publication 1990 to 2002 were used, in which stereotactic coordinates were made available exclusively for tasks submitted to nonpathological subjects. These activation tasks were either directly compared to each other or

Results

Thirty-five clusters were located in the left hemisphere; 15 were in the right hemisphere and 5 clusters were constituted by isolated peaks dispersed in the brain with a high spatial standard deviation (many of these peaks were located in white matter and some even fell out of the brain). The aim of this work was to provide a global view of the results published in the last few years concerning two main controversies related to the dual route of reading framework. For this reason, we chose to

Discussion

This method of spatial segregation resulted in a set of clusters of reliable activations that corresponded in large parts to structures previously described as playing a key role in reading. A first question that we wished to investigate in the light of this method of review concerned the possible specialization of a brain area for the processing of visual words.

Conclusions

This metanalysis based on the gathering and spatial segregation of activation peaks obtained in reading studies revealed an overall reliability of published results. Despite methodological and experimental differences inherent to the comparison of studies issued in worldwide laboratories, a consensus can be drawn within the technique's spatial limitation as to which sites are critical for identified processes.

The main result consists of the demonstrated suitability of the dual route model

Acknowledgements

We thank Laure Zago and Emmanuel Mellet for thoughtful comments on the manuscript. We are grateful to the two anonymous referees, the constructive comments of which allowed us to substantially improve the manuscript. This work was presented in part at the 8th International Conference on Functional Mapping of the Human Brain, June 2–6 2002, Sendai, Japan.

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