Corresponding to lesions of left occipito-temporal (OT) regions in acquired cases, we found a dysfunction of this region in our developmental cases who failed to exhibit responsiveness of left OT regions to the length of words and pseudowords. This abnormality in the left OT cortex was accompanied by absent responsiveness to increased sublexical reading demands in phonological inferior frontal gyrus (IFG) regions. Interestingly, there was no abnormality in the left superior temporal cortex which—corresponding to the onological deficit explanation—is considered to be the prime locus of the reading difficulties of developmental dyslexia cases.

Introduction

Recent studies on the manifestation of developmental reading problems established an interesting behavioral similarity to a form of acquired dyslexia referred to as letter-by-letter (LBL) reading. As suggested by the term letter-by-letter reading, the critical manifestation is an abnormal effect of word length, that is, number of letters, on reading time. To illustrate, Cohen et al. [1], reported linear increases of reading time with increases in word length in acquired LBL readers, ranging up to 400 ms per each additional letter in words from 3 to 9 letters. Similar, although less dramatic, length related reading latency increases were reported for English, German, and Italian dyslexic children and adolescents [2]–[4]. An abnormal word-length effect of developmental dyslexia cases was not only observed for latencies of reading aloud responses but also for visual inspection time in eye movement studies [5], [6]. In terms of the prominent cognitive dual-route model of visual word processing (e.g., [7]), both the loss of efficient (i.e., length-independent) visual word processing in acquired LBL reading and the difficulty to attain efficient word processing in developmental dyslexia may be traced to a dysfunction of the lexical reading route. The critical component of the lexical route is the orthographic word lexicon which contains representations of the letter sequence of frequently read words. Such orthographic word entries allow fast visual whole-word recognition, that is, parallel assimilation of letter strings and direct access to word phonology and meaning. Frequent absence of such orthographic word entries results in reliance on the slow sublexical reading route. This route achieves access to word phonology by serial sublexical orthographic-phonological recoding which obviously gives rise to the abnormal length effect on reading time for words. However, developmental dyslexia cases suffer not only from an abnormal length effect for words, but they also exhibit inefficient sublexical processing of the unfamiliar letter strings of pseudowords (e.g., [8]), which may be attributed to frequent absence of larger sublexical multi-letter recognition units and adherence to serial grapheme-phoneme coding instead. Furthermore, even when dyslexic readers rely on lexical route processing of words, they still were found to exhibit a reading speed deficit [6], [9]–[11].

In the field of acquired dyslexia, there is growing consensus that the loss of efficient word processing and the emergence of LBL reading is caused by lesions affecting the left ventral occipito-temporal (OT) cortex, specifically the Visual Word Form Area (VWFA), or connections to or from the VWFA [1], [12]–[16]. Similarly, one may hypothesize that the difficulty with fast fluent reading of developmental dyslexia cases may be caused by a congenital dysfunction of the OT cortex. However, this hypothesis is quite different from the dominant explanatory framework in the field of developmental dyslexia (e.g., [17]). Here, the main dyslexic difficulty is seen in the acquisition of the sublexical route, that is, in self-reliant phonological word decoding. This difficulty is seen as arising from a verbal-phonological deficit which affects the identification of phonemes in spoken words which, in turn, affects the mapping of graphemes onto phonemes which, in turn, affects the acquisition of self-reliant phonological word decoding which, in turn, affects orthographic learning. In correspondence with the phonological deficit explanation, reviews of imaging studies summarize the findings as speaking for a primary dysfunction of posterior language areas (i.e., posterior superior temporal gyrus/sulcus and adjacent parietal regions) and consider underactivation of left OT regions as secondary to the primary dysfunction of left temporo-parietal (TP) region [18]–[22].

Evidence for the phonological deficit explanation and specifically for a profound dyslexic difficulty with the acquisition of self-reliant word decoding is largely based on English language which is an outlier with respect to grapheme-phoneme regularity [23]. In more typical alphabetic orthographies with transparent grapheme-phoneme correspondences, reading accuracy for short words and pseudowords approaches ceiling after a couple of months of instruction [24], [25]. Even for dyslexic children, the mentioned reading fluency impairment typically occurs in the context of high reading accuracy (e.g., Dutch: [26], Finnish: [27], Greek: [28], Hebrew: [29], Italian: [30], Norwegian: [31], Spanish: [32]). Direct German-English comparisons with similar words and pseudowords confirmed the difference in reading accuracy [33], [34]. To illustrate, for low frequency words, Landerl et al. [33] found that accuracy was about 93% for German dyslexic children compared to only about 50% for their English peers. The ease of accurate phonological word reading in regular orthographies is of theoretical importance as it raises doubts that poor orthographic learning (i.e., reduced storage of letter strings for words or larger segments) is secondary to difficulty with accurate phonological reading. This then raises further doubts whether observed dysfunctions of the left OT regions in dyslexic readers are secondary to a primary dysfunction of left posterior language regions. The alternative possibility is that the fluency problem of dyslexic readers in regular orthographies – similar to acquired cases of LBL reading – may be caused by a primary dysfunction of left OT regions engaged by highly efficient lexical and sublexical route processes. There is already some support for this latter hypothesis from functional imaging studies with German-speaking dyslexic children and adults who suffer from the characteristic reading speed problem [35]–[38].

The present fMRI study extended this line of research by focusing specifically on dyslexic abnormalities in the brain response to increased length (number of letters) of words and pseudowords. As mentioned above, dyslexic readers similar to LBL readers exhibited abnormal increases of reading time with increasing word length. For studying abnormal brain responses, we extended a recent imaging study with nonimpaired readers from our lab [39] by adding a dyslexic sample. This study manipulated item length with short items (words and pseudowords) consisting of 3–5 letters and long ones of 6–10 letters. With respect to the mentioned reviews of imaging studies, several findings of Schurz et al. [39] are important. Firstly, the processing of both words and pseudowords led to marked activation in left OT and left inferior frontal gyrus (IFG) regions, but not in left temporal regions. Secondly, the activation pattern in both the OT and the IFG regions corresponded to expectations from lexical processing of words and sublexical processing of pseudowords as there was no effect of length on the brain response to words, but a substantial effect in the response to pseudowords. Of main interest with respect to a primary or secondary dysfunction of left OT regions is the activation pattern shown by the present dyslexic sample. Let us first consider expectations from an only secondary dysfunction, that is, less engagement by lexical whole-word recognition and sublexical multi-letter recognition of otherwise fully functional left OT regions. From this hypothesis one would expect left OT activation to correspond to the behavioral response pattern shown by our dyslexic sample. Compared to the nonimpaired sample, our dyslexic readers exhibited generally prolonged response latencies and a stronger length effect on response latencies for both words and pseudowords. When fully functional left OT regions of dyslexic readers are engaged by slow serial letter string processing resulting in the mentioned latency pattern, one would expect increased activation and a stronger length effect on activation. This pattern is not expected from a primary dysfunction of left OT regions. From this hypothesis one would expect – compared to controls – generally reduced activation and, specifically, absence of a length effect on activation.