Tuning of the human left fusiform gyrus to sublexical orthographic structure

“Observations that left occipitotemporal activation was observed for pseudowords with increased activation as letter strings became more word-like (Binder et al., 2006) led to suggestions that learning to read tuned the receptive properties of the underlying neurons to combinations of letters (such…”

“Binder et al. (2006) recently showed that activation increases monotonically with bigram frequency in the left occipito-temporal region (but not the right), at the usual main peak of the VWFA, indicating a fine tuning to frequent letter combinations.”

“Previous studies showed that the left fusiform gyrus is responsive to orthographic structure during visual word recognition (Binder et al., 2006), leading researchers to suggest that the role of the left fusiform is to integrate features into elaborate schemes that represent whole words or objects (Starrfelt and Gerla…”

“Part of our results overlap with those of a recent study by Binder et al. (2006), who collected fMRI data while subjects were presented with letter strings at four levels of positional bigram frequency, ranging from very low to high.”

“Indeed, in expert alpha-betic readers, the VWFA is organized in a posterior-to-anterior hierarchy 42–44 : posterior parts respond to individual letters 43 (irrespective of case 44 ), whereas anterior parts respond to letter combinations such as bigrams 42,45 .”

“…cognitive task such as word recognition. fMRI studies of the developmental functional neuroanatomy of reading have provided evidence related to the developmental dynamics that occur in brain circuits that support reading (Booth et al. 2001, 2004; Schlaggar et al. 2002; Shaywitz et al. 2002, 2004;…”

“(2009), Binder et al. (2005, 2006), Burton et al. (2005), Chee et al.”

“This conclusion led to the ‘word shape’ hypothesis, according to which some form of supra-letter or holistic information about a printed word (e.g., the word envelope generated by a specific combination of ascending, descending, and neutral letters; Bouma, 1973) is used to identify the word.”

“Interestingly, previous studies in the sighted have suggested a visual anterior-posterior word processing chain along the left ventral occipitotemporal cortex, with preference for semantics anteriorly and word form posteriorly [31–33].”

“Not only has this area been shown to be positively correlated with graphotactic probability in functional brain-imaging studies of healthy readers (Binder et al. 2006; Vinckier et al. 2007), but it is also one of the major areas that, when damaged, leads to a type of acquired dyslexia known as pure…”

“In summary, our results therefore provide strong support for theories of experience-driven plasticity of the neural representations underlying reading (Baker et al., 2007; Binder et al., 2006; Dehaene et al., 2005; Vinckier et al., 2007), establishing that this learning does not just apply to lower-level representatio…”

“The reader is referred to the works of Booth et al (2004); Binder et al (2006); Pugh (2006); and others for further insights about developing neural substrates supporting these facets of language so critical for reading proficiency.”

“Such deficits at multiple levels are in line with converging evidence that the occipitotemporal cortex has more than one function and responds to multiple levels of sublexical orthographical structures (Binder et al., 2006; Dehaene et al., 2002; Vinckier et al., 2007; Wydell et al., 2003).”

“Considering the positive correlation of fMRI activation in ROI 5 with bigram frequency (Binder et al., 2006), one may suggest that ROI 5 and the posterior MTG constitute an anatomically connected tandem involved in grapheme-to-phoneme mapping.”

“This finding is consistent with consistent with greater activation in the context of more efficient recognition at the whole word level (Binder et al., 2006; Vinckier et al., 2007; Levy et al., 2008; Glezer et al., 2009).”

“…recognition (knowing that A and a are the same letter), learning of specific letter shapes (e.g. Hebrew versus Roman script), and compiling statistics of letter co-occurrence (bigrams), all of which have now been related to the VWFA (Baker et al., 2007; Binder et al., 2006; Dehaene et al., 2001).”

“This finding is consistent with proposals in which the posterior–anterior axis of the left fusiform is characterized as instantiating increasingly abstract, complex, and eventually modality-independent lexical processing (Vinckier et al, 2007 ; Binder, Medler, Westbury, Liebenthal, & Buchanan, 2006 ; Dehaene, Cohen, S…”

“Critically, activation in this area to letter-strings increases with their similarity to actual words[6, 7], especially in more anterior VWFA[8], suggested that it actually comprises a succession of detectors responding to progressively more abstract lexico-semantic aspects of the letter-strings.”

“…found that within the VOT, the left fusiform gyrus (FG; Table 1) is consistently activated across a wide range of numerical tasks (Arsalidou & Taylor, 2011), consistent with its hypothesized role in processing orthographic structure (Binder, Medler, Westbury, Liebenthal, & Buchanan, 2006).”

“Identification of this VOT site, analogous to macaque infero-temporal cortex, permitted detailed, mechanistic investigations to proceed, producing a prolific literature (Cohen et al., 2004; Binder et al., 2006; Gaillard et al., 2006; Baker et al., 2007; Vinckier et al., 2007; Turkeltaub et al., 2008; Glezer, Jiang & R…”

“Four left hemisphere regions were chosen because they were identified in our previous effective connectivity studies as part of the language network involved in the phonological judgment of visually presented words (Bitan et al., 2005, 2006).”

“Some authors entertain the hypothesis that the VOT represents full words (lexical) [81,82,88,92,93] and memory for words [94].”

“…alexia (Cohen et al. 2003, Gaillard et al. 2006, Leff et al. 2001, Warrington & Shallice 1980), (c) VOT responses are sensitive to bigram frequency (Binder et al. 2006, Vinckier et al. 2007), (d ) there is a word-specific pattern of orthographic priming in VWFA (Dehaene et al. 2001), and (e) VWFA…”

“Orthographic processing would then proceed in a posterior-anterior sweep through left fusiform, known to be sensitive to orthographic structure (e.g., Binder, Medler, Westbury, Liebenthal, & Buchanan, 2006; Cohen et al., 2000; Dehaene et al., 2005).”

“…predominantly in the left hemisphere, involving in (a) visual analysis: early visual areas (BA 17, 18, and 19) and midfusiform gyrus (BA 19, 37) [Binder et al., 2006; Cohen et al., 2000; Devlin et al., 2006; Gaillard et al., 2006; James et al., 2005; Mechelli et al., 2007; Vigneau et al.,…”

“by performance measures), both known to affect activity in the VWFA (Booth et al. 2003; Binder et al. 2006).”

“We next used techniques from machine learning in iEEG data from P1 and P4 to assess the sensitivity of lmFG to sublexical, orthographic statistics (bigram frequency) that has been hypothesized as an indicator for a visual word form system (16, 21).”

“The findings of Binder et al. (2006) that the OT region responded to manipulations of orthographic familiarity at the sub-word level necessitated holding bigram frequency constant across conditions. Given that we controlled for bigram frequency, we are able to conclude that OT is sensitive to whole-word orthographic f…”

“Recent evidence for prelexical tuning of the VWFA was provided by Binder et al. (2006), who found that OT cortex activation systematically increased with increasingly higher letter sequence probability (i.e., bigram-frequency) of a nonword.”

“This region is usually equally activated by real words and readable pseudowords but less by nonwords (consonant strings for instance) and shows, as we found here, a gradually increasing response to alphabetic stimuli with increasing letter probability, thus with higher word-likeness (Binder et al., 2006).”

“However, in recent years more and more experimental evidence is gained over the more general role of the LOT [12] reflecting an operation common to the processing of words [46], word sub-units [19], pictures [47], objects [48], or stored visual forms and structures in general [49].”

“N IH -PA Author M anuscript N IH -PA Author M anuscript N IH -PA Author M anuscript increasingly more “abstract” orthographic functions (Cohen, et al., 2003; Vinckier et al., 2007; Binder et al., 2006).”

“Binder et al. (2006) gathered evidence that this area is especially sensitive to sublexical bigram frequency—a pivotal element of our study design.”

“Xue and colleagues (2005) found strong left-hemispheric dominance in 12-year-old Chinese children, and Chan and colleagues (2009) found that, in Chinese readers, only the left-hemisphere visual system shows a spatial hierarchical organization of brain responses to increasingly languagelike word forms, as occurs for La…”

“Activation in VWFA is hierarchically organized so that the strength of activation increases with orthographic regularities (Vinckier et al., 2007) and bigram frequency ( Binder, Medler, Westbury, Liebenthal, & Buchanan, 2006 ).”

“This proposal found ground in the equivalent levels of activation detected for words and pseudowords at the level of the vWFA (Dehaene et al. 2002; Binder et al. 2006; Vinckier et al. 2007).”

“This approach removes variation both within and between conditions that can be explained by a linear function of RT (Binder et al. 2006; Graves et al. 2010).”

“If no absolute visual field position information is present, the neural circuitry could encode relative position implicitly by representing ordered letter strings (bigrams, trigrams, and so forth) (34, 35).”

“One fMRI study found larger activation for more “word-like” nonwords compared to nonwords with low frequency letter constellations in a letter detection task (Binder et al., 2006).”

“This region has been strongly associated with orthographic processing in adult reading (Binder et al., 2006; Cohen et al., 2000; Gaillard et al., 2006; Dehaene et al., 2002; Jobard et al., 2003) and spelling (Rapp and Lipka, 2011; Purcell et al.”

“The VWFA has been related to prelexical representation of visual words, responding preferentially to letter strings than to other categories of visual stimuli (for a review, see Cohen & Dehaene, 2004), and to word and word-like (pseudowords) stimuli than consonant strings ( Binder, Medler, Westbury, Liebenthal, & Buch…”

“Using fMRI, Binder et al. (2006) found that the brain region that is sensitive to positional bigram frequencies is the left lateral fusiform gyrus, which is the visual word form area (VWFA), a brain region that is particularly responsive to words and pseudowords compared to other types of visual…”

“The lexical interpretation would be consistent with the recent findings reported by Binder, Medler, Westbury, Liebenthal, and Buchanan (2006) using an fMRI methodology.”

“12–14) and have shown that it probably hosts multiple orthographic representations of letters (15, 16), bigrams (17), and short words (18).”

“, 2003; Kourtzi and Kanwisher, 2001; Yovel and Kanwisher, 2004), and its crucial role in orthographic processing is widely accepted and has been demonstrated in numerous studies (Baker et al., 2007a; Binder et al., 2006; Bruno et al., 2008; Cohen et al., 2002; Dehaene and Cohen, 2011; Dehaene et al., 2002, 2005; Gleze…”

“More generally, a critical point regarding orthographic redundancy is that it naturally covaries with other factors known to impact visual word recognition, such as pronunceability (Binder et al., 2006), word frequency (Adams, 1981), or orthographic neighborhood (Andrews, 1992).”

“…the broad expanse of the FG, a region labeled the Visual Word Form Area (VWFA), located at roughly y=−50, is thought to mediate pairwise letter associations, or bigrams (Binder et al., 2006; Dehaene and Cohen, 2011; Dehaene et al., 2005; Dien, 2009a; McCandliss et al., 2003; Polk and Farah, 1997).”

“When written stimuli respect increasingly well the statistics of words in the known language, they elicit increasingly greater activity in the VWFA ( 72 ).”

“, 2004), frequent bigrams (Vinckier et al., 2007; Binder et al., 2006), high demands on visual discrimination (Rogers et al.”

“Specifically, we have shown that rather than processing prelexical information, such as commonly occurring letter combinations (Binder et al., 2006; Cohen and Dehaene, 2004; Dehaene and Cohen, 2011) the VWFA is finely tuned to whole real words (Glezer et al., 2009) AC C EP TE D M AN U SC R IP T and…”

“, 2001) and word recognition (Nobre et al., 1994; Pammer et al., 2004; Binder et al., 2006), among others.”

“…operation common to the processing of words with regular (Kronbichler et al., 2007) or irregular (Bruno et al., 2008) orthographies, word sub-units (Binder et al., 2006), pictures (Starrfelt and Gerlach 2007), objects (Bar et al., 2001), or stored visual forms and structures in general (Joseph and…”

“…hemisphere mid-fusiform gyrus/occipito-temproal sulcus has been identified as an important component of the reading network (Baker et al., 2007; Binder et al., 2003, 2006; Booth et al., 2002; Carreiras et al., 2007; Cohen et al., 2000, 2002, 2004; Dehaene et al., 2002, 2004; Fiez et al., 1999;…”

“Precisely, in the left anterior and middle fusiform gyrus (at the location of the Visual Word Form Area reported in previous studies, e.g., Cohen et al., 2002; Jobard et al., 2003; Binder et al., 2006), precentral gyrus, SMA and IFG tri, the effect of stimulus visibility was significantly (or marginally, p ≤ .”

“Neuroimaging results indicate that the VWFA is sensitive to the familiarity of subword letter combinations like bigrams and trigrams (Vinckier et al., 2007; Binder et al., 2006).”

“…Baker et al., 2007; Brem et al., 2010; Dehaene et al., 2010) and is not sensitive to low-level features of written words, such as size, position, font, or letter case (Dehaene et al., 2004; Binder et al., 2006; Vinckier et al., 2007; Glezer et al., 2009; Qiao et al., 2010; Braet et al., 2012).”

“…have shown that activation in this region ismodulated by the familiarity of sublexical orthographic features (e.g., the frequency of pairs or triplets of letters) with frequent features eliciting higher activation relative to less frequent features (Binder et al., 2006; Vinckier et al., 2007).”

“As a matter of fact, a wealth of research indicates that the vOTC is the brain region that is sensitive to the orthographic familiarity of letter strings (Binder et al., 2006; Dehaene and Cohen, 2011).”

“shape representations (Binder et al., 2006; Dehaene et al., 2005; Glezer et al., 2009; Vinckier et al., 2007), independent of the specific visual features that define these shapes.”

“…al., 2006; Brem et al., 2009; Maurer et al., 2005, 2006; Xue and Poldrack, 2007), while fine-tuning refers to the sublexical and whole word levels (Binder et al., 2006; Dehaene et al., 2005; Glezer et al., 2009; Kronbichler et al., 2004; Vinckier et al., 2007) as for example reflected by…”

“…regions within this network play different roles in LD. Extrastriate regions have been linked with orthographic processes such as visual feature extraction and mapping visual patterns onto lexical representations (Petersen et al. 1990; Binder et al. 2003, 2006; Cohen et al. 2003; Gold et al. 2006).”

“This should be most evident in areas previously implicated in semantic processing such as the ITS (Binder et al., 2009; Graves et al., 2010) and AG (Binder et al., 1997, 2005, 2009; Price and Mechelli, 2005; Price, 2012).”

“Turning to Open-bigram coding, Binder et al. (2006) found that activity in the VWFA was correlated with the frequency of (contiguous) bigrams in letter strings presented to subjects.”

“Furthermore, fMRI research has provided evidence for the existence of such letter combination representations in the VWFA (Binder et al., 2006; Vinckier et al., 2007), and our own computational modeling work has shown how letter combinations can emerge during orthographic learning (Hannagan et al., 2013).”

“Keywords: ECoG, MEG, N400, speech processing”