Interhemispheric cooperation and non-cooperation during word recognition: Evidence for callosal transfer dysfunction in dyslexic adults
Introduction
Interhemispheric interaction during word recognition has been investigated by experiments in which individual word stimuli are presented unilaterally in left visual field (LVF) or the right visual field (RVF), or when identical word stimuli are presented simultaneously to both visual fields (bilateral redundant trials) (e.g. Barnett et al., in press, Hellige, 1993, Marks and Hellige, 1999, Marks and Hellige, 2003, Mohr et al., 1994a, Mohr et al., 1996). The organisation of the visual pathways ensures that in the bilateral condition, both hemispheres are initially stimulated with the same word, whereas in the unilateral conditions, only one hemisphere is stimulated initially. Tasks based on this design may give us clues as to whether the two hemispheres cooperate or interact when processing the same stimulus (Hellige, 1993). Numerous studies have shown that redundant bilateral presentation leads to significantly better processing in healthy adult participants (in terms of accuracy and latency) compared with the condition where only the language dominant left hemisphere is stimulated (e.g. Barnett et al., in press, Hellige, 1993, Mohr et al., 1994a, Mohr et al., 1996). The redundant bilateral advantage with words was reported to be absent in a split-brain patient with complete commissurotomy (Mohr, Pulvermüller, Rayman, & Zaidel, 1994b) and in schizophrenic patients, who have been argued to have abnormal interhemispheric processing (Barnett et al., in press). Thus, the bilateral advantage has been taken as evidence for interhemispheric cooperation and seems to be strongly dependent on the intactness and efficient functioning of the corpus callosum.
What could be occurring in the brain during redundant bilateral presentation? We are only aware of two neuroimaging studies that have used lateralised (rather than central) word presentation in order to investigate the contribution and functioning of the two cerebral hemispheres during visual word recognition. These studies have proposed that all written words, regardless of the position in the visual field in which they appear, are projected to one orthographic processing area, the so-called ‘visual word-form area’ in the left mid fusiform gyrus (Cohen et al., 2000, Cohen et al., 2002). Within 250 ms of viewing a written word, this system analyses the information needed to identify a word, despite variations in print, script, font, size, and retinal position (McCandliss, Cohen, & Dehaene, 2003). Thus when Cohen et al. (2002) analysed fMRI responses to words projected briefly in the LVF or the RVF, they found responses in the visual word form area to words presented in both visual fields (though stronger to RVF than to LVF words). No activation was observed at the homologous site in the right hemisphere. The visual word form area is thought to play a pivotal role in linking visual processing of written words in occipital areas through to more anterior temporal, parietal, and frontal areas for the purpose of both semantic access and phonological retrieval (Dehaene, Cohen, Sigman, & Vinckier, 2005). Some have argued that the visual word form area is not specifically sensitive to letter strings, but plays a role in the more general integration of visual, phonological, and semantic information contributing, for example, to visual object recognition as well as to reading (e.g. Devlin et al., 2006, Price and Friston, 2003, Price and Friston, 2005).
In line with the view that there is a single orthographic processing system in the left hemisphere, the callosal relay hypothesis (Zaidel, Clarke, & Suyenobu, 1990) proposes that a word presented to the LVF, reaching the right hemisphere, has to be relayed to the left hemisphere via the corpus callosum in order to activate the neuronal networks in the language regions. This callosal relay causes a time delay and loss of stimulus quality and accounts for some or all of the RVF advantage typically reported in a range of tasks involving word recognition (see Ellis, 2004, Hellige, 1993, Zaidel et al., 1990). During redundant bilateral presentation, it is reasonable to assume that the RVF word would reach the visual word form area more directly, whereas the LVF word would need to be relayed via the corpus callosum. If the LVF input reaches the visual word form area while the RVF input is still being processed, then the two inputs should summate and facilitate the resolution of the word form, leading to more accurate and faster recognition. A key factor in generating a bilateral advantage would thus appear to be efficient callosal transfer from the right hemisphere to the left hemisphere, in time for LVF input to converge with processing of the same item presented to the left hemisphere. Finally, while the existence of a bilateral advantage for word recognition is well established, unfamiliar nonwords do not show a bilateral advantage for either accuracy of report (Hellige, Taylor, & Eng, 1989) or speed and accuracy of responding in the lexical decision task (Mohr et al., 1994a, Mohr et al., 1996). The capacity of stimuli to show a bilateral advantage when two versions are presented rather than one would therefore seem to be dependent on the pre-existence of representations of those stimuli that have been built up through experience.
Developmental dyslexia is a neurological disorder that is typically characterised by an unexpected and severe reading difficulty (Vellutino, Fletcher, Snowling, & Scanlon, 2004). An influential theory proposes a specific phonological deficit in the way the brain represents, stores, and retrieves the phonological attributes of words (see Snowling, 2000). Support for this view comes from behavioural evidence that dyslexics perform particularly poorly on tasks requiring phonological awareness, such as phoneme counting, deletion, substitution, and nonword repetition (Vellutino et al., 2004). This behavioural evidence is supported by studies linking the phonological deficits to atypical brain activation and anatomical differences. Neuroimaging studies have revealed a number of anatomical abnormalities in the left hemisphere that are consistent across different orthographies and remain when behavioural performance is matched (e.g. Brunswick et al., 1999, Galaburda et al., 1985, Paulesu et al., 2001, Shaywitz et al., 2003). Left hemisphere dysfunctions conceivably reflect a phonological deficit given the left hemisphere’s role in many phonological tasks during reading (Jobard et al., 2003, Mechelli et al., 2005, Mechelli et al., 2003).
It has also been proposed that reading difficulties in dyslexia may be as the result of an interhemispheric communication deficit; that is, an abnormal integration, transfer, or collaboration of tactile, auditory, and visual information between the hemispheres (see Beaton, 1997). The interhemispheric deficit theory of dyslexia has a long history. Orton (1925) argued that reading difficulties are characterised by an absence of functional asymmetry caused by impaired interhemispheric transfer. However, subsequent studies of lateralisation in dyslexia have been mixed in outcome. Boles and Turan (2003) reviewed visual half-field studies of word recognition and concluded that dyslexics and controls do not differ in lateralisation. Bryden (1988) reviewed dichotic listening studies and found a tendency toward reduced lateralisation in dyslexics, but with considerable variability across studies. Since then studies by Obrzut and colleagues (Boliek et al., 1988, Obrzut et al., 1989), and by Kershner and Micallef, 1992, Bloch and Zaidel, 1996 have found no overall differences between dyslexics and normal subjects. More recently, however, various methods have been employed to test the interhemispheric deficit theory of dyslexia and morphological, electrophysiological, computational, and behavioural techniques have highlighted some anomalies which could underlie part or all of the problems experienced by dyslexics (e.g. Badzakova-Trajkova et al., 2005, Duara et al., 1991, Fabbro et al., 2001, Robichon and Habib, 1998, Rumsey et al., 1996, Shillcock and Monaghan, 2001).
Studies have looked for a structural concomitant to possible impaired interhemispheric communication by measuring the midsagittal surface of the corpus callosum using magnetic resonance imaging (MRI). The corpus callosum is a bundle of mostly myelinated fibers that is the main structure serving information transfer between the hemispheres. MRI studies with dyslexics have indicated corpus callosum abnormalities involving the splenium (Duara et al., 1991, Rumsey et al., 1996, Rumsey et al., 1999), the isthmus (Rumsey et al., 1996, Rumsey et al., 1999) and the genu (Hynd et al., 1995). Robichon and Habib (1998) carried out a morphometric MRI study of the corpus callosum in 16 dyslexic adults and 12 controls. While controlling for overall brain size, they found that the dyslexics’ callosa were more circular and rounded in shape compared to the controls, and they reported abnormalities in the isthmus (Robichon & Habib, 1998). Similarly, Duara et al. (1991) found differences in posterior areas (i.e. the isthmus and splenium) in dyslexics’ callosa compared to controls. The splenium and isthmus contain fibers from the temporal and posterior parietal cortex and connect the angular gyri, which are considered to play a role in reading. The splenium and isthmus are also the only parts of the corpus callosum concerned with connecting the two visual cortices within the occipital lobes (Rumsey et al., 1999). Thus, abnormalities in posterior corpus callosum areas could be associated with left hemisphere reading and language dysfunctions reported in dyslexics. This possibility is supported by evidence that children with callosal agenesis demonstrate specific problems on phonological tasks that dyslexics typically find difficult (e.g. rhyme identification, phoneme manipulation, and nonword reading) (Temple, Jeeves, & Vilarroya, 1990).
The corpus callosum abnormalities reported in dyslexia have, however, been inconsistent (see Chiarello et al., 2006, Larsen et al., 1992, Witelson, 1985). Some studies have found larger areas of the corpus callosum in dyslexic participants compared to controls (Duara et al., 1991, Robichon and Habib, 1998), while others have reported smaller areas (Von Plessen et al., 2002). It is not yet established whether differences in callosal size correspond to numbers of interhemispheric fibers or myelinated fibers, or even to more glial cells (Aboitiz, Scheibel, Fisher, & Zaidel, 1991). Further, while research has shown that handedness, age, and gender have direct impacts on the anatomy and development of the corpus callosum, in many studies these factors have not been controlled. Taken together, the anatomical evidence suggests that dyslexic brains may be characterised by anatomical abnormalities of the corpus callosum, but it is certainly not clear what the precise nature of that callosal abnormality might be, or whether it is consistent across dyslexic individuals.
Returning to functional rather than anatomical evidence, some support for the interhemispheric deficit theory of dyslexia comes from tachistoscopic half-field and dichotic listening experiments (Gross-Glenn & Rothenberg, 1984), and from studies of inter-manual transfer of tactile information (e.g. Beaton, Edwards, & Peggie, 2005). Delays in callosal transfer and increased error rates in dyslexics have been observed in finger localisation tasks (Fabbro et al., 2001, Moore et al., 1996; though see Sotozaki & Parlow, 2006). Studies have found that dyslexics perform significantly more poorly relative to controls in conditions where callosal transfer of motor information is necessary (e.g. Moore et al., 1995, Moore et al., 1996). However, in many of these studies the chronological and reading ages of the participants have not been controlled, complicating the interpretation of the findings. When reading age was controlled by Beaton et al. (2005), no differences were observed between dyslexics and controls on a finger localisation task. Thus, this behavioural literature provides suggestive but certainly not conclusive evidence for a general interhemispheric transfer deficit in dyslexia. We note, though, that the hypotheses proposed here rely only on dyslexics having problems in transferring visual information from one hemisphere to the other across posterior parts of the corpus callosum.
The preceding literature review points to the importance of interhemispheric interaction for normal reading efficiency, and some evidence for an interhemispheric transfer deficit in at least some dyslexic individuals. However, the evidence for interhemispheric processing deficits in dyslexia is mixed, consequently difficult to interpret, and often limited by lack of control of confounding variables and small sample sizes. In the present study, we explore the assumption that the efficiency of interaction between the cerebral hemispheres, rather than the specific processes performed by each, and the individual differences in this process, can influence visual word recognition. We report three experiments using the redundant bilateral design which investigated functional lateralization and interhemispheric cooperation in dyslexic adults using experimental tasks aimed to reveal effects of laterality and interhemispheric cooperation in matched controls. To our knowledge, no previous study has investigated the redundant bilateral advantage in individuals with dyslexia. Previous studies employing similar designs with normally reading adults have used lexical decision tasks with words and nonwords (e.g. Barnett et al., in press, Mohr et al., 1994a). However, lexical decision requires a decision component that may dilute or distort the effects of perceptual encoding on overt performance, and dyslexic individuals have particular problems with nonword reading (e.g. Snowling, 2000). Thus, tasks requiring report of briefly-presented words in unilateral (non-redundant) and bilateral (redundant) conditions were chosen. The dependent variable was accuracy of correct response. Experiment 1 investigated LVF, RVF, and bilateral (BVF) report in dyslexic and control adults for briefly-presented words. Experiment 2 investigated whether controls and dyslexics show an advantage when redundant stimuli are presented simultaneously to the upper and lower visual fields; that is, when the advantage is not dependent upon efficient callosal transfer of a whole word from the right to the left hemisphere. Experiment 3 explored whether partial word cues (first and last letters) presented to one hemisphere can combine with whole words presented to the opposite hemisphere to facilitate word recognition and lead to a bilateral advantage.
Section snippets
Experiment 1
Word report accuracy during unilateral LVF and RVF presentation was compared to performance during redundant bilateral presentation. We anticipated that controls would show a bilateral advantage in report accuracy compared to performance on the RVF condition, whereas if dyslexics are affected by an interhemispheric transfer deficit, they might show a reduced or absent bilateral advantage. A deficit in interhemispheric transfer could also cause an enhanced RVF advantage for the dyslexic group,
Experiment 2
The visual word form area is believed to receive inputs from words presented anywhere in space (Cohen et al., 2000, Cohen et al., 2002, McCandliss et al., 2003). Therefore, a redundancy gain should not be dependent upon inputs that are lateralised to the LVF or RVF. Summation and facilitation should be observed if two identical stimuli are presented anywhere in the visual field, as long as they are capable of reaching the visual word form area simultaneously. Zaidel and Rayman (1994) compared
Experiment 3
It cannot automatically be assumed that the bilateral advantage is underpinned by the two stimuli summating or facilitating activation of word recognition. It has been argued that the bilateral advantage could be due to ‘probability summation’ across two presentations of the same item (see Badzakova-Trajkova et al., 2005). The notion here is that both copies of the same stimulus are processed simultaneously and in parallel, with the response of the participant being determined by whichever
The RVF advantage in dyslexics and controls
The callosal relay hypothesis (Zaidel et al., 1990) proposes that the RVF advantage for word processing is due to the callosal relay that occurs for the LVF trials (from the RH to the language areas in the left hemisphere) which causes a time delay and loss of stimulus quality. It could be predicted that if dyslexics have poor callosal transfer then they should show poorer LVF performance and hence a larger RVF advantage than controls. A RVF advantage can be defined as the difference between
General discussion
The three experiments reported here compared normal adult readers with adult compensated dyslexics. All the participants were university students performing at a high level in their studies. In comparison with the normal readers, the dyslexics showed the classic pattern of reduced vocabulary and digit span, slow reading of real words, less accurate and efficient nonword reading, less well developed phonological awareness (as shown in performance on the spoonerisms test), and poorer spelling. In
Acknowledgments
These experiments formed part of Lisa Henderson’s dissertation for the MSc in Reading, Language and Cognition at the University of York, funded by the Economic and Social Research Council (ESRC). We thank Maggie Snowling and Meesha Warmington for advice on recruitment and assessment of dyslexic adults. We also thank the reviewers for their valuable comments.
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