The following is an extract from an in-press book: Psychological Science Can Inform

The Teaching of Reading by Keith Rayner, Barbara Foorman, David Pesetsky, Charles A. Perfetti, and Mark S. Seidenberg. Published by the American Psychological Society.

Figure 4 to be added

4.2 The View from Cognitive Neuroscience

Research using cognitive neuroscience methods has begun to add to a picture of how reading works in the brain. Brain imaging methods such as Functional Magnetic Resonance Imaging (fMRI) and Positron Emission Tomography (PET) provide information about the functional neuroanatomy of reading by identifying brain structures involved in reading tasks. These imaging methods provide spatial information to a centimeter or even millimeter scale. However, since these methods provide limited temporal information, questions about the time course of reading are better addressed by Event Related Potentials (ERP) methods.

The standard imaging question may appear to be "What lights up in the brain when words are read?" Indeed, the attraction of brain imaging methods is their ability to display areas of the brain where activation levels co-vary with the task. A study that can vary the consistency of a spelling pattern in a target word can then show that area A shows more activation than area B when the target word has property X (such as lexicality or spelling consistency pattern) rather than property Y. The conclusion then becomes that area A is responsible for processing property X. There is no doubt that neuroimaging carried out with this logic will inform understanding of the neural substrates that are engaged by reading tasks. However, neuroimaging can go beyond this identification when imaging results are connected to results obtained by other methods, including behavioral, ERP, and patient studies. Such results can strengthen previous conclusions and stimulate a search for further understanding of how reading works.

4.2.A Brain Imaging. The general method in neuroimaging requires comparisons between images made during the performance of a reading task and those made during base line conditions. A simple comparison that has provided basic data on reading is one between reading aloud a single word and looking at a small fixation cross. The results of such a comparison identify regions that show increases in activation during the reading task, whether or not this activation is unique to reading. For example, primary motor cortex is activated during reading not because it uniquely supports reading, but because it is involved with movements of the mouth required by oral reading. Identifying areas that play a more distinctive role in reading itself require other comparisons. For example, producing a simple word in response to a random string of letters should involve the basic visual and modal production components of reading, allowing the additional activation observed during the reading task to be attributed to distinctive processes involving orthography and phonology.

Research following this general approach has identified a number of brain regions that play some role in word reading. For skilled readers there are lateralized functions across several brain regions, with greater activity in the left hemisphere for frontal, temporal, parietal, and occipital sites (Crosson, et al., 1999; Price, 1998; Simos, Basile, & Papanicolaou, 1997; Small, Noll, Perfetti, & Hlustik, 1996). Imaging studies have sought precise locations to link to specific orthographic, phonological and semantic components of word identification (Crosson et al., 1999; Pugh,Shaywitz,Shaywitz,& Shankweiler, 1997) in inferior frontal cortex, the left temporoparietal cortex and the left basal temporal cortex. Other areas are also identified in some studies, but these three are sufficient to give a general characterization of the functional neuroanatomy underlying the three component knowledge sources that are needed in word reading -- orthographic, phonological, and semantic (see Figure 4).

Orthographic knowledge is distinctive to reading, whereas phonological and semantic information are part of language itself. An obvious candidate for how the brain supports orthography is that the areas of the brain that function in object recognition, especially the occipital cortex, also are functional in the perception of printed words. In examining this general question, comparisons have focused on words vs pictures and on different kinds of letter strings. In this second kind of comparison, words are compared with pseudowords and with strings of artificial letters or false fonts. The search for an area that is dedicated to printed words (a "word form" area) has led to some strong candidates, especially in an area near the temporal-occipital border, the left middle fusiform gyrus. This area responds differently to nonwords than to words and pseudowords (Fiez & Petersen, 1998). In patients with lesions in temporal-occipital areas, severe disturbances in whole word reading with a reliance on letter-by-letter readout of a word (pure alexia) have been reported (Patterson & Lambon Ralph, 1999). Still, the basis of these rare alexia cases is not completely clear. Deficits in low level processes can impair the ability to generate whole word representations (Behrmann et al, 1998).

The second major word reading component is the transformation of an orthographic form into a phonological form. How the brain carries out this task is of great interest, because this phonological decoding process is the major achievement of learning how to read and failure in this task is the major source of reading failures. The ability to read pseudowords has become an indicator of reading skill and the corresponding inability to read pseudowords has become the marker for phonological dyslexia (Coltheart et al, 1993). Patient studies have identified two brain regions where lesions lead to deficits in phonological decoding. One region is the left inferior frontal lobe and the other is temporoparietal cortex. Lesions in one or both of these areas are associated with difficulty in reading pseudowords (Fiez & Petersen, 1998; Patterson & Lambon Ralph, 1999). Patients with these lesions tend to read words relatively well (compared to pseudowords), as if they are able to use a stored lexicon that remains intact with these lesions. Such a disassociation is what is expected by Dual Route theories. Recent evidence from direct electrical stimulation of the temporoparietal region produces an interesting convergence with the patient data. The ability of normal readers to name pseudowords is disrupted by this stimulation, but their ability to name real words is not (Simos et al, 2000).

There is convergence for this picture from neuroimaging studies of normal readers. Both left frontal and temporoparietal regions are active in reading in various tasks that require or encourage phonological processing (Demonet et al, 1996). Furthermore, imaging studies of developmental dyslexics report lower levels of activation in these regions compared with skilled readers (Rumsey et al, 1999;Shaywitz et al, 1998). Such results converge with the hypothesis that a phonological deficit is a core problem of children and adults with severe reading problems.

The functional details within these two broadly defined left frontal and temporoparietal regions in the roles they play in phonological decoding have several possibilities. For example, the temporoparietal region may support auditory phonology whereas the frontal region supports articulatory phonology. Another possibility is a more general frontal/posterior division of cognitive labor, in which frontal regions support more effortful, controlled processing (as required for word pronunciation) and posterior regions support more automatic processing. Especially intriguing is a third possibility, that different brain regions support sublexical vs lexical processes (Fiez & Petersen, 1998; Price, 1998) with sublexical processing the primary responsibility of left frontal regions and lexical processes the primary responsibility of the posterior regions. Although some studies indeed have reported greater activation in frontal regions for pseudowords, where sublexical processes appear dominant (Fiez & Petersen, 1998), a simple picture of function to structure mapping appears to be unlikely.

Neuroimaging results are also relevant for semantic processing at the word level. For example, basal temporal regions are a candidate for semantic processing because they respond to a range of tasks that require the retrieval of word names and concepts (Price, 1998). And, just as phonological dyslexia has been linked to left frontal and temporoparietal regions, basal temporal lesions have been linked to acquired surface dyslexia. Surface dyslexics have problems with reading words lexically as whole words (as opposed to sublexical units). Thus, their problem is manifest on words that contain inconsistently pronounced spelling patterns or so-called "irregular" words (e.g. choir). Patients with basal temporal lesions tend to show the alexic pattern and a more general deficit in picture naming (Peterson & Lambon Ralph, 1999). Nevertheless, it is far from clear whether there is a single meaning-pronunciation area. Overlapping regions in the basal temporal area have been identified for picture and word naming; however, within this general region, there appear to be differential activation (across frontal vs. posterior areas of the fusiform gyrus) for naming pictures vs naming words (Moore & Price, 1999).

In any case, it appears that left temporal regions are not the only support for semantic processing. Left frontal regions have been found to play a role in semantic tasks across many studies in English (Fiez, 1997). Because phonological production has typically been a component of the tasks studied (e.g. verb generation), a purely semantic component may not have been clearly isolated. However, these regions have been identified even in Chinese word generation tasks with the additional result that left frontal activation increases for words that have vague (and hence difficult-to-retrieve) meanings (Tan, Spinks, Gao, Liu, & Perfetti, 2000). Since naming is involved in both types of words, such a result points toward the region's involvement in meaning retrieval, perhaps the effort it requires. It appears that broad networks of brain regions support various aspects of word reading, including semantics as well as phonology, and that simple function-structure mappings generally should not be expected.

In studies of differences in reading skill, imaging studies have found higher skill associated with lateralization to the left hemisphere (Pugh et al., 1997; Segalowitz, Wagner, & Menna, 1992). Dyslexic readers can be differentiated from non-dyslexic readers on the basis of brain activation, but the differential pattern that distinguishes dyslexics from non-dyslexics appears to not be the same one that distinguishes non-dyslexics of varying skill from each other. Dyslexia, whether developmental or acquired, is associated with brain circuitry responsible for attention (Pugh et al., 1997) and phonological processing (Georgiewa, et al., 1999; Small, Flores, & Noll, 1998). Segalowitz et al. (1992) suggest that different predictors are required depending on whether the reader's ability is below or above some threshold. In addition, structural differences have been found to distinguish dyslexics from non-dyslexics (Semrud-Clikeman et al., 1996).

4.2.B. Event-related Potentials. ERP data, based on the recording of electrical activity measured at head surface electrodes, provides temporal information about brain activation that complements the spatial information obtained by neuroimaging methods. Researchers using ERP methods hope to time-lock brain activity to a particular sensory event (like the presentation of a word). The voltages associated with brain activity vary in both polarity and magnitude over time, resulting in a series of electrical "peaks and valleys". For example, when readers are presented with a semantic incongruity, a relative large negative potential (i.e., a valley) occurs about 400 ms after the presentation of the stimulus (this is termed a N400 wave). The peaks and valleys in the brainwave signal that are typically examined, the N200, P300, N400, and P600, are sensitive to cognitive mechanisms involved in interpreting stimulus events, so are especially relevant for reading and language tasks.

Traditionally, much of the ERP research related to reading processes has dealt with the later occurring components (such as the N400 and P600). While these measures certainly occur within the time frame of typical responses in lexical decision and naming experiments, as we noted when discussing eye movements, the eyes have typically moved on to another word within about 250 ms during reading. And, since the durations of the eye fixations are strongly influenced by the characteristics of the fixated word, it is of interest to determine if similar effects can be obtained in the early components of the ERP waveform (Posner & DiGirolamo, 2000; Sereno, Rayner, & Posner). Indeed, there is now evidence suggesting that early ERP components, occurring 130-200 ms after the onset of a word are sensitive to lexical properties of the word (Rudell & Hua, 1997; Sereno et al., 1998). In general, ERP studies converge with those using PET and fMRI to examine brain function during reading (Posner, Abdullaev, McCandliss, & Sereno, 1999). Thus, ERP data (Bentin, Mouchetant-Rostaing, Giard, Echallier, & Pernier, 1999; Martin-Loeches, Hinojosa, Gomez-Jarabo, & Rubia, 1999), like imaging data, show an early orthographic/lexical component in word reading. Its latency is short, less than 200 ms, and it location is in occipital and occipital-temporal regions, and mainly in the left-hemisphere. This is consistent with the idea that learned forms of the writing system acquire a functionally distinct status within the visual processing system. For orthographic inputs that allow phonological processing, a second stage is reached in temporal areas within 350 ms. For inputs that are processed to the semantic level, anterior temporal and frontal regions show their roles within 400 to 450 ms.

4.2.C. Implications for Learning to Read. The knowledge gained from neuroscience methods is becoming informative with respect to questions related to skilled reading and reading problems. The big question for learning to read, how the brain supports the acquisition of reading skill, remains to be addressed. However, there are some relevant studies that illustrate the promise of neuroscience methods for the study of how the brain responds to training. For example, repeated practice affects ERP components presumably reflecting gains in efficiency through specific learning (Rudell & Hua, 1997). Moreover, such learning can actually influence brain development and neuronal connectivity. A recent fMRI study found a thicker band of callosal connective fibers between parietal lobes for literate than for illiterate subjects (Castro-Caldas et al., 1999). Another study designed to shift an acquired dyslexic from a whole word reading strategy to a phonological reading strategy found that activation patterns in the brain changed following the intervention (Small et al., 1998). In both studies, the conclusion is that learning produced an alteration in brain circuitry and there is the implication that neuronal connectivity remains plastic into adulthood.

We can illustrate this kind of conclusion for an ability assumed to be central to learning to read -- phonological awareness. Castro-Caldas et al (1998) examined oral language processing in illiterate adults in Portugal (this group were fully functional socially and the circumstances of their illiteracy were the traditional rural norms in place until recently). The key comparison concerned the repetition of words versus pseudowords for illiterate vs literate individuals in response to spoken stimuli. With real words, literates and illiterates performed comparably and showed similar brain activation patterns. But with pseudowords, illiterates performed more poorly and their brain activation patterns were not the same as for literates. Castro-Caldas et al. suggested that literacy acquired during childhood affects the functional organization of the brain. What is interesting, of course, is that this conclusion is not about reading itself, but about language: Literacy alters the way brain deals with spoken language. Cognitive neuroscience methods promise to be useful across many issues in the study of reading -- the components of word identification, cross-language comparisons, the acquisition of skill, and even comprehension. There remains much to learn about the specific brain regions that support these specific processes. And there is much more to learn about the brain reorganizes itself during learning to read.
 
 

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