Alexia and related reading disorders

Neurol Clin N Am 21 (2003) 549–568

Alexia and related reading disorders Daniel Bub, PhD Department of Psychology, Faculty of Social Sciences, University of Victoria, Victoria, BC V8W 3P5, Canada

Reading is a fairly recent cultural development and usually is acquired only by special instruction and with considerable effort. As such, it differs from spoken language, and some of the mechanisms for processing text must diverge from those determining the ability to produce and comprehend speech. The fact that brain damage can affect reading in previously literate people without any associated impairment of spoken language, or even of spelling and writing, was known long before the theoretic significance of acquired dyslexia attracted the interest of modern researchers trained in cognitive psychology. For example, Dejerine [1] presented the now famous case of Oscar C. to the Biological Society in Paris, recounting how the highly educated textile merchant found himself completely unable to read after suffering a cerebrovascular accident on the 25th of October 1887. The case of Oscar C. has been reviewed in some detail elsewhere [2,3]. The type of theoretic inferences that were prompted by such cases a hundred years ago provide a fascinating, if somewhat truncated, preview of the contemporary debate now provoked by the same clinical phenomena. Dejerine argued that a specialized system develops in skilled readers in the left angular gyrus representing the stored visual description of single letters and letter combinations making up whole words. For Oscar C., in Dejerine’s account, the subcortical component (ie, white matter) of his lesion must have disconnected the representation of visual words—their stored orthographic form—from both visual cortices. Thus, the patient could spell (by using the internally generated sound of the word to retrieve the preserved orthographic form), but he was no longer able to access directly

This work was supported by a grant from the Networks of Centers of Excellence Program through the Canadian Language and Literacy Research Network. Department of Psychology, University of Victoria, P.O. Box 3050, STN CSC, Victoria, BC V8W 3P5, Canada. E-mail address: [email protected] 0733-8619/03/$ - see front matter Ó 2003, Elsevier Inc. All rights reserved. doi:10.1016/S0733-8619(02)00099-3

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the internal representation of the word’s orthography from vision. Oscar C. experienced words (and even single letters) as meaningless, unfamiliar designs, even the words that he himself had written just minutes previously, or so it seemed to Dejerine. The syndrome of pure alexia or alexia without agraphia has continued to fascinate and puzzle since the first cases were documented. At issue is the question of the specificity of the disorder and its theoretic significance. Even the earliest analyses provoked controversy. Wernicke, for example, remained strongly opposed to the idea of a separate visual representation for words and conceded only that the shape of letters need be stored for reading to take place via a transcoding mechanism that converts print into auditory language [4]. A further question concerned whether or not it was possible to affect the reading of words and letters without impairing the recognition of other kinds of material, such as numbers. Again, this evidence is relevant to the issue of the specificity of localized reading mechanisms. According to Dejerine, Oscar C. had no trouble identifying numbers, thus he claimed the deficit was limited to the perception of orthography. An accompanying report by Landolt, the famous ophthalmologist who examined Oscar C. before referring him to Dejerine, is not consistent with this claim. Landolt observed that even in carrying out simple addition, the patient proceeded with extreme slowness and seemed unable to recognize the value of several digits at the same time. The type of acquired dyslexia described by Dejerine that interested the neurologists of the 19th century is now referred to as letter-by-letter (LBL) reading, because most patients still can decipher a word by laboriously identifying each letter in sequence. Dejerine argued that in these cases, the damage has not prevented identification of smaller orthographic units, such as individual letters and even syllables [5]. The syndrome is part of a group of acquired reading disorders considered peripheral dyslexias, because they are the result of impairment to functional components that prevent the normal synthesis of the orthographic form of words. The purpose of a written word is to convey sound and meaning to the reader. Impairments to these processing stages that follow orthographic synthesis cause a variety of acquired reading disorders that together are known as the ‘‘central’’ dyslexias. The distinction between perceptual systems that derive the visual form of a word from letters, and those that derive meaning and sound from orthography, is a reasonable one and is consistent with much that is known about the cognitive organization of language. It also is reasonable to assume that dyslexia can be the result of damage to one or the other (or in mixed cases, both) of these processing subdivisions. A summary of the types of peripheral and central dyslexias described in the literature is presented in Table 1. At the same time, a number of background considerations must be considered regarding the present system for classifying types of acquired dyslexia.

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Table 1 Summary of peripheral and central dyslexias Peripheral dyslexias Attentional dyslexia

Neglect dyslexia

Letter-by-letter reading

Surface features Intereference occurs between letters in words within the same sentence. Reading of isolated words is intact. Letters in particular spatial regions are omitted or replaced, either at the beginning or ends of words. Patients read laboriously by explicitly attending to individual letters in the word. Reading is very slow and reading speed is affected by the length of the word.

Central dyslexias

Surface features

Nonsemantic reading (sometimes referred to as surface dyslexia)

Words that incorporate the regular correspondences between spelling and sound are pronounced correctly (eg, ‘‘mint’’, ‘‘glint’’, ‘‘flint’’). Words that violate the regular correspondence (eg, ‘‘pint’’) are mispronounced and ‘‘regularized’’ (the pronunciation given to ‘‘pint’’ rhymes with ‘‘mint’’). Patients are severely impaired in their ability pronounce nonsensical written words (eg, ‘‘sife’’). Patients produce semantic errors when reading words (‘‘dog’’ is misread as ‘‘cat’’). They also make visual errors (‘‘cat’’ read as ‘‘cot’’) or responses that seem to reflect the mixture of a visual followed by a semantic error (‘‘cat’’ read as ‘‘bed’’, presumably via ‘‘cot’’ as the intermediary). Accuracy is influenced by the semantic and grammatic features of the word. Patients are impaired in their ability to pronounce nonsensical written words. Reading words is relatively intact. No semantic errors are present.

Deep dyslexia

Phonological dyslexia

Remarks on classification It is possible for two different cases to satisfy the current definition of a dyslexic subtype, even though the underlying functional deficit may vary substantially between them. This complication would not be serious if all cases of dyslexia given the same label were related in a systematic fashion (ie, they all reflected a range of conceptually related deficits occurring at a particular level of the reading system). Unfortunately, the way in which acquired dyslexia is now classified permits the following more problematic outcome: two cases that satisfy the definition of a particular form of acquired dyslexia, even though the functional deficits in the two cases are in

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completely different parts of the reading system. For example, the ability to assign a pronunciation to a novel word not previously encountered in written form demands special abilities that involve the analysis of orthographic units and the mapping of these units to speech constituents. At present, all cases with damage to any part of this complex reading mechanism—either at the level of orthographic processes or at the level of processes dealing with the assembly of speech from orthography—are categorized as instances of phonologic dyslexia, a syndrome described in more detail later. This example illustrates the point that the same classification can be given to cases of dyslexia with impairments to fundamentally different cognitive processes. The implications of this peculiarity in classification schemas are complex and cannot adequately be dealt with here. Many researchers argue that there is no problem with the heterogeneity of cases inherent in a category such as phonologic dyslexia, if the purpose is to learn about the organization of the reading mechanism by studying individual patients [6]. The author believes the vagaries of the present system of classification cannot be so easily brushed aside. The definitions of dyslexic subtypes now in use, instead of reflecting a systematic conceptual organization, often are quite arbitrary. Sometimes a particular form of dyslexia refers to what may be a compensatory strategy on the part of the patient to decipher a word (eg, LBL reading). Sometimes the definitions mean that a particular type of reading task is no longer performed adequately (eg, phonologic dyslexia now refers to people who cannot derive the sound of a novel or nonsensical word). Other subtypes refer to a theoretic conjecture about the general type of mechanism that has been damaged (for example, attentional dyslexia). At the least, the lack of a sophisticated taxonomy of the acquired dyslexias reduces the possibility of developing insights into the relationships that may exist between subtypes. In this regard, the current approach to classification differs fundamentally from the systems that have been developed and proved so useful in the biologic sciences; however, these categories, like those of any taxonomic system, may be altered and restructured as an understanding of reading and its impairment develops over time.

Peripheral dyslexias Peripheral dyslexias are the result of impairment to processes that convert letters on the page into an abstract representation of visual word forms. This representation of the word’s orthography normally is constructed rapidly, by assembling multiple letters into spelling units ranging in size from bigrams (eg, the sequence ) to syllables and morphemes (eg, the sequence ). Evidence from acquired dyslexia indicates several processing systems that, if disrupted, severely impair the rapid conversion of letters into orthographic forms. Two of these dyslexic subtypes—attentional dyslexia and neglect dylexia—are in many cases the result of damage to

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components of visual attention that clearly serve a more general function than reading. Indeed, Shallice [7] distinguishes between these dyslexic subtypes, which he categorizes with other disorders of visual attention, such as hemineglect of space, and peripheral dyslexia associated with LBL reading. He considers at least some instances of the latter disorder as the outcome of impairments to orthographic processes that are specialized for reading. Shallice, in drawing this distinction, shows a theoretic commitment that the author cannot maintain in this review. Attentional and neglect dyslexias are considered as legitimate types of peripheral dyslexia associated with impairment of visual processes involved in the normal perception of a word’s orthographic form. The question of whether or not a type of peripheral dyslexia exists that reflects damage to processes specific to the encoding of the word form itself, rather than to more domain-general perceptual processes, is evaluated in a discussion of rival interpretations of LBL reading.

Attentional dyslexia This form of dyslexia is the result of a rare disorder of attentional control associated with damage to the left parietal lobe in which interference occurs between many elements from the same category present together in the patient’s field of view [8,9]. The deficit affects the reading of words in sentences—because there are many words visible at the same time—but not the reading of a single word displayed in isolation. It also affects the ability to identify the letters in a word, even though the patient can read the word correctly. The task becomes one of identifying a single letter among many competitors of the same type, and the deficit again becomes manifest. Shallice [7] asks why the patients cannot use their knowledge of spelling to name the letters after they had just read the word correctly. The answer, he points out, is that the patients actually misperceive the letters when asked to identify them, and this evidence overrules any previous response to the word. The ability to read an isolated word but not its constituent letters has been documented since the end of the nineteenth century and was termed literal dyslexia by He´caen [10]. The conventional form of literal dyslexia, however, is the result of difficulty in retrieving the names of letters rather than their identity. Attentional dyslexia, by contrast, is not merely the result of anomia for letters or of response competition between the target and distractors. These patients make many errors when they are asked to identify a digit flanked by other digits, but the error rate drops to near zero when the target is changed to a set of dots to be counted [7]. In both instances, the naming of a number is required, but errors occur only when the distractors are the same type of item as the target.

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Interpretation of the deficit in attentional dyslexia begins with the idea that many objects present in the visual field are processed simultaneously. The flow of information must be controlled by a filter that protects the ongoing analysis of a focused target from the competing activation accruing to irrelevant objects [11]. Damage to this filter—a kind of gating mechanism—impairs selection so that processing of the target is contaminated by other elements active at the same time. Where, in the stream of processing from visual features to whole words, does the filter operate? There are two proposals in the literature on this question. Shallice [7] argues that the dyslexic errors occur because the filter control mechanism does not prevent letters in parts of the visual field outside the location of the target word from activating orthographic units. The outcome is that elements of the target word are replaced by competing letters, and the target is misidentified. A similar error can be found in normal readers attempting to read a word occurring at the same time as another word, each one presented for a brief duration and followed immediately by a random pattern made up of letter features. Under these conditions, the letters in a competing word tend to replace letters in the same position of the target word [12]. For example, if ‘‘hand’’ (the distractor) accompanies ‘‘lank’’ (the target), observers may perceive the word ‘‘land,’’ but not ‘‘dank.’’ Such ‘‘migration errors’’ occur in normal readers operating under brief viewing conditions and in cases of attentional dyslexia. This account of the deficit responsible for attentional dyslexia assumes that it occurs before the perceptual categorization of words. Warrington et al [9] suggest that in certain cases the source of interference may be beyond this point, affecting the transmission from visual word forms to more central levels of processing responsible for sound and meaning. They describe a patient who showed no interference in identifying a word when it was flanked by letters, but considerable interference when the target word was flanked by other words. Similarly, many mistakes occurred when the patient was asked to identify a letter flanked by other letters but not when the letters were flanked by words. Errors tended to be complete substitutions of other flanking items, perseverations of a previous response, or responses completely unrelated to the items on display. The important factor governing interference from nontarget positions, at least in this case, was that items accompany the target from the same category. Thus, the concept of an attentional filter that gates the parallel output of letter analyzers during the processing of a single word may not be sufficient. According to Warrington et al, a second filter must exist that controls the orderly transmission from the parallel activation of visual word forms to the sequential encoding of each word’s sound and meaning. Thus, competition may arise in the transmission route from letter units onto word forms and at the level of the word form system itself, where simultaneously activated units of the same type (words or letters) may compete for access to more central levels of processing. It remains to be seen whether or not two

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different filters must be invoked to account for the varieties of error in attentional dyslexia. A rudimentary diagram of the components of the reading system, with an indication of where attentional filtering and other forms of attention may operate, is presented in Fig. 1. The relationship between these and other components represented in the diagram becomes clear in the analysis of the various dyslexic subtypes.

Neglect dyslexia Failure to attend to one part of space (ie, neglect) can occur after brain damage. The location of the damage most frequently associated with a neglect of space is in the right parietal lobe [13], although neglect can be observed after damage to several other cortical and subcortical structures [14]. In neglect dyslexia, reading is impaired because the patient misidentifies letters in particular spatial regions of an isolated word or group of words [15,16]. In left neglect dyslexia, the initial letters of the word may be

Fig. 1. Flow diagram of processes involved in translating print into sound. Note the two ways in which the pronunciation of a word can be accomplished: (1) by mapping the orthographic form directly to pronunciation, by-passing the meaning, or (2) the orthography maps directly onto meaning and thence to pronunciation. The skilled reader carries out both options concurrently. The component, ‘‘attentional processes,’’ includes filtering mechanisms disrupted in attentional dyslexia and other spatial processes that are affected in neglect dyslexia. Peripheral dyslexias reflect damage to components prior to the synthesis of an orthographic form from letters, whereas central dyslexias are the result of disruption to processes occurring after the orthographic form has been derived.

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substituted (eg, ‘‘hand’’ read as ‘‘band’’), added to (eg, ‘‘land’’ read as ‘‘bland’’), or omitted (eg, ‘‘hand’’ read as ‘‘and’’). In right neglect dyslexia, these errors occur at the end of the word. Some investigators believe that neglect dyslexia invariably is associated with a general visual neglect of space, but this form of dyslexia can occur in the absence of neglect for nonverbal material [17]. Neglect dyslexia also can be seen for one spatial region in the word (say, the leftmost part of the word) in association with neglect of the opposite spatial region (the rightmost part) for a nonverbal array of items [18]. The existence of neglect dyslexia suggests a faulty allocation of attention to one side of the word and that mechanisms of spatial attention play an important role in normal reading [19]. The error pattern across patients is complex and suggests that more than one principle must be understood before arrival at an adequate interpretation of neglect dyslexia. First, patients often make more errors to pronounceable nonsense words than real words [20,21]. A detailed analysis of errors in one case [22] suggests that neglect errors to words and nonsense words markedly increase when the target overlaps in the last three letters with many other existing words in the vocabulary, especially when these words are more common than the target. For example, if ‘‘lark’’ is the target, the words ‘‘mark,’’ ‘‘dark,’’ ‘‘park,’’ and ‘‘shark’’ share the last three letters and are more frequent. In the case of a nonsense word, of course, there often are many more familiar word competitors sharing the last three letters. Arguin and Bub [22] also found that the number of neglect errors increased if the first letter of these ‘‘orthographic competitors’’ was similar visually to the first letter of the target word. It seems that neglect of the letters in the first position of a word or nonword can still afford access to orthographic units based on partial letter information. There is evidence that responses are not merely the result of explicit attempts to guess the word from the last few letters, but in fact reflect dynamic and automatic interaction between word and letter activation [22,23]. If the target is a word, the correct response may dominate over competitors because an actual word representation exists that is fully compatible with the information accumulating from letter analysis. Nonsense words have no such unique entry at the word level and yield many more neglect errors. In addition to the effect of words and nonsense words on performance, a further issue concerns the nature of the spatial impairment associated with neglect dyslexia. It has been argued that three kinds of spatial representations are needed for visual processing and, therefore, also for reading [24]. This idea is motivated by the fact that changes in word location and orientation do not affect all patients in the same way. If neglect errors increase when the word is presented horizontally to the left of fixation compared with the word presented to the right of fixation [25], the inference is that the spatial deficit includes a retinocentric component. Hillis and

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Caramazza [26] argue that at this level, neglect dyslexia is associated with a reduced efficiency in processing that increases as a function of distance from fixation in the contralesional field. At the next level, a deficit in attending to the word as a stimulus-centered spatial representation results in the same number of errors to the initial letters regardless of the position of the word in retinotopic space. A word such as ‘‘bookend’’ or ‘‘xxxend’’ should yield correct identification of the embedded word ‘‘end’’ and neglect of the first part of the whole array of letters. The words ‘‘book end’’ or ‘‘xxx end’’ result in errors at the beginning of both letter strings or words (ie, ‘‘hook bend’’), because two separate stimulus-centered representations are constructed in this instance. Hillis and Caramazza [26] state that the error rate in a stimulus-centered impairment increases as a function of the number of letters from the center of the word and the number of spaces between letters. Finally, impairment of attention at the level of abstract letter identities (graphemes) results in neglect of the positions corresponding to the beginning of the actual word itself, even when the array is presented in a nonstandard orientation (eg, mirror-reversed or vertical). After reviewing many cases of neglect dyslexia, Haywood and Coltheart [27] conclude that the differences between them offer strong support for the claim that three types of spatial representation are involved in reading and can be separately affected by brain damage. At the same time, there are conceptual limitations inherent in this framework. Although neglect dyslexia seems to reflect a disorder of spatial attention, there is no explanation in terms of attentional mechanisms per se. Rather, there are assumptions of distinct spatial frames in which words are represented and conjectures about how these frames are distorted to yield the pattern of errors observed in different patients. But what principles of spatial attention underlie the particular distortions in the spatial frames at each level? The challenge is to arrive at a deeper understanding of neglect errors in terms of the spatial organization imposed on linear arrays of symbols (letters, numbers, and so forth) and the mechanisms of attention that operate on these frames. The theoretic need for a particular type of spatial representation depends on the understanding of the mechanisms of attention and how they operate on different spatial arrays. A brief discussion of the challenge posed by a particular computational model of attentional dyslexia further illustrates the controversial nature of arguments based on multiple spatial reference frames. Mozer [28] has applied a connectionist model of two-dimensional object recognition and spatial attention to neglect and neglect dyslexia. The model is complex and the details of its architecture are not presented here [23,29]. It suffices to state that the model includes an explicit description of an attentional mechanism (AM) and that it operates entirely within a viewer-centered reference frame using eye fixation. There is no appeal to object-centered representations.

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Nevertheless, the AM model successfully reproduces many experimental phenomena that have been taken as evidence for object-centered representations. For example, the model successfully simulates a result by Arguin and Bub [30] in which subjects were asked to name a target letter presented in a horizontal array containing four elements (see Fig. 2 for a depiction of the display). The other three elements were filled circles. The letter could appear in one of eight positions on the screen, called the viewer-relative position. It also could appear in one of four positions relative to the circles, called the object-relative position. The investigators varied viewer-relative and object-relative positions independently, yielding 32 display configurations. This paradigm allowed for the comparison of performance across different object-relative positions when the viewer-relative position was held constant. Whereas normal subjects showed no effect of object-relative position, a patient with neglect showed increasing response time with leftward target displacement in the array. Because an effect of object-relative position was obtained when unconfounded with viewer-relative position, the data was interpreted as supporting the idea that neglect can occur within an object-based frame of reference. The fact that the AM model provides an

Fig. 2. (A) The set of possible locations (X) occupied by the target relative to the central fixation point (F). The target has a viewer-relative position in this display because location is defined relative to stable landmarks in the environment (eg, the edge of the screen) and also relative to the subject’s body and point of ocular fixation. (B) The second type of display varies the position of the target within the stimulus array (ie, the target has a stimulus-relative position) while holding viewer-relative position constant. Here, ‘‘extreme left,’’ for example, means the extreme left of the four-element display. The target was a letter chosen on each trial from the set, ‘‘B, C, J, K, P, T, V, and Z.’’ A single target was always presented along with three distractors ( filled circles).

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accurate simulation of these (and other analogous) results, while appealing only to a viewer-centered spatial reference frame, seriously challenges the idea that three spatial frames are needed to explain the performance of patients with neglect dyslexia. Regardless of how this controversy is ultimately resolved, the reading errors in neglect dyslexia suggest that letter information in certain locations of the word is seriously underspecified or completely lost. The most straightforward possibility is that the deficit in attention has abolished completely the correct orthographic form of the word, especially when the patient makes many omission errors in attempts to identify it. Several studies, however, have looked for evidence that words in neglect dyslexia may still gain access to meaning, even though conventional reading tests suggest otherwise. At issue is the functional role of visual attention in word identification and the nature of the reading process that is disrupted. For example, La`davas et al [31] tested a patient with a large right-hemisphere lesion and a corresponding severe left-sided neglect. The patient had intact visual fields, but could not identify words briefly displayed (for one fifth of a second) to the left (5.5 degrees) of fixation, nor even reliably detect their presence. Nevertheless, a word presented in this way exerted a subtle influence on the speed with which the patient identified a word occurring immediately afterwards in the attended (right) visual field. If the unattended word on the left was related semantically to the target word on the right, reading speed to the target was measurably faster compared with a baseline condition in which the unattended and target words were unrelated semantically. Similar results have been obtained by other researchers indicating implicit semantic access of words in neglect dyslexia [32,33]. Reading errors in neglect dyslexia, therefore, need not suggest that access to meaning has been disrupted completely. Only certain tasks (including explicit word identification) require attention to visual features in specific locations of a spatial reference frame. The deficit in neglect dyslexia does not completely abolish either the identification of letters or the activation of word-level information.

Letter-by-letter reading LBL reading refers to the laborious approach of deciphering a word in cases of pure alexia, or pure ‘‘word blindness’’ [1], and is characterized by extremely slow performance on a variety of reading tasks and very large effects of word length on response time. Spelling often is intact in these patients, yet they struggle to read what they have written once the memory of the text has faded. The lesion associated with LBL reading is in the prestriate cortex of the dominant occipital lobe, sometimes, although not always, accompanied by damage to callosal fibers in the splenium of the corpus callosum or forceps major [34,35]. In most LBL readers, the lesion

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results in a dense right visual field deficit. Leff and colleagues [36] have shown that patients without pure alexia but with compete destruction of the left primary visual cortex or its afferents show abnormal effects of word length on reading speed (approximately 50 ms/letter). A sufficiently severe hemianopia renders the reader less able to encode the letters of longer words, but a look beyond this fact is necessary to arrive at an explanation of LBL reading, where the time to identify a word typically is slowed by one half a second or more for every additional letter. It is tempting to infer that the LBL reader has lost all perception of the word as an orthographic pattern and is simply using a compensatory strategy in which each letter is silently named or overtly sounded out to arrive at its identity via a kind of oral spelling. This interpretation is the one originally favored by Dejerine in his account of pure alexia. According to this view, articulated more recently by Warrington and Shallice [37], a specialized mechanism, the visual word form, is situated in the left posterior cortex and parses letter strings into familiar orthographic units (ranging in size from syllables to whole words) and categorizes them perceptually. This automatic synthesis of letters into higher-order reading units normally allows for rapid and accurate word identification. Conceivably, LBL readers have lost the use of the word-form system and no longer perceive higher-level perceptual units in written words. The strong version of this claim—that damage to the word-form system (or alternatively, to the input codes that access the system) is so extensive that written words have the status of random letters strings for LBL readers—has been refuted in several ways. First, it is possible to demonstrate, using appropriate controls for guessing, that LBL readers actually perceive letters in words more accurately than letters in random strings [38,39]. This word-superiority effect, also readily observed in normal readers, does not support the idea that words have the same perceptual status as random letters for any given case of LBL reading. A second result further complicating the idea that the disorder reflects simply a serial, context-free identification of letters is the repeated demonstration that some LBL readers show implicit identification of words under conditions that preclude the laborious identification of individual letters [40–42]. These experiments invite the same general conclusions as other comparable demonstrations previously mentioned regarding neglect dyslexia: the deficit in LBL reading has not completely abolished access to higher level information, despite the limits on perception that seem apparent when the patient is attempting to explicitly identify the word. Even a careful examination of the variables affecting explicit identification does not fit easily with the claim that LBL reading is simply a context-free, sequential analysis of the letters constituting a word. Reading speed is affected by factors connected with the familiarity of a word and its meaning: length effects are reduced when LBL readers identify words that occur more frequently in printed form or words that refer to highly ’’imageable’’

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concepts [43]; that is, words associated with ideas that can be easily imagined visually. What is the nature of the core deficit, then, that underlies LBL reading, if not a complete destruction of the ability to encode the visual form of a word? An alternative view is that this form of dyslexia is the outcome of a perceptual deficit that reduces the quality of letter analysis, particularly when attention is distributed over an array of letters. Patients resort to a strategy that involves selectively attending to individual letters in order to enhance their activation, thus they manifest LBL reading. The deficit, by this account, does not completely eliminate direct access to visual word forms [43]. Incomplete activation of letters still permits words to become partially active, although at levels that are insufficient to permit explicit identification. The weak activation of words can aid sequential letter analysis because word forms, once they have been even weakly contacted, begin to feed their activity back to processes occupied with letter identification. The notion of interactive activation between letters and words might explain why LBL readers appear on the one hand to rely on a sequential analysis of letters, and on the other to continue to show sensitivity to many of the word-level variables (frequency, imageability, and so forth) that affect the performance of normal readers. If LBL reading actually is the result of a perceptual impairment that occurs prior to the representation of visual word forms, the question is whether or not the deficit is particular to orthographic material or whether or not it extends to other kinds of visual displays. The issue of the domain specificity of LBL, central to the correct interpretation of the disorder and to an understanding of the impact of learning to read on perceptual systems, is addressed here. Is it necessary to develop specialized mechanisms for analyzing the shapes of letters in a sequential array? It is not difficult to show that LBL readers are impaired relative to age-matched controls on a variety of perceptual tasks [39,44]. No one, however, has shown convincingly a definite causal relationship between impairment on such tasks and reading performance. Evidence from functional imaging studies with normal readers provides some support for the existence of perceptual processes in the left extrastriate cortex specialized for letters and visual words [45,46]. Polk and Farah [47] demonstrate that in a neural network architecture learning via simple Hebbian rules, the frequent co-occurrence of letters presented with other letters and digits with other digits, led the network to segregate its representations for these two kinds of elements. The possibility remains, then, that LBL readers have an impairment that specifically disrupts the quality of letter perception in an orthographic sequence, although there is not yet full understanding of the nature of the process by which the patients ultimately arrive at the identity of a word. It remains to be seen whether or not LBL reading is an adequate term for describing this form of dyslexia. The evidence does suggest, though, that an adequate functional interpretation of the neurologic damage responsible for LBL reading cannot simply

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be based on the idea that the lesion has disconnected the visual representation of letters from orthographic perceptual units, however intuitively appealing such a notion might appear at first glance [1,2]. Letter perception continues to make contact with word-level information in LBL readers, although not with sufficient precision or strength of activation to generate fluent reading. The effort of the LBL reader to decipher the word seems more than just a labored sequential analysis of individual letters.

Central dyslexias Central dyslexias are the result of a disruption to processes involved in the analysis of the sound and meaning of written words. Interpretation of these disorders rests on a theoretic distinction between two ways in which the pronunciation of a word can be derived in the normal reader. The orthography can gain direct entry to meaning and the conceptual representation is then used to produce the name of the word. For example, the letter sequence in ‘‘shark’’ activates the meaning from the visual word form, and the label for the concept is retrieved after the word is understood. At the same time, and independently of this semantic reading route to the word’s pronunciation, there is another route, which converts the orthography to a pronunciation, using correspondences between spelling and sound. This nonsemantic route generates the pronunciation of shark, for example, by using knowledge of the sound derived from the reader’s experience with many words containing this segment (‘‘mark,’’ ‘‘lark,’’ ‘‘bark,’’ and so forth) and smaller segments (the pronunciation of , , , and so forth). Rival views of these two reading routes continue. One approach considers that the mechanism for translating subword units into sound uses different computational principles from the system that mediates the identification and comprehension of whole words and operates completely independently from it [48]. An alternative framework does not distinguish between reading processes on the basis of word and subword elements. Instead, all pronounceable written forms are believed processed by a single mechanism that performs differently for words and nonsense words on the basis of interactions between orthographic input units, output units that enable the pronunciation of the word and meaning [49]. Nonsense words, by definition, are not supported by any meaning, nor does their pronunciation correspond exactly to any familiar word. Damage to a unitary model can yield different effects depending on whether or not a spelling pattern corresponds to a known word that has a definite meaning or whether or not the pattern corresponds to a nonsensical word, even though no explicit distinction between words and nonsense words is built into the model. On this account, the processing units responsible for computing the pronunciation of actual words obtain

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additional inputs from their stored meaning and from the activation of orthographic units. Certain words (for example, less common words with unusual pronunciations given their spelling) have been learned by the model (and, some claim, by normal adult readers) so that they require the coactivation of meaning and the activation of orthography for a correct response [57]. Nonsense words of course, make no use of any supporting activation from meaning, so damage to the model that substantially interferes with the contribution of the meaning of a word to its pronunciation results in poor performance on words that rely partially on this source of activation, whereas nonsense words show no such impairment. In contrast, damage to the model that preserves the influence of meaning, but affects the direct mapping between orthographic units and the units matching their pronunciation, may yield poorer performance on nonsense words than real words, because words retain the additional support of the activation generated by their meaning. The major subtypes of central dyslexias reflect impairment either to the semantic reading or to the nonsemantic reading mechanism. Nonsemantic reading Patients with severe impairment to semantic processes, associated with left temporal damage, may retain the ability to read words aloud without access to meaning. The ability to pronounce the word correctly depends on several factors. Words that incorporate regular correspondences between spelling and sound (ie, words that have a predictable pronunciation, such as ‘‘hint,’’ ‘‘mint,’’ ‘‘lint,’’ and ‘‘stint’’); as well as, regular novel or nonsensical words (eg, ‘‘yint’’) are named with normal speed and accuracy. Words that violate these regularities (eg, ‘‘pint’’) are mispronounced and the errors reflect the application of more conventional spelling-to-sound associations (eg, ‘‘pint’’ is mispronounced or ‘‘regularized’’ to conform to the usual rendering of [50–52], so that the pronunciation rhymes with ‘‘mint’’). These errors are more likely to occur for less frequent exception words. A fairly common word, such as ‘‘love,’’ might be correctly read, but a less common one, such as ‘‘shove,’’ often is misread. All regular forms of the ending , as in ‘‘wove,’’ ‘‘grove,’’ ‘‘stove,’’ and so forth, are correctly pronounced. Readers with dyslexia have great difficulty with exception words, such as ‘‘yacht’’ and ‘‘colonel.’’ The term ‘‘nonsemantic reading’’ refers to the form of the disorder in which regular words are pronounced quite accurately. Some patients experience difficulty even with these items, although exception words lead to even greater difficulty. The convention now is to call such cases ‘‘surface dyslexia’’ to distinguish them from the purer variety of nonsemantic reading [7]. There is good evidence that the tendency to regularize a word is tied closely to a failure to access its semantic representation. A close correlation exists for individual patients between the loss of comprehension of an

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orthographic exception word and the probability that it is misread as a regularization [53]. This reading pattern also emerges gradually in patients showing a slow deterioration in semantic knowledge, for example in cases of semantic dementia [54] or Alzheimer’s dementia [55]. Finally, a semantic variable (the imageability of a word) affects the ease with which even normal readers can derive the pronunciation of written exception words: naming latency is slower for less imageable exception words than for comparable highly imageable words that are orthographic exceptions [56]. Understanding the characteristic features of nonsemantic reading has benefited substantially from computational models of the disorder. An influential framework adopted by Plaut [57] is a connectionist-parallel architecture in which the orthography, pronunciation (phonology), and meaning of words are represented as distributed patterns of activity over three separate groups of neuron-like processing units. There are cooperative and competitive interactions among units, augmented by additional mapping units that mediate between semantic, phonologic, and orthographic representations. Plaut [49] trained the model to develop connections between orthography and phonology in the context of support from concurrent semantic activation. Removing the semantic component after training yielded the same tendency to regularize less familiar exception words in semantic reading as in nonsemantic reading (for an alternative computational approach to modeling nonsemantic reading, see Coltheart et al [48]). Semantic reading (deep and phonologic dyslexia) Deep dyslexia occurs after extensive left hemisphere damage and can be described as the reverse of the deficit responsible for nonsemantic reading. In deep dyslexia, patients can only assemble the pronunciation of a word by first accessing its meaning. Thus, the ability to use subword elements to name a word unfamiliar to the reader or a nonsense word (eg, ‘‘jick’’) is completely abolished. The pattern of performance in deep dyslexia has additional features of interest that suggest further impairment to the semantic reading mechanism itself. Patients produce semantic errors when reading words (‘‘dog’’ is misread as ‘‘cat’’). They also make visual errors (‘‘cat’’ read as ‘‘cot’’) or responses that seem to reflect the mixture of a visual followed by a semantic error (‘‘cat’’ read as ‘‘bed,’’ presumably via ‘‘cot’’ as the intermediary). Finally, reading accuracy is influenced by the semantic and grammatic features of the word: concrete, highly imageable words are read better than abstract, low imageable words; nouns are read better than adjectives; adjectives are read better than verbs; and verbs are read better than function words (eg, ‘‘and,’’ ‘‘but,’’ ‘‘if,’’ and so forth). Coltheart [58] has claimed that performance in deep dyslexia is based on a right-hemisphere reading system and has suggested that studies of this disorder may not be relevant to theories of normal reading. Opposing this

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view is the striking demonstration that normal readers can produce semantic and visual reading errors if asked to perform a semantic search among words presented under conditions of rapid serial visual presentation [59]. The continuously changing display creates a jumbled impression of words and letters, so that readers find it difficult to use letter-level information to check on their impression of the word. The perception that ‘‘dog’’ was presented rather than ‘‘cat,’’ cannot be easily overridden by checking for the letter ‘‘d’’, because this letter may have occurred in a previous or subsequent word. Under these demanding exposure conditions, normal readers respond that the word ‘‘steeple’’ occurred, in response to ‘‘church’’, for example. There are several informative computational models of deep dyslexia using a similar connectionist architecture to the framework developed for nonsemantic reading [60,61]. This model translates orthography to phonology by first contacting semantic representations and can be damaged in a variety of ways to yield the characteristic pattern of errors in deep dyslexia [57]. The principle governing the occurrence of semantic and visual errors is that patterns of activation in the network tend to be similar for words that have many letters in common and for words sharing many semantic features. Patients with phonologic dyslexia share the same difficulty as patients with deep dyslexia in reading nonsense words (although generally not to the same degree), but do not make semantic errors when reading words. It is tempting to assume the two dyslexias are related and, indeed, Glosser and Friedman [62] argue that they fall on a continuum of severity of impairment with patients who have phonologic dyslexia relying on a more intact semantic reading route than patients who have deep dyslexia. Patients with phonologic dyslexia almost always reveal impairments in their ability to carry out tasks requiring the manipulation of sound elements, even when these tasks use auditory rather than written segments. This observation raises the similar questions to those that emerge in the analysis of LBL reading: How domainspecific is the mechanism that determines the translation of subword orthographic units into sound? What deficits have led to the disruption of this mechanism in phonologic dyslexia? (Coltheart [63] has a discussion of these and other related issues regarding phonological dyslexia.) Summary Peripheral dyslexias are the result of impairment to processes that convert letters on the page into an abstract orthographic representation. Many aspects of these disorders are difficult to understand in depth. Invariably, there is evidence that some type of word-level perception occurs rapidly in many patients with LBL reading or neglect dyslexia, yet apparently contradictory evidence indicates that part of the word has been misperceived or that the letters must be analyzed laboriously for conscious identification to occur. Current theories attempt to synthesize these different aspects of the patients’ performance, but their development is at an early stage. Questions

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remain also about the domain specificity of the perceptual impairment in LBL reading and about the nature of spatial attention and spatial frames in neglect dyslexia and other forms of attentional disorder. Current understanding of central dyslexias has perhaps advanced further. Welldeveloped computational models exist of these dyslexias, as do plausible experimental techniques for revealing the activity of semantic and nonsemantic routes in normal readers. Nevertheless, the difficult issue of domain specificity arises again with respect to some of the mechanisms invoked, and in this regard, central and peripheral dyslexias continue to pose the same challenge. Acknowledgment The author gratefully acknowledges the moral support of John Farquerson during the preparation of this manuscript. References [1] Dejerine J. Contribution a l’e´tude anatomo-pathologique et clinique des differentes varie´te´s de ce´cite´-verbale. Me´moires Socie´te´ Biologique 1892;4:61–90. [2] Damasio AR, Damasio H. The anatomic basis of pure alexia. Neurology 1983;33:1573–83. [3] Bub DN, Arguin M, Lecours AR. Jules Dejerine and his interpretation of pure alexia. Brain Lang 1993;45:531–59. [4] Eggert GH. Wernicke’s works on aphasia. The Hague (The Netherlands): Mouton; 1977. [5] Dejerine J, Pe´lissier A. Contribution a l’e´tude de la ce´cite verbale pure. Encephale 1914; 1:1–28. [6] Coltheart M. Phonological dyslexia: past and future issues. Cognitive Neuropsychology 1996;13:749–62. [7] Shallice T. From neuropsychology to mental structure. Cambridge (England): Cambridge University Press; 1988. [8] Shallice T, Warrington EK. The possible role of selective attention in acquired dyslexia. Neuropsychologia 1977;15:31–41. [9] Warrington EK, Cipolotti L, McNeil J. Attentional dyslexia: a single case study. Neuropsychologia 1993;31:871–85. [10] He´caen H. Introduction a` la neuropsychologie. Paris: Librairie Larousse; 1972. [11] Treisman A, Souther J. Search asymmetry: a diagnostic for preattentive processing of separate features. J Exp Psychol [Gen] 1985;114:285–310. [12] Mozer M. Letter migration in word perception. J Exp Psychol [Hum Percept] 1983;9: 531–46. [13] Vallar G, Perani D. The anatomy of unilateral neglect after right-hemispheric stroke lesions. Aclinical/CT scan correlation study in man. Neuropsychologia 1986;24:609–22. [14] Damasio AR, Damasio H, Chui HC. Neglect following damage to frontal lobe or basal ganglia. Neuropsychologia 1980;18:123–32. [15] Arguin M, Bub DN. Evidence for an independent stimulus-centred spatial reference frame from a case of visual hemineglect. Cortex 1993;29:349–57. [16] Haywood M, Coltheart M. Neglect dyslexia and the early stages of visual word recognition. Neurocase 2000;6:33–44. [17] Patterson KE, Wilson B. A ROSE is a ROSE or a NOSE: a deficit in initial letter identification. Cognitive Neuropsychology 1990;7:447–77.

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