تقویت ظرفیت یادگیری کلمه پنهان از طریق رسم الخط در زبان پریشی

The ability to learn to use new words is thought to depend on the integrity of the left dorsal temporo-frontal speech processing pathway. We tested this assumption in a chronic aphasic individual (AA) with an extensive left temporal lesion using a new-word learning paradigm. She exhibited severe phonological problems and Magnetic Resonance Imaging (MRI) suggested a complete disconnection of this left-sided white-matter pathway comprising the arcuate fasciculus (AF). Diffusion imaging tractography confirmed the disconnection of the direct segment and the posterior indirect segment of her left AF, essential components of the left dorsal speech processing pathway. Despite her left-hemispheric damage and moderate aphasia, AA learned to name and maintain the novel words in her active vocabulary on par with healthy controls up to 6 months after learning. This exceeds previous demonstrations of word learning ability in aphasia. Interestingly, AA's preserved word learning ability was modality-specific as it was observed exclusively for written words. Functional magnetic resonance imaging (fMRI) revealed that in contrast to normals, AA showed a significantly right-lateralized activation pattern in the temporal and parietal regions when engaged in reading. Moreover, learning of visually presented novel word–picture pairs also activated the right temporal lobe in AA. Both AA and the controls showed increased activation during learning of novel versus familiar word–picture pairs in the hippocampus, an area critical for associative learning. AA's structural and functional imaging results suggest that in a literate person, a right-hemispheric network can provide an effective alternative route for learning of novel active vocabulary. Importantly, AA's previously undetected word learning ability translated directly into therapy, as she could use written input also to successfully re-learn and maintain familiar words that she had lost due to her left hemisphere lesion.

Previous studies on the neural substrates of learning have delineated a general framework of complementary hippocampal and cortical systems in binding and consolidating memories for novel contents (McClelland, McNaughton, & O'Reilly, 1995) such as new word–referent pairs (Davis & Gaskell, 2009), respectively. Moreover, functional neuroimaging evidence indicates that the left dorsal temporo-frontal pathway involved in word production is also crucial for learning new active vocabulary (Hickok and Poeppel, 2007 and Rodríguez-Fornells et al., 2009). The available evidence from aphasia is in line with these views. Meinzer et al. (2010) showed that the extent of damage to the left hippocampus and surrounding tissue predicts language therapy outcomes in aphasia. Moreover, the few studies on acquisition of new active vocabulary in aphasia indicate that chronic lesions in the left cortical language areas, even in mild aphasia, can severely hamper acquisition and maintenance of novel words (Grossman and Carey, 1987, Gupta et al., 2006, McGrane, 2006, Tuomiranta et al., 2011 and Tuomiranta et al., 2012). In the present paper, we extend this current knowledge on the neurocognition of word learning by presenting behavioral and structural–functional neuroimaging data from a case of aphasia (AA) with a disconnected left dorsal temporo-frontal pathway who nevertheless learned and maintained new active vocabulary on par with healthy controls. The imaging data were expected to shed light on the alternative neural pathways that our patient is using to enable her remarkable learning and maintenance of novel words. We employed a well-studied new-word learning paradigm that involves learning of the names of ancient farming equipment (Laine & Salmelin, 2010). Learning was evaluated with spontaneous naming of the novel objects, a measure that is particularly demanding for individuals with aphasia who almost always suffer from anomia (Laine & Martin, 2006). We employed novel word learning rather than the more traditional approach of re-teaching premorbidly mastered words that have become inaccessible in aphasia, because we wanted to specifically target the word learning mechanisms that encode and store new word–referent associations. Re-teaching of familiar but inaccessible words for an aphasic individual is clinically of utmost importance but, in terms of basic research, makes it difficult to separate the involvement of word learning mechanisms from memory retrieval where access to lost words is re-gained through phonological or semantic cues given by the therapist. Over the last four decades, different aspects of verbal learning in aphasia have been probed in experimental studies. Early studies quantified aphasic individuals' ability to re-learn to produce familiar words (e.g., Sarno, Silverman, & Sands, 1970) or compared the learning rate and capacity of aphasic versus healthy participants with word list learning tasks (e.g., Tikofsky, 1971). More recently, the effects of short-term memory on verbal learning in aphasia have been a focus of inquiry (e.g., Freedman & Martin, 2001; Martin & Saffran, 1999). Several investigations have also added challenge to the verbal learning tasks through introducing partly novel materials (e.g., Breitenstein et al., 2004, Freed et al., 1995, Marshall et al., 2001 and Marshall et al., 1992). Of particular interest for the present paper are studies that have utilized a design where genuinely novel referents have been paired with genuinely novel names (Grossman and Carey, 1987, Gupta et al., 2006, Laganaro et al., 2006, McGrane, 2006, Morrow, 2006, Tuomiranta et al., 2011 and Tuomiranta et al., 2012). Looking at active vocabulary acquisition as measured by spoken naming, of these investigations one showed practically no learning (Gupta et al., 2006), one probed only passive vocabulary (Morrow, 2006), and one did not measure naming accuracy (Laganaro et al., 2006). Three investigations reported statistically significant short-term novel word learning that varied between aphasic participants (McGrane, 2006, Tuomiranta et al., 2011 and Tuomiranta et al., 2012). Not surprisingly, in the latter two studies that included also healthy controls, the performance levels of the individuals with aphasia were impaired. Only two studies (Grossman and Carey, 1987 and Tuomiranta et al., 2012) reported some long-term maintenance of novel referent-word pairs in aphasic participants, and in the latter study that included healthy controls, the long-term maintenance of the aphasic individuals was significantly impaired. In summary, the previous literature indicates that some individuals with aphasia are able to acquire at least some novel active vocabulary, even though their learning outcomes are impaired in relation to normal performance both in the short-term and long-term. Nevertheless, these findings inspired us to look further into the word learning abilities of individuals with aphasia and led to the discovery of the present case which, to our surprise, showed learning and maintenance of novel active vocabulary on par with healthy controls. Current views on the neural substrates of language differentiate two major left-sided pathways: a dorsal stream (linking perisylvian language areas and inferior frontal regions) for sound-motor connections and a ventral stream (connecting temporal and prefrontal regions via the extreme capsule) for auditory comprehension (Hickok and Poeppel, 2007, Kümmerer et al., 2013, Parker et al., 2005, Saur et al., 2008, Saur et al., 2010 and Ueno et al., 2011). The lesion in our patient affected especially a major component of the dorsal pathway, namely the arcuate fasciculus (AF), a large left-lateralized (Catani et al., 2007 and Nucifora et al., 2005) white-matter fiber bundle with three segments (Catani, Jones, & ffytche, 2005). In humans, the direct segment of the AF connects the posterior part of the superior and middle temporal regions (Wernicke's territory) to the posterior frontal regions (Broca's territory) (Catani et al., 2005 and Fernández-Miranda et al., 2008). The AF has been linked to the transmission, manipulation, and articulation of phonological information, verbal working memory, and verbal repetition of speech (Catani and Mesulam, 2008, Hickok and Poeppel, 2007, Marchina et al., 2011, Rilling et al., 2008 and Saur et al., 2008). AF lesions (Damasio & Damasio, 1980) as well as damage to the left supramarginal gyrus (SMG) and the temporo-parietal junction (Fridriksson et al., 2010) have been associated with conduction aphasia. The indirect segment of the AF is divided into the anterior part, linking Broca's territory and adjacent premotor areas with the inferior parietal cortex (Geschwind's territory), and the posterior section, connecting the inferior parietal cortex with Wernicke's territory (Catani et al., 2005 and Fernández-Miranda et al., 2008). Crucially to the present investigation, as an interface between phonological input and articulatory representations, the left AF is considered to be necessary for learning to produce new words (Aboitiz, 2012, Hickok and Poeppel, 2007, Rodríguez-Fornells et al., 2009 and Schultze et al., 2012). This view predicts that learning of new active vocabulary becomes impaired if the left AF is disconnected. However, to our knowledge, the effects of left AF disconnection on the acquisition and long-term maintenance of novel words have not been examined before. Given the intactness of our patient's right hemisphere including the right AF, it is of interest to see to what extent right-hemispheric structures could contribute to her word learning. Interestingly, recent functional neuroimaging results indicate considerable variability in normal individuals' engagement of right-hemispheric regions e.g., in reading (Seghier, Lee, Schofield, Ellis, & Price, 2008).

Using a deterministic fiber tracking algorithm tractography in order to examine AF connections, we found that AA had all three sections intact in her right hemisphere (see Fig. 1(C)) but, the direct segment of the AF and the posterior part of the indirect segment were disconnected in AA's left hemisphere. Although we were unable to reconstruct the left-sided AF using deterministic tractography, likely due to a loss in FA following the infarct, we were able to visualize left fronto-parietal pathways corresponding to the anterior section of the left AF using probabilistic tractography. Hence, the anterior part of the indirect segment of the left AF was likely preserved (Fig. 1(B)). However, this statement has to be interpreted with caution because both the presence of disruptions in anatomical connections or axonal degeneration in the lesioned region and the potential artifacts produced by the implanted clip, may reduce the strength of the evidence for the affected track. A voxel-based (using TBSS) FA comparison of white-matter integrity between AA and a group of seven healthy control participants indicated a significant reduction in FA in left superior and middle temporal, inferior parietal and inferior frontal gyri in AA (see Fig. 3). Visual comparison with tracts from the average control dataset (Fig. 3) implicated damage to the left AF (dorsal system) and tracts passing through the external/extreme capsule (ventral system including the inferior fronto-occipital fasciculus – IFOF) (Saur et al., 2008). However, the lower FA in the inferior frontal and external/extreme capsule regions may not be reliable due to a metallic clip affecting signal in these areas locally (see Fig. 1(A)). Statistical comparison of the right-sided AF between AA and controls revealed no significant differences (all p > .2) in FA or tract volume (see Table 2). Table 2. FA and volume values for direct and indirect (anterior and posterior) segments of the arcuate fasciculus (AF) reconstructed using deterministic tractography in healthy controls and AA. FA, Fractional Anisotropy; Vol, volume of tract; –, failure in reconstruction of the tract using deterministic tractography. Participant Left direct Left anterior Left posterior Right direct Right anterior Right posterior Vol FA Vol FA Vol FA Vol FA Vol FA Vol FA Control 1 6.58 .49 7.07 .46 4.21 .49 6.16 .50 2.42 .43 2.99 .43 Control 2 5.62 .45 3.98 .43 4.91 .45 4.88 .50 4.54 .44 3.98 .47 Control 3 5.78 .55 4.22 .51 .57 .51 – – 6.46 .48 1.82 .55 Control 4 9.12 .50 4.78 .50 .57 .45 5.05 .54 5.46 .47 2.87 .47 Control 5 3.02 .51 4.29 .49 11.4 .52 5.58 .49 1.57 .42 .46 .42 Control 6 8.25 .50 6.48 .46 1.95 .46 7.34 .54 5.75 .46 3.37 .46 Control 7 8.58 .51 1.24 .48 3.42 .51 6.81 .52 2.92 .47 1.98 .47 AA – – – – – – 6.35 .47 4.78 .46 1.14 .45 Table options 3.2. Behavioral word learning performance To test the claim that the left dorsal speech processing pathway is crucial in word learning (Hickok and Poeppel, 2007 and Rodríguez-Fornells et al., 2009), we probed acquisition and maintenance of new active vocabulary in AA and five healthy age-matched controls. The learning curves on spontaneous naming (Fig. 2(B)) showed rapid acquisition and good long-term maintenance of the novel words in the five controls. AA's word learning was somewhat slower than in the control group (Yates' corrected χ2 = 6.67, df = 1, p < .01; responses summed over all learning sessions up to post-training), although she did eventually achieve a 100% naming accuracy. Not unexpectedly, the controls varied in their word learning speed. AA's learning did not differ statistically from the slowest normal learner (Yates' corrected χ2 = .18, df = 1, p = .67). Moreover, AA's long-term maintenance up to 6 months post-training was comparable to that of the controls (Fisher's exact test, one-tailed, p = .31, responses summed over the maintenance period). In fact, only one of the five healthy controls showed as high overall maintenance as AA. AA's self-report suggested that seeing the novel word in written form was crucial for her learning. To verify this, we conducted a similar, short-term word learning experiment (behavioral Experiment 2) with novel word–picture pairs separately for written-only and auditory-only input. The learning curves in Fig. 2(C) show clearly that it was indeed the written-only input that resulted in superior learning in AA. We also tested whether AA's remarkable word learning ability through orthographic input translated into a clinically relevant treatment for her persistent word-finding difficulty (behavioral Experiment 3; Fig. 2(D)). A post-training picture naming test after 18 days of training showed successful acquisition of all the 42 trained items, and AA performed well also during the 9-weeks follow-up. The training effect was item-specific with no generalization to the 21 untrained control items. Naming in sentence context (using action images that differed from the object-only images used in training) was also at a high level post-training, showing that AA's word learning ability was not limited to the training context or to the specific stimulus pictures used. Rather, the learned words were available to her in connected speech, too.