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Neurocase: The Neural Basis of Cognition Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/nncs20
Improved verbal learning in the semantic variant of primary progressive aphasia when using semantic cues ab
ab
Nicholas J. Milano , John B. Williamson a
& Kenneth M. Heilman
ab
Department of Neurology, University of Florida College of Medicine, Gainesville, FL, USA
b
Malcom Randall Veteran’s Affairs Medical Center, Gainesville, FL, USA Published online: 11 Mar 2014.
Click for updates To cite this article: Nicholas J. Milano, John B. Williamson & Kenneth M. Heilman (2015) Improved verbal learning in the semantic variant of primary progressive aphasia when using semantic cues, Neurocase: The Neural Basis of Cognition, 21:3, 345-350, DOI: 10.1080/13554794.2014.894081 To link to this article: http://dx.doi.org/10.1080/13554794.2014.894081
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Neurocase, 2015 Vol. 21, No. 3, 345–350, http://dx.doi.org/10.1080/13554794.2014.894081
Improved verbal learning in the semantic variant of primary progressive aphasia when using semantic cues Nicholas J. Milanoa,b*, John B. Williamsona,b and Kenneth M. Heilmana,b a
Department of Neurology, University of Florida College of Medicine, Gainesville, FL, USA; bMalcom Randall Veteran’s Affairs Medical Center, Gainesville, FL, USA
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(Received 25 March 2013; accepted 28 January 2014) The semantic variant of primary progressive aphasia (PPA-S) is characterized by impairments in confrontation naming and single word comprehension. Although episodic memory may be relatively spared, there can be impairment in verbal learning tasks. We report a patient with PPA-S and impaired verbal learning who was tested to learn if when provided with semantic categories, her learning would improve. A 70-year-old right-handed woman with a 2-year history of progressive difficulties with word finding, naming, and memory was tested for language and memory deficits using the Hopkins Verbal Learning Test-Revised (HVLT-R). She was then retested with the HVLT-R after being provided with the three semantic categories to which these words belonged. Confrontation naming was impaired on the Boston Naming Test. Sentence repetition was normal. Comprehension testing with word picture matching and sentence comprehension was normal. On a test of semantic associations, Pyramids and Palm Trees, she was impaired. She was also impaired on tests of verbal learning (HVLT-R) (total: 13) but not recall. When a different version of the HVLT-R was given with the semantic categories of the words given beforehand, her scores improved (total: 26). This patient with PPA-S had an impairment of verbal learning, but not delayed recall. When given a semantic category cue beforehand, her verbal learning performance improved. This observation suggests that this patient did not spontaneously use semantic encoding. Using a semantic cueing strategy may help other patients with PPA-S improve their capacity for verbal learning. Keywords: semantic dementia; primary progressive aphasia; semantic cueing; verbal memory; word list learning
Semantic memory can be defined as the knowledge of facts, objects, and word meanings (Tulving, 1972, 1983). A syndrome of progressive impairment in semantic memory in the setting of cerebral atrophy was described in three patients by Warrington (1975). This syndrome was coined semantic dementia (SD) by Snowden, Goulding, and Neary (1989) and further described by Hodges, Patterson, Oxbury, and Funnell (1992) as a syndrome of progressive fluent aphasia with anomia and impaired single word comprehension associated with temporal lobe atrophy. More recently, the syndrome has been classified as the semantic variant of primary progressive aphasia (PPA-S). Diagnostic criteria require impaired confrontation naming and single word comprehension with additional features including impaired object knowledge, surface dyslexia, spared repetition, and spared speech production (Gorno-Tempini et al., 2011). PPA-S is associated with anterior temporal lobe atrophy, often more severe on the left (Galton et al., 2001; Gorno-Tempini et al., 2004; Mummery et al., 2000), and the pathology is typically TAR DNA-binding protein-43 (TDP43) positive inclusions as seen in frontotemporal lobar degeneration (Davies et al., 2005; Hodges et al., 2004).
Episodic memory is the storage of temporally specific personal experiences or events (Tulving, 1972, 1983). In initial descriptions, patients with SD had relatively preserved episodic memory (Hodges & Patterson, 1996; Hodges et al., 1992; Warrington, 1975), and have later been shown to have normal performance on nonverbal memory tasks (Bozeat, Lambon, Patterson, Garrard, & Hodges, 2000; Hodges & Graham, 2001; Scahill, Hodges, & Graham, 2005). Further, autobiographical memory is preserved for recent events (Graham & Hodges, 1997; Nestor, Graham, Bozeat, Simons, & Hodges, 2002; Piolino, Belliard, Desgranges, Perron, & Eustache, 2003), and may be preserved for the entire lifetime (Moss, Kopelman, Cappelletti, Davies, & Jaldow, 2003; Westmacott, Leach, Freedman, & Moscovitch, 2001). In contrast to nonverbal episodic memory and autobiographical memory, patients with SD are significantly impaired in tasks of verbal memory such as word learning lists (Graham, Patterson, Powis, Drake, & Hodges, 2002; Scahill, Hodges, & Graham, 2005). It has been argued that this verbal episodic memory impairment is the result of the arbitrary relationship between words and their meaning compared to the systematic semantic storage of visual
*Corresponding author. Email: [email protected]fl.edu This work was authored as part of the Contributor’s official duties as an Employee of the United States Government and is therefore a work of the United States Government. In accordance with 17 U.S.C. 105, no copyright protection is available for such works under U.S. Law.
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objects (Benedet, Patterson, Gomez-Pastor, & Luisa Garcia de la Rocha, 2006; Graham et al., 2002; Hodges & Graham, 2001; Lambon Ralph & Howard, 2000). There is evidence that semantic cueing may be beneficial in the treatment of anomia in SD (Bier et al., 2009; Dressel et al., 2010; Henry, Beeson, & Rapcsak, 2008), but the effects of semantic cueing on verbal learning and episodic memory have not been evaluated. We present a patient with probable PPA-S whose word learning significantly improved after receiving semantic category cues.
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Case report A 70-year-old right-handed woman with a master’s degree level of education was seen at a cognitive and memory disorders clinic. She described a 2-year history of language and memory impairment, which began with word finding difficulties and forgetting names. Over time, her symptoms gradually worsened. She began to have difficulty remembering previous conversations and would make semantic paraphasic errors such as stating “moon” instead of “sun.” She had no other cognitive complaints, no behavioral or personality changes, and no changes in her movements or gait. Additional neurologic symptoms included tinnitus for the previous 4 years and frequent headaches. Her headaches would occur 2–3 times a week and were described as having a pulsing character, which could be relieved by over the counter analgesics. She had a past medical history of gastroesophageal reflux disease and restless leg syndrome. Her only medication was melatonin for insomnia. Her maternal aunt had an unknown type of dementia and both her mother and sister had a history of ischemic strokes. Her general physical examination, including ophthalmologic and cardiac exams, was unremarkable with the exception of a blood pressure of 161/74. Her general
neurological examination was normal with no frontal release signs. Approximately 3 years prior to our visit, the patient had magnetic resonance imaging (MRI) of her brain completed as a precaution due to her family history of stroke. This was completed approximately 1 year prior to her onset of symptoms. The patient reported that it was normal, but on our review, we observed mild left anterior temporal lobe atrophy. A repeat MRI of her brain was completed 3 months prior to our visit due to her cognitive symptoms. It showed progression of her left anterior temporal lobe atrophy as well as onset of mild left frontal atrophy (Figure 1). Also evident was mild to moderate subcortical leukoaraiosis. Further workup included laboratory screenings for reversible causes of dementia, which were negative. The patient received a battery of neuropsychological tests (see Table 1 for a summary). She scored a 27/30 on the Folstein Mini-Mental Status Exam (MMSE) having missed the recall of all three objects. Her Montreal Cognitive Assessment score was 22/30 losing points on naming, repetition, letter F fluency, and word recall (1/5). She was mildly impaired on a test of phonemic fluency with the letters “F, A, S” (28 words, z = −1.6; Heaton norms) and moderately to severely impaired on semantic (animal) fluency (9 words, z = −2.8; Heaton norms). She was able to repeat and was able to follow single and multistep commands without impairment. Working memory was assessed using digit span and she performed within the average range (forward: 7 digits, z = 0.6; reverse: 4 digits, z = −0.33). Baddeley, Gathercole, and Papagno (1998) describe nonword repetition as a relatively pure test of the phonological loop of working memory. When our patient was asked to repeat nonwords such as flig or flanlop, she did not make any errors. She had no evidence of neglect or visuospatial abnormalities. During our initial visit, she was given the short form of the Boston Naming Test (BNT) and was only able to
Figure 1. (a) A transverse section of an MRI of the patient’s brain showing left anterior temporal lobe atrophy. (b) A coronal section showing the same.
Neurocase Table 1.
Neuropsychological testing.
Test
Result
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MMSE HVLT free recall HVLT delayed recall Boston Naming Test Phonemic fluency F A S Semantic fluency (animals) Word picture matching Pyramids and Palm Trees Pictures Words
z-Score
27/30 13/36 (1, 5, 7) 6/12 20/60 28 9 8 11 9 Normal 45/52 40/52
−2.22 −0.96 −3.9 −1.6
−2.8 Normal, >90% 86.5% 76.9%
correctly name 5/15 pictures with no cueing for a predicted total score of 20 (z = −3.9; Heaton norms). Three of her errors were superordinate taxonomic errors such as naming the octopus an animal. The remaining errors were characterized by her giving descriptions of the objects. For example, she described a stethoscope as “something you would put in your ears to listen.” At a subsequent visit, approximately 2 weeks later, her naming and semantic deficits were further evaluated. The odd and even items of the BNT were given in succession with a modified administration. Semantic cues were provided on half of the items and no cues were provided on the other half of items. Her scores were improved, though still impaired compared to our initial visit, but there was no difference between the versions given with and without semantic category cueing (no cueing, odds: 15/30, predicted total score: 30, z = −3.1; with cueing, evens: 16/30, predicted total score: 32, z = −3.1). During the noncued version, she was able to correctly name three items which are shared with the short form of the BNT given at our initial visit. During the cued version, she was able to correctly name four items which she was previously unable to name. She had normal performance, not missing any items, on a single word comprehension test during which she had to choose the correct picture when verbally given a word. She was impaired on the Pyramids and Palm Trees test of semantic associations scoring first 45/52 (86.5%) on pictures and then 40/52 (76.9%) on words (clinical cutoff: 90%).
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To evaluate her memory at our initial visit, she was given the Hopkins Verbal Learning Test-Revised (HVLT-R). The HVLT-R is a supraspan word list learning task with 12 words from 3 semantic categories (e.g., animals, precious stones, and dwellings). During this task, the examiner reads the list of words, and the patient is asked to state the words that they remember. Three trials are given in succession and the number of words the patient remembers in each trial is added up for a free recall score. After an approximately 20-min delay, the patient is again asked for the words they can remember from the list. The number of remembered words is the patient’s delayed recall score. Finally, recognition is tested using a list of 24 words (12 correct words, 6 related words, and 6 unrelated words), and the patient is asked to state if each word was on the initial list. Our patient was given Form 1 of the HVLT-R (semantic categories: animals, precious stones, and dwellings). Her score on free recall was a total of 13, z = −2.22 (Trial 1: 1, z = −2.85; Trial 2: 5, z = −1.81; Trial 3: 7, z = −1.35). Her delayed recall was six words (z = −0.96) and she had significant improvement with recognition (12/12 true positive words with 2 false positive related word errors; Discrimination Index: 10, z = −0.40). To better characterize her word learning and verbal memory deficit, different versions of the HVLT-R were repeated using different strategies. These were completed during the same visit as her initial HVLT-R, approximately 1 h later. First, the patient was told that she would receive credit for descriptions of words on the list as well as the actual words. For this task, she was given Form 5 (with words from the following semantic categories: occupations, sports, and vegetables). Her score mildly improved to a 19, z = −1.13 (Trial 1: 4, z = −1.35; Trial 2: 7, z = 0.86; Trial 3: 8, z = 0.85), but in no case was she able to describe a word she could not name. Next the patient was given the semantic categories of the word list beforehand (Form 4: birds, articles of clothing, and carpenter’s tools). Using this strategy, the patient significantly improved to a score of 26, z = 0.15 (Trial 1: 8, z = 0.65; Trial 2: 8, z = −0.38; Trial 3: 10, z = 0.15) (Table 2). This gives a change in z-score between her initial un-cued version of the HVLT-R and subsequent cued version of 2.37 (Trial 1: 3.5; Trial 2: 1.43; Trial 3: 1.5). Delayed recall was not assessed on these additional versions of the HVLT-R.
Table 2. HVLT results. HVLT condition Initial Patient description Semantic cueing Total change in z-score
Trial 1
Trial 2
Trial 3
1 (z = −2.85) 4 (z = −1.35) 8 (z = 0.65) 3.5
5 (z = −1.81) 7 (z = 0.86) 8 (z = −0.38) 1.43
7 (z = −1.35) 8 (z = 0.85) 10 (z = 0.15) 1.5
Total 13 (z = −2.22) 19 (z = −1.13) 26 (z = 0.15) 2.37
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Discussion Based on the patient’s history, examination, and imaging findings, this patient best fits a diagnosis of PPA-S. She had impairment of confrontation naming as well as evidence of semantic knowledge deterioration on a test of semantic associations, Pyramids and Palm Trees. Although she had not yet met criteria for the diagnosis of PPA-S due to her normal single word comprehension, this pattern has been described in early stages of the disease (Czarnecki et al., 2008). Our patient significantly improved her word learning with semantic category cueing on the HVLT-R. Her improvement in performance was over 2 standard deviations between her initial un-cued HVLT-R score and the subsequent cued version (change in z-score = 2.37) moving her from the impaired to average range. Further, each of her individual trials improved by more than a standard deviation (Trial 1: 3.5; Trial 2: 1.43; Trial 3: 1.5). This may indicate that she did not spontaneously use her semantic knowledge to aid in encoding the initial word list. Patients with SD are able to recognize previously viewed, perceptually identical, objects and faces regardless of underlying semantic knowledge (Graham, Simons, Pratt, Patterson, & Hodges, 2000; Simons, Graham, Galton, Patterson, & Hodges, 2001). However, when the objects are perceptually altered (phone with touch pad versus circular dial), SD patients can only recognize the objects for which they have underlying semantic knowledge. This indicates that perceptual information can be used to form nonverbal episodic memories without semantic knowledge, but when perceptual information changes or is incomplete, semantic knowledge is needed to support memory formation. Words have minimal perceptual information and therefore activation of their associated semantic knowledge would be expected to be vital for episodic memory formation. Supporting this theory comes from the finding that normal individuals recall true words more accurately than nonwords (Hulme, Maughan, & Brown, 1991). Once a patient with SD begins to lose their semantic knowledge, previously known words no longer activate semantic knowledge, which may explain poor performance on verbal memory tasks (Benedet et al., 2006; Graham et al., 2002; Hodges & Graham, 2001; Lambon Ralph & Howard, 2000). In fact, patients with SD recall known words more accurately than words for which they no longer have knowledge (Jefferies, Jones, Bateman, & Ralph, 2004, 2005; Knott, Patterson, & Hodges, 1997, 2000). Our patient appeared to be in the early stages of her disease. Although she had not fully lost her semantic knowledge of the words on the HVLT-R, she may not have been fully activating their associated semantic meanings which aid encoding and support the formation of verbal episodic memories. When our patient was cued
with semantic categories prior to being given the word list, the associated semantic knowledge may have been externally activated to support verbal episodic memory formation. Our patient had complained of not remembering previous conversations and semantic cueing may be a potential treatment strategy for verbal learning and episodic memory impairments in patients with PPA-S. An alternative explanation is that the benefit of semantic cueing was due to the presence of mild to moderate ischemic white matter changes. White matter disease has been shown to affect fronto-subcortical functions and the pre-provision of semantic categories may have alleviated some of the prefrontal organizational burdens involved in the encoding process, facilitating easier free retrieval of information. The contribution of white matter disease in the behavioral phenomenology of cortical neurodegenerative diseases is still unclear and further studies would be required to test this hypothesis. Although semantic cueing has been shown to improve naming in some patients with SD (Bier et al., 2009; Dressel et al., 2010; Henry et al., 2008), it did not help our patient. Her performance improved between her initial and subsequent visits on both the un-cued and cued versions of the BNT, but there was no difference between these two conditions. The reason for this memory-naming dissociation, with semantic cueing failing to improve naming but improving episodic memory, is not clear. However, this dissociation does suggest that the disorder of naming was caused by a different mechanism than the impairment in word learning. There are several possible explanations for this dissociation. As stated, in patients with SD, episodic memory is relatively intact, and memory encoding may require less semantic processing than confrontation naming. Thus semantic cueing may have been insufficient to improve this patient’s naming, but sufficient to improve her memory. Alternatively, it was noted that when this patient could not name a picture she often would give a superordinate category, such as animal, or describe what she was viewing. These responses suggest that she was able to recognize these pictures and thus while viewing these pictures she was accessing her semantic representations. Therefore, it is possible that her naming was impaired because some of these semantic representations may have not been able to access her lexicon, and her ability to access her lexicon was not improved by semantic cues. In contrast, when performing word list learning, the test words provided by the examiner were able to access her lexicon, but they did not access her semantic representations. With cueing, however, the words did access her semantic representations which aided memory encoding. Future studies will have to test these hypotheses, but the impairment in naming in our patient may be related to an impairment of lexical access.
Neurocase
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An additional implication of our findings is that semantic cueing on verbal learning tasks may be able to differentiate PPA-S from Alzheimer’s disease (AD). Both of these disorders are associated with impaired naming and memory, and these two disorders cannot be differentiated by verbal episodic memory tasks alone (Scahill, Hodges, & Graham, 2005). However, unlike our patient, when given similar semantic category cues patients with AD do not improve their verbal learning (Buschke, Sliwinski, Guslansky, & Lipton, 1997). This may be explained by that fact that AD involves a true deficit of episodic memory whereas the poor verbal episodic memory impairment in PPA-S may be the result of impaired semantic activation. Further studies, however, would be required to test this hypothesis. Acknowledgments This work was supported in part by the State of Florida Memory Disorders Clinics and the Veteran’s Affairs Research Service.
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Neurocase: The Neural Basis of Cognition Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/nncs20
Improved verbal learning in the semantic variant of primary progressive aphasia when using semantic cues ab
ab
Nicholas J. Milano , John B. Williamson a
& Kenneth M. Heilman
ab
Department of Neurology, University of Florida College of Medicine, Gainesville, FL, USA
b
Malcom Randall Veteran’s Affairs Medical Center, Gainesville, FL, USA Published online: 11 Mar 2014.
Click for updates To cite this article: Nicholas J. Milano, John B. Williamson & Kenneth M. Heilman (2015) Improved verbal learning in the semantic variant of primary progressive aphasia when using semantic cues, Neurocase: The Neural Basis of Cognition, 21:3, 345-350, DOI: 10.1080/13554794.2014.894081 To link to this article: http://dx.doi.org/10.1080/13554794.2014.894081
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Neurocase, 2015 Vol. 21, No. 3, 345–350, http://dx.doi.org/10.1080/13554794.2014.894081
Improved verbal learning in the semantic variant of primary progressive aphasia when using semantic cues Nicholas J. Milanoa,b*, John B. Williamsona,b and Kenneth M. Heilmana,b a
Department of Neurology, University of Florida College of Medicine, Gainesville, FL, USA; bMalcom Randall Veteran’s Affairs Medical Center, Gainesville, FL, USA
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(Received 25 March 2013; accepted 28 January 2014) The semantic variant of primary progressive aphasia (PPA-S) is characterized by impairments in confrontation naming and single word comprehension. Although episodic memory may be relatively spared, there can be impairment in verbal learning tasks. We report a patient with PPA-S and impaired verbal learning who was tested to learn if when provided with semantic categories, her learning would improve. A 70-year-old right-handed woman with a 2-year history of progressive difficulties with word finding, naming, and memory was tested for language and memory deficits using the Hopkins Verbal Learning Test-Revised (HVLT-R). She was then retested with the HVLT-R after being provided with the three semantic categories to which these words belonged. Confrontation naming was impaired on the Boston Naming Test. Sentence repetition was normal. Comprehension testing with word picture matching and sentence comprehension was normal. On a test of semantic associations, Pyramids and Palm Trees, she was impaired. She was also impaired on tests of verbal learning (HVLT-R) (total: 13) but not recall. When a different version of the HVLT-R was given with the semantic categories of the words given beforehand, her scores improved (total: 26). This patient with PPA-S had an impairment of verbal learning, but not delayed recall. When given a semantic category cue beforehand, her verbal learning performance improved. This observation suggests that this patient did not spontaneously use semantic encoding. Using a semantic cueing strategy may help other patients with PPA-S improve their capacity for verbal learning. Keywords: semantic dementia; primary progressive aphasia; semantic cueing; verbal memory; word list learning
Semantic memory can be defined as the knowledge of facts, objects, and word meanings (Tulving, 1972, 1983). A syndrome of progressive impairment in semantic memory in the setting of cerebral atrophy was described in three patients by Warrington (1975). This syndrome was coined semantic dementia (SD) by Snowden, Goulding, and Neary (1989) and further described by Hodges, Patterson, Oxbury, and Funnell (1992) as a syndrome of progressive fluent aphasia with anomia and impaired single word comprehension associated with temporal lobe atrophy. More recently, the syndrome has been classified as the semantic variant of primary progressive aphasia (PPA-S). Diagnostic criteria require impaired confrontation naming and single word comprehension with additional features including impaired object knowledge, surface dyslexia, spared repetition, and spared speech production (Gorno-Tempini et al., 2011). PPA-S is associated with anterior temporal lobe atrophy, often more severe on the left (Galton et al., 2001; Gorno-Tempini et al., 2004; Mummery et al., 2000), and the pathology is typically TAR DNA-binding protein-43 (TDP43) positive inclusions as seen in frontotemporal lobar degeneration (Davies et al., 2005; Hodges et al., 2004).
Episodic memory is the storage of temporally specific personal experiences or events (Tulving, 1972, 1983). In initial descriptions, patients with SD had relatively preserved episodic memory (Hodges & Patterson, 1996; Hodges et al., 1992; Warrington, 1975), and have later been shown to have normal performance on nonverbal memory tasks (Bozeat, Lambon, Patterson, Garrard, & Hodges, 2000; Hodges & Graham, 2001; Scahill, Hodges, & Graham, 2005). Further, autobiographical memory is preserved for recent events (Graham & Hodges, 1997; Nestor, Graham, Bozeat, Simons, & Hodges, 2002; Piolino, Belliard, Desgranges, Perron, & Eustache, 2003), and may be preserved for the entire lifetime (Moss, Kopelman, Cappelletti, Davies, & Jaldow, 2003; Westmacott, Leach, Freedman, & Moscovitch, 2001). In contrast to nonverbal episodic memory and autobiographical memory, patients with SD are significantly impaired in tasks of verbal memory such as word learning lists (Graham, Patterson, Powis, Drake, & Hodges, 2002; Scahill, Hodges, & Graham, 2005). It has been argued that this verbal episodic memory impairment is the result of the arbitrary relationship between words and their meaning compared to the systematic semantic storage of visual
*Corresponding author. Email: [email protected]fl.edu This work was authored as part of the Contributor’s official duties as an Employee of the United States Government and is therefore a work of the United States Government. In accordance with 17 U.S.C. 105, no copyright protection is available for such works under U.S. Law.
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objects (Benedet, Patterson, Gomez-Pastor, & Luisa Garcia de la Rocha, 2006; Graham et al., 2002; Hodges & Graham, 2001; Lambon Ralph & Howard, 2000). There is evidence that semantic cueing may be beneficial in the treatment of anomia in SD (Bier et al., 2009; Dressel et al., 2010; Henry, Beeson, & Rapcsak, 2008), but the effects of semantic cueing on verbal learning and episodic memory have not been evaluated. We present a patient with probable PPA-S whose word learning significantly improved after receiving semantic category cues.
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Case report A 70-year-old right-handed woman with a master’s degree level of education was seen at a cognitive and memory disorders clinic. She described a 2-year history of language and memory impairment, which began with word finding difficulties and forgetting names. Over time, her symptoms gradually worsened. She began to have difficulty remembering previous conversations and would make semantic paraphasic errors such as stating “moon” instead of “sun.” She had no other cognitive complaints, no behavioral or personality changes, and no changes in her movements or gait. Additional neurologic symptoms included tinnitus for the previous 4 years and frequent headaches. Her headaches would occur 2–3 times a week and were described as having a pulsing character, which could be relieved by over the counter analgesics. She had a past medical history of gastroesophageal reflux disease and restless leg syndrome. Her only medication was melatonin for insomnia. Her maternal aunt had an unknown type of dementia and both her mother and sister had a history of ischemic strokes. Her general physical examination, including ophthalmologic and cardiac exams, was unremarkable with the exception of a blood pressure of 161/74. Her general
neurological examination was normal with no frontal release signs. Approximately 3 years prior to our visit, the patient had magnetic resonance imaging (MRI) of her brain completed as a precaution due to her family history of stroke. This was completed approximately 1 year prior to her onset of symptoms. The patient reported that it was normal, but on our review, we observed mild left anterior temporal lobe atrophy. A repeat MRI of her brain was completed 3 months prior to our visit due to her cognitive symptoms. It showed progression of her left anterior temporal lobe atrophy as well as onset of mild left frontal atrophy (Figure 1). Also evident was mild to moderate subcortical leukoaraiosis. Further workup included laboratory screenings for reversible causes of dementia, which were negative. The patient received a battery of neuropsychological tests (see Table 1 for a summary). She scored a 27/30 on the Folstein Mini-Mental Status Exam (MMSE) having missed the recall of all three objects. Her Montreal Cognitive Assessment score was 22/30 losing points on naming, repetition, letter F fluency, and word recall (1/5). She was mildly impaired on a test of phonemic fluency with the letters “F, A, S” (28 words, z = −1.6; Heaton norms) and moderately to severely impaired on semantic (animal) fluency (9 words, z = −2.8; Heaton norms). She was able to repeat and was able to follow single and multistep commands without impairment. Working memory was assessed using digit span and she performed within the average range (forward: 7 digits, z = 0.6; reverse: 4 digits, z = −0.33). Baddeley, Gathercole, and Papagno (1998) describe nonword repetition as a relatively pure test of the phonological loop of working memory. When our patient was asked to repeat nonwords such as flig or flanlop, she did not make any errors. She had no evidence of neglect or visuospatial abnormalities. During our initial visit, she was given the short form of the Boston Naming Test (BNT) and was only able to
Figure 1. (a) A transverse section of an MRI of the patient’s brain showing left anterior temporal lobe atrophy. (b) A coronal section showing the same.
Neurocase Table 1.
Neuropsychological testing.
Test
Result
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MMSE HVLT free recall HVLT delayed recall Boston Naming Test Phonemic fluency F A S Semantic fluency (animals) Word picture matching Pyramids and Palm Trees Pictures Words
z-Score
27/30 13/36 (1, 5, 7) 6/12 20/60 28 9 8 11 9 Normal 45/52 40/52
−2.22 −0.96 −3.9 −1.6
−2.8 Normal, >90% 86.5% 76.9%
correctly name 5/15 pictures with no cueing for a predicted total score of 20 (z = −3.9; Heaton norms). Three of her errors were superordinate taxonomic errors such as naming the octopus an animal. The remaining errors were characterized by her giving descriptions of the objects. For example, she described a stethoscope as “something you would put in your ears to listen.” At a subsequent visit, approximately 2 weeks later, her naming and semantic deficits were further evaluated. The odd and even items of the BNT were given in succession with a modified administration. Semantic cues were provided on half of the items and no cues were provided on the other half of items. Her scores were improved, though still impaired compared to our initial visit, but there was no difference between the versions given with and without semantic category cueing (no cueing, odds: 15/30, predicted total score: 30, z = −3.1; with cueing, evens: 16/30, predicted total score: 32, z = −3.1). During the noncued version, she was able to correctly name three items which are shared with the short form of the BNT given at our initial visit. During the cued version, she was able to correctly name four items which she was previously unable to name. She had normal performance, not missing any items, on a single word comprehension test during which she had to choose the correct picture when verbally given a word. She was impaired on the Pyramids and Palm Trees test of semantic associations scoring first 45/52 (86.5%) on pictures and then 40/52 (76.9%) on words (clinical cutoff: 90%).
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To evaluate her memory at our initial visit, she was given the Hopkins Verbal Learning Test-Revised (HVLT-R). The HVLT-R is a supraspan word list learning task with 12 words from 3 semantic categories (e.g., animals, precious stones, and dwellings). During this task, the examiner reads the list of words, and the patient is asked to state the words that they remember. Three trials are given in succession and the number of words the patient remembers in each trial is added up for a free recall score. After an approximately 20-min delay, the patient is again asked for the words they can remember from the list. The number of remembered words is the patient’s delayed recall score. Finally, recognition is tested using a list of 24 words (12 correct words, 6 related words, and 6 unrelated words), and the patient is asked to state if each word was on the initial list. Our patient was given Form 1 of the HVLT-R (semantic categories: animals, precious stones, and dwellings). Her score on free recall was a total of 13, z = −2.22 (Trial 1: 1, z = −2.85; Trial 2: 5, z = −1.81; Trial 3: 7, z = −1.35). Her delayed recall was six words (z = −0.96) and she had significant improvement with recognition (12/12 true positive words with 2 false positive related word errors; Discrimination Index: 10, z = −0.40). To better characterize her word learning and verbal memory deficit, different versions of the HVLT-R were repeated using different strategies. These were completed during the same visit as her initial HVLT-R, approximately 1 h later. First, the patient was told that she would receive credit for descriptions of words on the list as well as the actual words. For this task, she was given Form 5 (with words from the following semantic categories: occupations, sports, and vegetables). Her score mildly improved to a 19, z = −1.13 (Trial 1: 4, z = −1.35; Trial 2: 7, z = 0.86; Trial 3: 8, z = 0.85), but in no case was she able to describe a word she could not name. Next the patient was given the semantic categories of the word list beforehand (Form 4: birds, articles of clothing, and carpenter’s tools). Using this strategy, the patient significantly improved to a score of 26, z = 0.15 (Trial 1: 8, z = 0.65; Trial 2: 8, z = −0.38; Trial 3: 10, z = 0.15) (Table 2). This gives a change in z-score between her initial un-cued version of the HVLT-R and subsequent cued version of 2.37 (Trial 1: 3.5; Trial 2: 1.43; Trial 3: 1.5). Delayed recall was not assessed on these additional versions of the HVLT-R.
Table 2. HVLT results. HVLT condition Initial Patient description Semantic cueing Total change in z-score
Trial 1
Trial 2
Trial 3
1 (z = −2.85) 4 (z = −1.35) 8 (z = 0.65) 3.5
5 (z = −1.81) 7 (z = 0.86) 8 (z = −0.38) 1.43
7 (z = −1.35) 8 (z = 0.85) 10 (z = 0.15) 1.5
Total 13 (z = −2.22) 19 (z = −1.13) 26 (z = 0.15) 2.37
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Discussion Based on the patient’s history, examination, and imaging findings, this patient best fits a diagnosis of PPA-S. She had impairment of confrontation naming as well as evidence of semantic knowledge deterioration on a test of semantic associations, Pyramids and Palm Trees. Although she had not yet met criteria for the diagnosis of PPA-S due to her normal single word comprehension, this pattern has been described in early stages of the disease (Czarnecki et al., 2008). Our patient significantly improved her word learning with semantic category cueing on the HVLT-R. Her improvement in performance was over 2 standard deviations between her initial un-cued HVLT-R score and the subsequent cued version (change in z-score = 2.37) moving her from the impaired to average range. Further, each of her individual trials improved by more than a standard deviation (Trial 1: 3.5; Trial 2: 1.43; Trial 3: 1.5). This may indicate that she did not spontaneously use her semantic knowledge to aid in encoding the initial word list. Patients with SD are able to recognize previously viewed, perceptually identical, objects and faces regardless of underlying semantic knowledge (Graham, Simons, Pratt, Patterson, & Hodges, 2000; Simons, Graham, Galton, Patterson, & Hodges, 2001). However, when the objects are perceptually altered (phone with touch pad versus circular dial), SD patients can only recognize the objects for which they have underlying semantic knowledge. This indicates that perceptual information can be used to form nonverbal episodic memories without semantic knowledge, but when perceptual information changes or is incomplete, semantic knowledge is needed to support memory formation. Words have minimal perceptual information and therefore activation of their associated semantic knowledge would be expected to be vital for episodic memory formation. Supporting this theory comes from the finding that normal individuals recall true words more accurately than nonwords (Hulme, Maughan, & Brown, 1991). Once a patient with SD begins to lose their semantic knowledge, previously known words no longer activate semantic knowledge, which may explain poor performance on verbal memory tasks (Benedet et al., 2006; Graham et al., 2002; Hodges & Graham, 2001; Lambon Ralph & Howard, 2000). In fact, patients with SD recall known words more accurately than words for which they no longer have knowledge (Jefferies, Jones, Bateman, & Ralph, 2004, 2005; Knott, Patterson, & Hodges, 1997, 2000). Our patient appeared to be in the early stages of her disease. Although she had not fully lost her semantic knowledge of the words on the HVLT-R, she may not have been fully activating their associated semantic meanings which aid encoding and support the formation of verbal episodic memories. When our patient was cued
with semantic categories prior to being given the word list, the associated semantic knowledge may have been externally activated to support verbal episodic memory formation. Our patient had complained of not remembering previous conversations and semantic cueing may be a potential treatment strategy for verbal learning and episodic memory impairments in patients with PPA-S. An alternative explanation is that the benefit of semantic cueing was due to the presence of mild to moderate ischemic white matter changes. White matter disease has been shown to affect fronto-subcortical functions and the pre-provision of semantic categories may have alleviated some of the prefrontal organizational burdens involved in the encoding process, facilitating easier free retrieval of information. The contribution of white matter disease in the behavioral phenomenology of cortical neurodegenerative diseases is still unclear and further studies would be required to test this hypothesis. Although semantic cueing has been shown to improve naming in some patients with SD (Bier et al., 2009; Dressel et al., 2010; Henry et al., 2008), it did not help our patient. Her performance improved between her initial and subsequent visits on both the un-cued and cued versions of the BNT, but there was no difference between these two conditions. The reason for this memory-naming dissociation, with semantic cueing failing to improve naming but improving episodic memory, is not clear. However, this dissociation does suggest that the disorder of naming was caused by a different mechanism than the impairment in word learning. There are several possible explanations for this dissociation. As stated, in patients with SD, episodic memory is relatively intact, and memory encoding may require less semantic processing than confrontation naming. Thus semantic cueing may have been insufficient to improve this patient’s naming, but sufficient to improve her memory. Alternatively, it was noted that when this patient could not name a picture she often would give a superordinate category, such as animal, or describe what she was viewing. These responses suggest that she was able to recognize these pictures and thus while viewing these pictures she was accessing her semantic representations. Therefore, it is possible that her naming was impaired because some of these semantic representations may have not been able to access her lexicon, and her ability to access her lexicon was not improved by semantic cues. In contrast, when performing word list learning, the test words provided by the examiner were able to access her lexicon, but they did not access her semantic representations. With cueing, however, the words did access her semantic representations which aided memory encoding. Future studies will have to test these hypotheses, but the impairment in naming in our patient may be related to an impairment of lexical access.
Neurocase
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An additional implication of our findings is that semantic cueing on verbal learning tasks may be able to differentiate PPA-S from Alzheimer’s disease (AD). Both of these disorders are associated with impaired naming and memory, and these two disorders cannot be differentiated by verbal episodic memory tasks alone (Scahill, Hodges, & Graham, 2005). However, unlike our patient, when given similar semantic category cues patients with AD do not improve their verbal learning (Buschke, Sliwinski, Guslansky, & Lipton, 1997). This may be explained by that fact that AD involves a true deficit of episodic memory whereas the poor verbal episodic memory impairment in PPA-S may be the result of impaired semantic activation. Further studies, however, would be required to test this hypothesis. Acknowledgments This work was supported in part by the State of Florida Memory Disorders Clinics and the Veteran’s Affairs Research Service.
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