This article was downloaded by: [Michigan State University] On: 04 March 2015, At: 18:22 Publisher: Routledge Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK
Neurocase: The Neural Basis of Cognition Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/nncs20
Efficacy of semantic–phonological treatment combined with tDCS for verb retrieval in a patient with aphasia a
a
ab
a
c
Rosa Manenti , Michela Petesi , Michela Brambilla , Sandra Rosini , Antonio Miozzo , cd
ad
Alessandro Padovani , Carlo Miniussi
a
& Maria Cotelli
a
IRCCS Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy
b
Center for Cognitive Science, Department of Psychology, University of Turin, Turin, Italy
c
Centre for Brain Aging and Neurodegenerative Disorders, Neurology Unit, University of Brescia, Brescia, Italy d
Click for updates
Department of Clinical and Experimental Sciences, National Neuroscience Institute, University of Brescia, Brescia, Italy Published online: 13 Jan 2014.
To cite this article: Rosa Manenti, Michela Petesi, Michela Brambilla, Sandra Rosini, Antonio Miozzo, Alessandro Padovani, Carlo Miniussi & Maria Cotelli (2015) Efficacy of semantic–phonological treatment combined with tDCS for verb retrieval in a patient with aphasia, Neurocase: The Neural Basis of Cognition, 21:1, 109-119, DOI: 10.1080/13554794.2013.873062 To link to this article: http://dx.doi.org/10.1080/13554794.2013.873062
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
Neurocase, 2015 Vol. 21, No. 1, 109–119, http://dx.doi.org/10.1080/13554794.2013.873062
Efficacy of semantic–phonological treatment combined with tDCS for verb retrieval in a patient with aphasia Rosa Manentia, Michela Petesia, Michela Brambillaa,b, Sandra Rosinia, Antonio Miozzoc, Alessandro Padovanic,d, Carlo Miniussia,d and Maria Cotellia* a
IRCCS Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy; bCenter for Cognitive Science, Department of Psychology, University of Turin, Turin, Italy; cCentre for Brain Aging and Neurodegenerative Disorders, Neurology Unit, University of Brescia, Brescia, Italy; dDepartment of Clinical and Experimental Sciences, National Neuroscience Institute, University of Brescia, Brescia, Italy
Downloaded by [Michigan State University] at 18:22 04 March 2015
(Received 8 May 2013; accepted 15 November 2013) Recent studies reported enhanced performance on language tasks induced by transcranial direct current stimulation (tDCS) in patients with aphasia. One chronic patient with non-fluent aphasia received 20 sessions of a verb anomia training combined with off-line bihemispheric tDCS applied to the dorsolateral prefrontal cortex (DLPFC) – anodal tDCS over left DLPFC plus cathodal tDCS over right DLPFC. A significant improvement in verb naming was observed at all testing times (4, 12, 24, and 48 weeks from post-entry/baseline testing) for treated and untreated verbs. Our findings show beneficial effects of verb anomia training in combination with tDCS in chronic aphasic patient, suggesting a long-lasting effect of this treatment. Keywords: non-invasive brain stimulation; naming; speech therapy
Neuropsychological investigations reported selective impairments in the production and comprehension of verbs in agrammatic aphasic patients. Verbs have been repeatedly investigated as distinct from nouns (i.e. objects) in patients with aphasia (see, for example, Caramazza and Hillis (1991)). Regarding object and action processing differences, several clinical observations have suggested that different cerebral areas are involved in the processing of nouns and verbs. A double dissociation between noun- and verbnaming performance in single cases has been reported (Miceli, Silveri, Nocentini, & Caramazza, 1988). Patients with a selective disorder for object naming usually have lesions centered in the left temporal lobe; conversely, a selective impairment in verb naming has been associated with larger lesions, usually extending to the left frontal cortex (Daniele, Giustolisi, Silveri, Colosimo, & Gainotti, 1994). Various studies have convincingly demonstrated that the lexical system is organized according to grammatical class. Furthermore, Damasio and colleagues suggested that mediation systems for verbs may be located at frontal and parietal sites (Damasio & Damasio, 1992; Damasio & Tranel, 1993). In addition to patient studies, functional imaging studies have also provided evidence for selective activations associated with noun and verb processing in healthy subjects (Perani et al., 1999; Shapiro, Moo, & Caramazza, 2006). In particular, verb naming seems to evoke stronger bilateral activation in the posterior middle-temporal cortex, *Corresponding author. Email: [email protected] © 2014 Taylor & Francis
at the left temporo–parietal junction and in the left frontal cortex compared to object naming (Liljeström et al., 2008). Although considerable work has been performed to investigate the relationship between impairments in verb naming and aphasia type (Miceli et al., 1988; Miceli, Silveri, Villa, & Caramazza, 1984), fewer studies have examined the effectiveness of treatments for impairments in verb naming (for a review, see Conroy, Sage, and Lambon Ralph (2006)). First, Marshall, Pring, and Chiat (1998) described a therapeutic approach in a post-stroke subject with a selective verb-retrieval deficit. Using comprehension, reading, and naming tasks, the authors encouraged the subject to process the semantics and the phonology of the targets to induce better verb retrieval, improving sentence production for the treated verbs, without a significant generalization of untreated items. Subsequently, two treatments were used to treat three patients with aphasia: phonological cueing treatment and semantic cueing treatment. These treatments resulted in an improvement in object naming in a previous study (Wambaugh, Doyle, Martinez, & Kalinyak-Fliszar, 2002). The authors aimed to verify the usefulness of these training techniques on verb naming, and they concluded that both treatments may potentially be applied to the retrieval of verbs and suggested further investigations (Wambaugh et al., 2002). Recently, semantic training has been tested by the same group in an individual with anomic aphasia (Wambaugh & Ferguson, 2007), demonstrating
Downloaded by [Michigan State University] at 18:22 04 March 2015
110
R. Manenti et al.
an increased performance with the trained verbs that was maintained at 6 weeks, but a lack of generalization to untreated verbs. Along the same line, Webster, Morris, and Franklin (2005) showed that a training technique that includes semantic, sentence completion, thematic roles, and sentence-generation tasks could induce an improvement in the retrieval of treated verbs in a patient with aphasia (PWA), but generalization was not evident. Accordingly, using sentence-based word retrieval training, Raymer and Kohen (2006) investigated the improvements in word and verb retrieval in one patient with non-fluent aphasia and one patient with fluent aphasia. The researchers reported that improvements were found only for nonfluent aphasia patients and that noun therapy is more efficacious than verb therapy. In addition, the same group showed that a gesture plus verbal treatment could have the potential to improve communication in nine patients with aphasia (Raymer et al., 2006). Furthermore, a verb-strengthening treatment was investigated in four patients with aphasia, indicating an effect on treated items and generalization to untreated verbs (Edmonds, Nadeau, & Kiran, 2009). Interestingly, Raymer et al. (2007) applied a semantic–phonological treatment (SPT) in eight post-stroke patients with a naming disorder showing an improvement in naming treated images and a minimal, but not significant, effect for untreated items. In this vein, a recent study investigated the beneficial effects of a repetition, orthographic and phonological treatment (decreasing cues) on noun and verb naming in four participants with aphasia (Conroy & Scowcroft, 2012). The data confirmed an improvement in the naming abilities after the treatment, but no evident generalization to untreated items. In a recent work the authors emphasized that argument structure and thematic role mapping training is effective for improving verb and sentence production in agrammatic post-stroke patients (Thompson, Riley, den Ouden, Meltzer-Asscher, & Lukic, 2013). Remarkably, the post-training improvement also resulted in a generalization to untrained verbs. See Table 1 for a review. There is increasing interest in the potential enhancement of cognitive rehabilitative treatment based on the non-invasive brain stimulation (NIBS) techniques, i.e. repetitive transcranial magnetic stimulation (rTMS) or transcranial direct current stimulation (tDCS), applied to specific cortical areas (Miniussi et al., 2008). Facilitation effects have been observed in patients with stroke and dementia when performing a variety of cognitive tasks. Specifically, in chronic aphasia patients, NIBS has been shown to increase the number of correct responses and to reduce the response times, with effects that can persist over time (for a review see Cotelli et al., 2011). Specifically, the potential of rTMS or tDCS to trigger adaptive neuroplasticity in neurological patients has been
related to three main mechanisms: (1) the reactivation of canonical networks, partly damaged or made dysfunctional by the cerebral lesion; (2) the recruitment of compensatory networks, mostly contralateral homologue cortical regions; (3) the additional recruitment of perilesional sub-optimally functioning areas (Miniussi & Rossini, 2011). In patients with aphasia following stroke, right-hemisphere overactivation has been explained by some authors as a “maladaptive” plasticity, which prevents recovery from aphasia (hemispheric competition hypothesis). Contralesional areas continue to play a role that is dysfunctional rather than compensatory in chronic aphasia in patients who have experienced a significant degree of recovery (Postman-Caucheteux et al., 2010). Following this line of reasoning, stimulation techniques have been used both for enhancing left hemisphere activity and reducing right one. There was a great debate in last few years about the significance of controlesional and/or ipsilateral areas activity in patients with post-stroke aphasia (Heiss & Thiel, 2006; Richter, Miltner, & Straube, 2008). Thiel et al. (2006) concluded that time of progression of brain lesions would be the factor which determines successful integration of the right hemisphere into the language network for compensation of lost left hemisphere language function. Following these results, patients with post-stroke aphasia characterized by a fast progression of the lesion would be reasonably characterized, as suggested by Postman-Caucheteux et al. (2010), by a dysfunctional rather than compensatory activity in the contralasional hemisphere. Size of the stroke is the most important factor in establishing whether the right hemisphere contributes beneficially reorganizing the language network in poststroke recovery or not (Torres, Drebing, & Hamilton, 2013). Patients that reported small lesions preferentially recruit left hemisphere perilesional areas without a beneficial involvement of the right hemisphere. In this case it is reasonable to apply excitatory tDCS to left hemisphere regions or/and cathodal tDCS to right hemisphere to inhibit maladaptive overactivation. It has been suggested that NIBS treatment protocol would be modified based on patient characteristics such as stroke size, location, and chronicity (Torres et al., 2013). Regarding tDCS, anodal tDCS (atDCS) has a general facilitation effect and causes membrane depolarization, whereas cathodal tDCS has a general inhibitory effect and causes membrane hyperpolarization (Liebetanz, Nitsche, Tergau, & Paulus, 2002). Both anodal and cathodal stimulation applied over the lesional (i.e. left) hemisphere and cathodal tDCS applied over the contralesional (i.e., right) hemisphere have been shown to improve comprehension and naming in post-stroke aphasia patients (Baker, Rorden, & Fridriksson, 2010). Recent studies in people with chronic stroke have shown that bihemispheric tDCS, where an anode is positioned over the affected region, and the cathode is located in
P1:LH TP, P2:LH FSCL
NA
P1:FL, P2:NF
P1:NF
P1:NF, P2:NF, P3:NC
P1:NF
Type of aphasia Comprehension, reading, and action naming; 1200’ in 14 w P1:SCT, P2: PCT, P3:SCT plus PCT; 5–20 sessions, 2–3 d/w Verb retrieval plus predicate argument structure knowledge; 30 45’ sessions, 3 d/w Sentence embedded word retrieval (nouns and verbs); 3–10 60’ sessions, 2 d/w
Therapy approach
none
none
none
none
from 18 to 180
P1:8, P2:51, P3:10, P4:99
P1:49, P2:9
P1:NF, P2:NF
P1:TM, P2:TM; P3:C, P4:C
P1: A
P1:LH FTP, P2:LH FTP, P3:LH FT, P4: LH FT
P1:NF, P2:NF, P3:NF, P4:NF
P1:LH FT, P2:LH FSCL, P3:LH FT, P4: P1:NF, P2:A, P3:A, LH F P4:NF
P1: LH TP, P2: LH FSCL
P1:LH, P2:LH, P3:LH, P4:LH
P1: LH P
none
Verb network strengthening; 120’ sessions, 2 d/w, till criterion Verb network strengthening; 24–30 120’ sessions, 2 d/w
Verb argument structure none training; 90’ sessions, 2 d/w, till criterion
Vanishing orthographic and 8 phonological cue; 10 30–40’ sessions, 1 d/w
20
6
Semantic feature training; 12 45–60’ sessions, 3 d/w
P1:5, P2:16, P3:52, P1:LH TP, P2:LH TO Th, P3:LH FP, P4: P1:C, P2:NF, P3:NF, P4: Gesture plus verbal training none P4:17, P5:7, P6:18, LH TP, P5:LH P, P6:LH FTP, P7: LH NF, P5:NF, P6:NF, (nouns and verbs); 10 60’ P7:62, P8:43, P9:41 FSCL, P8: LH TP, P9:LH TP P7:NF, P8:FL, P9:FL sessions, 2–3 d/w P1: LH FT, P2: LH FSCL, P3: LH FT, P1: NF, P2: NF, P3:NF, SPT; 10 60’ sessions, 2–3 d/w 5 P1:93, P2 52, P3:75, P4:49, P5:120, P4: LH F, P5: LH FT, P6: LH FT, P7: P4:NF, P5:NF, P6:NF, P6:48, P7:4, P8:9 LH P, P8: LH F P7:FL, P8:A
P1:60, P2:72
P1:72
NA
P1:LH
Lesion site
Followup (weeks)
Generalization of effects
↑verb naming; ↑noun naming maintained at FU ↑treated verb and treated noun naming, maintained at FU ↑verb naming; ↑verb production in sentences; ↑argument structure production
yes
Not assessed
trend
yes
trend
trend
none
trend for nouns
none
↑verb naming; ↑complex sentences production in P2: ↑verb naming; ↑noun naming; ↑complex sentence production ↑verb naming; ↑noun naming; ↑gesture production ↑treated verb naming; ↑treated noun naming; ↑communicative effectiveness ↑treated verb naming maintained at FU; ↑verbal productivity ↑verb naming; ↑noun naming
none
↑verb naming in P3 and P1
↑verb naming; trend ↑sentence production
Results
Notes: F = frontal; O = occipital; P = parietal; T = temporal; Th = thalamic; SCL = subcortical lesion; LH = left hemisphere; NA = not available; A = anomic aphasia; C = conduction aphasia; FL = fluent aphasia; NF = non-fluent aphasia; TM = transcortical motor; NC = not classified; PCT = phonological cueing treatment; SCT = semantic cueing treatment; SPT = semantic–phonological treatment, w = week; d = days; ↑: improvement. FU = follow-up after treatment end.
4
4
Thompson et al. (2013)
1
Wambaugh and Ferguson (2007) Edmonds et al. (2009)
4
8
Raymer et al. (2007)
Conroy and Scowcroft (2012)
9
Raymer et al. (2006)
2
P1:10, P2:96, P3:22, P4:21
2
Raymer and Kohen (2006)
Edmonds and Babb (2011)
P1: 50
1
Webster et al. (2005)
P1:43, P2: 22, P3:54
3
Wambaugh et al. (2002)
P1:12
1
Number of Time post-stroke (onset patients in months)
Review of the studies that applied verb anomia training in patients with aphasia.
Marshall et al. (1998)
Study
Table 1.
Downloaded by [Michigan State University] at 18:22 04 March 2015
Neurocase 111
Downloaded by [Michigan State University] at 18:22 04 March 2015
112
R. Manenti et al.
the opposite hemisphere, can facilitate motor recovery (Lefebvre et al., 2013; Lindenberg, Renga, Zhu, Nair, & Schlaug, 2010). In healthy young participants, right cathodal and left atDCS have been simultaneously applied over homologue posterior parietal cortices inducing neglect-like effects (Giglia et al., 2011). Moreover, another important issue is the optimal time to apply tDCS in relation to a neurorehabilitation protocol, i.e., online, concurrently with the training, or offline, before the training (Monti et al., 2013). The choice depends on the hypotheses about the neural mechanisms supporting the behavioral effects (Nitsche et al., 2003; Nitsche & Paulus, 2000; Nitsche et al., 2003b; Vines, Norton, & Schlaug, 2011; Volpato et al., 2013). Several studies have used online tDCS delivered during a language rehabilitation (Baker et al., 2010; Cotelli et al., 2011; Fiori et al., 2011; Floel et al., 2011; Fridriksson, Richardson, Baker, & Rorden, 2011; Kakuda, Abo, Uruma, Kaito, & Watanabe, 2010; Kang, Kim, Sohn, Cohen, & Paik, 2011; Martin et al., 2009; Naeser et al., 2010). The offline approach uses tDCS to prime the system at rest in preparation for a rehabilitation to be performed after stimulation (Holland & Crinion, 2012). The findings reported above suggest that the application of NIBS improves object-naming performance, but no study has investigated the effects of combining verb anomia training and tDCS in Patients with Aphasia (PWA) suffering from verb-naming deficits. In a previous single case report Finocchiaro et al. (2006) reported an improved ability to name verb pictures after the administration of rTMS over the prefrontal cortex in a patient with primary progressive aphasia. Starting with the SPT that seems to be useful in trainings aimed at improving the verb-naming abilities in patients with aphasia (Conroy & Scowcroft, 2012; Raymer et al., 2007), the present study reports the results of a combined tDCS and SPT approach administered to a PWA. Therefore, the main purpose of the present study was to investigate whether or not the application of off-line bihemispheric tDCS to the dorsolateral prefrontal cortex (DLPFC) (increasing left hemisphere activity and inhibiting right one) combined with SPT resulted in improvements of language performance in one PWA. We chose to apply tDCS before the language training on the basis of the encouraging results of our previous study highlighting an improvement of naming performance in patients with aphasia (Cotelli et al., 2011). More specifically, we hypothesized that this type of stimulation may lead to improved language production performance. In addition, an important goal of the present study was to verify whether the language benefits might persist after the end of the stimulation. Moreover, we investigated the possibility of inducing generalization effects of the treatment.
Figure 1. CT of the PWA. All the axial slices (thickness of 5 mm) in which a lesion was present are shown in a radiological convention (left side of brain is on the right).
Methods Case history The PWA was a 49-year-old right-handed female with 8 years of education. She had suffered a left middle cerebral artery infarction 8 months before entry into the study. The PWA underwent a neurological assessment, complete neuropsychological assessment, and a computerized tomography (CT) scan (see Figure 1) showing left frontal ipodensity consistent with the infarct of the left middle cerebral artery. The patient presented non-fluent speech, but no verbal dyspraxia. The abilities to understand single words, to repeat and read single words were preserved. She had little difficulty in naming objects but presented greater verb-naming deficits. She did not show clinical evidence of depression, clinical signs of hearing or vision impairment, or a past history of epilepsy, psychosis, major depression, alcohol abuse, and/or drug addiction. Moreover, the patient did not use psychopharmacological agents that could interfere with the test performance or diagnosis. The Local Human Ethics Committee approved the protocol.
Behavioral assessment The participant was assessed before the treatment (baseline), at the end of 4 weeks of the treatment, and at 12, 24, and 48 weeks follow-up evaluation (see Figure 2). Cognitive assessment included neuropsychological tests for non-verbal reasoning (Raven-colored progressive matrices) and verbal fluency (phonemic and semantic). All the tests were administered and scored according to standard procedures (Lezak, Howieson, & Loring, 2004). In addition, language functions were formally assessed with the full Italian version of the Aachener Aphasie Test (AAT) (Luzzatti et al., 1994) and with the object- and action-naming subtests, the comprehension and sentence comprehension subtests of the Battery for the Analysis of the Aphasic Deficit (BADA; (Miceli, Laudanna, Burani, & Capasso, 1994). Moreover, communication and functional abilities were tested using the
Downloaded by [Michigan State University] at 18:22 04 March 2015
Neurocase
113
Figure 2. Experimental therapy protocol of tDCS combined with individualized computerized verb anomia training. (a) bihemispheric tDCS was applied for 25 minutes before aphasia training (25 minutes). (b) Cognitive and experimental assessments were administered before the beginning of the 4-weeks treatment, after the end of the treatment, and 12, 24, and 48 weeks after the beginning.
Stroke and Aphasia Quality of Life Scale-39 – SAQOL39 (Lincoln, 1982; Posteraro et al., 2006). It consists of 39 items, divided into four subdomains (physical, communication, psychosocial, and energy). The maximum score for each subscale, and the total score is 5 (ranging from 0 to 5); a higher score indicates a higher quality of life. The neuropsychological and linguistic assessment is summarized in Table 2. Formal speech evaluation revealed deficits in repetition. International PictureNaming Task revealed selective difficulties with verb naming. Furthermore, an experimental task was applied to select the stimuli to be used during individualized speech therapy applied after transcranial stimulation. To select the stimuli for the individualized speech therapy and to test for generalization effects, the patient completed two oral-naming tasks. The oral-naming task was repeated on two consecutive days to ensure a stable baseline before introducing therapy and to select the therapy items. The stimuli for the oral-naming task were 129 black-andwhite 2-dimensional line drawings representing actions (Bates et al., 2000). Verbs were displayed using
Presentation software v. 12.0 (neurobehavioral systems: http://www.neurobs.com), with each picture being presented for a maximum of 10 seconds. The participant was asked to name each picture as accurately as possible, and her oral responses were recorded. The 58 stimuli that were incorrectly named in at least in one of the two naming sessions were included in the rehabilitation list. The rehabilitation list was further split into two sets (29 stimuli each): the “therapy” list, including the items to be treated (treated items), and the “control” list, with items that were not to be treated (untreated items). The two lists were balanced for a number of variables that can influence the participant’s performance; more specifically, these variables included the individual percentage of correctly named pictures during the two assessment sessions (one time, 50%, or never, 0%, across two sessions), the target word frequency, the number of syllables, and the number of letters. At the end of the procedure used to select the “therapy” and “control” lists, the participant obtained a personalized set of items, which ensured the within- and across-subject validity of the design. At the end of the treatment and at the follow-up visits, all treated and
114 Table 2.
R. Manenti et al. Clinical features and language assessments.
Downloaded by [Michigan State University] at 18:22 04 March 2015
Baseline Non-verbal reasoning Raven-colored progressive matrices 33/36 Verbal fluency Fluency-phonemic 9 Fluency-semantic 36 Aachener Aphasie Test (AAT) Token test (errors) 9/50 Repetition 132/150 Written language 86/90 Naming 118/120 Comprehension 111/120 Battery for the Analysis of the Aphasic Deficits (BADA) Sentence comprehension 55/60 Object-naming subtest 30/30 Verb-naming subtest 26/28 Object comprehension subtest 40/40 Verb comprehension subtest 20/20 Stroke and Aphasia Quality Of Life Scale-39 (SAQOL-39) Physical 3.7/5 Communication 3.6/5 Psychosocial/mood 3.4/5 Energy 3.3/5 Overall score 3.6/5 International Picture-Naming Project Task Verb naming 89/129 Object naming 345/349
4 weeks
12 weeks
24 weeks
48 weeks
34/36
34/36
34/36
35/36
15* 37
12* 35
8 35
19* 34
7/50 140/150 86/90 120/120 116/120
5/50 137/150 82/90 117/120 116/120
5/50 142/150 84/90 119/120 115/120
7/50 143/150 87/90 116/120 117/120
58/60 30/30 27/28 40/40 20/20
58/60 30/30 26/28 40/40 20/20
58/60 30/30 26/28 40/40 20/20
58/60 30/30 26/28 40/40 19/20
3.2/5 3.9/5 4.1/5 3.5/5 3.3/5
3.8/5 3.9/5 4.1/5 3.8/5 3.9/5
4.8/5 3.7/5 4.3/5 3.3/5 4.3/5
4.4/5 4.3/5 2.8/5 3.5/5 3.8/5
346/349
345/349
344/349
347/349
Notes: The score ranges from 0 (higher difficulties) to 5 (no difficulties) for Stroke and Aphasia Quality of Life Scale. Bold data indicate scores below cutoff. Asterisks indicate significant difference compared with Baseline assessment (Reliable Change Index-RCI, p-value < 0.05).
untreated items corresponding to the 4 weeks of the experiment were tested.
Verb anomia training The participant underwent 25 minutes of individualized speech therapy immediately following each tDCS treatment on a daily basis for four weeks. In general, the protocol incorporated a semantic–phonological question protocol (see Raymer et al. (2007)). The patient was seated in front of a computer screen in a quiet room while the individualized speech therapy protocol was displayed using Presentation software v. 12.0 (neurobehavioral systems: http://www.neurobs.com). The examiner presented the target verb and provided the correct verb for the participant to repeat three times. The verb was produced in the third person, present tense. With the picture remaining in front of the participant, the examiner then proceeded to a series of four questions with two alternatives. Two questions related to the semantic attributes of the target word, and two questions related to the phonologic attributes of the target word. The questions were counterbalanced across sessions such that 50% of the correct answers corresponded to the first alternative. See below for the detailed procedure of a rehabilitated stimulus.
Step 1 – Similarity question: Is the target picture similar to …..? (e.g. “Target: to Close”, Is it similar to fasten or to play?). Step 2 – Associate question: Does the target verb have to do with …. or with ….? In this case, the associate word was always a noun (e.g. “Target: to Close”, Does it have to do with melon or with jacket?). Step 3 – Initial phoneme question: Does the target word start with …. or with ….? (e.g. “Target: to Close”, Does it start with /cl/ or with /pr/?). Step 4 – Rhyme question: Does the target word sound like …. or like ….? (e.g. “Target: to Close”, Does it sound like table or like nose?). Step 5 – At the end of the semantic–phonological questions, a sentence completion was requested (e.g. “Target: to Close”, He ….. the zipper.). In the case of any mistake during the procedure, the trial was repeated after Step 5.
tDCS We selected the DLPFC as a target area due to the beneficial effects obtained after stimulation of this area combined with object-naming training in PWAs in our
Downloaded by [Michigan State University] at 18:22 04 March 2015
Neurocase previous study (Cotelli et al., 2011). We decided to apply atDCS over the lesional hemisphere to facilitate the activity of the left hemisphere, combined with cathodal tDCS over the contralesional hemisphere with the aim of inhibiting maladaptive overactivation in the right hemisphere (Baker et al., 2010; Cotelli et al., 2011; Floel et al., 2011; Kang et al., 2011; You, Kim, Chun, Jung, & Park, 2011). We apply off-line tDCS approach in which tDCS was delivered before verb anomia training (see Figure 2). The patient received 4 weeks of bihemispheric tDCS of the DLPFC combined with individualized speech therapy. Each week of the tDCS treatment consisted of five sessions that comprised a total of 50 minutes/day (25 minutes of tDCS followed by 25 minutes of individualized speech therapy). See Figure 2 for the study design. The stimulation was delivered by a battery-driven constant current stimulator (neuroConn GmbH, Ilmenau, Germany) through a pair of saline-soaked sponge electrodes (7 × 5 cm). A constant current of 2 mA was applied for 25 minutes (current density 0.057 mA/cm2), with a ramping period of 10 seconds both at the beginning and at the end of the stimulation. The electrodes were kept firm by elastic bands, and an electroconductive gel was applied under the electrodes before the montage to reduce contact impedance. The anodal electrode was placed on the left DLPFC, whereas the cathodal electrode was placed over the right DLPFC.
Results An improvement in the linguistic functional skills was recorded exclusively in psychosocial/mood (baseline: 3.4, 4 weeks: 4.1) and communication (baseline: 3.6, 4
115
weeks: 3.9) subscales of the SAQOL-39. No changes were shown in the energy and physical subscales. The patient did not show any change in Raven-colored progressive matrices, semantic fluency, AAT subtests, and BADA subtests. After training we found an improvement in phonemic fluency (4 weeks vs. baseline: Reliable Change Index-RCI = 10.6; 12 weeks vs. baseline: Reliable Change Index-RCI = 5.3; 48 weeks vs. baseline: Reliable Change Index-RCI = 17.7) (Eisen, Ranganathan, Seal, & Spiro 3rd, 2007; Jacobson & Truax, 1991). See Table 2 for details. Significant effects were found for the experimental verb-naming task. We calculated the percentage of correct responses at baseline for the therapy and control lists, respectively. The correct percentage at baseline corresponds to the number of items correctly named in one out of the two naming assessment sessions, divided by two, and then divided by the total number of items in the list (both the therapy and control lists included the same number of items), multiplied by 100. To assess the improvement of the patient, we compared the baseline with the performances after 4, 12, 24, and 48 weeks using χ2 comparisons that were Yates-corrected for the naming of both the treated and the untreated items. Additionally, to examine the generalization of the effects to untreated items, we compared the accuracy scores for the trained and untrained items for each time-point using Yates-corrected χ2 comparisons. Regarding the experimental naming, for both the treated and untreated items, the participant showed improvement after four weeks of treatment, compared to baseline. Moreover, both of these improvements were still significant at 12, 24, and 48 weeks. In the comparison between the treated and untreated items, the patient showed a greater improvement with the treated items compared to the
Figure 3. Accuracy acquired in verb naming plotted separately for treated and untreated stimuli. Performances recorded at baseline, 4, 12, 24, and 48 weeks are displayed. Asterisks indicate significant differences (p < 0.05).
116 Table 3.
R. Manenti et al. Experimental verb naming at all time-points for the treated and untreated items. Treated items Correctness %
Baseline 4 weeks 12 weeks 24 weeks 48 weeks
31 97 83 93 93
Untreated items
Comparison with baseline χ2 χ2 χ2 χ2
= = = =
91.69, 53.06, 78.97, 78.97,
p p p p
< < <
Neurocase: The Neural Basis of Cognition Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/nncs20
Efficacy of semantic–phonological treatment combined with tDCS for verb retrieval in a patient with aphasia a
a
ab
a
c
Rosa Manenti , Michela Petesi , Michela Brambilla , Sandra Rosini , Antonio Miozzo , cd
ad
Alessandro Padovani , Carlo Miniussi
a
& Maria Cotelli
a
IRCCS Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy
b
Center for Cognitive Science, Department of Psychology, University of Turin, Turin, Italy
c
Centre for Brain Aging and Neurodegenerative Disorders, Neurology Unit, University of Brescia, Brescia, Italy d
Click for updates
Department of Clinical and Experimental Sciences, National Neuroscience Institute, University of Brescia, Brescia, Italy Published online: 13 Jan 2014.
To cite this article: Rosa Manenti, Michela Petesi, Michela Brambilla, Sandra Rosini, Antonio Miozzo, Alessandro Padovani, Carlo Miniussi & Maria Cotelli (2015) Efficacy of semantic–phonological treatment combined with tDCS for verb retrieval in a patient with aphasia, Neurocase: The Neural Basis of Cognition, 21:1, 109-119, DOI: 10.1080/13554794.2013.873062 To link to this article: http://dx.doi.org/10.1080/13554794.2013.873062
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions
Neurocase, 2015 Vol. 21, No. 1, 109–119, http://dx.doi.org/10.1080/13554794.2013.873062
Efficacy of semantic–phonological treatment combined with tDCS for verb retrieval in a patient with aphasia Rosa Manentia, Michela Petesia, Michela Brambillaa,b, Sandra Rosinia, Antonio Miozzoc, Alessandro Padovanic,d, Carlo Miniussia,d and Maria Cotellia* a
IRCCS Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy; bCenter for Cognitive Science, Department of Psychology, University of Turin, Turin, Italy; cCentre for Brain Aging and Neurodegenerative Disorders, Neurology Unit, University of Brescia, Brescia, Italy; dDepartment of Clinical and Experimental Sciences, National Neuroscience Institute, University of Brescia, Brescia, Italy
Downloaded by [Michigan State University] at 18:22 04 March 2015
(Received 8 May 2013; accepted 15 November 2013) Recent studies reported enhanced performance on language tasks induced by transcranial direct current stimulation (tDCS) in patients with aphasia. One chronic patient with non-fluent aphasia received 20 sessions of a verb anomia training combined with off-line bihemispheric tDCS applied to the dorsolateral prefrontal cortex (DLPFC) – anodal tDCS over left DLPFC plus cathodal tDCS over right DLPFC. A significant improvement in verb naming was observed at all testing times (4, 12, 24, and 48 weeks from post-entry/baseline testing) for treated and untreated verbs. Our findings show beneficial effects of verb anomia training in combination with tDCS in chronic aphasic patient, suggesting a long-lasting effect of this treatment. Keywords: non-invasive brain stimulation; naming; speech therapy
Neuropsychological investigations reported selective impairments in the production and comprehension of verbs in agrammatic aphasic patients. Verbs have been repeatedly investigated as distinct from nouns (i.e. objects) in patients with aphasia (see, for example, Caramazza and Hillis (1991)). Regarding object and action processing differences, several clinical observations have suggested that different cerebral areas are involved in the processing of nouns and verbs. A double dissociation between noun- and verbnaming performance in single cases has been reported (Miceli, Silveri, Nocentini, & Caramazza, 1988). Patients with a selective disorder for object naming usually have lesions centered in the left temporal lobe; conversely, a selective impairment in verb naming has been associated with larger lesions, usually extending to the left frontal cortex (Daniele, Giustolisi, Silveri, Colosimo, & Gainotti, 1994). Various studies have convincingly demonstrated that the lexical system is organized according to grammatical class. Furthermore, Damasio and colleagues suggested that mediation systems for verbs may be located at frontal and parietal sites (Damasio & Damasio, 1992; Damasio & Tranel, 1993). In addition to patient studies, functional imaging studies have also provided evidence for selective activations associated with noun and verb processing in healthy subjects (Perani et al., 1999; Shapiro, Moo, & Caramazza, 2006). In particular, verb naming seems to evoke stronger bilateral activation in the posterior middle-temporal cortex, *Corresponding author. Email: [email protected] © 2014 Taylor & Francis
at the left temporo–parietal junction and in the left frontal cortex compared to object naming (Liljeström et al., 2008). Although considerable work has been performed to investigate the relationship between impairments in verb naming and aphasia type (Miceli et al., 1988; Miceli, Silveri, Villa, & Caramazza, 1984), fewer studies have examined the effectiveness of treatments for impairments in verb naming (for a review, see Conroy, Sage, and Lambon Ralph (2006)). First, Marshall, Pring, and Chiat (1998) described a therapeutic approach in a post-stroke subject with a selective verb-retrieval deficit. Using comprehension, reading, and naming tasks, the authors encouraged the subject to process the semantics and the phonology of the targets to induce better verb retrieval, improving sentence production for the treated verbs, without a significant generalization of untreated items. Subsequently, two treatments were used to treat three patients with aphasia: phonological cueing treatment and semantic cueing treatment. These treatments resulted in an improvement in object naming in a previous study (Wambaugh, Doyle, Martinez, & Kalinyak-Fliszar, 2002). The authors aimed to verify the usefulness of these training techniques on verb naming, and they concluded that both treatments may potentially be applied to the retrieval of verbs and suggested further investigations (Wambaugh et al., 2002). Recently, semantic training has been tested by the same group in an individual with anomic aphasia (Wambaugh & Ferguson, 2007), demonstrating
Downloaded by [Michigan State University] at 18:22 04 March 2015
110
R. Manenti et al.
an increased performance with the trained verbs that was maintained at 6 weeks, but a lack of generalization to untreated verbs. Along the same line, Webster, Morris, and Franklin (2005) showed that a training technique that includes semantic, sentence completion, thematic roles, and sentence-generation tasks could induce an improvement in the retrieval of treated verbs in a patient with aphasia (PWA), but generalization was not evident. Accordingly, using sentence-based word retrieval training, Raymer and Kohen (2006) investigated the improvements in word and verb retrieval in one patient with non-fluent aphasia and one patient with fluent aphasia. The researchers reported that improvements were found only for nonfluent aphasia patients and that noun therapy is more efficacious than verb therapy. In addition, the same group showed that a gesture plus verbal treatment could have the potential to improve communication in nine patients with aphasia (Raymer et al., 2006). Furthermore, a verb-strengthening treatment was investigated in four patients with aphasia, indicating an effect on treated items and generalization to untreated verbs (Edmonds, Nadeau, & Kiran, 2009). Interestingly, Raymer et al. (2007) applied a semantic–phonological treatment (SPT) in eight post-stroke patients with a naming disorder showing an improvement in naming treated images and a minimal, but not significant, effect for untreated items. In this vein, a recent study investigated the beneficial effects of a repetition, orthographic and phonological treatment (decreasing cues) on noun and verb naming in four participants with aphasia (Conroy & Scowcroft, 2012). The data confirmed an improvement in the naming abilities after the treatment, but no evident generalization to untreated items. In a recent work the authors emphasized that argument structure and thematic role mapping training is effective for improving verb and sentence production in agrammatic post-stroke patients (Thompson, Riley, den Ouden, Meltzer-Asscher, & Lukic, 2013). Remarkably, the post-training improvement also resulted in a generalization to untrained verbs. See Table 1 for a review. There is increasing interest in the potential enhancement of cognitive rehabilitative treatment based on the non-invasive brain stimulation (NIBS) techniques, i.e. repetitive transcranial magnetic stimulation (rTMS) or transcranial direct current stimulation (tDCS), applied to specific cortical areas (Miniussi et al., 2008). Facilitation effects have been observed in patients with stroke and dementia when performing a variety of cognitive tasks. Specifically, in chronic aphasia patients, NIBS has been shown to increase the number of correct responses and to reduce the response times, with effects that can persist over time (for a review see Cotelli et al., 2011). Specifically, the potential of rTMS or tDCS to trigger adaptive neuroplasticity in neurological patients has been
related to three main mechanisms: (1) the reactivation of canonical networks, partly damaged or made dysfunctional by the cerebral lesion; (2) the recruitment of compensatory networks, mostly contralateral homologue cortical regions; (3) the additional recruitment of perilesional sub-optimally functioning areas (Miniussi & Rossini, 2011). In patients with aphasia following stroke, right-hemisphere overactivation has been explained by some authors as a “maladaptive” plasticity, which prevents recovery from aphasia (hemispheric competition hypothesis). Contralesional areas continue to play a role that is dysfunctional rather than compensatory in chronic aphasia in patients who have experienced a significant degree of recovery (Postman-Caucheteux et al., 2010). Following this line of reasoning, stimulation techniques have been used both for enhancing left hemisphere activity and reducing right one. There was a great debate in last few years about the significance of controlesional and/or ipsilateral areas activity in patients with post-stroke aphasia (Heiss & Thiel, 2006; Richter, Miltner, & Straube, 2008). Thiel et al. (2006) concluded that time of progression of brain lesions would be the factor which determines successful integration of the right hemisphere into the language network for compensation of lost left hemisphere language function. Following these results, patients with post-stroke aphasia characterized by a fast progression of the lesion would be reasonably characterized, as suggested by Postman-Caucheteux et al. (2010), by a dysfunctional rather than compensatory activity in the contralasional hemisphere. Size of the stroke is the most important factor in establishing whether the right hemisphere contributes beneficially reorganizing the language network in poststroke recovery or not (Torres, Drebing, & Hamilton, 2013). Patients that reported small lesions preferentially recruit left hemisphere perilesional areas without a beneficial involvement of the right hemisphere. In this case it is reasonable to apply excitatory tDCS to left hemisphere regions or/and cathodal tDCS to right hemisphere to inhibit maladaptive overactivation. It has been suggested that NIBS treatment protocol would be modified based on patient characteristics such as stroke size, location, and chronicity (Torres et al., 2013). Regarding tDCS, anodal tDCS (atDCS) has a general facilitation effect and causes membrane depolarization, whereas cathodal tDCS has a general inhibitory effect and causes membrane hyperpolarization (Liebetanz, Nitsche, Tergau, & Paulus, 2002). Both anodal and cathodal stimulation applied over the lesional (i.e. left) hemisphere and cathodal tDCS applied over the contralesional (i.e., right) hemisphere have been shown to improve comprehension and naming in post-stroke aphasia patients (Baker, Rorden, & Fridriksson, 2010). Recent studies in people with chronic stroke have shown that bihemispheric tDCS, where an anode is positioned over the affected region, and the cathode is located in
P1:LH TP, P2:LH FSCL
NA
P1:FL, P2:NF
P1:NF
P1:NF, P2:NF, P3:NC
P1:NF
Type of aphasia Comprehension, reading, and action naming; 1200’ in 14 w P1:SCT, P2: PCT, P3:SCT plus PCT; 5–20 sessions, 2–3 d/w Verb retrieval plus predicate argument structure knowledge; 30 45’ sessions, 3 d/w Sentence embedded word retrieval (nouns and verbs); 3–10 60’ sessions, 2 d/w
Therapy approach
none
none
none
none
from 18 to 180
P1:8, P2:51, P3:10, P4:99
P1:49, P2:9
P1:NF, P2:NF
P1:TM, P2:TM; P3:C, P4:C
P1: A
P1:LH FTP, P2:LH FTP, P3:LH FT, P4: LH FT
P1:NF, P2:NF, P3:NF, P4:NF
P1:LH FT, P2:LH FSCL, P3:LH FT, P4: P1:NF, P2:A, P3:A, LH F P4:NF
P1: LH TP, P2: LH FSCL
P1:LH, P2:LH, P3:LH, P4:LH
P1: LH P
none
Verb network strengthening; 120’ sessions, 2 d/w, till criterion Verb network strengthening; 24–30 120’ sessions, 2 d/w
Verb argument structure none training; 90’ sessions, 2 d/w, till criterion
Vanishing orthographic and 8 phonological cue; 10 30–40’ sessions, 1 d/w
20
6
Semantic feature training; 12 45–60’ sessions, 3 d/w
P1:5, P2:16, P3:52, P1:LH TP, P2:LH TO Th, P3:LH FP, P4: P1:C, P2:NF, P3:NF, P4: Gesture plus verbal training none P4:17, P5:7, P6:18, LH TP, P5:LH P, P6:LH FTP, P7: LH NF, P5:NF, P6:NF, (nouns and verbs); 10 60’ P7:62, P8:43, P9:41 FSCL, P8: LH TP, P9:LH TP P7:NF, P8:FL, P9:FL sessions, 2–3 d/w P1: LH FT, P2: LH FSCL, P3: LH FT, P1: NF, P2: NF, P3:NF, SPT; 10 60’ sessions, 2–3 d/w 5 P1:93, P2 52, P3:75, P4:49, P5:120, P4: LH F, P5: LH FT, P6: LH FT, P7: P4:NF, P5:NF, P6:NF, P6:48, P7:4, P8:9 LH P, P8: LH F P7:FL, P8:A
P1:60, P2:72
P1:72
NA
P1:LH
Lesion site
Followup (weeks)
Generalization of effects
↑verb naming; ↑noun naming maintained at FU ↑treated verb and treated noun naming, maintained at FU ↑verb naming; ↑verb production in sentences; ↑argument structure production
yes
Not assessed
trend
yes
trend
trend
none
trend for nouns
none
↑verb naming; ↑complex sentences production in P2: ↑verb naming; ↑noun naming; ↑complex sentence production ↑verb naming; ↑noun naming; ↑gesture production ↑treated verb naming; ↑treated noun naming; ↑communicative effectiveness ↑treated verb naming maintained at FU; ↑verbal productivity ↑verb naming; ↑noun naming
none
↑verb naming in P3 and P1
↑verb naming; trend ↑sentence production
Results
Notes: F = frontal; O = occipital; P = parietal; T = temporal; Th = thalamic; SCL = subcortical lesion; LH = left hemisphere; NA = not available; A = anomic aphasia; C = conduction aphasia; FL = fluent aphasia; NF = non-fluent aphasia; TM = transcortical motor; NC = not classified; PCT = phonological cueing treatment; SCT = semantic cueing treatment; SPT = semantic–phonological treatment, w = week; d = days; ↑: improvement. FU = follow-up after treatment end.
4
4
Thompson et al. (2013)
1
Wambaugh and Ferguson (2007) Edmonds et al. (2009)
4
8
Raymer et al. (2007)
Conroy and Scowcroft (2012)
9
Raymer et al. (2006)
2
P1:10, P2:96, P3:22, P4:21
2
Raymer and Kohen (2006)
Edmonds and Babb (2011)
P1: 50
1
Webster et al. (2005)
P1:43, P2: 22, P3:54
3
Wambaugh et al. (2002)
P1:12
1
Number of Time post-stroke (onset patients in months)
Review of the studies that applied verb anomia training in patients with aphasia.
Marshall et al. (1998)
Study
Table 1.
Downloaded by [Michigan State University] at 18:22 04 March 2015
Neurocase 111
Downloaded by [Michigan State University] at 18:22 04 March 2015
112
R. Manenti et al.
the opposite hemisphere, can facilitate motor recovery (Lefebvre et al., 2013; Lindenberg, Renga, Zhu, Nair, & Schlaug, 2010). In healthy young participants, right cathodal and left atDCS have been simultaneously applied over homologue posterior parietal cortices inducing neglect-like effects (Giglia et al., 2011). Moreover, another important issue is the optimal time to apply tDCS in relation to a neurorehabilitation protocol, i.e., online, concurrently with the training, or offline, before the training (Monti et al., 2013). The choice depends on the hypotheses about the neural mechanisms supporting the behavioral effects (Nitsche et al., 2003; Nitsche & Paulus, 2000; Nitsche et al., 2003b; Vines, Norton, & Schlaug, 2011; Volpato et al., 2013). Several studies have used online tDCS delivered during a language rehabilitation (Baker et al., 2010; Cotelli et al., 2011; Fiori et al., 2011; Floel et al., 2011; Fridriksson, Richardson, Baker, & Rorden, 2011; Kakuda, Abo, Uruma, Kaito, & Watanabe, 2010; Kang, Kim, Sohn, Cohen, & Paik, 2011; Martin et al., 2009; Naeser et al., 2010). The offline approach uses tDCS to prime the system at rest in preparation for a rehabilitation to be performed after stimulation (Holland & Crinion, 2012). The findings reported above suggest that the application of NIBS improves object-naming performance, but no study has investigated the effects of combining verb anomia training and tDCS in Patients with Aphasia (PWA) suffering from verb-naming deficits. In a previous single case report Finocchiaro et al. (2006) reported an improved ability to name verb pictures after the administration of rTMS over the prefrontal cortex in a patient with primary progressive aphasia. Starting with the SPT that seems to be useful in trainings aimed at improving the verb-naming abilities in patients with aphasia (Conroy & Scowcroft, 2012; Raymer et al., 2007), the present study reports the results of a combined tDCS and SPT approach administered to a PWA. Therefore, the main purpose of the present study was to investigate whether or not the application of off-line bihemispheric tDCS to the dorsolateral prefrontal cortex (DLPFC) (increasing left hemisphere activity and inhibiting right one) combined with SPT resulted in improvements of language performance in one PWA. We chose to apply tDCS before the language training on the basis of the encouraging results of our previous study highlighting an improvement of naming performance in patients with aphasia (Cotelli et al., 2011). More specifically, we hypothesized that this type of stimulation may lead to improved language production performance. In addition, an important goal of the present study was to verify whether the language benefits might persist after the end of the stimulation. Moreover, we investigated the possibility of inducing generalization effects of the treatment.
Figure 1. CT of the PWA. All the axial slices (thickness of 5 mm) in which a lesion was present are shown in a radiological convention (left side of brain is on the right).
Methods Case history The PWA was a 49-year-old right-handed female with 8 years of education. She had suffered a left middle cerebral artery infarction 8 months before entry into the study. The PWA underwent a neurological assessment, complete neuropsychological assessment, and a computerized tomography (CT) scan (see Figure 1) showing left frontal ipodensity consistent with the infarct of the left middle cerebral artery. The patient presented non-fluent speech, but no verbal dyspraxia. The abilities to understand single words, to repeat and read single words were preserved. She had little difficulty in naming objects but presented greater verb-naming deficits. She did not show clinical evidence of depression, clinical signs of hearing or vision impairment, or a past history of epilepsy, psychosis, major depression, alcohol abuse, and/or drug addiction. Moreover, the patient did not use psychopharmacological agents that could interfere with the test performance or diagnosis. The Local Human Ethics Committee approved the protocol.
Behavioral assessment The participant was assessed before the treatment (baseline), at the end of 4 weeks of the treatment, and at 12, 24, and 48 weeks follow-up evaluation (see Figure 2). Cognitive assessment included neuropsychological tests for non-verbal reasoning (Raven-colored progressive matrices) and verbal fluency (phonemic and semantic). All the tests were administered and scored according to standard procedures (Lezak, Howieson, & Loring, 2004). In addition, language functions were formally assessed with the full Italian version of the Aachener Aphasie Test (AAT) (Luzzatti et al., 1994) and with the object- and action-naming subtests, the comprehension and sentence comprehension subtests of the Battery for the Analysis of the Aphasic Deficit (BADA; (Miceli, Laudanna, Burani, & Capasso, 1994). Moreover, communication and functional abilities were tested using the
Downloaded by [Michigan State University] at 18:22 04 March 2015
Neurocase
113
Figure 2. Experimental therapy protocol of tDCS combined with individualized computerized verb anomia training. (a) bihemispheric tDCS was applied for 25 minutes before aphasia training (25 minutes). (b) Cognitive and experimental assessments were administered before the beginning of the 4-weeks treatment, after the end of the treatment, and 12, 24, and 48 weeks after the beginning.
Stroke and Aphasia Quality of Life Scale-39 – SAQOL39 (Lincoln, 1982; Posteraro et al., 2006). It consists of 39 items, divided into four subdomains (physical, communication, psychosocial, and energy). The maximum score for each subscale, and the total score is 5 (ranging from 0 to 5); a higher score indicates a higher quality of life. The neuropsychological and linguistic assessment is summarized in Table 2. Formal speech evaluation revealed deficits in repetition. International PictureNaming Task revealed selective difficulties with verb naming. Furthermore, an experimental task was applied to select the stimuli to be used during individualized speech therapy applied after transcranial stimulation. To select the stimuli for the individualized speech therapy and to test for generalization effects, the patient completed two oral-naming tasks. The oral-naming task was repeated on two consecutive days to ensure a stable baseline before introducing therapy and to select the therapy items. The stimuli for the oral-naming task were 129 black-andwhite 2-dimensional line drawings representing actions (Bates et al., 2000). Verbs were displayed using
Presentation software v. 12.0 (neurobehavioral systems: http://www.neurobs.com), with each picture being presented for a maximum of 10 seconds. The participant was asked to name each picture as accurately as possible, and her oral responses were recorded. The 58 stimuli that were incorrectly named in at least in one of the two naming sessions were included in the rehabilitation list. The rehabilitation list was further split into two sets (29 stimuli each): the “therapy” list, including the items to be treated (treated items), and the “control” list, with items that were not to be treated (untreated items). The two lists were balanced for a number of variables that can influence the participant’s performance; more specifically, these variables included the individual percentage of correctly named pictures during the two assessment sessions (one time, 50%, or never, 0%, across two sessions), the target word frequency, the number of syllables, and the number of letters. At the end of the procedure used to select the “therapy” and “control” lists, the participant obtained a personalized set of items, which ensured the within- and across-subject validity of the design. At the end of the treatment and at the follow-up visits, all treated and
114 Table 2.
R. Manenti et al. Clinical features and language assessments.
Downloaded by [Michigan State University] at 18:22 04 March 2015
Baseline Non-verbal reasoning Raven-colored progressive matrices 33/36 Verbal fluency Fluency-phonemic 9 Fluency-semantic 36 Aachener Aphasie Test (AAT) Token test (errors) 9/50 Repetition 132/150 Written language 86/90 Naming 118/120 Comprehension 111/120 Battery for the Analysis of the Aphasic Deficits (BADA) Sentence comprehension 55/60 Object-naming subtest 30/30 Verb-naming subtest 26/28 Object comprehension subtest 40/40 Verb comprehension subtest 20/20 Stroke and Aphasia Quality Of Life Scale-39 (SAQOL-39) Physical 3.7/5 Communication 3.6/5 Psychosocial/mood 3.4/5 Energy 3.3/5 Overall score 3.6/5 International Picture-Naming Project Task Verb naming 89/129 Object naming 345/349
4 weeks
12 weeks
24 weeks
48 weeks
34/36
34/36
34/36
35/36
15* 37
12* 35
8 35
19* 34
7/50 140/150 86/90 120/120 116/120
5/50 137/150 82/90 117/120 116/120
5/50 142/150 84/90 119/120 115/120
7/50 143/150 87/90 116/120 117/120
58/60 30/30 27/28 40/40 20/20
58/60 30/30 26/28 40/40 20/20
58/60 30/30 26/28 40/40 20/20
58/60 30/30 26/28 40/40 19/20
3.2/5 3.9/5 4.1/5 3.5/5 3.3/5
3.8/5 3.9/5 4.1/5 3.8/5 3.9/5
4.8/5 3.7/5 4.3/5 3.3/5 4.3/5
4.4/5 4.3/5 2.8/5 3.5/5 3.8/5
346/349
345/349
344/349
347/349
Notes: The score ranges from 0 (higher difficulties) to 5 (no difficulties) for Stroke and Aphasia Quality of Life Scale. Bold data indicate scores below cutoff. Asterisks indicate significant difference compared with Baseline assessment (Reliable Change Index-RCI, p-value < 0.05).
untreated items corresponding to the 4 weeks of the experiment were tested.
Verb anomia training The participant underwent 25 minutes of individualized speech therapy immediately following each tDCS treatment on a daily basis for four weeks. In general, the protocol incorporated a semantic–phonological question protocol (see Raymer et al. (2007)). The patient was seated in front of a computer screen in a quiet room while the individualized speech therapy protocol was displayed using Presentation software v. 12.0 (neurobehavioral systems: http://www.neurobs.com). The examiner presented the target verb and provided the correct verb for the participant to repeat three times. The verb was produced in the third person, present tense. With the picture remaining in front of the participant, the examiner then proceeded to a series of four questions with two alternatives. Two questions related to the semantic attributes of the target word, and two questions related to the phonologic attributes of the target word. The questions were counterbalanced across sessions such that 50% of the correct answers corresponded to the first alternative. See below for the detailed procedure of a rehabilitated stimulus.
Step 1 – Similarity question: Is the target picture similar to …..? (e.g. “Target: to Close”, Is it similar to fasten or to play?). Step 2 – Associate question: Does the target verb have to do with …. or with ….? In this case, the associate word was always a noun (e.g. “Target: to Close”, Does it have to do with melon or with jacket?). Step 3 – Initial phoneme question: Does the target word start with …. or with ….? (e.g. “Target: to Close”, Does it start with /cl/ or with /pr/?). Step 4 – Rhyme question: Does the target word sound like …. or like ….? (e.g. “Target: to Close”, Does it sound like table or like nose?). Step 5 – At the end of the semantic–phonological questions, a sentence completion was requested (e.g. “Target: to Close”, He ….. the zipper.). In the case of any mistake during the procedure, the trial was repeated after Step 5.
tDCS We selected the DLPFC as a target area due to the beneficial effects obtained after stimulation of this area combined with object-naming training in PWAs in our
Downloaded by [Michigan State University] at 18:22 04 March 2015
Neurocase previous study (Cotelli et al., 2011). We decided to apply atDCS over the lesional hemisphere to facilitate the activity of the left hemisphere, combined with cathodal tDCS over the contralesional hemisphere with the aim of inhibiting maladaptive overactivation in the right hemisphere (Baker et al., 2010; Cotelli et al., 2011; Floel et al., 2011; Kang et al., 2011; You, Kim, Chun, Jung, & Park, 2011). We apply off-line tDCS approach in which tDCS was delivered before verb anomia training (see Figure 2). The patient received 4 weeks of bihemispheric tDCS of the DLPFC combined with individualized speech therapy. Each week of the tDCS treatment consisted of five sessions that comprised a total of 50 minutes/day (25 minutes of tDCS followed by 25 minutes of individualized speech therapy). See Figure 2 for the study design. The stimulation was delivered by a battery-driven constant current stimulator (neuroConn GmbH, Ilmenau, Germany) through a pair of saline-soaked sponge electrodes (7 × 5 cm). A constant current of 2 mA was applied for 25 minutes (current density 0.057 mA/cm2), with a ramping period of 10 seconds both at the beginning and at the end of the stimulation. The electrodes were kept firm by elastic bands, and an electroconductive gel was applied under the electrodes before the montage to reduce contact impedance. The anodal electrode was placed on the left DLPFC, whereas the cathodal electrode was placed over the right DLPFC.
Results An improvement in the linguistic functional skills was recorded exclusively in psychosocial/mood (baseline: 3.4, 4 weeks: 4.1) and communication (baseline: 3.6, 4
115
weeks: 3.9) subscales of the SAQOL-39. No changes were shown in the energy and physical subscales. The patient did not show any change in Raven-colored progressive matrices, semantic fluency, AAT subtests, and BADA subtests. After training we found an improvement in phonemic fluency (4 weeks vs. baseline: Reliable Change Index-RCI = 10.6; 12 weeks vs. baseline: Reliable Change Index-RCI = 5.3; 48 weeks vs. baseline: Reliable Change Index-RCI = 17.7) (Eisen, Ranganathan, Seal, & Spiro 3rd, 2007; Jacobson & Truax, 1991). See Table 2 for details. Significant effects were found for the experimental verb-naming task. We calculated the percentage of correct responses at baseline for the therapy and control lists, respectively. The correct percentage at baseline corresponds to the number of items correctly named in one out of the two naming assessment sessions, divided by two, and then divided by the total number of items in the list (both the therapy and control lists included the same number of items), multiplied by 100. To assess the improvement of the patient, we compared the baseline with the performances after 4, 12, 24, and 48 weeks using χ2 comparisons that were Yates-corrected for the naming of both the treated and the untreated items. Additionally, to examine the generalization of the effects to untreated items, we compared the accuracy scores for the trained and untrained items for each time-point using Yates-corrected χ2 comparisons. Regarding the experimental naming, for both the treated and untreated items, the participant showed improvement after four weeks of treatment, compared to baseline. Moreover, both of these improvements were still significant at 12, 24, and 48 weeks. In the comparison between the treated and untreated items, the patient showed a greater improvement with the treated items compared to the
Figure 3. Accuracy acquired in verb naming plotted separately for treated and untreated stimuli. Performances recorded at baseline, 4, 12, 24, and 48 weeks are displayed. Asterisks indicate significant differences (p < 0.05).
116 Table 3.
R. Manenti et al. Experimental verb naming at all time-points for the treated and untreated items. Treated items Correctness %
Baseline 4 weeks 12 weeks 24 weeks 48 weeks
31 97 83 93 93
Untreated items
Comparison with baseline χ2 χ2 χ2 χ2
= = = =
91.69, 53.06, 78.97, 78.97,
p p p p
< < <
