European Journal of Neuroscience
European Journal of Neuroscience, Vol. 38, pp. 3513–3518, 2013
doi:10.1111/ejn.12344
COGNITIVE NEUROSCIENCE
Anodal transcranial direct current stimulation over the supramarginal gyrus facilitates pitch memory Nora K. Schaal,1,2 Victoria J. Williamson1 and Michael J. Banissy1,3 1
Department of Psychology, Goldsmiths, University of London, London, UK € t Du €tsstraße 1, Du €r Experimentelle Psychologie, Heinrich-Heine-Universita €sseldorf, Universita €sseldorf 40225, Germany Institut fu 3 Institute of Cognitive Neuroscience, University College London, London, UK 2
Keywords: cognitive psychology, music perception, non-invasive brain stimulation, recognition and recall, short-term memory for pitch
Abstract Functional neuroimaging studies have shown activation of the supramarginal gyrus during pitch memory tasks. A previous transcranial direct current stimulation study using cathodal stimulation over the left supramarginal gyrus reported a detrimental effect on short-term pitch memory performance, indicating an important role of the supramarginal gyrus in pitch memory. The current study aimed to determine whether pitch memory could be improved following anodal stimulation of the left supramarginal gyrus. The performances of non-musicians on two pitch memory tasks (pitch recognition and recall) and a visual memory control task following anodal or sham transcranial direct current stimulation were compared. The results show that, post-stimulation, the anodal group but not the control group performed significantly better on both pitch memory tasks; performance did not differ on the face memory task. These findings provide strong support for the causal involvement of the left supramarginal gyrus in the pitch memory process, and highlight the potential efficacy of transcranial direct current stimulation as a tool to improve pitch memory.
Introduction Memory for relative pitch across an emerging melody plays a key role in online music perception. Several brain areas are involved in the process of working memory, with functional imaging studies emphasizing the importance of frontal, temporal and parietal brain areas [for reviews, see Baddeley (2003) and Bor et al. (2003)]. Pitch memory processes are known to engage similar regions (Zatorre et al., 1994; Koelsch et al., 2009; Jerde et al., 2011), and one neural region in particular that has commonly been implicated in neuroimaging studies of pitch memory is the supramarginal gyrus (SMG). Gaab et al. (2003) showed that pitch memory recruits a network of neural regions, including the superior temporal gyri, bilateral posterior dorsolateral frontal regions, bilateral superior parietal regions, bilateral lobes V and VI of the cerebellum, the supramarginal gyri, and the left inferior frontal gyrus. The activation of the left SMG was of special interest, as the results revealed a significant correlation between the level of functional activation and task performance (with higher levels of activation being linked to superior task performance) (Gaab et al., 2003). Further evidence of the crucial and particular role of the left SMG for pitch memory was found in another study showing increased activation after 5 days of training of pitch memory in ‘strong learners’ as compared with ‘weak learners’ or participants with no training (Gaab et al., 2006).
Correspondence: Nora K. Schaal, 2Institut f€ur Experimentellen Psychologie, as above. E-mail:
[email protected] Received 4 February 2013, revised 22 July 2013, accepted 24 July 2013
Overall, these results strongly suggest that the left SMG is involved in the storage of short-term memory for pitch information. Although functional magnetic resonance imaging is of clear utility, it cannot tell us about the causal role of neural regions in pitch memory. For this, non-invasive brain stimulation techniques [e.g. transcranial magnetic stimulation; transcranial direct current stimulation (tDCS)] are better suited, because they enable cortical excitability in an area to be directly manipulated (Nitsche & Paulus, 2001; Liebetanz et al., 2002; Antal et al., 2004; Rogalewski et al., 2004). tDCS is a non-invasive brain stimulation method that can be used to modulate neural populations beneath targeted brain areas in order to suppress (with cathodal stimulation) or facilitate (with anodal stimulation) cortical excitability under the site of stimulation (Nitsche & Paulus, 2000; Cohen Kadosh et al., 2010; Ladeira et al., 2011). A prior tDCS study has shown that cathodal stimulation over the left SMG leads to a significant deterioration in pitch memory performance (Vines et al., 2006), but that study did not include an anodal condition or a control task to demonstrate that the influence of tDCS applied to the left SMG was specific to pitch memory rather than general memory processes. This study sought to build on these findings by investigating whether anodal stimulation of the SMG, as opposed to sham stimulation, can facilitate pitch memory performance. Two pitch memory tasks, a recognition task and a recall task, were used in order to determine whether the left SMG is crucial across different pitch memory paradigms. In addition, a face memory task was included as a control task, in order to examine whether tDCS applied to the left SMG results in task-specific pitch memory facilitation. It was
© 2013 Federation of European Neuroscience Societies and John Wiley & Sons Ltd
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Each participant completed a pretest phase and a tDCS phase. The two sessions took place on two different days, with at least 48 h between them.
were identical, and in 50% they varied; in the latter case, two tones of the second sequence were presented in the reversed position (list probe method). Participants had to decide whether the two sequences were the same or different. After their decision was recorded, participants were presented with a 2-s long pink noise burst to minimize carry-over effects before the next trial was played. Sequence length started at two tones, and then increased and decreased according to the participant’s performance, by use of a two-up, one-down adaptive tracking procedure (two right answers = increase in sequence length by one tone; one wrong answer = decrease in sequence length of one tone). The task was complete when the procedure had run for eight reversals. Examples of the stimuli can be found at http://www.gold. ac.uk/music-mind-brain/amusia/memoryproject/. In the pretest phase, participants also completed a short single pitch recognition task in order to ensure that they were able to discriminate the three different tones that were used in the pitch recall task (Williamson et al., 2010), which was part of the tDCS session. In the exposure phase of this pretest, participants heard a C-major (C4, E4, G4) chord followed by a sequence of the three tones (lowC4, medium-G4, and high-B4) played in succession, 10 times. In the test phase, a C-major chord was played as a get-ready signal, followed after a 2-s pause by one of the three tones. The participant was required to mark on a grid if the tone was the low, medium or high one. There were 12 trials, where each tone was randomly presented four times. Participants had to score at least 10 of 12 to qualify for the second phase of the study.
Pretest phase
tDCS phase
A preliminary test was included to match the two groups (anodal or sham stimulation) in terms of their baseline pitch memory abilities. First, the participants filled in the self-report questionnaire of the Goldsmiths Musical Sophistication Index (Gold-MSI) version 0.9 (M€ ullensiefen et al., 2011) to evaluate their level of musical training. The participants valued statements on a seven-point scale from ‘completely disagree’ to ‘completely agree’. The questionnaire consists of 71 statements and has seven dimensions: Subjective Importance, Perception and Production, Musical Training, Emotional Engagement, Bodily Engagement, Creativity, and Event-seeking and Openness. The dimension of interest of the questionnaire ‘Musical Training’ contains seven statements, so the highest score that can be achieved is 63 points. Pitch memory was tested with a recognition span task (Williamson & Stewart, 2010). On each trial, the participants listened to the stimuli via headphones. The musical stimuli (tone sequences) were formed of 10 triangle-waveform tones (equally tempered, whole tone steps) with fundamental pitches ranging from 262 Hz (C4) to 741 Hz (F#5). Tones were 500 ms in length, with a 383-ms pause between tones when they were in sequence. On each trial, participants were presented with two tone sequences of equal length, with an intersequence interval pause of 2 s. On 50% of trials the two sequences
At least 2 days after the pretest phase, participants returned to complete the tDCS session. The participants were matched and randomly split into two groups, one group receiving anodal tDCS and the other sham stimulation. The tDCS parameters were as follows. The active electrode (5 9 5 cm = 25 cm²) was placed over the left SMG. The area was located by using area CP3 of the international 10–20 system for electroencephalogram electrode placement. Many studies have used the 10–20 system before to place the electrodes on the area of interest, and this method of localization has been reported to be reliable and successful (Antal et al., 2004; Rogalewski et al., 2004; Vines et al., 2006). The left SMG has been ascribed to more than one area of the 10–20 system [e.g. TP3 in Gaab et al. (2003) and Vines et al. (2006)]; however, CP3 is a common location for targeting the left SMG (Mottaghy et al., 2002), and was therefore chosen as the site for the present study. The reference electrode (5 9 7 cm = 35 cm) was placed over the right supraorbital area. A small active electrode and a slightly larger reference electrode were used, because this enables much more selective and focally precise stimulation (Nitsche et al., 2007). The electrodes were covered in saline-soaked sponges. A constant-current stimulator (NeuroComm, DC-Stimulator Plus) was used, and delivered a 2-mA current during 20 min of stimulation with a 15-s fade-in time and a 15-s fade-out time for the anodal stimulation. For the sham condition, an identical setup was used, but the stimulator was turned on for only 15 s; this evokes the sensation of being stimulated, but does not lead to a neurophysiological change that can influence performance (Gandiga et al., 2006). It has been shown that naive subjects cannot distinguish between sham and active tDCS stimulation (Gandiga et al., 2006). The first 10 min of the stimulation period was used to describe the three different memory tasks to the participants. The order of the three memory tasks was counterbalanced with a latin-square design.
expected that the group receiving anodal stimulation would outperform the sham group on both pitch memory tasks.
Materials and methods Participants Twenty-four (16 female; eight male) non-musicians (< 2 years of formal musical training in the past, and not playing an instrument regularly at present) took part. All participants reported being righthanded and having normal healthy hearing ability. For the tDCS session, the 24 participants were split into two groups (anodal and sham stimulation). Subjects across both groups were matched by gender, age, and pitch memory span performance (identified by a pretest completed at least 2 days before the tDCS session), and were randomly allocated to one of the groups (see Table 1 for full demographic details). The local ethics committee of Goldsmiths, University of London approved this study in accordance with the Declaration of Helsinki. All participants gave informed written consent to participate in the study. Materials and procedure
Table 1. Characteristics and matching criteria of the two groups
Group
N
Gender, female/male
Age (years), mean (SD)
Pitch memory span pretest (tones), mean (SD)
Sham Anodal
12 12
8/4 8/4
27.42 (7.76) 28.75 (8.75)
6.22 (1.40) 6.33 (0.94)
Independent-samples t-tests confirmed no group differences for age (t22 = 0.395, P = 0.70, NS) and pretest pitch memory span (t22 = 0.228, P = 0.82, NS).
© 2013 Federation of European Neuroscience Societies and John Wiley & Sons Ltd European Journal of Neuroscience, 38, 3513–3518
Improving pitch memory 3515 All together, the three memory tasks of the tDCS session took approximately 35–40 min. The first memory task was the pitch recognition span task, which was conducted exactly as described in the pretest phase. The second memory task was a pitch recall (as opposed to recognition) task (Williamson et al., 2010), where participants were presented with single sequences made from three different tones (low-C4, medium-G4, and high-B4) and asked to recall them. The three tones were recorded on a Disklavier, and the length of each tone was edited to 800 ms in AUDITION with a 200-ms silent pause on the end. Tone sequences varied in length from four to eight tones, and were created by using all of the three tones, without any immediate repetitions. Six trials were presented for each sequence length, beginning with four tones and ending with eight tones (blocked). A practice phase with five trials (one for each sequence length) was conducted before the test phase to ensure that participants understood the task demands. In order to recall the tone sequences, participants were provided with an answer booklet containing blank grids of three rows in height (representing high, medium and low tones) and a number of columns according to the sequence length (Williamson et al., 2010). On each trial, a C-major chord was played in order to signal the onset of a sequence to be remembered. Participants then listened to the sequence, while the response answer booklet was turned upsidedown, and were instructed to listen to the contour (movement of the tones) and try to memorize it. As soon as the sequence finished, the participant turned over the booklet and ticked the boxes of the grid to recall the melody. For example, if a four-tone sequence comprised ‘B4–G4–C4–B4’, the correct answer would be to tick ‘High– Medium–Low–High’ on the grid. When happy with their responses, participants turned over the booklet again and pressed the spacebar to begin the next trial. The third and final memory test presented during tDCS was the Cambridge Face Memory Test long form (Russell et al., 2009), which was used as a control task. The Cambridge Face Memory Test long form was chosen because it is a visual memory task that does not require any auditory or phonological encoding. The test contained a total of 102 trials (preceded by three practice trials), split over four sections. In the task, participants attempted to memorize six unfamiliar male faces from three different views, and were then tested on their ability to recognize these faces in a three-alternative forced-choice task. The first section began by testing recognition with the same images that were used during training. This was followed by a section involving presentation of novel images that showed the target faces from untrained views and lighting conditions. A third section consisted of novel images with visual noise added. The final section contained trials in which distractor images were repeated more frequently, targets and distractors contained more visual noise than the images in the third section, cropped (showing only internal features) and uncropped (showing hair, ears, and necks, which had not been shown in the previous sections) images were used, and images showing the targets and distractors making emotional expressions were included. The percentage of correct responses was measured. Statistical analysis For the pitch recognition task, span was calculated by considering the mean sequence length of the last six reversals (the first two reversals were excluded as practice). An independent-samples t-test was used to compare performance on this task between the two groups after stimulation. In addition, paired-samples t-tests were
applied to compare performance within groups between the pretest and stimulation phase. For the pitch recall memory task, the percentage of correct answers was calculated. Both overall accuracy score and scores for correct recall for every sequence length were considered. Two outliers in the results of the pitch recall task were excluded from the analysis. In each case, the outlying participants performed more than two standard deviations (SDs) away from their group mean score. An independent-samples t-test was applied to analyse overall performance between the two groups, and a two (group) by five (sequence length) mixed ANOVA was used to check performance across different sequence lengths. For the Cambridge Face Memory Test long form, the percentage of correctly identified faces was used, and the between-group performance was analysed with an independent-samples t-test. Additionally, a three (task) by two (group) mixed ANOVA was applied to compare performances in the pitch recognition task, the pitch recall task, and the Cambridge Face Memory Test long form.
Results Pretest Gold-MSI The mean score on the musical training scale from the Gold-MSI questionnaire was 17.46 (out of 63): 16.00 for the sham group, and 18.92 for the anodal group. An independent-samples t-test showed that the mean difference was not significant [t22 = 1.032, P = 0.31, not significant (NS)]. Pitch recognition An independent t-test confirmed that the mean pitch memory group scores from the pretest phase were not significantly different (Fig. 1A) (t22 = 0.0228, P = 0.82, NS). tDCS session Task 9 group interaction In order to determine whether there was a task 9 group interaction, the scores for each task were transformed into z-scores, and a two (group) by three (task) mixed ANOVA was then conducted. The analysis revealed a main effect of group (F1,22 = 8.99, P < 0.01), which was attributable to the anodal group achieving higher z-scores overall than the sham group. The results also showed a significant task 9 group interaction (F1,41,31,03 = 4.21, P < 0.05; Greenhouse– Geisser correction). On the basis of this interaction, we examined performance differences between groups separately. Note that further analysis was carried out on both z-scores and true performance statistics (e.g. percentage correct and pitch span) for all three tests. The pattern of results was identical across both scoring methods, so only the span and percentage correct scores are presented here, in order to give an accurate reflection of performance on the chosen tests. Furthermore, for the pitch memory task, we also conducted a within-group pre-tDCS vs. post-tDCS comparison, as participants completed this task pre-tDCS and post-tDCS (this was not the case with the other two tasks). Pitch recognition The anodal group had a mean score of 7.17 tones (SD 1.26) and the sham group had a mean score of 5.28 (SD 0.80). An independent-
© 2013 Federation of European Neuroscience Societies and John Wiley & Sons Ltd European Journal of Neuroscience, 38, 3513–3518
3516 N. K. Schaal et al. A
B
C
D
Fig. 1. (A) Pitch recognition pretest. To ensure that groups were matched at baseline for pitch memory abilities, all participants completed a pitch recognition span task prior to the tDCS session. No significant differences in performance were found between the groups. (B) Pitch recognition post-tDCS. Following tDCS, the anodal group significantly outperformed the sham group on the same pitch span task used during the pretest. (C) Pitch memory recall. During the tDCS session, participants’ pitch memory recall abilities were also tested. The anodal group significantly outperformed the sham group. (D) Cambridge Face Memory Test long form (CFMT). Face memory performance did not differ between the anodal group and the sham group following tDCS, indicating that the effects were not attributable to general memory enhancement. The error bars indicate the standard error of mean. *P < 0.001.
samples t-test for the scores of the two groups after stimulation revealed a significant result (t22 = 4.4, P < 0.001), indicating that the anodal group performed significantly better than the sham group (r = 0.68; Fig. 1B). On comparison of the scores of the pretest and the tDCS phases within the groups, paired-samples t-tests revealed significant results for the sham group (t11 = 2.90, P < 0.05) and the anodal group (t11 = 2.33, P < 0.05), indicating that, whereas the sham group showed a significant reduction relative to their baseline performance, the anodal group showed a significant improvement relative to their baseline performance.
length, and the performance of both groups decreased as sequence length increased. Cambridge Face Memory Test long form The results of the Cambridge Face Memory Test long form showed that the performance of both groups was nearly equal (sham group, 65.52%; anodal group, 63.97%). A parametric independent-samples t-test revealed a non-significant result (t22 = 0.406, P = 0.692, NS; Fig. 1D).
Discussion Pitch recall The results of the pitch recall task were evaluated by calculating the percentage of correct answers. Scores of correct recall for every sequence length (five different sequence lengths) and an overall score were calculated. Two outliers in the results of the pitch recall task were excluded from the analysis. In each case, the outlying participants performed more than two SDs away from their group mean score. An independent-samples t-test indicated that the overall group performance in the pitch recall task differed significantly (t20 = 4.48, P < 0.001), with the anodal group scoring significantly higher than the sham group (77.57 vs. 61.63%; effect size r = 0.71; Fig. 1C). Next, the group differences in performance across each sequence length were compared. A two (group) by five (sequence length) mixed ANOVA showed a main effect of sequence length (F4,80 = 34.64, P < 0.001) and a main effect of group (F1,20 = 18.50, P < 0.001). A sequence length 9 group interaction was not found (F4,80 = 0.59, P = 0.67, NS). The anodal group performed significantly better than the sham group at every sequence
This study sought to examine the involvement of the left SMG in pitch memory and, specifically, to test the hypothesis that anodal tDCS of this region would enhance pitch memory abilities. Anodal tDCS of the left SMG was associated with improved performance on the pitch recognition task and superior performance of the anodal group than of the sham group in the pitch recall task. No effect was found on visual face memory performance. The results therefore affirm that the left SMG plays a crucial role in the pitch memory abilities of healthy adults, and indicate the potential utility of tDCS as a tool to improve this capacity. The findings are in line with previous brain imaging and brain stimulation studies, which have highlighted a role for the left SMG in pitch memory (Gaab et al., 2003, 2006; Vines et al., 2006). For example, functional neuroimaging has shown that inter-individual variability in SMG activation during pitch memory is correlated with superior pitch memory performance (Gaab et al., 2003). Furthermore, a tDCS study of pitch memory reported a decline in performance in a pitch recognition memory task after cathodal tDCS targeted at the left SMG (Vines et al., 2006). Our findings are in
© 2013 Federation of European Neuroscience Societies and John Wiley & Sons Ltd European Journal of Neuroscience, 38, 3513–3518
Improving pitch memory 3517 accordance with these studies, and contribute additional evidence that the left SMG plays a causal role in pitch recognition. Whereas the anodal group significantly improved their pitch memory performance, the group receiving sham stimulation in the tDCS session showed a deterioration in pitch recognition performance, which may be attributable to a fatigue effect. In this context, the increase in performance observed with anodal stimulation appears more striking, because it implies that the increase in performance has overcome the typical reduction in performance that is seen in the absence of stimulation. The present study builds on previous work by utilizing a second pitch memory task to examine the role of the left SMG in general pitch recall. Participants in the anodal group performed significantly better than the group with no active stimulation across both pitch recall and recognition tasks. This point extends previous findings to show that the SMG is not only involved in pitch recognition tasks but is also crucial for pitch memory in general. One reasonable interpretation of the findings is that the SMG supports the storage of pitch-based information (Sakurai et al., 1998; Gaab et al., 2003; Vines et al., 2006). Importantly for this conclusion, tDCS of the left SMG had no influence on a visual face memory task, implying that the left SMG is specifically involved in auditory pitch memory and not general short-term memory. This conclusion is in accordance with the finding that single-pulse transcranial magnetic stimulation over the SMG has no effect on a visual task, but has an effect on phonological and semantic tasks, which automatically require computing of the sound of the word and therefore auditory involvement (Stoeckel et al., 2009). This specificity of SMG memory function is also in accordance with recent findings of a functional magnetic resonance imaging study by Ellis et al. (2013), who looked at the influence of musical training on brain network activation during music perception. The authors reported peak activation at the supramarginal gyrus and Heschl’s gyrus, with a leftward asymmetry and an interaction effect of musical training and activation level. In contrast, a study by the same group found the greatest difference in activation between melodic and rhythmic melodic in the region of the right superior temporal gyrus (Ellis et al., 2012). Mathys et al. (2010) showed that cathodal stimulation over the left and right Heschl’s gyrus (an area adjacent to SMG) led to a deterioration in performance on a pitch direction discrimination task, with a more pronounced effect in the right hemisphere. It will be interesting for future studies to examine the extent to which tDCS of the SMG modulates pitch memory relative to other acoustic cues such as timbre (e.g. instrument or voice recognition) or rhythm memory, and to further investigate the lateralization of brain areas that are involved in pitch memory processing. It is important to note in this regard that, although the effects of tDCS are known to be fairly homogeneous under the stimulation electrode, they can spread throughout the functional networks involved in task performance (e.g. Holland et al., 2011). In this context, although the effects of anodal stimulation are likely to be homogeneous under the site of the active electrode (lSMG), the behavioural consequences may reflect not only changes in this brain area, but also functional interactions within interconnected cortical regions (e.g. primary auditory cortex). In a broader context, our finding that anodal tDCS may be a useful tool to improve cognitive performance is in line with findings in other domains, e.g. social cognition (Santiesteban et al., 2012), numerical cognition (Cohen Kadosh et al., 2010), and perception (Tseng et al., 2012). Indeed, in other cognitive domains, pairing
repeated sessions of anodal tDCS with training paradigms has been shown to have enduring benefits (Cohen Kadosh et al., 2010). The effect sizes for our enhancement in pitch memory following anodal tDCS of the left SMG were relatively large, and this indicates the potential utility of tDCS as a tool to improve pitch memory in cases where this process is impaired (Gosselin et al., 2009; Williamson & Stewart, 2010). Moreover, one broader implication of our findings is that repeated sessions of anodal tDCS targeted at the left SMG may be used as a tool to aid interventions to improve pitch memory processing, and this is something that we are currently investigating further. In summary, the current study has demonstrated that anodal tDCS targeted at the left SMG enhances short-term pitch recognition and recall, but not memory for visual materials. The findings add to the growing body of evidence highlighting the importance of the left SMG for pitch memory.
Acknowledgements This work was supported by grants from the British Academy (PF100123) and Royal Society (RG110354) awarded to M. J. Banissy.
Abbreviations Gold-MSI, Goldsmiths Musical Sophistication Index; NS, not significant; SD, standard deviation; SMG, supramarginal gyrus; tDCS, transcranial direct current stimulation.
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