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Schaal1, V. Krause2, K. Lange1, M.J. Banissy3, V.J. Williamson4,5 and B. Pollok2 1Department of Experimental Psychology, Heinrich-Heine-University, Düsseldorf, Germany, 2Institute of Clinical Neuroscience and Medical Psychology, Medical Faculty, Heinrich-Heine-University, Düsseldorf, Germany, 3Department of Psychology, Goldsmiths University of London, London, UK, 4Lucerne University of Applied Sciences and Arts, Lucerne, Switzerland and 5Department of Music, University of Sheffield, Sheffield, UK Address correspondence to Nora K. Schaal, Department of Experimental Psychology, Heinrich-Heine-University Düsseldorf, Universitätsstraße 1, 40225 Düsseldorf, Germany. Email: [email protected] For music and language processing, memory for relative pitches is complex skill whereby one has to integrate higher-order cogni- $OWNLOADED FROM highly important. Functional imaging studies have shown activation of tive functions and control very fine motor movements (Wan a complex neural system for pitch memory. One region that has been and Schlaug 2010). Evidence cited in support of a link shown to be causally involved in the process for nonmusicians is the between musical training and neuroplasticity includes consist- supramarginal gyrus (SMG). The present study aims at replicating this ent age of onset effects (Barrett et al. 2013 for a review). Thus, finding and at further examining the role of the SMG for pitch memory it is likely that the brain adapts to these exceptional demands in musicians. Nonmusicians and musicians received cathodal tran- (Münte et al. 2002; Gaser and Schlaug 2003). HTTPCERCOROXFORDJOURNALSORG scranial direct current stimulation (tDCS) over the left SMG, right Functional imaging studies investigating neural networks of SMG, or sham stimulation, while completing a pitch recognition, pitch pitch memory in nonmusicians have shown involvements of recall, and visual memory task. Cathodal tDCS over the left SMG led frontal, temporal, and parietal areas (Zatorre et al. 1994; to a significant decrease in performance on both pitch memory tasks Koelsch et al. 2009; Jerde et al. 2011). More specifically, in sub- in nonmusicians. In musicians, cathodal stimulation over the left SMG jects with no or very little musical training, Gaab et al. (2003) had no effect, but stimulation over the right SMG impaired perform- showed that pitch memory recruits a network of neural ance on the recognition task only. Furthermore, the results show a regions, including the superior temporal gyri, bilateral pos- more pronounced deterioration effect for longer pitch sequences indi- terior dorsolateral frontal regions, bilateral superior parietal cating that the SMG is involved in maintaining higher memory load. No regions, bilateral lobes V and VI of the cerebellum, the supra- AT 5NIVERSITATS 5ND ,ANDESBIBLIOTHEK ON !PRIL stimulation effect was found in both groups on the visual control task. marginal gyri, and the left inferior frontal gyrus. The activation These findings provide evidence for a causal distinction of the left and of the left supramarginal gyrus (SMG) was of particular interest right SMG function in musicians and nonmusicians. as higher activation in this region was linked to superior pitch memory performance (Gaab et al. 2003). Keywords: cathodal stimulation, expertise, functional involvement, To investigate the causal involvement of specific brain areas plasticity, supramarginal gyrus in pitch memory, noninvasive brain stimulation methods, such as transcranial magnetic stimulation (TMS) and transcranial direct current stimulation (tDCS), are useful, as they enable the Introduction manipulation of cortical excitability in a targeted area (Nitsche The musicians’ brain has been studied extensively as a model and Paulus 2001; Antal et al. 2004). Whereas anodal tDCS for neuroplasticity over the last 2 decades (Herholz and leads to a facilitation of neural activity, cathodal tDCS sup- Zatorre 2012; Merette et al. 2013 for recent overviews). Find- presses the cortical excitability under the site of stimulation ings from cross-sectional brain imaging studies comparing (Nitsche and Paulus 2000; Cohen Kadosh et al. 2010; Ladeira brain structures of musicians and nonmusicians suggest that et al. 2011). Previous tDCS studies have supported the causal multiple anatomical differences exist including motor areas involvement of the left SMG in pitch memory recognition by (Jäncke et al. 1997), gray matter volume in Heschl’s gyrus showing a deterioration of performance after cathodal stimu- (Schneider et al. 2002) and the corpus callosum (Schlaug et al. lation (Vines et al. 2006) and an improvement of pitch memory 1995). Furthermore, studies have shown different activation on a recognition and recall task (but not visual memory) after patterns for musicians and nonmusicians for several cognitive anodal stimulation in nonmusicians (Schaal et al. 2013). To tasks (e.g., verbal and tonal memory: Schulze, Zysset et al. date however, there are no tDCS studies of the SMG in trained 2011; processing rhythms: Herdener et al. 2012; pitch percep- musicians, so the causal role of the left SMG in superior pitch tion: Habibi et al. 2013). A longitudinal intervention study by memory performance remains to be tested. Hyde et al. (2009) found that after 15 months of musical train- One other relevant feature of SMG activation during music ing children show anatomical differences in the motor hand processing in musicians and nonmusicians has been contrary area, corpus callosum, and right auditory cortex compared hemispheric patterns. Gaab and Schlaug (2003) revealed stron- with a control group. ger activation in the right SMG in musicians compared with non- Even though such longitudinal studies are relatively sparse, musicians during a pitch memory task when performances of the reasons behind the specialization of neural structures in both groups were matched, indicating different underlying cog- individuals with musical training can be traced back to the fact nitive processing. However, several other studies have reported that learning an instrument requires extensively regular and stronger activation in the left SMG in musicians during music lis- deliberate practice (Ericsson et al. 1993), often starting at a tening (Seung et al. 2005) and pitch memory (Ellis et al. 2013). very young age. Furthermore, playing an instrument is a highly Schulze, Zysset et al. (2011) compared verbal (memorizing © The Author 2014. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: [email protected] syllables) and tonal (memorizing pitches) working memory in musicians group, 3 outcomes are possible: (1) cathodal stimu- musicians and nonmusicians and revealed overlapping acti- lation over the left SMG results in deterioration of pitch vation patterns including the left inferior parietal lobe (corre- memory performance, as stronger activation in the left SMG of sponding to the location of the SMG), in both groups for the musicians was found by Ellis et al. 2013, (2) cathodal tDCS memory processes. Furthermore, in the musician group, over the right SMG would lead to a drop in pitch memory per- additional activation was found in the right globus pallidus, formance, as musicians show more right hemispheric acti- right caudate nucleus, and left cerebellum during tonal working vation for musical memory (Gaab and Schlaug 2003), or (3) no memory suggesting that musicians use a specialized and more stimulation effect would be found as musicians activate a more complex neural system for memorizing pitches. complex neural system for the pitch memory process and can An important note in this context is that the functional mag- compensate for any stimulation modulations (Schulze, Zysset netic resonance imaging (fMRI) studies mentioned above et al. 2011). all used recognition tasks to investigate neural correlates of pitch memory (Zatorre et al. 1994; Gaab et al. 2003; Gaab and Schlaug 2003; Koelsch et al. 2009; Jerde et al. 2011; Schulze, Materials and Methods Zysset et al. 2011; Ellis et al. 2013). In general, short-term $OWNLOADED FROM memory can be tested by 2 response methods, recognition and Participants recall. Whereas recognition relies on a monitoring process for Forty-one nonmusicians and 38 musicians took part in the pretesting phase of the experiment and 36 participants from each group returned re-presented stimuli, recall tasks include more demanding pro- for the tDCS session (4 participants had to be excluded for health duction processes. A study comparing memory for auditorily reasons and 3 subjects did not return for the second session). Nonmusi- and visually presented words has shown that underlying activity cians were defined as individuals with <2 years of musical training in the of neural structures varies depending whether recall or recog- past and who were not playing an instrument at present. They were all HTTPCERCOROXFORDJOURNALSORG nition processes were required (Cabeza et al. 2003). This is students, mostly psychology students, at the Heinrich-Heine-University often traced back to different strategies used in different task in Düsseldorf, and received either course credits or 6 Euro per hour for their participation. The musicians were all students of a professional procedures. Furthermore, activation differences found in studies music college aiming to make music as their profession and all had at using different recognition tasks may also be due to subtle least 10 years of formal musical training. Six string players, 12 wind but important task demand differences which require varying players, 8 singers, 7 pianists, and 3 musicians playing a plucked instru- memory processes such as maintenance and rehearsal. For ment comprised the musicians group. None of the musicians were absol- example, the study by Gaab et al. (2003) used a recognition task ute pitch possessors. Musicians received 6 Euro per hour for their which only emphasized maintenance of pitch information, participation as well as travel expenses. All participants were self-report right-handed and reported normal whereas the task demands in the study by Schulze, Zysset et al. AT 5NIVERSITATS 5ND ,ANDESBIBLIOTHEK ON !PRIL hearing abilities. For the tDCS session, nonmusicians and musicians (2011) required maintenance and explicitly instructed partici- were split into 3 groups, depending on type and location of stimulation pants to use rehearsal processes. These task demand differences (i.e., left SMG vs. right SMG vs. sham). Groups were matched by age, could explain why the activation found in the SMG in the study sex, musical training, as evaluated by the dimension Musical Training by Gaab et al. (2003) is more inferior than the inferior parietal from the Goldsmiths Musical Sophistication Index questionnaire activation found by Schulze, Zysset et al. (2011). (Gold-MSI, Müllensiefen et al. 2014), and general pitch memory abil- The aim of the present study is to investigate whether func- ities, which were evaluated in a pretest session. See Table 1 for full demographical details. tional differences of the SMG can be found between musicians Additionally, 4 participants (2 nonmusicians and 2 musicians) came and nonmusicians in pitch memory and to clarify whether any back a third time to take part in a neuronavigation session to control such differences can be attributed to memory task demands. the location of stimulation targeting at either the left or right SMG. The Therefore, performances on 2 pitch memory tasks (recognition ethics committee of the Medical Department of the Heinrich-Heine- and recall) and a visual control task were investigated follow- University in Düsseldorf approved this study and all subjects gave their ing cathodal tDCS over the left SMG, right SMG, or sham stimu- informed written consent to participate. lation. In line with previous studies, we hypothesized that in nonmusicians, cathodal stimulation over the left SMG would Materials and Procedure lead to a deterioration of performance on both pitch memory All participants completed 2 parts, preliminary testing and the tDCS tasks (Vines et al. 2006; Schaal et al. 2013). Regarding the session, which were at least 48 h apart. Table 1 Characteristics of participants Group Stimulation group N Sex Mean age (in years) Musical training score—Gold-MSI Pretest pitch memory recognition (range: 7–49) task (in tones) Nonmusicians Cathodal lSMG 12 4 Males 23.3 ± 4.5 12.83 ± 5.2 5.86 ± 1.1 8 Females Cathodal rSMG 12 3 Males 21.7 ± 2.3 14.58 ± 4.8 5.84 ± 1.5 9 Females Sham lSMG 12 5 Males 26.2 ± 8.3 15.50 ± 5.5 5.99 ± 1.2 7 Females Musicians Cathodal lSMG 12 5 Males 22.5 ± 2.7 42.08 ± 3.9 7.24 ± 0.9 7 Females Cathodal rSMG 12 5 Males 23.9 ± 4.2 42.42 ± 3.9 7.24 ± 1.0 7 Females Sham lSMG 12 3 Males 23.8 ± 3.0 41.50 ± 1.7 7.35 ± 1.2 9 Females 2 Pitch Memory in Nonmusicians and Musicians • N.K. Schaal et al. Preliminary Testing does not lead to a neurophysiological change that can influence per- Preliminary testing was conducted in order to match the stimulation formance. It has been shown that naive subjects cannot distinguish groups on musical training and general pitch memory abilities. The between sham and active tDCS stimulation (Gandiga et al. 2006). pitch memory span task (Williamson and Stewart 2010) was used to The first 10 min of the stimulation period were used to familiarize the test general pitch memory capacity. The participants listened to the participants with the memory tasks. Altogether the 3 memory tasks stimuli via headphones (AKG Pro Audio, K77). Tone sequences were of the tDCS session took ∼35–40 min. The order of the 3 memory tasks formed of 10 triangle-waveform tones (equally tempered, whole tone was counterbalanced using a latin-square design. steps) with fundamental pitches ranging from 262 Hz (C4) to 741 Hz The pitch memory recognition task (pitch span task) was conducted (F#5). Tones were 500-ms long with a 383-ms pause between tones exactly in the same manner as in the preliminary test. For the pitch when they were in sequence. For each trial, 2 tone sequences of equal memory recall task (Williamson et al. 2010), 3 tones (C4 = 262 Hz, length were presented, with an intersequence interval pause of 2 s. On G4 = 392 Hz, and B4 = 494 Hz) were recorded, played by a piano (Dis- 50% of trials, the 2 sequences were identical and in 50% they varied; in klavier Pro, Yamaha Corporation), and edited to .wav files using the latter case 2 tones of the second sequence were presented in the re- Adobe Audition. Each tone was 800-ms long, edited in Adobe Audi- versed position (i.e., list probe method). The task was to decide tion, and a 200-ms pause was added to the end so that every file was whether the 2 sequences were the same or different. After the partici- 1-s long. Pitch sequences were 4–8 tones long and made up of the 3 pant’s decision was recorded, a 2-s long pink noise burst was pre- different tones (low: C4, medium: G4, high: B4) without direct rep- sented to minimize carry-over effects before the next trial. Sequences etition (there was always a movement in the contour). There were 5 $OWNLOADED FROM were 2 tones long to start with and then increased and decreased ac- blocks (one for each sequence length: 4, 5, 6, 7, and 8 tones) with 6 cording to the participant’s performance. A 2-up, one-down adaptive trials each. To ensure that task demands were clear, a short practice tracking procedure (2 right answers = increase in sequence length by phase with 5 trials (one for each sequence length) was conducted one tone, one wrong answer = decrease in sequence length by one before the first test block. The stimuli were presented via speakers tone) was used. The task was complete when the procedure had run and the participants received an answer booklet, containing blank for 8 reversals. The longest sequence played to this sample was 11 grids of 3 rows in height (representing high, medium, and low tones) tones long. and a number of columns according to the sequence length, and a pen HTTPCERCOROXFORDJOURNALSORG To ensure that participants were able to discriminate the 3 different for their responses. To signal the onset of a test sequence, a C-major tones that were used in the main pitch recall task (Williamson et al. chord (C4, E4, and G4) was played at the beginning of a trial. Partici- 2010), which was part of the tDCS session, the participants also com- pants then listened to the first sequence (4 tones long), while the pleted a short single pitch recognition test. In the exposure phase of answer booklet was turned upside-down and were instructed to listen this preliminary test, participants heard a C-major (C4, E4, G4) chord to the contour (movement of the tones) and try to memorize it. They followed by a sequence of the 3 tones (low-C4, medium-G4, and were instructed to turn over the booklet as soon as the sequence fin- high-B4) played in succession, 10 times. In the test phase, a C-major ished and to tick the boxes to record their memory of the pitch se- chord was played as a get-ready signal, followed after a 2-s pause by quence. For example, if for a 4-tone-long sequence, the tones “C4–G4– one of the 3 tones. The participant was required to mark on a grid, if B4–C4” were played, the correct answer would be to tick the boxes the tone was the low, medium, or high one. There were 12 trials, “low–medium–high–low” on the grid. When happy with their where each tone was randomly presented 4 times. Participants had to response, the subjects turned over the booklet again and triggered the AT 5NIVERSITATS 5ND ,ANDESBIBLIOTHEK ON !PRIL score at least 10 out of 12 to qualify for the main tDCS phase of the next sequence by pressing the spacebar. study. A visual task was included as control condition. The Cambridge After the 2 pitch memory tasks, the participants filled in a German Face Memory Test—long form (CFMT+, Russell et al. 2009) was chosen version of the self-report questionnaire of the Gold-MSI version 1.0 as it does not require any auditory or phonological encoding, but has (Müllensiefen et al. 2014) to evaluate their level of musical training. previously been shown to be sensitive to detecting differences in face The participants scored statements on a 7-point scale from “completely memory performance (e.g., Russell et al. 2009). In this task partici- disagree” to “completely agree”. The questionnaire consists of 38 state- pants were instructed to memorize 6 unfamiliar male faces from 3 ments and comprises 5 dimensions: Active Engagement, Perceptual different views and were then tested on their ability to recognize them Abilities, Musical Training, Emotions and Singing Abilities. The di- in a 3-alternative forced-choice task. The test comprises 102 trials (pro- mension of interest Musical Training contains 7 statements, so the ceeded by 3 practice trials), subdivided into 4 sections varying in diffi- score range is 7–49 points. culty. The first section of the task tested recognition with the same images that were used during training. This was followed by a section involving presentation of novel images that show the target faces from tDCS Session untrained views and lighting conditions in the test phase. A third At least 2 days after the preliminary test, participants returned to com- section consisting of novel images with visual noise added. The final plete the tDCS session. The participants from both groups (nonmusi- section contained trials in which distractor images repeated more fre- cians and musicians) were matched as described above and randomly quently, targets and distractors contained more visual noise than the split into 3 stimulation groups: one group receiving cathodal tDCS over images in the third section, cropped (only showing internal features) the left SMG, another group receiving cathodal stimulation over the and uncropped images (showing hair, ears, and necks, which had not right SMG and the third group receiving sham stimulation over the left been shown in the previous sections) were used, and images showing SMG. 2 the targets and distractors making emotional expressions were included. The active electrode (5 × 5 cm = 25 cm ) was placed over either the The first and second sections used a trial-by-trial recognition paradigm, left or right SMG. The areas were located using area CP3 for the left whereas sections 3 and 4 employed a more long-term memory – and CP4 for the right hemisphere according to the international 10 20 approach. The percentage of correct responses was measured. system for electroencephalogram electrode placement, successfully used in previous studies to place the electrodes over the targeted site (Antal et al. 2004, Rogalewski et al. 2004, Vines et al. 2006). CP3 and Neuronavigation CP4 are common locations for targeting the SMG on either hemisphere To validate the location of stimulation and to show that the electrode (Mottaghy et al. 2002; Schaal et al. 2013). The reference electrode was placed over the targeted area of the SMG (Brodmann area 40) a (5×7cm=35cm2) was placed over the contralateral supraorbital area. Neuronavigation session was conducted with a small exemplary sample A slightly smaller active electrode compared with the size of the refer- of 4 participants (2 musicians and 2 nonmusicians). To reconstruct the ence electrode was used to receive a more selective and focally precise procedure of the tDCS session the international 10–20 system was used stimulation (Nitsche et al. 2007). The electrodes were covered in saline- to locate the area of the left (CP3) and right (CP4) SMG on the partici- soaked sponges. The 2 active stimulation groups received 20 min of pant’s scalp. After marking this localization with a highlighter, the Neu- 2-mA stimulation including 15 s fade-in and fade-out time. An identical ronavigation (Localite GmbH, Sankt Augustin, Germany) procedure setup was used for the sham group, but the stimulator was only turned began with measuring the head using predefined points (i.e., left and on for the first 30 s. This evokes the sensation of being stimulated but right preauricular points and nasion). After mapping the anatomical Cerebral Cortex 3 landmarks onto a standardized brain, 2 markers were inserted according the prestimulation and one for the poststimulation phase. to the highlighted points on the scalp located at CP3 and CP4. The Where appropriate, all post hoc tests were subject to sequential fi program then identi ed the Talairach coordinates for the markers. Bonferroni correction (Holm 1979) in order to compensate for multiple tests and to protect type I errors. Therefore, for every Results post hoc set P-values were ranked and the smallest P-value was tested with a Bonferroni correction including all tests, the Pitch Memory Recognition Task second smallest was tested involving one less test and so forth As participants completed the pitch span task twice (in the pre- for the remaining tests. fi liminary session and after tDCS) a mixed factorial analysis of var- Before stimulation a signi cant main effect of group, F1,66 = iance (ANOVA) with time (pre vs. poststimulation) as a within 24.16, P < 0.001 was revealed. The main effect of stimulation subject factor and group (nonmusicians vs. musicians) and group as well as the group × stimulation group interaction were fi stimulation group (cathodal left SMG vs. cathodal right SMG vs. nonsigni cant (P-values > 0.92). Poststimulation, the ANOVA fi sham) as between subject factors was conducted. The analysis revealed a signi cant main effect of group, F1,66 = 25.72, P < 0.001 and a significant group × stimulation group interaction, revealed a trend for the factor time, F1,66 =3.67,P = 0.06, and a nonsignificant result for factor stimulation group, F = 1.18, F2,66 =5.16,P = 0.016. The main effect of stimulation group was $OWNLOADED FROM 2,66 fi P = 0.32, whereas the main effect of factor group was significant, nonsigni cant (P =0.082). F = 31.21, P < 0.001. The interactions time × group, time × Furthermore, independent sample t-tests were applied in 1,66 fi stimulation group and group × stimulation group are all non- order to dissolve the signi cant group × stimulation group significant (P > 0.14) but the time × group × stimulation group interaction of the poststimulation session. In the stimulation fi group receiving cathodal tDCS over the left SMG, a highly sig- interaction yielded a signi cant result, F = 4.73, P = 0.012. HTTPCERCOROXFORDJOURNALSORG 2,66 fi Data are summarized in Table 2. ni cant difference of the factor group was revealed, t(22) = 5.96, In order to explore the significant time × group × stimulation P < 0.001. In the stimulation group receiving cathodal tDCS fi group interaction, 2 univariate ANOVAs were applied, one for over the right SMG, the result was nonsigni cant, t(22) = 0.88, P = 0.39, and in the sham group, a trend towards superior per- formance of the musicians compared with the performance of Table 2 nonmusicians was present, t(22) = 2.32, P = 0.06. This series of Overview of performances for all 3 stimulation groups in nonmusicians and musicians results suggests that the musicians’ superior performance in all Group Stimulation Pitch memory Pitch memory recall CFMT+ percent stimulation groups before stimulation was not present group recognition task (in task (percent correct) anymore after stimulation only in the group who received cath- tones) correct) odal tDCS over the right SMG. AT 5NIVERSITATS 5ND ,ANDESBIBLIOTHEK ON !PRIL Nonmusicians Cathodal 5.04 ± 0.8 72.56 ± 8.2 62.26 ± 11.4 To explore this interesting finding, a pre- and poststimula- lSMG Cathodal 6.08 ± 1.0 80.95 ± 4.9 66.58 ± 8.0 tion comparison in the musicians group receiving cathodal rSMG stimulation of the right SMG was applied and showed a Sham lSMG 6.26 ± 1.1 80.75 ± 6.2 63.24 ± 12.8 significant result, t(11) = 2.76, P = 0.02 indicating that cathodal Musicians Cathodal 7.11 ± 0.9 90.37 ± 5.8 60.93 ± 15.3 lSMG stimulation over the right SMG in musicians led to a deterio- Cathodal 6.42 ± 0.9 91.67 ± 4.5 62.83 ± 6.8 ration of pitch memory performance. Additionally, in nonmu- rSMG sicians a pre- and poststimulation comparison in the group Sham lSMG 7.25 ± 1.0 91.09 ± 4.3 66.99 ± 8.9 receiving cathodal tDCS over the left SMG revealed a signifi- Note: The bold values highlight the group performances which show a significant deterioration cant deterioration of pitch memory, t(11) = 3.67, P = 0.008 after cathodal stimulation. (see Fig. 1). Figure 1. Bargraphs representing the results of the pitch memory recognition task. A mixed factorial ANOVA with the factors time (pre vs. poststimulation), group (nonmusicians vs. musicians) and stimulation group (cathodal left SMG vs. cathodal right SMG vs. sham) reveals a significant time × group × stimulation group interaction, F2,66 = 4.73, P = 0.012. In nonmusicians, cathodal tDCS over the left SMG leads to a significant deterioration of pitch recognition (t(11) = 3.67, P = 0.008), while in musicians cathodal tDCS over the right SMG results in declined performance (t(11) = 2.76, P = 0.02). 4 Pitch Memory in Nonmusicians and Musicians • N.K. Schaal et al. Pitch Memory Recall Task 0.001) indicating that performances decreased as sequence An ANOVA with factors group (nonmusicians vs. musicians) length increased. Furthermore, the ANOVA confirmed signifi- and stimulation group (cathodal left SMG vs. cathodal right cant main effects of group (P < 0.001) and stimulation group SMG vs. sham) on overall recall performance scores yielded (P = 0.017) and also showed significant interaction effects of main effects of group, F1,66 = 89.5, P < 0.001, and stimulation sequence length × group (P <0.001) and group × stimulation group, F2,66 = 5.14, P = 0.008, and a significant group × group (P = 0.023). The sequence length × stimulation group as stimulation group interaction, F2,66 = 3.15, P = 0.049. Data are well as the 3-way interaction sequence length × group × summarized in Table 2. stimulation group were nonsignificant (P-values > 0.155). Post hoc independent sample t-tests with sequential Bonfer- In order to further investigate the significant sequence roni correction (Holm 1979) in nonmusicians showed signifi- length × group and group × stimulation group interaction, per- cant differences between the group receiving cathodal formance on the pitch memory recall task for every sequence stimulation over the left SMG and the groups receiving stimu- length (percent correct for 4-tone-long sequences, 5-tone-long lation over the right SMG, t(22) = 3.04, P = 0.018, and sham sequences etc.) was analyzed. In nonmusicians, the ANOVA re- fi stimulation, t(22) = 2.76, P = 0.024. The group with cathodal vealed nonsigni cant main effects of factor stimulation group tDCS over the left SMG performed significantly below the for 4-, 5- and 6-tone-long sequences (P-values > 0.10). For the $OWNLOADED FROM sham group, and the group stimulated with cathodal tDCS over 7-tone sequences a significant main effect of factor stimulation 2 the right SMG (Fig. 2A). The difference between the groups re- group was found, F2,35 = 5.86, P < 0.01, ηp = 0.26. Post hoc ceiving cathodal tDCS over the right SMG and sham stimu- comparisons (Tukey-HSD) revealed significant differences lation was nonsignificant, t(22) = 0.08, P = 0.93. between the group receiving tDCS over the left SMG and the For the musicians group, no significant differences in overall sham group (P < 0.01) and a marginally significant difference HTTPCERCOROXFORDJOURNALSORG performance could be found in the 3 stimulation groups (P > between the groups receiving cathodal tDCS over the left or 0.55), indicating that cathodal stimulation over the left or right right SMG (P = 0.054). For 8-tone-long sequences, also a sig- SMG did not affect task performance. nificant main effect of factor stimulation group was found, 2 A 5 × 2 × 3 mixed factorial ANOVA with sequence length (5) F2,35 = 8.25, P < 0.001, ηp = 0.33, with significant differences as the repeated measure variable and group (2) and stimulation between the group receiving tDCS over the left SMG and the group (3) as between subject variables revealed a significant other 2 groups (cathodal tDCS over right SMG vs. sham stimu- main effect of sequence length, F4,264 = 144.35, P <0.001,anda lation, P-values < 0.01). These results indicate that the group follow-up trend analysis revealed a significant linear trend (P < who received cathodal tDCS over the left SMG showed a deterioration in their performance on longer sequences with higher memory load only (Fig. 2B). When conducting the AT 5NIVERSITATS 5ND ,ANDESBIBLIOTHEK ON !PRIL same analysis for every sequence length in the musicians group, all 5 ANOVAs reported P-values > 0.381 for the main effect of stimulation group, confirming that on the recall task no stimulation effects could be found on the performance of any sequence length in the musicians group. Cambridge Face Memory Test—Long Form For the CFMT+, an ANOVA was conducted with factors group (nonmusicians vs. musicians) and stimulation group (cathodal left SMG vs. cathodal right SMG vs. sham). The results revealed neither significant main effects nor interaction (P-values > 0.48). Data are summarized in Table 2. As the CFMT+ uses 2 different recognition memory paradigms, a trial-by-trial para- digm in Part 1 (blocks 1 and 2) and a more long-term memory approach in Part 2 (blocks 3 and 4), separate ANOVAs were conducted on the percent correct scores for each part with the factors group and stimulation group: no significant main effects or interactions were found (P-values > 0.19). Overall, the evidence strongly suggests that there is no effect of stimu- lation on the visual control task in either musicians or nonmu- sicians, thereby indicating that the SMG are not causally involved in the process of remembering faces. Figure 2. (A) For the pitch recall task, there is a significant main effect of stimulation Neuronavigation group in nonmusicians showing that performance of the group receiving cathodal tDCS The evaluation of the targeted site of all 4 sample participants over the left SMG is below the group receiving cathodal stimulation over the right SMG confirmed that the site which was stimulated corresponds to and sham stimulation (P-values < 0.05). (B) When looking at the performance in Brodmann area 40, the location of the SMG. The averaged nonmusicians for every sequence length, the analysis reveals significant differences of − − the factor stimulation group for longer sequences (7 and 8 tones) indicating that the Talairach coordinates were 44; 43; 49 for the left SMG and deterioration of pitch memory after cathodal stimulation over the left SMG is more 45; −48; 55 for the right SMG corresponding to Brodmann area pronounced in trials with higher memory load. 40 (Fig. 3). Cerebral Cortex 5 neuroplasticity and revealed structural differences compared with nonmusicians (e.g., Schlaug et al. 1995; Jäncke et al. 1997; Schneider et al. 2002; Gaser and Schlaug 2003; Hyde et al. 2009), but to our best knowledge this is the first study to show functional differences in pitch memory tasks using non- invasive brain stimulation. As opposed to the nonmusicians, the pitch memory performance of the musicians group did not show a detrimental effect of cathodal tDCS over the left SMG, neither in the recognition nor recall task. But, cathodal stimu- lation to the right SMG led to a decrease in their pitch recog- nition span. A recent electroencephalography study by Habibi et al. (2013) suggested that the left hemisphere involved in tasks dif- ferentiated nonmusicians and musicians, as they found behav- ioral and electrophysiological differences when stimuli were $OWNLOADED FROM presented to the right ear. The present data are in line with this idea, showing that musicians and nonmusicians have a differ- entiated causal involvement of the left SMG during pitch memory tasks. However, when looking at the involvement of the right SMG in the present study, a causal distinction was found as well, indicating that the neural distinction for the HTTPCERCOROXFORDJOURNALSORG pitch memory process between musicians and nonmusicians is not limited to the left hemisphere. The fact that musicians do not demonstrate a causal involve- ment of the left SMG in pitch memory is surprising as several fMRI studies have shown increased activation of the left SMG Figure 3. Localization of the left (−44; −43; 49) and right SMG (45; −48; 55) averaged across an exemplary sample of 4 participants (2 nonmusicians and 2 in musicians and in participants after receiving musical train- musicians) using neuronavigation. ing (Gaab et al. 2006; Ellis et al. 2013). One possible expla- nation for this apparent contradiction is that trained musicians are able to compensate the suppression of a particular brain AT 5NIVERSITATS 5ND ,ANDESBIBLIOTHEK ON !PRIL Discussion area during tDCS by activating other areas of their complex The present study investigated the causal involvement of the neural network for pitch memory. Schulze, Zysset et al. (2011) left and right SMG in pitch memory ability, as determined by showed that musicians activate unique and additional neural pitch memory recall and recognition paradigms, and how this areas for tonal memory including the right globus pallidus, right involvement varies in musicians and nonmusicians indicating caudate nucleus, and left cerebellum. Furthermore, Andoh and functional differences. Whereas cathodal stimulation over the Zatorre (2013) have shown an interhemispheric compensation left SMG led to a deterioration of performance in both pitch effect by combining TMS and fMRI during a melody discrimi- memory tasks in nonmusicians, the musicians showed a nation task. When they applied repetitive TMS over the right decline only in recognition pitch memory performance and in- Heschl’s gyrus, an increase of activation was identified in the terestingly, only after cathodal tDCS over the right SMG. left hemisphere, thereby revealing potential compensation In the nonmusicians group, cathodal tDCS over the left SMG mechanisms across brain areas, in addition, the same study led to a significant deterioration of task performance on the found positive correlation between the extent of compensated pitch recognition task as well as on the pitch recall task com- increase of activation in the left Heschl’s gyrus and faster reac- pared with the groups receiving cathodal tDCS over the right tion times (Andoh and Zatorre 2013). SMG or sham stimulation. These findings are in line with pre- Another possible explanation for the lack of a left SMG tDCS vious studies showing the activation and causal involvement of effect in musicians relates to the way in which this population specifically the left SMG in the pitch memory process in non- reacts to brain stimulation. A recent study revealed that bilat- musicians (Gaab et al. 2003; Vines et al. 2006). These results eral tDCS over the primary motor cortex showed no effect on also extend previous findings showing that anodal tDCS over fine finger movements of pianists (Furuya et al. 2013), while bi- the left SMG leads to superior pitch memory in nonmusicians hemispheric tDCS over the motor cortex in nonmusicians led (Schaal et al. 2013). In addition, the more detailed analysis of to a facilitation of such movements (Vines et al. 2008). The the sequence lengths used in the pitch recall task of the results of the musicians were explained to be traced back present study showed that the effect of cathodal tDCS over the either simply to a ceiling effect as pianists have developed ex- left SMG is significant for longer pitch sequences only. This tremely exact finger movements during their many years of new evidence adds to the literature by suggesting that nonmu- training and deliberate practice or to the neuroplasticity of a sicians rely more heavily on the left SMG when they are re- musician’s brain, which has already optimized its function to quired to either store or rehearse a large amount of material in highly complex musical demands and is therefore less sensitive pitch memory (Sakurai et al. 1998; Gaab et al. 2003; Vines to stimulation effects (Furuya et al. 2013). et al. 2006). In the musician group of the present study, suppression of The present study also revealed key differences between the the right SMG with cathodal tDCS resulted in a deterioration of effects of SMG tDCS on musicians and nonmusicians. A variety pitch memory recognition performance and leads to the as- of studies have looked at musicians’ brains as a model of sumption that musicians evoke a more right lateralized 6 Pitch Memory in Nonmusicians and Musicians • N.K. Schaal et al. network for pitch memory. It has been shown that musicians All the above evidence leads to the conclusion that the dispose a more equalized neuroanatomy and function in both SMG in general is involved in more demanding pitch memory hemispheres (Patston et al. 2007; Bermudez et al. 2009). Fur- processes and—particularly—in the storage of pitch infor- thermore, Gaab and Schlaug (2003) reported higher activation mation (Sakurai et al. 1998; Rinne et al. 2009). This is also in of the right SMG in musicians compared with nonmusicians accordance with a study by Wehrum et al. (2011) who reported when behavioral performance was matched. The pitch memory the activation of the SMG in a pitch discrimination task in span task of the present study measures the capacity of pitch children only in harder trials with subtle pitch changes and memory information that can be held in the memory system and not during easier trials with robust changes. Furthermore, a adapts to individual performance level. Therefore, it ensures review of behavioral performances in fMRI studies, reveals that that every nonmusician and musician is pushed to their limit of those which reported activation in the SMG also found lower memory ability. The results of the pitch span task indicate that performances on the pitch memory task (Gaab et al. 2003; the right SMG is involved particularly in higher task demands in Rinne et al. 2009; Schulze, Zysset et al. 2011) compared musicians, while in nonmusicians the left SMG may be more with studies which do not show an activation of the SMG and strongly involved in such tasks. In this context, Foster and high task performances of 90% (Zatorre et al. 1994; Jerde et al. Zatorre (2010) conducted an fMRI study on melody transposi- 2011). $OWNLOADED FROM tion with musicians and nonmusicians and revealed a key role Regarding the CFMT+ (Russell et al. 2009), the results show, of the intraparietal sulcus (IPS) for melody transposition (also as expected, no effect of cathodal stimulation (Schaal et al. see Foster et al. 2013) and showed that the activation of the right 2013), neither over the left nor right SMG, indicating that the IPS could predict task performance in both groups. As the IPS is causal involvement of the left and right SMG, respectively, is located adjacent to the SMG, this correlational finding is very in- specific to pitch memory in the present study. Even though the teresting, especially, as melody transposition also requires pitch visual control task is not perfectly matched in terms of task HTTPCERCOROXFORDJOURNALSORG memory and relies on maintaining relative pitch information. procedure and demands, the lack of modulation effect across Another possible explanation for the involvement of the right conditions, the trial-by-trial working memory paradigm in Part SMG in the pitch memory recognition task of this group could 1 and the more long-term memory approach in Part 2, strongly be that the musicians usually use their visual-motor represen- supports the specific involvement of the SMG in pitch tation to memorize pitch sequences: the right SMG has been memory. Furthermore, the performance on the visual control shown to be activated during sight reading in musicians task did not differ between musicians and nonmusicians, con- (Sergent et al. 1992). When interrupting this additional memory firming that musicians do not show overall superior memory resource by suppressing the activity of the right SMG by catho- abilities (Tierney et al. 2008). dal tDCS, the musicians’ performance deteriorates to the level of Finally, the present data show that the musicians outper- AT 5NIVERSITATS 5ND ,ANDESBIBLIOTHEK ON !PRIL the nonmusicians ability as shown in the present results. formed the nonmusicians on both pitch memory tasks indicat- As well as specific differences, general task demands differ- ing that, as experts in the auditory domain, they have developed ences between recall and recognition tasks must also be con- and dispose a pronounced memory system that allows them to sidered. Schulze, Mueller et al. (2011) showed that different memorize more musical material (Williamson et al. 2010; neural activation patterns emerged in musicians during a pitch Schulze et al. 2011). However, the analysis of the recall task also memory recognition task depending on whether unstructured shows that musicians as well as nonmusicians show a linear (atonal) or structured (tonal) material was used. Similar differ- decline of pitch memory performance, as sequence length in- entiations have also been shown for a spatial task (Bor et al. creases, showing that memory capacity is limited (Baddeley 2003) and when using audio-visual material (Bor et al. 2004). 1986). It can be proposed that the decline in performance in Both these studies indicate that strategy is an important factor in nonmusicians after cathodal tDCS over the left SMG that was memory tasks which could also be responsible for the lack of only significant in longer sequences with higher memory load effect on the present recall task (which uses a tonal and struc- might also be found in the musicians group (probably with tured approach) after cathodal stimulation of the right SMG in right hemispheric specialization) if sequences were longer musicians. It is likely that musicians were able to chunk the (up to 10 tones per sequence). This hypothesis needs to be in- pitch information in the recall task (Schulze, Mueller et al. 2011) vestigated in future research. In this context, it is also important and that this strategy relies on other neural systems, which are to note that the study uses a cross-section approach by compar- less sensitive to stimulation effects. ing musicians and nonmusicians, and therefore we cannot rule No effect of stimulation was found on the pitch recall task in out preexisting structural and functional differences. In order to musicians. One factor that may contribute to this finding is that shed further light on this issue a study including participants musicians performed at ceiling (91% accuracy). However, with a broader range of musical experience and a correlation another consideration is that different memory tasks, and task analysis with years of training would be desirable. demands may recruit different neural networks. For example, In summary, the present study provides evidence for the a tDCS study by Berryhill et al. (2010) showed impaired different and distinctive causal involvement of the SMG in working memory performance on a recognition but not a nonmusicians and musicians in the pitch memory process. recall task, after cathodal stimulation over the right inferior A significant downward modulation of pitch memory perform- parietal cortex, therefore indicating that different processes ance (recognition and recall) after cathodal tDCS over the left and underlying neural circuits were involved. Moreover, in the SMG was only found in nonmusicians. In the musicians group, present nonmusicians group, the diminished performance in a selective effect was found on the pitch recognition task but the pitch recall task after cathodal tDCS over the left SMG was only after stimulation of the right SMG. These combined only significant for longer sequences with higher memory results suggest a hemispheric specialization of the SMG for demands. pitch memory depending on musical expertise and training. 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Banissy b,f a Department of Experimental Psychology, Heinrich-Heine-University, 40225 Du¨sseldorf, Germany b Department of Psychology, Goldsmiths, University of London, SE14 6NW, London, UK c Lucerne University of Applied Sciences and Arts, 6003 Lucerne, Switzerland d Department of Music, University of Sheffield, S3 7RA, Sheffield, UK e Brain and Behavior Laboratory, Institute of Cognitive Neuroscience, National Central University, Jhongli 320, Taiwan f Institute of Cognitive Neuroscience, University College London, London, UK g Institute of Clinical Neuroscience and Medical Psychology, Medical Faculty, Heinrich-Heine-University, Du¨sseldorf, Germany article info abstract Article history: Brain stimulation studies have previously demonstrated a causal link between general Received 17 October 2014 pitch memory processes and activity within the left supramarginal gyrus (SMG). Building Reviewed 17 November 2014 on this evidence, the present study tested the impact of left SMG stimulation on two Revised 20 November 2014 distinct pitch memory phases, retention and encoding. Repetitive transcranial magnetic Accepted 20 November 2014 stimulation (rTMS) was employed during the retention stage (Experiment 1) and the Action editor Chris Chambers encoding phase (Experiment 2) of a pitch recognition task. Stimulation was applied on a Published online 15 December 2014 trial-by-trial basis over the left SMG (target site) or the vertex (control site). A block without TMS was also completed. In Experiment 1, rTMS over the left SMG during pitch retention Keywords: led to significantly increased reaction times compared to control conditions. In Experiment Pitch memory 2 no rTMS modulation effects were found during encoding. Experiment 3 was conducted as Transcranial magnetic stimulation a control for non-specific stimulation effects; no effects were found when rTMS was Retention applied over the left SMG at the two different time points during a perceptual task. Taken Left supramarginal gyrus together, these findings highlight a phase-specific involvement of the left SMG in the retention phase of pitch memory, thereby indicating that the left SMG is involved in the maintenance of pitch information. © 2014 Elsevier Ltd. All rights reserved. * Corresponding author. Heinrich-Heine-University Du¨ sseldorf, Department of Experimental Psychology, Universitatsstraße€ 1, 40225 Du¨ sseldorf, Germany. E-mail address: [email protected] (N.K. Schaal). http://dx.doi.org/10.1016/j.cortex.2014.11.011 0010-9452/© 2014 Elsevier Ltd. All rights reserved. cortex 64 (2015) 310e317 311 first sequence). Finally, a control experiment was conducted 1. Introduction to test for non-specific disruption effects of rTMS. In Experi- ment 3, participants completed a perceptual task while rTMS Functional brain imaging studies of pitch memory have was applied over the left SMG at the two time points used in revealed the involvement of a complex neural system in pa- Experiments 1 and 2. rietal, temporal and frontal areas (e.g., Koelsch et al., 2009). One area that is consistently highlighted across studies is the left supramarginal gyrus (SMG) (Ellis, Bruijn, Norton, Winner, 2. Experiment 1 and 2 & Schlaug, 2013; Gaab, Gaser, Zaehle, Jancke,€ & Schlaug, 2003). Recently, studies using transcranial direct current 2.1. Experiment 1 and 2 methods stimulation (tDCS) have implied that the left SMG is causally involved in pitch memory processes (Schaal, Williamson, & 2.1.1. Participants Banissy, 2013; Vines, Schnider, & Schlaug, 2006). Suppressing 27 participants took part with a mean age of 27.22 years left SMG function using cathodal tDCS leads to a deterioration (SD ± 6.51, range 18e38 years). 13 (seven female) subjects in pitch recognition ability (Vines et al., 2006), while increasing participated in Experiment 1, and 14 (eight female) in Experi- left SMG excitability with anodal tDCS results in a facilitation ment 2. Participants were all non-musicians (less than two of pitch memory (Schaal et al., 2013). In combination, these years of musical training in the past, not playing an instru- studies provide evidence that left SMG activity is important for ment at present) and right-handed (see Table 1 for demo- the output of pitch memory, but the exact role of the left SMG graphical details). The study was approved by the ethics in the pitch memory process remains unknown. committee of Goldsmiths, University of London and partici- Another issue with previous work is that tDCS provides a pants gave informed written consent. relatively large window in which cortical excitability within a To evaluate musical training, the Musical Training Dimen- brain region can be modulated. In this regard, it is not clear sion from the Goldsmiths Musical Sophistication Index (Gold- whether the left SMG plays a causal role throughout the pitch MSI, Mu¨ llensiefen, Gingras, Musil, & Stewart, 2014) was used. memory process or in specific phases. Two major time- This Gold-MSI dimension is comprised of 7 items that assess an specific phases of pitch memory are of interest to the pre- individual's musical training and practice habits. The partici- sent study: encoding and retention. In the encoding phase, pant is asked to rank the items on a seven-point agreement new pitch information is perceived and the tones are encoded scale, giving a possible score range of between 7 and 49 points. in relative relationships with each other, whereas in the The mean score from our sample was 10.9 points, confirming retention interval this same information is maintained and that they had little or no musical training in the past. rehearsed. Schulze, Mu¨ ller, and Koelsch (2011) showed that encoding and retention in auditory memory rely on disso- 2.1.2. Materials ciable brain activations. A pitch memory recognition task was created, modeled on the Transcranial magnetic stimulation (TMS) is a method bet- pitch memory span task (Williamson & Stewart, 2010) that ter suited for investigating a phase-specific involvement of the was used in one of our previous brain stimulation studies left SMG in pitch memory. This method enables a spatially (Schaal et al., 2013). The task parameters were adjusted to and temporally precise modulation of neural mechanisms on match the TMS parameters. a trial-by-trial basis (Walsh & Cowey, 2000). For example, 5 Hz 80 pairs of six tone long pitch sequences were created. In 40 repetitive TMS (rTMS) over the precuneus has been shown to trials the two sequences were the same (same tones in iden- interfere with a visual working memory task differently when tical order) and 40 were different (same tones in both se- applied in the retention interval or during the re-presentation quences but in the latter sequence two tones were in reversed of the recognition probe (Luber et al., 2007). This finding order). All sequences were created from a pool of 10 triangle- demonstrates the effective use of TMS for interfering with the waveform tones (equally tempered, whole tone steps) with time-specific stages of a memory process. fundamental pitches ranging from 262 Hz (C4) to 741 Hz (F#5). Here, we used rTMS to examine the causal role of the left Tones were 350 msec long, with a 150 msec pause at the end of SMG at different time-specific phases of the pitch memory each tone, so in total each sequence was 3 sec long. process (retention and encoding), by adopting a similar phase- In order to create the pitch sequences, the tones were specific stimulation design to Luber et al. (2007). In Experiment randomly sampled with the restriction that beginning and end 1, we examined the role of the left SMG in the retention phase tones were counterbalanced. There were no direct repetitions of pitch memory. In Experiment 2, we focused on the encoding of a tone and adjacent tones were at least two whole tones phase. In both experiments, participants completed a pitch memory recognition task, where they heard two six-tone long pitch sequences and judged whether they were the same or different (a protocol adapted from Williamson & Stewart, Table 1 e Demographical details of participants for 2010). Participants completed this task under three stimula- Experiments 1, 2 and 3. tion condition: rTMS over the left SMG; rTMS over the vertex N Age Gold-MSI- Musical (active control site); No TMS. The onset of stimulation was Score training varied between each experiment with rTMS being applied Experiment 1 13 (7f/6m) 26.2 years 12.2 0.77 years either during the retention phase (after hearing the first Experiment 2 14 (8f/6m) 28.2 years 9.5 0.32 years sequence) or during the encoding phase (while hearing the Experiment 3 12 (7f/5m) 23.9 years 10.5 0.58 years 312 cortex 64 (2015) 310e317 apart. In the different trials, we counterbalanced for the po- checked constantly between trials. On every trial (24 trials per sition of the two reversed tones as well as the size of their tone block; two blocks with active stimulation) 3 sec long rTMS was interval. applied in the retention interval (starting as soon as the first Each trial consisted of two sequences (either same or sequence finished playing and ending with the onset of the different) with an inter-sequence interval of 3 sec. The second sequence; Experiment 1) or encoding interval (rTMS is sequence length of six tones was chosen as previous studies triggered with the onset and duration of the first sequence; have shown that non-musicians have a mean capacity score Experiment 2) of the trial. of six tones on the related pitch memory span task (Schaal et al., 2013; Williamson & Stewart, 2010). A pilot study with 2.1.4. Procedure 12 participants confirmed that sequences were at the desired Experiments 1 and 2 used a within-subject design. The order level of difficulty (Mean: 74.5% correct). of blocks (block 1, 2 and 3) as well as the order of stimulation As three blocks were required for the TMS procedure, three (No TMS, rTMS over the left SMG and rTMS over the vertex) blocks of 24 trials (12 same, 12 different) were created, leaving were counterbalanced. 8 trials for a practice block. The three blocks were matched for To begin with the participants completed the practice difficulty based on the results of the first pilot test. A second phase of the pitch recognition task. In every trial two six-tone pilot test was then conducted, with 10 novel participants who long sequences were played through speakers at a comfort- completed the blocks in counterbalanced order and confirmed able listening level and the participant indicated by button that all three blocks were of equal difficulty (mean scores: press whether the sequences were the same or different. They 71.3%, 74.5%, 70.0%). were instructed to use their index and middle finger of their right hand to press “1” for same and “2” for different. Partici- 2.1.3. TMS protocol pants heard a burst of pink noise after each trial to minimize TMS was applied by a figure of eight shaped coil (70 mm carry over effects (Fig. 1 details the exact procedure). In- diameter) using a Magstim Super Rapid Stimulator (Magstim structions were given on screen and participants were asked Co., UK). The Stimulator was set to 60% intensity of the to respond as accurately and quickly as possible. After maximum stimulator output as per previous studies (e.g., completing the practice phase, the two stimulation sites, the Pitcher, Garrido, Walsh, & Duchaine, 2008; Tseng et al., 2010). left SMG and the vertex, were marked on the participant's rTMS was applied for every trial and a rTMS train lasted scalp. Finally, before beginning the experiment, one test trial 3 sec at 5 Hz (15 pulses). The coil was placed either over the of 3 sec of 5 Hz rTMS was applied to each site of stimulation, in targeted area, the left SMG or the vertex. The vertex was order to check that the participant was fine with the experi- included as a control site in order to control non-specific ef- ence of rTMS. The participants all reported that the perceptual fects such as tactile and auditory sensations. The left SMG was sensations for both stimulation sites were the same. located using CP3 of the 10e20 system for electrode place- Participants were instructed to concentrate on the se- ment, which has been shown to be a reliable method to quences they heard and to ignore the TMS pulses as far as identify this brain region (Mottaghy, Doring,€ Mu¨ ller-Gartner,€ possible. Instructions were given on screen, the coil was Topper,€ & Krause, 2002; Schaal et al., in press). The vertex placed according to the stimulation condition and the first was identified as the middle of the head, by measuring the block began, containing 24 trials. After completing one block point equidistant between the inion and nasion as well as the (with a short pause in the middle to exchange coils), a five left and right intertragal notches. minute break was taken before starting the next block. After The coil was placed above the stimulation site (left SMG or participants completed all three blocks, they filled in the Gold- vertex) throughout the trials and the correct localization was MSI questionnaire. In Experiment 1 rTMS was applied during Fig. 1 e Timing of a single trial for Experiments 1 and 2. In Experiment 1, 5 Hz rTMS was applied during the retention period and in Experiment 2, rTMS was applied during encoding of the first sequence. cortex 64 (2015) 310e317 313 the retention phase of each trial and in Experiment 2 rTMS but not encoding phase of pitch memory. However, it was applied during the encoding phase of the first pitch remained possible that this effect may be due to a non-specific sequence. modulation of motor performance. The left SMG has been reported to be involved in the process of motor attention 2.2. Experiment 1 and 2 results (Rushworth, Ellison, & Walsh, 2001) and, given the spatial distance between the left SMG and the motor cortex, one Median reaction times for correct trials were calculated, as might posit that the results of Experiment 1 could result from well as percent correct and d’ scores for the analysis of accu- an interference with motor responses. To address this possi- racy. The data from percent correct and the d’ score analysis bility, we conducted a control experiment in which rTMS was revealed the same pattern, so only the analysis from the more applied either late (reflecting the timing of the stimulation sensitive measure of d’ scores are reported in the following during retention) or early (timing of the encoding interference) results section. while participants completed a perceptual task (“is the last For the statistical analysis, three outliers were excluded tone higher or lower than the second to last tone?”) in which from the sample. One participant had reaction times more memory demands were minimal. than four standard deviations above the group mean and two participants had accuracy scores below chance in at least one 3.1. Experiment 3 methods block, indicating that they did not meet the task demands. 3.1.1. Participants 2.2.1. Reaction time analyses Twelve participants (seven female) with a mean age of 23.92 For Experiment 1, a repeated measure ANOVA was conducted years (SD ± 2.19, range 20e27 years) took part in Experiment 3. with stimulation condition (rTMS over left SMG vs rTMS over They were all non-musicians (less than two years of musical vertex vs No TMS) as the within-subject factor and reaction training in the past, not playing an instrument at present) times as the dependent variable. This analysis revealed a with a mean of 0.58 years of musical training and a mean ¼ ¼ main effect of stimulation condition [F(2,22) 6.50, p .006, Gold-MSI score of 10.5 (Table 1, see Section 2.1.1 for informa- 2 hp ¼ .371]. Contrasts revealed that the reaction times obtained tion about the Gold-MSI questionnaire). The ethics committee during rTMS over the left SMG were significantly slower than of the Medical Department of the Heinrich-Heine-University ¼ reaction times when rTMS was over the vertex [F(1,11) 21.66, in Du¨ sseldorf approved this study and participants gave ¼ h2 ¼ p .001, p .663] and also significantly slower than No TMS informed written consent. ¼ ¼ h2 ¼ performance [F(1,11) 5.10, p .045, p .317]. In sum, the results indicated that stimulation over the left SMG during the 3.1.2. Materials retention phase significantly disrupted the reaction times for The same six-tone long sequences were used. Experiment 3 pitch memory (Fig. 2). also consisted of three experimental blocks and a practice For Experiment 2, the same repeated measure ANOVA was block. Only the second sequence of every sequence pair was conducted. Unlike Experiment 1, there was no main effect of used for the perceptual task in Experiment 3. The three blocks ¼ ¼ stimulation condition for reaction times [F(2,22) 1.33, p .285, (24 trials each) all consisted of 12 trials where the last tone 2 hp ¼ .108]. When applying rTMS during encoding of the pitch compared to the second to last tone was higher and 12 trials sequence in the memory process, no differences were found where it was lower. (Fig. 2). Finally, a post-hoc analysis across the two experiments 3.1.3. TMS protocol was conducted. A mixed ANOVA on reaction times with The TMS parameters were the same as those reported in stimulation condition as the within-subject factor and experiment Experiment 1 and 2. The timeline for the TMS application was (Experiment 1 vs Experiment 2) as the between-subject factor, identical even though in Experiment 3 no first sequence was revealed a significant stimulation condition*experiment interac- played. The 3 sec long rTMS trains were either applied ¼ ¼ h2 ¼ tion [F(2,44) 6.83, p .003, p .237], confirming the differ- 3 sec before the tone sequence (late condition) or 6 sec before ential involvement of the left SMG during the retention and the tone sequence (early condition). A block without rTMS was encoding phases of pitch memory. also included. Stimulation was applied over the left SMG. 2.2.2. Accuracy analyses 3.1.4. Procedure For Experiments 1 and 2, two seperate repeated measure Participants completed three blocks of the perceptual task as ANOVAs were conducted with stimulation condition (3) as the part of the within subject design. The order of blocks (block 1, within-subject factor and accuracy measured by d’. No sig- 2 and 3) as well as the order of stimulation (no TMS, late rTMS ¼ nificant differences were found in Experiment 1 [F(2,22) .68, over the left SMG and early rTMS over the left SMG) were ¼ h2 ¼ ¼ ¼ p .519, p .058] or Experiment 2 [F(2,22) .19, p .832, counterbalanced. 2 hp ¼ .017] (Fig. 2). Before the experiment, participants completed a practice block of the perception task. After a 6 sec long pause (in which rTMS was applied at two different time points in the experi- 3. Experiment 3 mental blocks) a six-tone-long sequence was played and participants were asked to judge whether the last tone was The findings from Experiment 1 and 2 suggest a phase-specific higher or lower than the second to last tone. As in the first two disruption by modulation of the left SMG during the retention experiments, participants were asked to give their response as 314 cortex 64 (2015) 310e317 Fig. 2 e A Bargraphs representing the median reaction time scores for all three blocks for Experiment 1 (left) and Experiment 2 (right). rTMS over the left SMG during the retention period (Experiment 1) led to a significant increase in reaction times. No modulating effects could be found when applying rTMS during encoding (Experiment 2). The error bars represent SEM **p ¼ .002, *p ¼ .046 B Bargraphs representing the accuracy scores (d′) for all three blocks for Experiment 1 (left) and Experiment 2 (right). No significant effects of stimulation condition were found. The error bars represent SEM. accurately and quickly as possible using their index and 3.2. Experiment 3 results middle finger of their right hand and the keys “1” for “lower” and “2” for “higher. Participants heard a burst of pink noise 3.2.1. Reaction time analysis between every trial to minimize carry-over effects. The group mean reaction times for the block without stimu- After the practice block, the location corresponding to the lation were 440.54 msec (SD ± 186.09), for the early rTMS left SMG was marked on the participants scalp and a test train condition 448.67 msec (SD ± 191.91) and for the late rTMS of TMS was applied over the left SMG in order to make par- condition 423.08 msec (SD ± 207.65). ticipants familiar with the sensation of the stimulation before A repeated measure ANOVA with stimulation condition (late starting the actual task and to ensure that they were fine with rTMS vs early rTMS vs No TMS) as the within subject factor the perceptual sensation of TMS (as per Experiment 1 and 2). and median reaction times as the dependent factor revealed ¼ ¼ Participants then completed the three experimental no main effect of stimulation condition [F(2,22) .363, p .699, 2 blocks. The procedure was the same as that reported in hp ¼ .032]. rTMS over the left SMG at the late (reflecting the Experiment 1 and 2, except that the task was perceptual in time point of the retention interval) or early (reflecting the nature and not a memory task. Stimulation was applied ac- encoding phase) time point did not affect reaction times cording to the stimulation condition either late (3 sec before during the perception task compared to No TMS. the tone sequence) or early (6 sec before the tone sequence) over the left SMG. After completing all three blocks, partici- 3.2.2. Accuracy analysis pants filled in the German version of the Gold-MSI question- The mean d’ scores, reflecting the accuracy performance, for naire (Schaal, Bauer, & Mu¨ llensiefen, 2014). the block without TMS were 1.60 (SD ± 0.71), for the early rTMS cortex 64 (2015) 310e317 315 condition 1.55 (SD ± 0.75) and the late rTMS condition 1.30 (Zatorre & Belin, 2001). This finding, alongside the present (SD ± 0.52). study, corroborates the idea that TMS is an effective tool for A repeated measures ANOVA with stimulation condition (3) investigating the causal involvement of brain areas in pitch as the within factor and d’ scores was conducted and also processing. ¼ showed no main effect of stimulation condition [F(2,22) 1.67, The involvement of the left SMG for the retention phase in 2 p ¼ .21, hp ¼ .132]. The analysis showed no effects of stimu- memory has also been shown by Romero, Walsh, and Papagno lation condition on accuracy performance. (2006), who investigated the causal involvement of left parie- tal areas (Brodmann's areas 44 and 40, the latter is comparable with the location of the left SMG) for verbal short-term 4. Discussion memory. They showed that rTMS, applied during the reten- tion phase over the targeted areas (compared to the vertex), This study sought to investigate the causal role of the left SMG affected phonological judgments. This finding is also in across different time-specific stages of pitch memory pro- accordance with other studies that have reported SMG acti- cessing. Using a non-invasive brain stimulation method vation during tonal and verbal rehearsal (Schulze, Zysset, (rTMS), we disrupted the pitch memory process during the Mueller, Friederici, & Koelsch, 2012) using fMRI, and which retention (Experiment 1) and encoding (Experiment 2) phases have demonstrated involvement of the SMG in phonological of a recognition pitch memory paradigm. In both cases, processing and reading tasks using TMS (Celsis et al., 1999; stimulation over the left SMG was compared to performance Hartwigsen et al., 2010; Stoeckel, Gough, Watkins, & Devlin, without stimulation as well as stimulation over the vertex 2009). In this context, one may suggest the left SMG plays a (control site). The results showed that only rTMS over the left modality general role in auditory memory retention. It will be SMG during retention resulted in a significant increase in re- important for future studies to examine this directly. action times, therefore supporting the theory that the left SMG There is some debate with regards to the lateralization of is causally involved in the ongoing maintenance of pitch in- neural activity relating to pitch memory. Imm et al. (2008) formation in memory. A third experiment confirmed that applied single-pulse TMS at different time points (ranging rTMS over the left SMG at the two stimulation time points of between 250 msec and 800 msec after stimulus onset) over the Experiment 1 and 2 (late and early) did not have an effect on dorsolateral prefrontal and inferior parietal regions. They motor responses to a perceptual task; thus our findings from found that during the pitch task reaction times increased Experiment 1 cannot be explained by a non-specific modula- when stimulation was applied over the right inferior parietal tion of the motor cortex or motor attention. Taken together, site for all time points and for the audio-verbal condition only our three experiments support the critical involvement of the single-pulse TMS at 450 msec over the left inferior parietal left SMG during retention of pitch information in memory. cortex increased reaction times (Imm et al., 2008). These re- The increase in reaction times when rTMS was applied sults contribute to the understanding of how specialized over the left SMG in the retention phase supports previous neural mechanisms may be involved in different auditory tDCS evidence showing that pitch memory can be modulated domains. With reference to our study, it should be noted that following anodal or cathodal stimulation over the left SMG the parietal site targeted by Imm et al. (2008) was more pos- (Schaal et al., 2013; Vines et al., 2006). Our findings extend this terior to the SMG and also that the working memory task used prior work by showing that modulating neural activity in the by Imm et al. (2008) has different, more complex demands left SMG leads to a phase-specific shift in the retention, but not compared to the pitch memory tasks used in our study. The the encoding phase of the pitch memory processes. Several selective hemispheric involvement of the SMG in our results is previous studies have postulated that the left SMG is involved more comparable to the pitch memory recognition tasks that in pitch memory retention (Gaab et al., 2003; Sakurai et al., have been shown to be left lateralized (Gaab et al., 2003; Vines 1998; Vines et al., 2006), but we provide the first casual evi- et al., 2006). Furthermore, a tDCS study from our laboratory dence for the specific role of the left SMG in the ongoing (Schaal et al., in press) revealed that only cathodal stimulation maintenance of pitch traces as opposed to earlier encoding over the left SMG but not the right SMG led to a deterioration processes. of pitch memory performance in non-musicians. The present study is a step forward in investigating neural A broader caveat related to TMS studies relates to the distinctions of the auditory memory system for the different choice of active control site, which in our study was the vertex stages of memory processing (encoding, retention), a largely (based on the common use of this region in visual and audi- unexplored field. Previous non-invasive brain stimulation tory domains; e.g., Romero et al., 2006; Pitcher et al., 2008; studies using tDCS have revealed causal relationships be- Andoh & Zatorre, 2013; Banissy et al., 2010). The choice of an tween targeted areas and pitch memory (Schaal et al., 2013; active control site is frequently contentious and there is the Vines et al., 2006) and pitch discrimination (Mathys, Loui, possibility that the vertex may produce less superficial scalp Zheng, & Schalug, 2010), but few have used non-invasive effects relative to left SMG stimulation. However, if superficial brain stimulation to probe how different stages of process- effects of TMS caused the slower reaction times reported in ing may be influenced by cortical modulation. One rare TMS Experiment 1 then we would expect a similar effect in study on melodic pitch perception investigated the effect of Experiment 2. As this was not the case, it is unlikely that the off-line TMS (stimulation before the task) on melody results reported in Experiment 1 are due to non-specific gen- discrimination and found significant modulation effects of eral effects of TMS. Additionally, we acknowledge that using 10 Hz rTMS targeted over the right Heschl's Gyrus (Andoh & the 10e20 system for electrode placement is not the most Zatorre, 2011), a region associated with melody perception precise method to localize the left SMG. This method is 316 cortex 64 (2015) 310e317 commonly used for targeting brain areas in brain stimulation Celsis, P., Boulanouar, K., Doyon, B., Ranjeva, J. P., Berry, I., studies (e.g., Gallace, Soravia, Cattaneo, Moseley, & Vallar, Nespoulus, J. L., et al. (1999). Differential fMRI responses in left 2014; Imm et al., 2008; Schaal et al., in press) even though posterior superior temporal gyrus and left supramarginal gyrus to habituation and change ditection in syllables and brain imaging guided targeting would be desirable in future tones. NeuroImage, 9, 135e144. studies to optimize the precession of TMS. Ellis, R. J., Bruijn, B., Norton, A. C., Winner, E., & Schlaug, G. (2013). A further broader issue raised by our study relates to the Training-mediated leftward asymmetries during music constraints of the relatively modest sample sizes used in TMS processing: a cross-sectional and longitudinal fMRI analysis. experiments. We tested 12e14 participants in each experi- NeuroImage, 75,97e107. € ment, which is commensurate with the majority of TMS ex- Gaab, N., Gaser, C., Zaehle, T., Jancke, L., & Schlaug, G. (2003). periments. Although consistent with other work, a sample of Functional anatomy of pitch memory- an fMRI study with sparse temporal sampling. NeuroImage, 19, 1417e1426. this size does limit the ability to detect small effects that may Gallace, A., Soravia, G., Cattaneo, Z., Moseley, G. L., & Vallar, G. be of theoretical interest. In this regard, it is worth mentioning (2014). Temporary interference over the posterior parietal that our data hints at two interesting potential effects: firstly, in cortices disrupts thermoregulatory control in humans. PLoS Experiment 1 the d' scores were the lowest when stimulation One, 9, e88209. was applied over the left SMG and secondly, the reaction times Hartwigsen, G., Baumgaertner, A., Price, C. J., Koehnke, M., in Experiment 2 were decreased when rTMS was applied over Ulmer, S., & Siebner, H. R. (2010). Phonological decisions require both the left and right supramarginal gyri. the left SMG during encoding. These potential effects, which Proceedings of the National Academy of Sciences, USA, 107, were in line with our hypothesis, may have reached signifi- 16494e16499. cance if sample size and subsequently power had been Imm, J.-H., Kang, E., Youn, T., Park, H., Kim, J. I., Kang, J. I., et al. enlarged. The issue of modest sample sizes in TMS studies is an (2008). Different hemispheric specializations for pitch and important area for wider consideration in the TMS community. audioverbal working memory. NeuroReport, 19,99e103. In conclusion the present study demonstrates a causal role Koelsch, S., Schulze, K., Sammler, D., Fritz, T., Mu¨ ller, K., & for the left SMG in the retention phase of pitch memory. In Gruber, O. (2009). Functional architecture of verbal and tonal working memory: an fMRI study. Human Brain Mapping, 30, doing so, the finding broadens our knowledge regarding the 859e873. involvement of the left SMG in the pitch memory process: only Luber, B., Kinnunen, L. H., Rakitin, B. C., Eslsasser, L., Stern, Y., & rTMS during the retention phase of the pitch sequence Lisanby, S. H. (2007). Facilitation of performance in a working recognition task, and not encoding, modulated performance. memory task with rTMS stimulation of the precuneus: This result confirms that the left SMG is selectively involved in frequency- and time-dependent effects. Brain Research, 1128, e the ongoing maintenance of pitch information in memory and 120 129. offers avenues for future investigations on this topic. Mathys, C., Loui, P., Zheng, X., & Schalug, G. (2010). Non-invasive brain stimuation applied to Heschl's gyrus modulates pitch discrimination. Frontiers in Psychology, 1, 193. Mottaghy, F. M., Doring,€ T., Mu¨ ller-Gartn€ er, H. W., Topper,€ R., & Acknowledgments Krause, B. J. (2002). Bilateral parieto-frontal network for verbal working memory: an interference approach using repetitive transcranial magnetic stimulation. European Journal of We would like to thank Sven Thones€ for preparing the audi- Neuroscience, 16, 1627e1632. tory material for the pitch task. Mu¨ llensiefen, D., Gingras, B., Musil, J., & Stewart, L. (2014). The The work was supported by grants from the DAAD and G.A. Musicality of non-musicians: an Index for assessing musical Lienert Stiftung awarded to NKS. VJW was supported by a Vice sophistication in the general Population. PLoS One, 9, e89642. Chancellor's Fellowship from the University of Sheffield. MJB Pitcher, D., Garrido, L., Walsh, V., & Duchaine, B. C. 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