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Enhancement of Auditory-Evoked Potentials in Musicians Reflects an Influence of Expertise but Not Selective Attention

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Enhancement of Auditory-Evoked Potentials in Musicians Reflects an Influence of Expertise but Not Selective Attention Enhancement of Auditory-evoked Potentials in Musicians Reflects an Influence of Expertise but not Selective Attention Simon Baumann, Martin Meyer, and Lutz Ja¨ncke Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/20/12/2238/1759351/jocn.2008.20157.pdf by guest on 18 May 2021 Abstract & Instrumental tones and, in some instances, simple sine-wave demonstrate that the effect of selective attention on the audi- tones were shown to evoke stronger auditory-evoked responses tory event-related potential (AEP) has a different time course in musicians compared to nonmusicians. This effect was taken and shows a different topography than the reproduced effect of as an example for plasticity in the auditory cortex elicited by music expertise at the N1 component or the previously demon- training. To date, however, it is unknown whether an enlarged strated effect at the P2 component. N1 peak potentials were cortical representation for (instrumental) tones or increased unaffected by attention modulation. These results indicate that neuronal activity provoked by focused attention in musicians the effect of music expertise, which was traced by current den- accounts for the reported difference. In an attempt to system- sity mapping to the auditory cortex, is not primarily caused by atically investigate the influence of attention on the processing selective attention, and it supports the view that increased AEPs of simple sine wave and instrumental tones, we compared on tones in musicians reflect an enlarged neuronal representa- auditory-evoked potentials recorded from musicians and non- tion for specific sound features of these tones. However, inde- musicians. During the electroencephalogram recording, the par- pendent from the N1–P2 complex, attention evoked an Nd-like ticipants were involved in tasks requiring selective attention negative component in musicians but not in nonmusicians, which to specific sound features such as pitch or timbre. Our results suggests that plasticity also affects top–down processes. & INTRODUCTION tential (AEP) components or components of its magnetic Increasing evidence demonstrates that the auditory equivalent, the auditory-evoked field (AEF) (Kuriki, Kanda, cortex is susceptible to plastic alterations. Animal studies & Hirata, 2006; Shahin et al., 2005; Shahin, Bosnyak, showed reorganization in the primary auditory cortex (AI) Trainor, & Roberts, 2003, but see Lutkenhoner et al., 2006 of adult cats after cochlea damage (Rajan, Irvine, Wise, & for counterevidence). These effects mainly pertain to the Heil, 1993) and frequency training in monkeys resulted in AEP/AEF1 negativity N1 and the positivity P2. Enhance- an increased neuronal representation of the trained fre- ment of these components is also found after training to quency bands (Recanzone, Schreiner, & Merzenich, 1993). discriminate specific sound features (Tremblay, Kraus, A seminal study that reported plasticity effects in the Mcgee, Ponton, & Otis, 2001; Menning, Roberts, & Pantev, human auditory cortex (Pantev et al., 1998) observed in- 2000). creased magnetoencephalography (MEG) responses to Referring to the studies by Recanzone et al. (1993) with piano tones compared to sine-wave tones for pianists but trained monkeys, higher N1 and P2 amplitudes in music not for nonmusicians. This observation was interpreted as experts are usually interpreted as evidence for an in- an effect of long-term piano training. Meanwhile, some creased neuronal representation of (instrumental) tones of the original findings have been slightly revised. Several caused by intensive music training. However, not only a studies employing electroencephalography (EEG) or MEG higher number of stimuli-sensitive neurons but also a have provided evidence that instrumental tones elicit top–down shift of attention may result in increased audi- increased responses compared to sine-wave tones in non- tory activation and, finally, in increased auditory compo- musicians, too (Lutkenhoner, Seither-Preisler, & Seither, nent amplitudes in musicians. In order to understand 2006; Meyer, Baumann, & Jancke, 2006; Shahin, Roberts, how plasticity affects the functional organization of the Pantev, Trainor, & Ross, 2005). Nevertheless, the direct human brain, it is imperative to distinguish between tran- contrast of musicians to nonmusicians has been shown to sient top–down attention effects caused by a different reveal increased amplitudes in several auditory-evoked po- relationship of musicians toward musical stimuli and permanent alteration of the functionality of the cortex caused by intensive training, which is independent of the University of Zurich, Zurich, Switzerland current mental state. D 2008 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 20:12, pp. 2238–2249 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.2008.20157 by guest on 29 September 2021 As it has been previously recognized, top–down atten- naire (AHQ) (Annett, 1970) and the Hand Dominance tion processes influence activity in sensory cortices. Early Test (HDT) ( Jancke, 1996; Steingruber, 1971), all sub- studies are reviewed in Mangun (1995) and Alho (1992). jects were consistently right-handed. A group of 13 non- In a seminal AEP study, Hillyard, Hink, Schwent, and musicians (NM) (5 women, 8 men, mean age ± SD of Picton (1973) observed a negative displacement for at- 26.2 ± 1.5 years), with no formal musical training and no tended versus ignored stimuli at the latency of the N1. history of musical instrument performance, and a sec- It was proposed that this effect was caused by an en- ond group of 13 musicians (M) (4 women, 9 men, mean hancement of the N1 component (Woldorff & Hillyard, age ± SD of 25.6 ± 3.4 years), with a formal training 1991; Hillyard et al., 1973). Na¨a¨ta¨nen (1982, 1990) and starting at a mean age of 7.7 ± 2.7 years, took part in this Na¨a¨ta¨nen, Gaillard, and Mantysalo (1978) observed an study. All but one of the musicians were either music Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/20/12/2238/1759351/jocn.2008.20157.pdf by guest on 18 May 2021 top–down attention effect in a dichotic selective-listening students or members of an orchestra/jazz band and they task, which emerged as a negative shift or ‘‘negative dif- practice their instruments daily between 1 and 5 hours. ference’’ (Nd) (Hansen & Hillyard, 1980) of the attended Most of the musicians play multiple instruments of stimulus AEP in relation to the unattended stimulus AEP. which the most abundant were piano, violin, trumpet, The negative displacement began after the N1 deflection, and saxophone. All of the subjects gave written consent typically between the peaks of the auditory N1 and the P2 in accordance with procedures approved by the local component. The slightly disparate findings of attention ethics committee and were paid for participation. effect latencies led to an ongoing debate to what extent We presented a total of eight different tones using early attention effects reflect altered N1 and P2 compo- Hifi-headphones (HD 25-1, Sennheiser, Wedemark, Ger- nents or independent, additional components. However, many). The presented stimuli comprised short piano independent of the interpretation, attention components tones, trumpet tones, violin tones, and sine-wave tones coinciding with the N1 or P2 as well as increased N1–P2 at two different pitches (F4/349 Hz and B4/466 Hz, components evoked by attention are potentially alterna- American notation). The total number of 1280 stimuli tive explanations for increased AEPs in musicians. was presented in four blocks of 320 stimuli each. Details Most of the plasticity studies described above ad- of the stimuli are shown in Figure 1 and are described in dressed the problem of confounding attention effects Meyer et al. (2006). The stimuli were matched for by employing visual distractors (e.g., silent cartoon mov- intensity and the tones were presented at a sound ies) to turn the participants’ attention away from the pressure level of 55 dB (double checked by applying a auditory modality. However, it cannot be ruled out that digital sound level meter2). Each of the four tone classes musicians, compared to nonmusicians, show a stronger (sine wave, piano, trumpet, and violin) was presented tendency to direct their attention unintentionally to 80 times in one experimental block and 320 times in the instrumental tones or to specific sound features such as entire experimental session. Each block was made up of pitch or timbre when it comes to sound perception 40 F4 tones and 40 B4 tones per tone class. Tones were because these sounds and acoustic features are of high presented for 400 msec followed by a 1600-msec inter- professional relevance to this group. We conducted the stimulus interval (ISI). present study to systematically investigate the influence Stimulation and recording of responses were con- of top–down attention to music-relevant sound features trolled by the software Presentation (Neurobehavioral on the previously demonstrated enhancement of the N1– Systems, Albany, CA, USA). Each session comprised four P2 complex in musical experts. The role of bottom–up different tasks organized in blocks: (1) undirected listen- attention, such as sensory filters, was not investigated in ing (control), (2) pitch discrimination, (3) target detec- this study. The primary aim is to address the questions: tion (sine-wave tone), and (4) target detection (one out For which AEP components can we replicate an ampli- of three instrumental
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