A protective effect of musical expertise on cognitive outcome following brain damage.pdf

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 REVIEW A Protective Effect of Musical Expertise on Cognitive Outcome Following Brain Damage? Diana Omigie  & Severine Samson Received: 11 July 2014 / Accepted : 22 October 2014 /Published online: 8 Novembe r 2014 # Springer Science+Business Media New York 2014 Abstract  The current review examines the possibility that training-rel ated changes that take place in the brains of musi- cians may have a beneficial effect on their cognitive outcome and recovery following neurological damage. First, we pro-  pose three different mechanisms by which training-related  brain changes might result in r elatively preserve d function in musicians as compared to non-musicians with cerebral le- sions. Next, we review the neuropsychological literature ex- amining musical ability in professional musicians following  brain damage, specifically of vascular, tumoral and epileptic aetiology . Finally , given that assessment of musician patients can greatly inform our understanding of the influence of  premorbid experience on postmorbid recovery , we suggest some basic guidelines for the future evaluation of relevant  patients. Keywords  Musicians  . Brain dama ge  .  Neuroplast icity  . Lesion  . Training  . Cognitive outcome Introduction In the general population, music listening constitutes a ubiq- uitous activity that fulfils a range of functions, from passing the time to managing a listener s mood (DeNora 2000). How- ever, a subset of the population also undergo various forms of intense training that allow them to master complex musical activities such as singing, skillfully playing a musical instru- ment, composing musical pieces or directing an orchestra. Such musical training necessarily involves the simultaneous recruitment of a diverse range of neural processes including those involved in perception and cognition and those con- cerned with motor planning and execution. Consequently, it may be hypothesised that individuals who, through intense  practice, have mastered their musical skills to a profession al level, should differ from those who have never undergone such intense training, and thus lack such expertise. In the words of Santiago Ramon y Cajal,  Every man, if he  so desires , can become the sculptor of his own brain .  The highly influentia l histologist, often referred to as the father of modern neuroscien ce, argued that the many hours of   mental and muscular gymnastics  that musicians undergo during their training brings about neuroana tomical changes that ren- der them different to their non-musician counterp arts (Ramon y Ca ja l 1904/1999). A cen tury later, t his pr opos al is supp orte d  by numerous stud ies that exploit advan cements in anatom ical scanning and image processing techniques to show that the structure of the musician brain does indeed differ from that of non-musicians. Thus, adding to the ever growing literature D. Omigie : S. Samson Laboratoire de Neurosciences Fonctionnelles et Pathologies, EA4559, Universi té de Lille, Villeneuv e d Ascq, France S. Samson Unité dEpilepsie, GHU Pitié-Salpêtrière, Paris, France D. Omigie Ce ntr e de Re che rche de l In sti tutdu Cerve au et de la Moe lle Ep inière (CR ICM), UMR _S 975, and Cent re MEG-EE G - CENIR,Univers ité Pierre et Marie Curie-Paris 6, Paris, France D. Omigie CNRS, UMR 7225, CRICM and Centre MEG-EEG, Paris, France D. Omigie Inserm, U 975, CRICM and Centre MEG-EEG, Paris, France D. Omigie (*) CRICM, UMR72 25 / U975, CNRS / UPMC / Inserm, Instit ut du Cerveau et de la Moëlle Épinière (ICM), GHU Pitié-S alpêtrière, 47 Boulevar d de l Hopital, Paris, France 75013 e-mail: [email protected] D. Omigie Music Department, Max Planck Institute for Empirical Aesthetics, Frankfur t am Main, Germany  Neurops ychol Rev (2014) 24:445   460 DOI 10.1007/s11065-014-9274-5

Transcript of A protective effect of musical expertise on cognitive outcome following brain damage.pdf

  • REVIEW

    A Protective Effect of Musical Expertise on Cognitive OutcomeFollowing Brain Damage?

    Diana Omigie & Severine Samson

    Received: 11 July 2014 /Accepted: 22 October 2014 /Published online: 8 November 2014# Springer Science+Business Media New York 2014

    Abstract The current review examines the possibility thattraining-related changes that take place in the brains of musi-cians may have a beneficial effect on their cognitive outcomeand recovery following neurological damage. First, we pro-pose three different mechanisms by which training-relatedbrain changes might result in relatively preserved function inmusicians as compared to non-musicians with cerebral le-sions. Next, we review the neuropsychological literature ex-amining musical ability in professional musicians followingbrain damage, specifically of vascular, tumoral and epilepticaetiology. Finally, given that assessment of musician patientscan greatly inform our understanding of the influence ofpremorbid experience on postmorbid recovery, we suggest

    some basic guidelines for the future evaluation of relevantpatients.

    Keywords Musicians . Brain damage . Neuroplasticity .

    Lesion . Training . Cognitive outcome

    Introduction

    In the general population, music listening constitutes a ubiq-uitous activity that fulfils a range of functions, from passingthe time to managing a listeners mood (DeNora 2000). How-ever, a subset of the population also undergo various forms ofintense training that allow them to master complex musicalactivities such as singing, skillfully playing a musical instru-ment, composing musical pieces or directing an orchestra.Such musical training necessarily involves the simultaneousrecruitment of a diverse range of neural processes includingthose involved in perception and cognition and those con-cerned with motor planning and execution. Consequently, itmay be hypothesised that individuals who, through intensepractice, have mastered their musical skills to a professionallevel, should differ from those who have never undergonesuch intense training, and thus lack such expertise.

    In the words of Santiago Ramon y Cajal, Every man, if heso desires, can become the sculptor of his own brain. Thehighly influential histologist, often referred to as the father ofmodern neuroscience, argued that the many hours of mentaland muscular gymnastics that musicians undergo duringtheir training brings about neuroanatomical changes that ren-der them different to their non-musician counterparts (Ramony Cajal 1904/1999). A century later, this proposal is supportedby numerous studies that exploit advancements in anatomicalscanning and image processing techniques to show that thestructure of the musician brain does indeed differ from that ofnon-musicians. Thus, adding to the ever growing literature

    D. Omigie : S. SamsonLaboratoire de Neurosciences Fonctionnelles et Pathologies,EA4559, Universit de Lille, Villeneuve dAscq, France

    S. SamsonUnit dEpilepsie, GHU Piti-Salptrire, Paris, France

    D. OmigieCentre de Recherche de lInstitut du Cerveau et de laMoelle Epinire(CRICM), UMR_S 975, and Centre MEG-EEG - CENIR, UniversitPierre et Marie Curie-Paris 6, Paris, France

    D. OmigieCNRS, UMR 7225, CRICM and Centre MEG-EEG, Paris, France

    D. OmigieInserm, U 975, CRICM and Centre MEG-EEG, Paris, France

    D. Omigie (*)CRICM, UMR7225 / U975, CNRS / UPMC / Inserm, Institut duCerveau et de la Molle pinire (ICM), GHU Piti-Salptrire, 47Boulevard de lHopital, Paris, France 75013e-mail: [email protected]

    D. OmigieMusic Department, Max Planck Institute for Empirical Aesthetics,Frankfurt am Main, Germany

    Neuropsychol Rev (2014) 24:445460DOI 10.1007/s11065-014-9274-5

  • demonstrating structural and functional neurological differ-ences in various populations as a result of their continuedengagement in a specific, intense and complex activity(Maguire et al. 2000; Draganski et al. 2004; Draganski andMay 2008; Jancke et al. 2009), musicians provide an excellentexample of how the brain changes with training and an in-valuable model of cerebral plasticity (Driemeyer et al. 2008;Hyde et al. 2009; see Herholz and Zatorre 2012 for review).

    In the current review, we examine the possibility thatmusical training might not only bring about structural andfunctional changes in the brain of healthy individuals, butmight also have an influence on their cognitive outcome andrecovery following cerebral damage. The existing literaturetends to focus on cognitive outcomes of musical functions inmusicians. However, despite the lack of evidence in the liter-ature as it currently stands, one prediction that could be madeis that these structural and functional changes may also influ-ence cognitive outcomes of non-musical functions. With re-gard to content, the first section of the paper suggests threespecific hypotheses regarding how training related differencesin the musician brain may be expected to bring about pre-served musical ability following brain damage. In the follow-ing section, we then present an overview of the neuropsycho-logical literature examining cognitive outcomes in musicalfunctioning in brain-damaged professional musicians, specif-ically those with lesions or who have undergone surgicalresection for epilepsy. Critically, we suggest that the exami-nation of this neuropsychological literature can provide im-portant insights: firstly, into the extent to which a patientsrecovery of a given function is based on their premorbidexperience and secondly, into the incidence and rate of moregeneral functional recovery in musicians as well as theirprofessional prospects following surgery. Finally, in the thirdsection of the paper, given the important insights, which, weargue, may arise from the current approach of assessing cog-nitive outcomes following brain damage, we suggest someguidelines for future research.

    1) Potential implications of training-related differences inthe musician brain.

    There are various ways in which the structure andfunction of the musican brain differs from that of non-musicians as a result of training. Based on these, at leastthree hypotheses can be proposed regarding factors thatmay bring about preserved musical function in braindamaged musicians.

    a) Anatomical changes resulting in a greater likelihoodof preserved substrates

    Recent advancements in anatomical scanning andimage processing techniques have greatly encouragedthe study of the ways in which the musician brain isstructurally different from that of non-musicians.

    Specifically, with the technique known as Voxel BasedMorphometry, it is now possible to carry out quantita-tive and statistically rigorous analysis of the grey andwhite matter concentration of the whole brain (Wrightet al. 1995), while other techniques like DiffusionMagnetic Resonance Imaging (dMRI) allow re-searchers to carry out detailed analysis of white matteranatomical features (Basser and Jones 2002; Johansen-Berg and Behrens 2009). These techniques, along withfunctional imaging methods, have shown that musi-cians brains are characterized by increased volume inseveral areas. For instance, in one of the first studies todemonstrate training-specific changes in cortical anat-omy, Elbert and colleagues (Elbert et al. 1995) usedmagnetic source imaging to show that in line with theincreased finger movements string players carry outwith the left hand, cerebral representations of the digitsof the left hand were substantially larger than those ofcontrols. The authors went as far as showing that thisgroup effect was absent in the right hand and smallestin the left thumb (in line with extent to which theseengage in fine finger movements). They also demon-strated a relationship between the observed changes incortical territory and the age at which the musiciansbegan to play their instrument.

    Schneider and colleagues (2002) showed that thegrey matter volume of the antero-medial portion of theHeschls gyrus, (considered the primary auditory cor-tex), was not only 130 % larger in musicians than non-musicians but also correlated with musical aptitude asmeasured by the Advanced Measures of MusicAudiation (AMMA) tonal test (Gordon 1989). Gaserand Schlaug (2003), in addition to confirming greymatter volume differences in auditory brain regionssuch as the left Heschls gyrus between musicians(professional keyboard players) and a matched groupof amateur and non-musicians, also provided evidencethat motor-related structures such as the primary motorand premotor regions as well as the cerebellum(Hutchinson et al. 2003) is expanded in musicians.Also striking is that the anterior half of the corpuscallosum (Schlaug et al. 1995; Schlaug 2001) has beenshown to be larger in musicians compared to non-musicians suggesting greater communication betweenthe hemispheres by virtue of a larger number of fibrescrossing through this region. More recently, in furtherdemonstration that musical training brings about arange of morphological and anatomical changes, whitematter structure has been shown to change with degreeof musical expertise (for instance, with years of pianotraining: Bengtsson et al. 2005) and results suggest thatmusicians have a larger volume and better organizationof connections between temporal and frontal lobe

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  • regions (Halwani et al. 2011). Interestingly Halwaniet al. (2011) not only found differences between mu-sicians and non-musicians in the macro and microstructure of the arcuate fasciculus but they were ableto show further differences between instrumentalistsand singers that could account for the long term vocalmotor training carried out by the latter. Finally, thatanatomical changes which were observed at the sen-sorimotor level after approximately a year of musicalpractice in children were accompanied by improve-ments in auditory perception and motor skills (Hydeet al. 2009) demonstrates the relationship betweenanatomical variations and musical abilities in musicalexperts (Foster and Zatorre 2010).

    The volume changes observed as a function ofexpertise are particularly pertinent when one considersthat the volume of preserved neural substrate followingbrain damage may be related to preservation of cogni-tive function. Such a hypothesis has already been putfoward in the vast literature on Brain and CognitiveReserve (Stern 2002). Models described in this litera-ture have sought to explain certain paradoxical phe-nomena in cerebral aging and stroke patients; such aswhy some older adults fail to show typical clinicalsymptoms of Alzheimers disease in life despite post-humous evidence that they had the pathology, or why astroke of a given magnitude may result in severeimpairment in one patient but not another. In one groupof models, reserve has been taken to describe an activeprocess whereby alternative strategies are used to carryout a function (Stern et al. 2005; Stern 2006). Howev-er, in another group of models, reserve is simply asso-ciated with the extent to which cerebral damage hasdepleted neural substrates (Mortimer et al. 1981;Katzman 1993; Satz 1993). This latter group of modelstends to allude to a theoretical construct known asbrain reserve capacity, which has been associated withsuch biological measures as number of synapses andbrain size. A major assumption of these models is thatbrain reserve capacity may differ across individuals butthat there exists a fixed threshold that must be reachedbefore deficits in brain function arise. Specifically,according to these models, differences in cognitiveoutcomes, given a lesion of a particular size (or adegenerative process), are observed due to the size ofbrain reserve capacity. The threshold of brain damagenecessary to bring about a given deficit is more quicklyreached in individuals with lesser brain reserve capac-ity than those with greater brain reserve capacity,resulting in greater likelihood of impairments in theformer.

    Performing structural MRI on a large group ofstroke patients, Srkm et al. (2009) demonstrated

    that those patients with less extensive damage to theauditory cortex and frontal lobe also showed less ex-tensive auditory and musical dysfunction. Such a find-ing supports the notion of a relationship between thevolume of preserved neural substrate and cognitiveoutcome. By extension, all else being equal (specifi-cally the size of a lesion), it may be predicted thatpreserved or near preserved cognitive outcome willbe more likely in an individual who possesses, beforedamage, more extensive substrate (larger brain reservecapacity) than in one who possesses less extensivesubstrate (smaller brain reserve capacity). The notionthat a greater quantity of neural substrate results insuperior function also finds support in studies showinga correlation between integrity of white matter struc-tures and both music cognitive ability and other typesof behaviour (Hyde et al. 2006; Catani and Mesulam2008; Loui et al. 2009; Johansen-Berg 2010;Johansen-Berg et al. 2010). In line with the literatureon reserve, we suggest that given the greater volume ofgrey and white matter and consequently greater brainreserve capacity inmusicians relative to non-musicians(in specific and non specific brain areas followingtraining), a lesion of a given size may be less likelyto result in clinical symptoms in the former relative tothe latter.

    b) Greater redundancy in the musician brain and accessto different strategies

    A growing body of literature suggests that musi-cians differ from non-musicians in terms of the dis-tribution of neural substrates involved in music pro-cessing (Ohnishi et al. 2011; Munte et al. 2002;Habibi et al. 2013). In a seminal study using thedichotic listening experimental technique, Bever andChiarello (1974) observed that as musicians capac-ity for musical analysis increases, the left hemispherebecomes increasingly involved in the processing ofmusic (p. 539). Indeed, a number of studies havenow demonstrated that, in addition to the holisticmanner (subserved by the right hemisphere) in whichnon-musicians process pitch patterns, musicians also,as initially proposed by Jackson (1932), carry outmore analytical forms of pitch pattern processingusing their left hemisphere. Peretz and Morais(1980) showed that, during a melody recognitiondichotic listening task, non-musician participantswho carried out more analytic processing (havingbecome aware of the dimensions manipulated bythe experimenter) had a right ear advantage (suggest-ing left hemisphere predominance) and in doing sodemonstrated that formal musical training is not nec-essary for involvement of the left hemisphere of thebrain. However, various lines of evidence suggest

    Neuropsychol Rev (2014) 24:445460 447

  • that musicians are generally less likely than non-musicians to limit themselves to one mode of process-ing. For instance, Peretz and Babai (1992) demon-strated that, when required to recognise melodies in aprobe recognition task, musicians were not confinedto the left hemisphere based analytic mode of process-ing but could flexibly use either contour or intervalinformation, involving global and analytic processingrespectively. Similarly, work fromHabibi et al. (2013)showed that while non-musicians will mostly rely onthe right hemisphere for detecting pitch deviations,musicians will usually recruit both hemispheres whilecarrying out such tasks.

    These studies are important in showing that themusician brain possesses a greater degree of redun-dancy than the non-musician brain and/or may haveaccess to multiple strategies for carrying out a musicaltask. The important implication of such a state ofaffairs is that brain damage may not have the samedegree of impact on musical skills in musicians andnon-musicians. Specifically, one hypothesis could bethat circumscribed damage, for instance limited to theright hemisphere, might result in preserved cognitivefunction in musicians who can easily use the lefthemisphere to carry out pitch and melody processing.In contrast, it could bring about impaired function innon-musicians who have not developed the left hemi-sphere based analytical processing of pitch informa-tion to an equivalent extent. Indeed, the current hy-pothesis shares a lot in common with the, previouslydiscussed, so called active cognitive reserve modelsthat suggest that preserved function may be observedin some individuals as a result of recruitment of alter-native brain networks that have not been damaged(Stern 2002; Stern et al. 2005; Stern 2006). In otherwords, those models which suggest that individualswho can use another strategy when a more standardone is impaired will be more likely to show preservedability compared to those individuals who have noalternative approaches.

    Such a notion of differences at the level of availablestrategies is distinct from the notion of differences inthe quantity of residual cerebral substrate as referred towhen describing the potential implications of differ-ences in anatomical changes in the musician brain.Indeed, the notion that differences in cognitive out-comemay be accounted for in terms of the availabilityof alternative cognitive strategies may also be seen inthe Reorganization of Elementary Functions (REF)model of Mogensen and Mal (2009). The authorsobserved that, very often in the neuropsychologicalliterature, functions may be preserved despite damageto what had been thought of as essential cerebral

    substrates for that function. To explain this phenome-non, these authors described cognitive ability withrespect to three different levels of realization. On themost basic level, they describe so called elementaryfunctions (EFs) as information processing modulestruly localized in the sense that they are mediated bylocal circuitry within a structure of the brain. Theyargue that these EFs, however, stand in contrast to so-called algorithmic strategies (ASs), which, in turn,are made up of numerous interacting EFs. Important-ly, the model proposes that the psychologicalfunctions, the third realization level, are more closelyassociated with ASs than with EFs. Specifically, itsuggests that the same surface phenomena or psycho-logical functions may arise from potentially numerousdifferent ASs, which in turn are comprised of aninteraction of different sets of EFs. Thus, accordingto Mogensen et al. (2009, 2011) the possession of agreater number of EFs may bring about greater oppor-tunities for the creation of new ASs, resulting in agreater likelihood of preserving a cognitive function.

    Importantly, findings showing that musicians usemore parts of the brain to carry out a given musicalfunction would seem to suggest that, due to plasticitymechanisms following high levels of training, musi-cians have an increased number of elementaryfunctions. The consequence of this, according toMogensen and Mal (2009), is a greater potentialnumber of algorithmic strategies resulting in a great-er tendency for preserved cognitive function follow-ing brain damage. It remains to be clarified to whatextent such changes due to musical training maybenefit non-musical function. However, the fact thatmusicians can make better use of both hemispheresduring musical processing has been put forward as areason why abilities in musicians may be robust tobrain surgery (Schulz et al. 2005).

    c) Greater metaplasticity in the musician brain.First referred to as such by Abraham and Bear

    (1996), metaplasticity may be defined as the plastic-ity of synaptic plasticity or in other words, the abilityto learn how to learn. Critically, it refers to the phe-nomenon whereby a synapses plasticity is influencedby its previous history.

    There is some initial evidence that musical trainingendows musicians with greater metaplasticity thannon-musicians. Ragert and colleagues (2004) soughtto examine the altered sensorimotor cortical represen-tation that had been shown to be induced by musicaltraining. Their study revealed that not only do musi-cians, when compared with non-musicians, have low-er discrimination thresholds in terms of tactile spatialacuity, but also that musicians had a greater capacity

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  • to further reduce these thresholds over the course of afew hours. They also showed that this effect in musi-cians correlated with how much they practiced on aregular basis and in doing so demonstrated a relianceof metaplasticity on extent of use. An increased ca-pacity for plastic reorganisation in musicians has alsobeen demonstrated in a Transcranial Magnetic Stim-ulation (TMS) study that showed greater motor corti-cal excitability and plasticity in musicians than innon-musicians (Rosenkranz et al. 2007). Watanabeand colleagues (2007) went further in showing thatmetaplasticity might be greater in musicians whostarted practice during the sensitive period of musicaldevelopment: within the first 7 years of life (Penhune2011). Importantly, these findings suggest that musi-cians will be better than non-musicians in relearningfunctions that have been impaired by brain damage.However, unfortunately, while efforts are being madeto relate the changes seen at a molecular level to thoseseen at a structural, functional and behavioural level(Zatorre et al. 2012), these links still remain unclearand further studies will be needed to understand, forinstance, how synaptic changes may be related toincreases in the grey and white matter observed inmusicians or the increased modulation of their so-matosensory and motor cortex excitability.

    In sum, we suggest three ways in which the musi-cian brain may be equipped to preserve musical func-tion, or alternatively encourage its significant recov-ery following brain damage. We now examine theliterature for any evidence to suggest that musicalfunction may indeed tend to be preserved in musi-cians despite brain damage.

    2) Neuropsychological literature on cognitive outcomesA number of reviews have examined general music

    cognitive outcomes in non-musician patients followingbrain lesions and surgery (Benton 1977; Marin and Perry1999; Samson 1999; Stewart et al. 2006; Lechevalieret al. 2007; Maguire 2012). While they do not omitreferring to cases where brain lesions result in cognitivedeficits like aphasia while leaving music intact (Hbertet al. 2003; Peretz et al. 2004; Wilson et al. 2006), thesereviews have tended to highlight the vast literature inwhich non-musicians acquire disorders of music listeningfollowing vascular, epileptic or traumatic lesion. Stroke,for instance, can cause a range of cognitive deficits withrespect to language, memory, attention and orientationand attempts have been made to look at patterns ofincidence (e.g. Tatemichi et al. 1994). Certainly, in thereviews of postmorbid musical abilities in non-musicians,the non-musicians reported on are shown to also sufferfrom some of such other deficits. Unfortunately the extentto which music is affected or spared compared to these

    other features is not clearly detailed due to a lack ofsystematic documentation of the full spectrum of cogni-tive impairments that may be seen in stroke and braindamaged patients. However we argue that perhaps evenmore interesting (and more plausible, given that they aremore likely to be tested) may be to specifically examinethe cognitive outcomes in professional musicians. Cer-tainly of specific interest would be the nature of theseoutcomes given the musicians extensive premorbid mu-sical ability.

    To this end, case reports were accumulated followingsearches on Pubmed and Psychinfo that employed thekeywords epilepsy, stroke, brain damage, lesion,tumour and musicians and were published from theyear 1900 onwards. Other relevant studies cited in thepapers obtained from these searches were included. Re-ports were limited to professional musicians and teachers,as opposed to amateur musicians, and only studies withsufficient detail (of the state of expressive and receptivemusical abilities) were included.

    Table 1 provides a summary of case reports of 35brain-damaged musicians following lesions of differentaetiologies (stroke, tumour and epilepsy surgery), whowere identified through this procedure. It is important tobear in mind that biases may exist in the literature where-by a musician who has lost function is more likely to bereported than one who has not (Stewart et al. 2006).Indeed, a first look reveals that in more than half of thecases (20 out of 35), musical abilities in musicians areimpaired following brain damage. Out of these 20 cases,the loss of musical abilities is accompanied by languagedeficits (12 patients: e.g. Souques and Baruk 1926; 1930;Alajouanine 1948; Jellinek 1956; Brust 1980, case 2)roughly in the same number of cases as it is not (8patients: e.g. Judd et al. 1979; McFarland and Fortin1982).1 Whereas, in half of the cases, there is at leastsome damage to both receptive and expressive musicalabilities (11 cases), in cases of dissociation, the loss ofreceptive but not expressive musical function (7 cases) ismore frequent than the reverse (2 cases). Further, inaddition to studies documenting severe and global impair-ments at either the receptive or expressive level or both, anumber of other cases demonstrate fairly isolated deficitsin specific skills such as music writing, music reading orthe discrimination and production of rhythm (9/20: e.g.Horikoshi et al. 1997; Midorikawa and Kawamura 2000;Di Pietro et al. 2004).

    1 In line with the evidence of double dissociation of musical and languagecognitive abilities, cases of loss of language ability without any loss inmusical ability are also seen (8 patients).

    Neuropsychol Rev (2014) 24:445460 449

  • Table1

    Asummaryof

    case

    reportsof

    braindamaged

    patients

    Author

    Details

    Musical

    expertise

    Aetiology

    Regions

    affected

    Language

    abilities

    Musicalabilities

    Specificmusic

    difficulty

    Receptive

    Expressive

    Alajouanine

    1948

    58yearsold

    Com

    poser

    Uncertain

    Likelylefthemisphere

    Impaired

    Spared

    Impaired

    Assal1973

    64yearsold

    Conductor/Pianist

    Infarction

    Lefthem

    isphere

    Impaired

    Spared

    Spared

    AssalandButtet1983

    54yearsold

    Pianist/O

    rganist+

    Musicteacher

    Lesion

    Leftposterior

    temporo-parietalregion

    Impaired

    Spared

    Spared

    Basso

    and

    Capitani1985

    67yearsold

    Violinist

    Infarction

    Bilateral:

    Lefttem

    poro

    parieto-occipital

    lobe

    andrightposterior

    temporalregion

    Impaired

    Spared

    Spared

    Botez

    and

    Wertheim1959

    20yearsold

    Accordionist

    Tum

    our

    Rightfrontallobe(posterior

    middleand

    superior

    frontalgyrus)+likelypars

    triangularis+likelysubcorticalregions

    Spared

    Spared

    Impaired

    Brust1980

    (case2)

    42yearsold

    Jazz

    bassist

    Infarction

    Leftposterior

    temporalregionandinferior

    parietallobule

    Impaired

    Impaired

    Impaired

    Cappelletti

    etal.2000

    51yearsold

    Pianist/G

    uitarist

    +Com

    poser

    Lesion

    Bilateral:Leftposterior

    temporallobe+

    smallerrightoccipito-tem

    poral-parietal

    junction

    Spared

    Impaired**

    Spared

    Reading,w

    riting

    DiP

    ietroetal.2004

    48yearsold

    Singer

    Infarction

    Leftsuperiortemporalgyrus,posterior

    part

    ofmiddletemporalgyrus,and

    inferior

    parietallobule

    Impaired

    Impaired**

    Impaired**

    Rhythm

    Fasanaro

    etal.1990

    72yearsold

    Violinist

    Infarction

    Lefttem

    poro-parieto-occipitalregion,

    splenium

    andthalam

    us(m

    edialregion)

    Impaired

    (mild

    anom

    icaphasia)

    Impaired**

    Spared

    Musicreading

    andwriting

    (pitch)

    Finkeetal.2012

    68yearsold

    Cellist

    Lesion

    Bilateral:Rightmedialtem

    porallobeand

    lefttemporal(largesections),frontaland

    insularcortex

    (smallersections).

    Impaired

    Spared

    Spared

    Galarza

    etal.2014

    36yearsold

    Jazz

    guitarist

    Resectiontotreat

    medically

    intractable

    epilepsy

    Lefttem

    porallobe(extensive)andpossible

    slightatrophyof

    frontaland

    parietallobes+

    abnorm

    allysm

    allrighthemispherevolume

    Spared

    Spared

    (Fully

    recovered)

    Spared

    (Fully

    recovered)

    Horikoshietal.1997

    26yearsold

    Pianist

    Resectionof

    hematom

    aLeftoccipito-tem

    poraldeepwhitematter

    surroundingthetrigone,posteriorhorn

    ofleftlateralventricleandsplenium

    ofthe

    corpus

    callosum

    Spared

    Impaired**

    Spared

    Musicreading

    Jellinek1956

    (case1)

    46yearsold

    Singer/Guitarist

    Glioma

    Leftfrontallobe

    Impaired

    Impaired

    Impaired

    Judd

    etal.1979

    51yearsold

    Com

    poser+

    Musicteacher

    Infarction

    Rightfronto-parietaland

    posteriortemporal

    regions

    Spared

    Impaired

    Impaired

    Judd

    etal.1983

    77yearsold

    Com

    poser

    Infarction

    Leftoccipito-tem

    porallobe

    Impaired

    Spared

    Spared

    Kaw

    amuraetal.2000

    57yearsold

    Trombonist

    Haemorrhage

    Leftparietal(angulargyrus)regions

    Impaired

    Impaired**

    Spared

    Musicreading

    andwriting

    LevinandRose(1979)

    58yearsold

    Drummer

    Resectionof

    tumour

    Leftsplenio-occipitalregionandoccipitalpole

    Spared

    Impaired

    Impaired

    (mild)

    Luriaetal.1965

    57yearsold

    Com

    poser

    Infarction

    Lefttem

    poraland

    inferior

    parietalregions

    Impaired

    Spared

    Spared

    Mavlov1980

    61yearsold

    Violinist+

    Musicteacher

    Infarction

    Leftposterior

    inferior

    parietaland

    parieto-temporalregions

    Impaired

    Impaired**

    Impaired

    Rhythm

    McFarland

    and

    Fortin1982

    78yearsold

    Organist

    Infarction

    Rightsuperior

    temporaland

    parietal(superior

    marginal)regions

    Spared

    Impaired

    (mild)

    Impaired

    450 Neuropsychol Rev (2014) 24:445460

  • Table1

    (continued)

    Author

    Details

    Musical

    expertise

    Aetiology

    Regions

    affected

    Language

    abilities

    Musicalabilities

    Specificmusic

    difficulty

    Receptive

    Expressive

    Midorikaw

    aand

    Kaw

    amura2000

    53yearsold

    Pianoteacher

    Lesion

    Leftsuperiorparietallobule(corticaland

    subcortical)

    Spared

    Impaired**

    Spared

    Musicwriting

    Midorikaw

    aetal.2003

    62yearsold

    Pianoteacher

    Infarction

    Leftsuperiortemporalgyrus

    toangulargyrus

    (parietalregion)

    Impaired

    Impaired**

    Impaired**

    Rhythm/S

    inging

    Russelland

    Golfinos2003

    (case1)

    28yearsold

    Singer

    Resectionof

    tumour

    RightHeschls

    gyrus

    Spared

    Spared

    (transient

    3weekdeficits)

    Spared

    (transient

    3weekdeficits)

    Schulzetal.2005

    (case1)

    45yearsold

    Organist

    Resectiontotreatm

    edically

    intractableepilepsy

    (benigntumour)

    Rightanterior

    andlateraltem

    porallobe

    extendingtohippocam

    pus

    Spared

    Spared

    (self-assessment)

    Spared

    (self-assessment)

    Schulzetal.2005

    (case2)

    45yearsold

    Trumpeter+

    musicteacher

    Resectiontotreatm

    edically

    intractableepilepsy

    (hippocampalsclerosis)

    Rightmediantemporallobeincluding

    hippocam

    pus

    Spared

    Spared

    (self-assessment)

    Spared

    (self-assessment)

    Schulzetal.2005

    (case3)

    34yearsold

    Organist

    Resectiontotreatm

    edically

    intractableepilepsy

    (hippocampalsclerosis)

    Leftm

    ediantemporallobeincludinganterior

    hippocam

    pusandinferior

    amygdala

    Spared

    Spared

    (self-assessment)

    Spared

    (self-assessment)

    Schnetal.2001

    65yearsold

    Organist

    Ischem

    iclesion

    Leftparieto-tem

    porallobe

    Spared

    Impaired**

    Spared

    Musicreading

    Signoretetal.1987

    77yearsold

    Com

    poser/

    organist

    Infarction

    Lefttem

    poro-parietalregion

    Impaired

    Spared

    Spared

    SouquesandBaruk

    1926;1930

    NS

    Pianoteacher

    Infarction

    Leftposterior

    superior

    temporalregionand

    angulargyrus(parietalregion)

    Impaired

    Impaired

    Impaired

    Stanzioneetal.1990

    26yearsold

    Musicteacher

    Lesion

    Leftposterior

    temporo-parietallobe

    Impaired

    (slightly

    anom

    ic)

    Impaired**

    Spared

    Musicreading

    Teraoetal.2006

    62yearsold

    Singer

    Infarction

    Rightsuperior

    temporalcortex,parietalregions

    (supramarginalgyrus

    andpostcentralgyrus),

    posteriorinsula

    Impaired

    (mild)

    Impaired

    Impaired

    Tzortzisetal.2000

    74yearsold

    Com

    poser

    Infarctionandor

    degenerativeatrophy

    Bilateral:Bothhemispheres

    Impaired

    Spared

    Spared

    Wertheimand

    Botez

    1961

    40yearsold

    Violinist

    Vascularinjury

    Leftposterior

    superior

    temporalgyrus

    Impaired

    (mild)

    Impaired

    Impaired

    (mild)

    Wilson

    etal.2013

    26yearsold

    Singer

    Resectiontotreatm

    edically

    intractableepilepsy

    Rightinferior

    andmiddletemporalgyrus,

    Parahippocam

    palgyrus,H

    ippocampus,

    Amygdala

    Spared

    Spared

    Spared

    Zatorre1989

    17yearsold

    Violinist

    Resectiontotreatm

    edically

    intractableepilepsy

    Leftanteriortemporallobeincluding

    hippocam

    pus.

    Impaired

    Spared

    Spared

    Impaired**

    indicatesgeneralpreservationof

    functionapartfromthespecificdifficultyreported

    inthespecificmusicdifficultycolumn

    Neuropsychol Rev (2014) 24:445460 451

  • Importantly, a closer examination shows that reportedmusical deficits are often predictable by the specific ce-rebral substrates affected. The superior temporal gyrushas been shown to be specialized in auditory processingmore generally and the processing of pitch, timbre andmelodic contours more specifically, using a range ofprocedures including cortical stimulation in patients dur-ing surgery (Celesia 1976), intracranial recordings inpresurgical patients (Ligeois-Chauvel et al. 1991) andlesion studies in non-musician humans (Samson 1999;Stewart et al. 2006). Accordingly, it may be noted thatthose musicians with extensive music receptive deficitshave tended to show at least some damage to the superiortemporal gyrus in line with this areas importance in suchprocessing (e.g.Wertheim and Botez 1961; McFarlandand Fortin 1982). Conversely, deficits of, for instance,music reading or writing tend to implicate other regions inthe occipital and parietal cortex: For instance, the patientfrom Midorikawa and Kawamura (2000) who presentedwith musical agraphia in the absence of any other expres-sive or receptive forms of amusia had damage to the leftupper parietal lobe in line with previous evidence of itsspecific role in agraphia, while similarly, the young pia-nist reported by Horikoshi et al. (1997) presented withdifficulties in music reading after brain damage that af-fected the left occipital parasplenial region but spared thesuperior temporal gyrus. Taken together, these studies areimportant in showing that musicians are highly suscepti-ble to deficits following cerebral damage and further thatin the majority of cases, the deficits shown by musicianpatients are predictable by the localization of damagedregions.

    However, having considered these cases of loss offunction in musician patients which constitute the major-ity of reports, it is interesting to consider those caseswhere preserved function has been reported. Indeed, giv-en the well documented bias in the literature whereby aloss of function is more likely to be documented than apreservation of function, it is interesting that up to 15 outof 35 patients were spared on both receptive and expres-sive musical function, often despite at least some damageto the temporal lobe area (Luria et al. 1965; Assal andButtet 1983; Judd et al.1983; Basso and Capitani 1985;Signoret et al. 1987). For instance, the patient of Bassoand Capitani (1985) continued to be able to play the pianoand to conduct his orchestra successfully despite a severeideomotor and ideational apraxia following damage toboth the left temporo-parieto-occipital lobe as well asthe posterior part of the right temporal lobe. The authorsobserved that, the patient was able to programme andexecute gestures with a high praxic content when theywere the motor expression of musical processing. Simi-larly interesting is the case of the blind organist who lost

    the ability to read the alphabet (braille) but continued tobe able to read and play music after damage to the lefttemporoparietal cortex (Signoret et al. 1987).2 Reviewingthe neuropsychological literature on music reading,Hebert and Cuddy (2006) would observe that althoughthere were numerous studies where musicians showedtext-reading difficulties in the absence of music-readingdifficulties, there was only one case of a musician show-ing a selective impairment in music reading i.e. without adeficit in text-reading as well (Cappelletti et al. 2000).The existence of a selection bias, whereby, for instance,less attention may be paid to a music reading disorderthan to a text reading disorder (even in musicians), shouldbe borne in mind. Nevertheless, it is relevant to considerhow authors have tried to account for the specific pres-ervation in the musical domain of an otherwise compro-mised function (Tzortzis et al. 2000). Indeed, to explainwhy their patient M.M., whose progressive aphasia afterdamage to both hemispheres led to a severe deficit innaming that failed to extend to the naming of musicalinstruments, Tzortzis et al. (2000) would suggest an effectof overlearning. Specifically, they would suggest thatthe intensive practice and early acquisition of music mayhave provided M.M. with protection against loss of mu-sical skills in the event of brain damage.

    At this point, it is perhaps worth considering the body ofanimal work that has examined the extent to whichoverlearningmay lead to protection following brain damage.In these experiments, more trials than the criterion neededfor mastery of a skill are presented to the animal model andthen the effect of such overtraining on the ability to relearnthe task following brain damage is reported. Indeed whilethere are some reports of failures of overlearning to beprotective (e.g. Bignami et al. 1968) there are nonethelessseveral case of overlearning resulting in preserved ability torelearn following brain damage (Chow and Survis 1958;Orbach and Fantz 1958; Weese et al. 1973)

    The majority of studies in the literature document musi-cians who have undergone damage after lesions due tostroke and tumours. However, it is important to considerthe aetiology of damage given the influence this might beexpected to have on outcome. Indeed, 9 out of the 35 casesreported involved resection (for intractable epilepsy or he-matomas or tumours) and it is interesting to note that in allbut two of these cases, a preservation or recovery of bothreceptive and expressive musical function was reported.Indeed, apart from the drummer patient of Levin and Rose(1979) who presented with a range of deficits (e.g. music

    2 Although these cases are in the left hemisphere, it is important to notethat left hemisphere damage can cause deficits as evidenced by the factthat all but 4 of the 20 previously reported to have impairments showedtheir deficits after damage to the left cerebral hemisphere. Why so fewcases of right hemisphere damage have been reported is not clear.

    452 Neuropsychol Rev (2014) 24:445460

  • reading and discrimination of pitch pattern and time interval)following resection of parts of left the occipital lobe in aprocedure that involved cutting part of the corpus callosum(the splenium), and the pianist from Horikoshi et al. (1997)who showed difficulty with music reading following dam-age to the occipital and temporo-parietal lobe, all the othermusicians showed only transient difficulty, if any, and aremarkable preservation of musical ability/ recovery of mu-sical function following lateral and medial temporal loberesection (7/9). Zatorre (1989) reported that, following ananterior left temporal lobectomy for the relief of medicallyintractable seizures, a 17-year-old epileptic pianist with ab-solute pitch showed no loss of function but rather an im-provement after surgery in the notation of single pianotones3 as well as high proficiency in the recall of three-note sequences despite showing an impairment in the equiv-alent verbal task (as is typically expected following a lefttemporal lobe lesion with a significant hippocampal resec-tion in the predominant hemisphere for language). Russelland Golfinos (2003) reported on a singer who immediatelyfollowing resection of right Heschls gyrus suffered verypoor pitch discrimination, melody recognition and singingability, but who, by 3 weeks post surgery, had recovered allmusical abilities. In another study, Schulz and colleagues(2005) required three musicians that had undergone unilat-eral temporal lobe epilepsy surgery to complete a question-naire about their musical abilities as well as to write a freereport about their professional training and expertise bothpre and post surgery. The authors reported that all partici-pants became seizure-free following their surgery, that therewas no deterioration in performance on neuropsychologicaltests of intelligence or learning, but, most importantly, thatnone of the patients suffered deterioration inmusical abilitieswith two rather reporting improvements in concentrationand learning amongst other abilities.4 Similarly, Galarzaand colleagues (2014) provided a retrospective report on ajazzmusician patient who not only had a resection of the lefttemporal lobe but also whose right hemisphere was abnor-mally small at 2 standard deviations below controls. Withrespect to outcome, the authors noted that although, follow-ing surgery, the patient showed a very impaired musicalability (along with severe amnesia), after only a few yearsthe musician enjoyed a return of his virtuoso status, alongwith a return of his memory abilities. Finally, a singer

    reported by Wilson et al. (2013) whose surgery for anepileptogenic lesion involved the resection of right inferiorand middle temporal lobe along with parts of the hippocam-pus, parahippocampus and amygdala, showed no musicalimpairments as a result but rather much improved singing(again likely due to the impact of the epileptogenic tissueperturbing the normal network).

    The reason for the higher preservation of function in thecases of temporal lobe resection reported here is likely thatthe early lesion, cerebral malformations or slow growingtumors that necessitated surgery (for example hippocampalsclerosis and benign tumour in the case of Schulz et al. 2005;and arteriovenous malformation in the case of Galarza et al.2014) may have allowed reorganization of brain regionsover and beyond that caused by training. Indeed, it is knownthat slow-growing lesions, such as arteriovenousmalformations bring about extensive brain re-organization(Maldjian et al. 1996; Desmurget et al. 2007) that can resultin spared function after surgery (Duffau et al. 2002) due tothe given function shifting to the outside of the lesion(Rosenow and Luders 2004). Certainly, it is clear that theconsequences of strokes, which damage healthy tissue, arelikely to differ from the consequences of surgical treatment,the aim of which is to remove only damaged non-functionaltissue. Specifically, as was seen here, it could be predictedthat the latter type of damage should result in little or no lossof cognitive function compared to the former.

    It is therefore interesting that these findings of preservedability inmusicians following temporal lobe surgery contrastsomewhat with those of non-musicians. Indeed, a series ofstudies examining the effect of temporal lobe resection onmusical perception in non-musicians have revealed deterio-rated performance as a result not just of right hemispheredamage (Kester et al. 1991; Milner 1962; Zatorre 1985;Samson and Zatorre 1988; Samson and Zatorre 1994) butalso of left temporal lobectomy in a range ofmusical abilitiesincluding learning, discrimination and memory of melodies,and discrimination of note intervals, rhythms and metres(Zatorre 1985; Samson and Zatorre 1992; Kester et al.1991; Ligeois-Chauvel et al. 1998; for review Samson1999; Maguire 2012). Although we do not propose tocompare the two groups given the difference in the evalua-tion approaches taken by those carrying out case studies ofmusical ability loss (not to mention the difficulty in compar-ing the initial abilities shown by the two groups), thissuggestion of a tendency of musicians and non-musiciansto show differing cognitive outcomes following surgery isworthy of note. We have suggested that these differencesmay arise from the structural and functional changes thattake place in the brain as a result of the musical training thatmusicians undergo. Some experimental evidence suggeststhat musical training can improve non-musical function (in aso-called transfer of learning) (for a review, see Besson et al.

    3 In those with temporal lobe epilepsy, cortical regions adjacent to the siteof the foci are often depressed leading to a worsening of cognitive ability.As suggested by Zatorre (1989), the improved performance afterwardsmay be explained by the removal of the epileptogenic focus which resultsin less cortical interference over the brain.4 As suggested by the authors, and as with Zatorre (1989) improvementsreported by these patients are likely due to the disappearance of seizuresand consequently the functional recovery of regions depressed by theepileptogenic focus.

    Neuropsychol Rev (2014) 24:445460 453

  • 2011). However there is currently no evidence in the litera-ture to support the hypothesis that training-related brainchanges might also have a beneficial effect on generalcognitive outcome and recovery following brain damage.We argue that this could be an interesting issue to address infuture studies.

    In conclusion, while themajority ofmusician participantsso far reported in the literature, show considerable impair-ment following brain damage, the preservation of function inat least a subset of musicians, particularly those who haveundergone temporal lobe resection, have raised some inter-est in those who have encountered these patients. The ques-tion of whether these individuals provide initial evidence ofpreservation of function due to intense training oroverlearning (Tzortzis et al. 2000), and the question ofwhether training-related brain changes might have a benefi-cial effect on general cognitive outcome remain open.However, we argue that it may be addressed by furtherstandardized documentation of musician patients. To thisend, we suggest a number of guidelines for future researchthat may make help to clarify the question of whetherpremorbid experience as seen in musical experts influencescognitive outcome and functional recovery following braindamage.

    3) Suggested guidelines for the future evaluation of relevantpatients

    Playing music depends on a number of complex cog-nitive and motor abilities and a loss of these abilitieswould have a debilitating impact on the professional lifeof a musician. Accordingly, assessment of musicianscognitive outcome following lesion and neurosurgery isclearly important for what it can tell us about functionalrecovery in musicians generally and therefore their pro-fessional prospects. However, on a more basic level, theassessment of outcome in musicians and non-musicians isimportant for what it can tell us about the extent to whichpatients chances of recovery of different functions isbased on premorbid experience. Further, such assessmentmay also provide insights into the extent to which anyadvantages shown by musicians, in terms of preservationof musical ability following damage, may be seen acrossdomains i.e. whether any such advantages may extend tothe preservation or functional recovery of non-musicalabilities. In this section we seek to encourage the detaileddocumentation of cognitive outcome that would makesuch analyses possible by providing guidelines for eval-uation of relevant patients in future research.

    First, we emphasise the need for a precise descriptionof the case in question in terms of age, duration and onsetof disease or neurological difficulty and localisation andaetiology of the lesion. Manual laterality should be deter-mined to infer cerebral representation of language. Theprevious musical experience and degree of expertise of

    the musician should also be determined. One ap-proach to quantifying expertise is to determine theamount of musical training in terms of the numberof hours of dedicated practice undergone (Fosterand Zatorre 2010; Foster et al. 2013). With esti-mates of practice hours per week for each year, acumulative measure of hours of musical practice may beobtained and considered alongside the age at which mu-sical training commenced. In addition, questionnaires thatdetermine musical ability based on multidimensionalcriteria may be used.

    A general comprehensive neuropsychological evalua-tion including an anamnesis of medical history to identifyany developmental learning disorders (e.g. dyslexia,dysorthographia, dysphasia, dyscalculia etc.) should thenbe carried out so as to allow examination of cognitiveoutcomes of non-musical functions. A measure of generalintellectual function is important to interpret other cogni-tive abilities including attention, orientation, perception,memory, executive, somatosensory, and motor function.Table 2 proposes a list of recommended investigations intocognitive functioning with examples of possible tests touse for each domain. Although this list is not exhaustiveand should be adapted to the level of the patients, itprovides suggestions about the functions that need to beinvestigated. A list of auditory and musical skills recom-mended to screen musical difficulties is detailed in Table 3.Note that the once again this list of musical functions is notexhaustive and is only to provide suggestions as to howone might initiate neuropsychological assessement ofmusicians. In the case of severe musical difficulties beingreported, a preliminary assessment of musical abilities withtheMontreal Battery for the Evaluation of Amusia (MBEA: Peretz et al. 2003) may be carried out, as the failure of amusician to perform normally on this very basic test ofmusical abilities would provide confirmation of severe lossof ability. Timing and synchronization to musical se-quences can be also assessed with tasks from the Batteryof Assesment of Auditory Sensorimotor and Timing Abil-ities (BAASTA, Farrugia et al. 2012). We also suggest thatthe investigators assess processing of other auditorysounds (environmental, vocal and verbal) in additionto musical sounds to in order to determine the extent ofdysfunction in the auditory sphere and to verify domainspecificity of any observed deficits.

    Finally, in the interests of disentanging potential effectsof musical training from other effects that may also influ-ence brain and cognitive reserve and metaplasticity, fac-tors such as education, occupation (as well as that of theparents), family income, parental language, diet, drinkingand smoking habits should also be reported. Details ofinvolvement in other intellectual and physical activitiesshould be solicited.

    454 Neuropsychol Rev (2014) 24:445460

  • Table 2 A list of recommended neuropsychological tests. Suggestions of tests are provided merely as information

    Domain Recommended tests

    General intellectual function Wechsler Adult Intelligence Scale (WAIS)Mattis Dementia Rating Scale (DRS)Ravens Progressive Matrices (for patients with language disorders)Mill Hill Vocabulary test or National Adult Reading Test (for patients withnon verbal or visuo-spatial disorders)

    Orientation and attention (and neglect) Orientation (Wechsler Memory Scale subtest)Digit symbol coding (WAIS subtest)d2 test of attentionPaced Auditory Serial Addition Test (PASAT)Verbal and non verbal Cancellation test

    Perception Phonological discriminationJudgment of line orientation (Benton)Embedded figures Test

    Visuo-construction Block design (WAIS subtest)Copy of the Rey Complex Figure

    Memory (verbal & nonverbal)

    -Short-term & working memory Wechsler Memory Scale subtests:- Audio-verbal span (forward and backward digit)- Visuo-spatial span (forward and backward block)- Letter-number sequencing

    -Long-term memory Wechsler Memory Scale subtests:- Verbal paired associate learning- Logical memory- Visual design reproduction- Face recognition

    Verbal learning tests using words (e.g. Rey Auditory Verbal Learning Test,California Verbal Learning Test, Free and Cued Selective Reminding Test)or non-sense words (e.g. Samson and Zatorre 1992)

    Non verbal learning tests using visual designs (e.g. Aggie Figure learning test,immediate and delayed recall of Rey complex Figure)

    Semantic memory tests (e.g. Pyramid and Palm Trees Test,Famous Face recognition)

    Language

    - Oral perception Phonological discriminationVerbal comprehension (Token test)

    - Oral production Visual (Boston naming task) and auditory (sound) naming testsSpelling of regular, irregular and non-sense wordsRepetition of words and sentences.

    - Written perception Reading of regular and irregular words and non-sense words.Reading of sentences (Chapman-Cook test).Word-picture matching

    - Written production Writing of regular, irregular and non-sense wordsCopying of words and sentences

    - Verbal fluency Word generation from semantic (e.g. animal, fruit) or phonemic (e.g. letter R or P) cues.Switching task (word generation from two categories in alternation, e.g. Vegetable - Surname).

    Numerical abilities WAIS Arithmetic Subtest

    Executive functions Trail making test (Part A and B)Stroop test (color identification, reading, interference and flexibility)Brixton test of spatial anticipationWinsconsin Card Sorting TestRuff Figural Fluency Test (generation of visual patterns)

    Somato-sensory and motor skills Edinburgh Handedness InventoryBimanual gestural sequencesTapping testSomato-sensory perception on hands, face and bodyTwo-point discriminationGestual praxies

    Neuropsychol Rev (2014) 24:445460 455

  • Table 2 (continued)

    Domain Recommended tests

    Emotion Recognition of emotional facesRecognition of emotional voicesTest of theory of mind

    Mood State-Trait Anxiety Inventory (STAI)Beck Depression Inventory (BDI)Profile of Mood State (POMS)

    Table 3 A list of recommendedexaminations of receptive andexpressive musical abilities

    Cognitive function Recommended tests

    RECEPTIVE

    Perceptual

    - Pitch (500-3000Hz)

    - Time (80300 ms)

    - Pitch discrimination

    - Timbre discrimination

    - Rhythm & Meterdiscrimination

    Adaptive tracking psychophysics (Kaernbach 1991)

    Threshold of frequency perception

    Threshold of anisochrony perception (Ehrl and Samson 2005)

    Pitch discrimination (control task, Zatorre and Samson 1991)

    Discrimination of temporal and spectral envelopes (Samson and Zatorre 1994)

    Metrical/non-metrical classification

    Rhythmic pattern reproduction (Wilson et al. 2002)

    Working memory Pitch discrimination with interference (Zatorre and Samson 1991)

    Long term memory

    - Non familiar music Learning and retention of unfamiliar musical excerpts(Samson and Zatorre 1992)

    Musical Paired Associate Learning (Wilson and Saling 2008)

    - Familiar music (to beadapted for eachcountry)

    Learning and retention of familiar and unfamiliar musical excerpts(Samson et al. 2012)

    Gating paradigm (Filipic et al. 2010)

    Famous melody matching

    Famous melody naming

    Distorted Tunes Test (Drayna et al. 2001)

    Emotional recognition Recognition of emotional categories (Vieillard et al. 2008)

    Rating of valence and arousal (Vieillard et al. 2008)

    Music reading Reading of notes and musical symbols (Hebert and Cuddy 2006)

    EXPRESSIVE

    Singing Vocal range (record and extract fundamental frequency)

    Short-term memory Pitch matching (repetition of single tones)

    Melodic serial span

    Long-term memory Familiar tune singing (with and without words) from title or auditory cueing

    Musical imagery (Zatorre and Halpern. 1993)

    Music writing Writing of notes and musical symbols

    Visual transcription of auditory or written musical sequences

    OTHER

    Mental imagery The Bucknell Auditory Imagery Scale (Halpern et al. 2004)

    Audiation questionnaire (Zatorre et al. 2010)

    Absolute pitch &Synesthesia

    Test of tone name recognition (Ward and Burns 1982; Zatorre andBeckett 1989; Keenan et al. 2001).

    Standardised test battery for study of Synesthesia (Eagleman et al. 2007)

    456 Neuropsychol Rev (2014) 24:445460

  • Conclusions

    A great deal of research has addressed the ways in whichmusician brains differ structurally and functionally from thoseof non-musicians as a result of long term training. The currentreview extended this work by not only proposing ways inwhich these structural and functional differences in the musi-cian brain may bring about preserved function followingcerebral damage (brain reserve, cognitive reserve andmetaplasticity), but also by examining the literature for anyevidence of such preserved musical function. Our reviewdemonstrated that in the majority of so-far reported cases,musicians have lost at least some musical function followingbrain damage. However, we also see that some musiciansshow a remarkable preservation of musical function despitedamage to areas of the brain that are normally associated withnormal musical functioning. Taking into consideration thebias towards reporting cases of impairment as opposed tocases of preserved function, we can conclude that preservationof function occurs at a significant rate and might beunderestimated. The fact that cases of temporal lobe resectiontend to result in preserved function, compared to, for instance,vascular accidents, emphasises the role that aetiology of dam-age may play and begs the question of whether some lesionedstructures may have a greater disposition for reorganisation.Unfortunately, given the lack of standardised testing of musi-cians following brain damage and the difficulty in makingdirect comparisons with non-musicians, it is difficult to tellhow significant the current findings are in terms of incidenceof preserved functions. Also the fact that most cases have beenreported after left hemisphere cerebral lesion is problematicand precludes testing of specific hypotheses, for instance withregard to whether musicians may be able to make use ofalternative strategies via different hemispheres.

    Evidence for the transfer of musical training effects to non-musical cognitive and executive functioning (Chan et al.1998; Schellenberg 2004; 2006; Bialystok and Depape2009; Moreno et al. 2011; Besson et al. 2011) has led to thesuggestion that musical training provides the sort of enrich-ment that may be of general cognitive benefit, for example inthe context of normal cognitive aging (Fauvel et al. 2013).Unfortunately, the tendency of studies reporting on braindamaged musician patients to focus on cognitive outcomesin musical, rather than non-musical function, limits our cur-rent ability to examine such effects. However, in our pre-scribed guidelines, we specifically encourage the extensiveassessment of cognitive outcomes in terms of non-musicalfunctions in musician patients following brain damage. Wesuggest that this should allow a better understanding of theextent to which music may have a beneficial effect on cogni-tive outcomes in non-musical as well as musical functionfollowing brain damage and in doing so, more broadlyinform our appreciation of the extent to which musical

    activity may be used to provide a more general protectiveeffect on brain function in the general population. Indeed it ispossible that this is not necessarily the case. It is worthconsidering that while Schellenberg (2004) showed a relation-ship between quantity of music lessons in childhood and IQ,he showed no differences between the test results ofmusic students and other students (such as lawyers, physiciansetc.) suggesting that music is akin to any scholarly activity thatrequires great levels of focused concentration anddiscipline (Schellenberg 2006).

    Finally, it is interesting to note that speculations thatpremorbid experience or expertise may influence cognitiveoutcome as identified in the music cognition literature resonateto some extent with those in the neuropsychological literaturedocumenting cognitive outcomes in visual artists (for reviewssee Rose 2004; Chatterjee 2004; Bogousslavsky and Boller2005; Zaidel 2005; Zaidel 2010; Zaidel 2013). Boller et al.(2005) proposed that in some artists the effect of cerebrallesions is different from that found in non-artists, perhapsbecause of an expanded cortical representation, secondary totheir lifelong formal training. In a similar vein, Zaidel (2010)would suggest that brain damaged artists go on producing artbecause of its dependence on several brain regions and onredundancy of art-related functional representation rather thanon a single cerebral hemisphere, region or pathway. Theseseem to overlap with our suggestions that musicians may showadvantage firstly because of extensiveness and therefore therobustness of cerebral substrates to damage and secondly,because of the high degree of redundancy in the musical brain.Such predictions have yet to be verified but the considerableoverlap in thinking across domains regarding the extent towhich premorbid experience may be expected to influencecognitive outcome suggests that this is an investigation worthyof further considered investigation.

    Acknowledgments This study has received funding from the FrenchMinistry (ANR-09-BLAN-0310-02), the Fondation Plan Alzheimer andthe Institut Universitaire de France to S.S.

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    A Protective Effect of Musical Expertise on Cognitive Outcome Following Brain Damage?AbstractIntroductionConclusionsReferences