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The Neural Causes of Congenital Amusia

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The Neural Causes of Congenital Amusia The Journal of Neuroscience, July 27, 2016 • 36(30):7803–7804 • 7803 Journal Club Editor’s Note: These short, critical reviews of recent papers in the Journal, written exclusively by graduate students or postdoctoral fellows, are intended to summarize the important findings of the paper and provide additional insight and commentary. For more information on the format and purpose of the Journal Club, please see http://www.jneurosci.org/misc/ifa_features.shtml. The Neural Causes of Congenital Amusia X Jian Chen1 and Jie Yuan2 1School of Psychological Sciences, University of Melbourne, Parkville, Victoria 3010, Australia, and 2Department of Psychology and Department of Biomedical Engineering, Tsinghua University, 100084 Beijing, China Review of Norman-Haignere et al. Congenital amusia is a lifelong disorder in cortex (DLPFC) were lower in amusics areas. Considering amusics can exhibit a pitch processing and music perception that than in healthy controls. A third possi- normal priming effect of note expectancy affects ϳ4% of the population (Peretz et al., bility, however, is that individuals with (faster response to expected notes) based on 2002; Peretz and Hyde, 2003). Despite hav- congenital amusia have abnormal pitch the musical pitch context (Omigie et al., ing normal hearing and speech recognition, responsive region(s) in their auditory 2012) and that some amusics have deficits in as well as no prior brain lesions or cognitive cortex, despite the fact that the auditory music perception but not pitch discrimina- deficits, individuals with congenital amusia cortex seems to have normal responses tion (Tillmann et al., 2009; Liu et al., 2010), have difficulty recognizing melodies and de- to pitch changes (Hyde et al., 2011; it is plausible that congenital amusia results tecting pitch changes (Peretz et al., 2002; Moreauet al., 2013; but see Albouy et al., from deficits in frontotemporal connectiv- Tillmann et al., 2009; Liu et al., 2010). Their 2013; Zendel et al., 2015). Norman- ity or dysfunctions in the frontal cortex. “musical deafness” is thought to reflect un- Haignere et al. (2016) examined the third Recent neurological findings support derlying impairments in pitch perception possibility by investigating pitch-specific this argument. Studies on individuals and memory. However, the underlying activation in the auditory cortex. Amusic with congenital amusia have revealed re- neural causes of congenital amusia are still subjects and age- and education-matched duced white matter density in the right actively debated. controls passively listened to harmonic inferior frontal gyrus (Hyde et al., 2006), Previous studies have suggested three tones and frequency-matched noise dur- cortical malformations in the right infe- possible neural causes for congenital am- ing an fMRI scan. Results revealed that: rior frontal gyrus and right auditory usia. One is that congenital amusia is as- (1) amusics and controls both exhibited cortex (Hyde et al., 2007), and abnormal sociated with reduced frontotemporal stronger activation in pitch-responsive deactivation in the right inferior frontal connectivity, which makes it difficult for voxels to harmonic tones than to noise gyrus (Hyde et al., 2011). A more recent people with the disorder to consciously in a similar anatomical location. (2) No magnetoencephalography study has also access pitch information encoded in their difference was found in pitch-responsive reported decreased low-gamma oscilla- auditory cortex (Loui et al., 2009; Hyde et voxels activation between amusics and tions in the right DLPFC during pitch al., 2011; Albouy et al., 2013, 2015; but see controls. (3) The selectivity of pitch- memory task (Albouy et al., 2013). These Chen et al., 2015). Alternatively, the responsive voxels in the auditory cortex studies, however, are unable to distin- pitch-related deficits may be caused by showed no difference between amusics guish whether congenital amusia is the re- dysfunctions in the frontal cortex (Hyde and controls. sult of weak connectivity or if it is due to et al., 2006, 2011; Albouy et al., 2013). For In sum, Norman-Haignere et al. (2016) the deficits in the prefrontal cortex. example, Albouy et al. (2013) revealed that low gamma oscillations (30–40 Hz demonstrated that pitch-responsive regions A recent study by Schaal et al. (2015) range) in the right dorsolateral prefrontal in amusics’ auditory cortex are comparable supports the possibility that the neural in extent, selectivity, and anatomical loca- causes of congenital amusia are located in tion to those of controls. These results there- the frontal cortex. Based on previous find- Received May 9, 2016; revised June 15, 2016; accepted June 17, 2016. We thank Xuejing Lu and Lauren Power for effective discussion, and fore suggest that the congenital amusia is ings (Albouy et al., 2013), Schaal et al. Lauren Power and two editors for proofreading. unlikely caused by deficits in these regions, (2015) demonstrated that modulating the The authors declare no competing financial interests. and combined with other studies (Hyde et right DLPFC with transracial alternating CorrespondenceshouldbeaddressedtoJieYuan,WeiqingBuilding, al., 2011; Moreau et al., 2013; Zendel et al., current stimulation (tACS) at 35 Hz selec- Room 311, Tsinghua University, 100084 Beijing, China. E-mail: 2015), they suggest that amusics’ pitch- tively improved pitch memory, but not [email protected]. DOI:10.1523/JNEUROSCI.1500-16.2016 processing deficits are due to impairments visual memory, in amusics. Participants Copyright © 2016 the authors 0270-6474/16/367803-02$15.00/0 in regions outside of the pitch-responsive received either 35 or 90 Hz tACS during a 7804 • J. Neurosci., July 27, 2016 • 36(30):7803–7804 Chen and Yuan • Journal Club pitch short-term memory span task and O, Caclin A, Tillmann B (2013) Impaired genital amusia: evidence from event-re- visual short-term span task. Results sh- pitch perception and memory in congenital lated potentials. Brain Cogn 81:337–344. owed that 35 Hz tACS significantly im- amusia: the deficit starts in the auditory cor- CrossRef Medline tex. Brain 136:1639–1661. CrossRef Medline Norman-Haignere SV, Albouy P, Caclin A, Mc- proved the behavioral performance in Albouy P, Mattout J, Sanchez G, Tillmann B, Ca- Dermott JH, Kanwisher NG, Tillmann B pitch memory task in amusics to the ex- clin A (2015) Altered retrieval of melodic in- (2016) Pitch-responsive cortical regions in tent that there was no significant perfor- formation in congenital amusia: insights from congenital amusia. J Neurosci 36:2986–2994. mance difference between amusics and dynamic causal modeling of MEG data. Front CrossRef Medline controls. Such results suggest a causal re- Hum Neurosci 9:20. CrossRef Medline Omigie D, Pearce MT, Stewart L (2012) Track- lationship between congenital amusia and Chen JL, Kumar S, Williamson VJ, Scholz J, Grif- ing of pitch probabilities in congenital amusia. fiths TD, Stewart L (2015) Detection of the dysfunctions in the prefrontal cortex, es- Neuropsychologia 50:1483–1493. CrossRef arcuate fasciculus in congenital amusia de- Medline pecially the right DLPFC. pends on the tractography algorithm. Front Given that individuals with congenital Peretz I, Ayotte J, Zatorre RJ, Mehler J, Ahad P, Psychol 6:9. CrossRef Medline Penhune VB, Jutras B (2002) Congenital amusia have normal pitch-responsive Hyde KL, Zatorre RJ, Griffiths TD, Lerch JP, amusia: a disorder of fine-grained pitch dis- Peretz I (2006) Morphometry of the amusic regions in the auditory cortex and an crimination. Neuron 33:185–191. CrossRef brain: a two-site study. Brain 129:2562–2570. increase of activity in the DLPFC can Medline CrossRef Medline lead to performance facilitation in a Peretz I, Hyde KL (2003) What is specific to mu- Hyde KL, Lerch JP, Zatorre RJ, Griffiths TD, Ev- sic processing? Insights from congenital amu- pitch memory task (Schaal et al., 2015; ans AC, Peretz I (2007) Cortical thickness in sia. Trends in Cognitive Sciences 7:362–367. Norman-Haignere et al., 2016), we might congenital amusia: when less is better than conclude that the impairments in right more. J Neurosci 27:13028–13032. CrossRef CrossRef Medline DLPFC are the main causes of congenital Medline Schaal NK, Pfeifer J, Krause V, Pollok B (2015) Hyde KL, Zatorre RJ, Peretz I (2011) Functional From amusic to musical?: Improving pitch amusia. It is also possible, however, that memory in congenital amusia with transcra- the applied stimulation of 35 Hz tACS has MRI evidence of an abnormal neural network for pitch processing in congenital amusia. nial alternating current stimulation. Behav modulated the connectivity between the Cereb Cortex 21:292–299. CrossRef Medline Brain Res 294:141–148. CrossRef Medline right DLPFC and the auditory cortex Liu F, Patel AD, Fourcin A, Stewart L (2010) In- Tillmann B, Schulze K, Foxton JM (2009) Con- rather than the right DLPFC itself. Fur- tonation processing in congenital amusia: dis- genital amusia: a short-term memory deficit ther study is needed to rule out this crimination, identification and imitation. for non-verbal, but not verbal sounds. Brain possibility. Brain 133:1682–1693. CrossRef Medline Cogn 71:259–264. CrossRef Medline Loui P, Alsop D, Schlaug G (2009) Tone deaf- Zendel BR, Lagrois ME´ , Robitaille N, Peretz I ness: a new disconnection syndrome? J Neu- (2015) Attending to pitch information inhib- References rosci 29:10215–10220. CrossRef Medline its processing of pitch information: the curi- Albouy P, Mattout J, Bouet R, Maby E, Sanchez G, Moreau P, Jolicœur P, Peretz I (2013) Pitch ous case of amusia. J Neurosci 35:3815–3824. Aguera PE, Daligault S, Delpuech C, Bertrand discrimination without awareness in con- CrossRef Medline.
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