Abstract
Music represents a salient stimulus for the brain with two key features: pitch and rhythm. Few data are available on cognitive analysis of music listening in musically naïve healthy participants. Beyond auditory cortices, neuroimaging data showed the involvement of prefrontal cortex in pitch and of cerebellum in rhythm. The present study is aimed at investigating the role of prefrontal and cerebellar cortices in both pitch and rhythm processing. The performance of fifteen participants without musical expertise was investigated in a listening discrimination task. The task required to decide whether two eight-element melodic sequences were equal or different according to pitch or rhythm characteristics. Before the task, we applied a protocol of continuous theta burst transcranial magnetic stimulation interfering with the activity of the left cerebellar hemisphere (lCb), right inferior frontal gyrus (rIFG), or vertex (Cz-control site), in a within cross-over design. Our results showed that participants were more accurate in pitch than rhythm tasks. Importantly, the reaction times were slower following rIFG or lCb stimulations in both tasks. Notably, frontal and cerebellar stimulations did not induce any motor effect in right and left hand. The present findings point to the role of the fronto-cerebellar network in music processing with a single mechanism for both pitch and rhythm patterns.
Similar content being viewed by others
References
Alexander ML, Henry ML (2015) The effect of pitch and rhythm difficulty on high school string sight-reading performance. String Res J 6:71–83. https://doi.org/10.1177/194849921500600005
Bengtsson SL, Ullén F (2006) Dissociation between melodic and rhythmic processing during piano performance from musical scores. Neuroimage 30:272–284. https://doi.org/10.1016/j.neuroimage.2005.09.019
Bengtsson SL, Ullén F, Ehrsson HH, Hashimoto T, Kito T, Naito E, Forssberg H, Sadato N (2008) Listening to rhythms activates motor and premotor cortices. Cortex 45:62–71. https://doi.org/10.1016/j.cortex.2008.07.002
Bianchi F, Hjortkjær J, Santurette S, Zatorre RJ, Siebner HR, Dau T (2017) Subcortical and cortical correlates of pitch discrimination: evidence for two levels of neuroplasticity in musicians. Neuroimage 163:398–412. https://doi.org/10.1016/j.neuroimage.2017.07.057
Brown S, Martinez MJ (2007) Activation of premotor vocal areas during musical discrimination. Brain Cogn 63:59–69. https://doi.org/10.1016/j.bandc.2006.08.006
Cannon JJ, Patel AD (2021) How beat perception co-opts motor neurophysiology. Trends Cogn Sci 25:137–150. https://doi.org/10.1016/j.tics.2020.11.002
Chan MMY, Han YMY (2022) The functional brain networks activated by music listening: a neuroimaging meta-analysis and implications for treatment. Neuropsychology 36:4–22. https://doi.org/10.1037/neu0000777
Daly I, Williams D, Hwang F, Kirke A, Miranda ER, Nasuto SJ (2019) Electroencephalography reflects the activity of sub-cortical brain regions during approach-withdrawal behaviour while listening to music. Sci Rep 9:9415. https://doi.org/10.1038/s41598-019-45105-2
Del Olmo MF, Cheeran B, Koch G, Rothwell JC (2007) Role of the cerebellum in externally paced rhythmic finger movements. J Neurophysiol 98:145–152. https://doi.org/10.1152/jn.01088.2006
Foti F, Mandolesi L, Cutuli D, Laricchiuta D, De Bartolo P, Gelfo F, Petrosini L (2010) Cerebellar damage loosens the strategic use of the spatial structure of the search space. Cerebellum 9:29–41. https://doi.org/10.1007/s12311-009-0134-4
Gordon CL, Cobb PR, Balasubramaniam R (2018) Recruitment of the motor system during music listening: an ALE meta-analysis of fMRI data. PLoS ONE 13:e0207213. https://doi.org/10.1371/journal.pone.0207213
Griffiths TD, Johnsrude I, Dean JL, Green GG (1999) A common neural substrate for the analysis of pitch and duration pattern in segmented sound? NeuroReport 10:3825–3830. https://doi.org/10.1097/00001756-199912160-00019
Holcomb HH, Medoff DR, Caudill PJ, Zhao Z, Lahti AC, Dannals RF, Tamminga CA (1998) Cerebral blood flow relationships associated with a difficult tone recognition task in trained normal volunteers. Cereb Cortex 8:534–542. https://doi.org/10.1093/cercor/8.6.534
Hommel, B (2013). Ideomotor action control: On the perceptual grounding of voluntary actions and agents. Action science: foundations of an emerging discipline, 113–136.
Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC (2005) Theta burst stimulation of the human motor cortex. Neuron 45:201–206. https://doi.org/10.1016/j.neuron.2004.12.033
James CE, Oechslin MS, Van De Ville D, Hauert CA, Descloux C, Lazeyras F (2014) Musical training intensity yields opposite effects on grey matter density in cognitive versus sensorimotor networks. Brain Struct Funct 219:353–366. https://doi.org/10.1007/s00429-013-0504-z
Janata P (2015) Neural basis of music perception. Handb Clin Neurol 129:187–205. https://doi.org/10.1016/B978-0-444-62630-1.00011-1
Jung J, Bungert A, Bowtell R, Jackson SR (2016) Vertex stimulation as a control site for transcranial magnetic stimulation: a concurrent TMS/fMRI study. Brain Stimul 9:58–64. https://doi.org/10.1016/j.brs.2015.09.008
Kasdan AV, Burgess AN, Pizzagalli F, Scartozzi A, Chern A, Kotz SA, Wilson SM, Gordon RL (2022) Identifying a brain network for musical rhythm: a functional neuroimaging meta-analysis and systematic review. Neurosci Biobehav Rev 136:104588. https://doi.org/10.1016/j.neubiorev.2022.104588
Koch G, Mori F, Marconi B, Codecà C, Pecchioli C, Salerno S, Torriero S, Lo Gerfo E, Mir P, Oliveri M, Caltagirone C (2008) Changes in intracortical circuits of the human motor cortex following theta burst stimulation of the lateral cerebellum. Clin Neurophysiol 119:2559–2569. https://doi.org/10.1016/j.clinph.2008.08.008
Koelsch S (2011) Toward a neural basis of music perception—a review and updated model. Front Psychol 2:110. https://doi.org/10.3389/fpsyg.2011.00110
Koelsch S (2014) Brain correlates of music-evoked emotions. Nat Rev Neurosci 15:170–180. https://doi.org/10.1038/nrn3666
Konoike N, Kotozaki Y, Jeong H, Miyazaki A, Sakaki K, Shinada T, Sugiura M, Kawashima R, Nakamura K (2015) Temporal and motor representation of rhythm in fronto-parietal cortical areas: an fMRI study. PLoS ONE 10:e0130120. https://doi.org/10.1371/journal.pone.0130120
Lega C, Vecchi T, D’Angelo E, Cattaneo Z (2016) A TMS investigation on the role of the cerebellum in pitch and timbre discrimination. Cerebellum Ataxias 3:6. https://doi.org/10.1186/s40673-016-0044-4
Leipold S, Brauchli C, Greber M, Jäncke L (2019) Absolute and relative pitch processing in the human brain: neural and behavioral evidence. Brain Struct Funct 224:1723–1738. https://doi.org/10.1007/s00429-019-01872-2
Nozaradan S, Schwartze M, Obermeier C, Kotz SA (2017) Specific contributions of basal ganglia and cerebellum to the neural tracking of rhythm. Cortex 95:156–168. https://doi.org/10.1016/j.cortex.2017.08.015
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113. https://doi.org/10.1016/0028-3932(71)90067-4
Palomar-García MÁ, Hernández M, Olcina G, Adrián-Ventura J, Costumero V, Miró-Padilla A, Villar-Rodríguez E, Ávila C (2020) Auditory and frontal anatomic correlates of pitch discrimination in musicians, non-musicians, and children without musical training. Brain Struct Funct 225:2735–2744. https://doi.org/10.1007/s00429-020-02151-1
Parsons LM, Petacchi A, Schmahmann JD, Bower JM (2009) Pitch discrimination in cerebellar patients: evidence for a sensory deficit. Brain Res 1303:84–96. https://doi.org/10.1016/j.brainres.2009.09.052
Patel AD, Iversen JR (2014) The evolutionary neuroscience of musical beat perception: the Action Simulation for Auditory Prediction (ASAP) hypothesis. Front Syst Neurosci 8:1–14. https://doi.org/10.3389/fnsys.2014.00001
Petacchi A, Laird AR, Fox PT, Bower JM (2005) Cerebellum and auditory function: an ALE meta-analysis of functional neuroimaging studies. Hum Brain Mapp 25:118–128. https://doi.org/10.1002/hbm.20137
Petrosini L, Picerni E, Termine A, Fabrizio C, Laricchiuta D, Cutuli D (2022) The Cerebellum as an embodying machine. Neuroscientist 2:10738584221120188. https://doi.org/10.1177/10738584221120187
Picazio S, Oliveri M, Koch G, Caltagirone C, Petrosini L (2013a) Continuous theta burst stimulation (cTBS) on left cerebellar hemisphere affects mental rotation tasks during music listening. PLoS ONE 8:e64640. https://doi.org/10.1371/journal.pone.0064640
Picazio S, Oliveri M, Koch G, Caltagirone C, Petrosini L (2013b) Cerebellar contribution to mental rotation: a cTBS study. Cerebellum 12:856–861. https://doi.org/10.1007/s12311-013-0494-7
Picazio S, Veniero D, Ponzo V, Caltagirone C, Gross J, Thut G, Koch G (2014) Prefrontal control over motor cortex cycles at beta frequency during movement inhibition. Curr Biol 24:2940–2945. https://doi.org/10.1016/j.cub.2014.10.043
Picazio S, Granata C, Caltagirone C, Petrosini L, Oliveri M (2015) Shaping pseudoneglect with transcranial cerebellar direct current stimulation and music listening. Front Hum Neurosci 9:158. https://doi.org/10.3389/fnhum.2015.00158
Picazio S, Ponzo V, Koch G (2016) Cerebellar control on prefrontal-motor connectivity during movement inhibition. Cerebellum 15:680–687. https://doi.org/10.1007/s12311-015-0731-3
Picazio S, Foti F, Oliveri M, Koch G, Petrosini L, Ferlazzo F, Sdoia S (2020) Out with the old and in with the new: the contribution of prefrontal and cerebellar areas to backward inhibition. Cerebellum 19:426–436. https://doi.org/10.1007/s12311-020-01115-9
Rauschecker JP (2011) An expanded role for the dorsal auditory pathway in sensorimotor control and integration. Hear Res 271:16–25. https://doi.org/10.1016/j.heares.2010.09.001
Reybrouck M, Vuust P, Brattico E (2021) Neural correlates of music listening: does the music matter? Brain Sci 11:1553. https://doi.org/10.3390/brainsci11121553
Rothwell JC (1997) Techniques and mechanisms of action of transcranial stimulation of the human motor cortex. J Neurosci Meth 74:113–122. https://doi.org/10.1016/s0165-0270(97)02242-5
Schubotz RI (2007) Prediction of external events with our motor system: towards a new framework. Trends Cogn Sci 11:211–218. https://doi.org/10.1016/j.tics.2007.02.006
Shenker JJ, Steele CJ, Chakravarty MM, Zatorre RJ, Penhune VB (2022) Early musical training shapes cortico-cerebellar structural covariation. Brain Struct Funct 227:407–419. https://doi.org/10.1007/s00429-021-02409-2
Tervaniemi M (2023) The neuroscience of music—towards ecological validity. Trends Neurosci 46:355–364. https://doi.org/10.1016/j.tins.2023.03.001
Thaut MH, Trimarchi PD, Parsons LM (2014) Human brain basis of musical rhythm perception: common and distinct neural substrates for meter, tempo, and pattern. Brain Sci 4:428–452. https://doi.org/10.3390/brainsci4020428
Tölgyesi B, Evers S (2014) The impact of cerebellar disorders on musical ability. J Neurol Sci 343:76–78. https://doi.org/10.1016/j.jns.2014.05.036
Vuust P, Heggli OA, Friston KJ, Kringelbach ML (2022) Music in the brain. Nat Rev Neurosci 23:287–305. https://doi.org/10.1038/s41583-022-00578-5
Yu M, Xu M, Li X, Chen Z, Song Y, Liu J (2017) The shared neural basis of music and language. Neuroscience 357:208–219. https://doi.org/10.1016/j.neuroscience.2017.06.003
Zhang L, Xie S, Li Y, Shu H, Zhang Y (2020) Perception of musical melody and rhythm as influenced by native language experience. J Acoust Soc Am 147:385. https://doi.org/10.1121/10.0001179
Funding
No funding was received for conducting this study.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Silvia Picazio, Barbara Magnani and Laura Petrosini. The first draft of the manuscript was written by Silvia Picazio and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Picazio, S., Magnani, B., Koch, G. et al. Frontal and cerebellar contributions to pitch and rhythm processing: a TMS study. Brain Struct Funct 229, 789–795 (2024). https://doi.org/10.1007/s00429-024-02764-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-024-02764-w