Open Access

A TMS investigation on the role of the cerebellum in pitch and timbre discrimination

  • Carlotta Lega1,
  • Tomaso Vecchi2, 3,
  • Egidio D’Angelo2, 3 and
  • Zaira Cattaneo1, 3Email author
Cerebellum & Ataxias20163:6

DOI: 10.1186/s40673-016-0044-4

Received: 3 November 2015

Accepted: 27 January 2016

Published: 2 March 2016

Abstract

Background

Growing neuroimaging and clinical evidence suggests that the cerebellum plays a critical role in perception. In the auditory domain, the cerebellum seems to be important in different aspects of music and sound processing. Here we investigated the possible causal role of the cerebellum in two auditory tasks, a pitch discrimination and a timbre discrimination task. Specifically, participants performed a pitch and a timbre discrimination task prior and after receiving offline low frequency transcranical magnetic stimulation (TMS) over their (right) cerebellum.

Results

Suppressing activity in the right cerebellum by means of inhibitory 1 Hz TMS affected participants’ ability to discriminate pitch but not timbre.

Conclusion

These findings point to a causal role of the cerebellum in at least certain aspects of sound processing and are important in a clinical perspective helping understanding the impact of cerebellar lesions on sensory functions.

Keywords

Pitch Timbre Transcranial magnetic stimulation (TMS) Auditory discrimination

Background

The cerebellum is traditionally considered a “motor controller” and its role in the acquisition of motor skills is well established [1, 2]. Nevertheless, accumulating evidence suggests that the cerebellum may play a critical role in non-motor functions, contributing to cognitive and emotional processing [36]. In particular, a cerebellar involvement has been found in high-order cognitive processes such as language [7], working memory [8], and spatial processing [9, 10]. Furthermore, the cerebellum seems to play a role in the generation of sensory predictions [11, 12], optimising perception [13]. Accordingly, patients with cerebellar lesions are often impaired in processing visual information, such as in deciding speed and direction of moving stimuli [14]. Neuroimaging evidence also shows that the cerebellum is significantly active in neurologically unimpaired individuals during sensory discrimination, such as visual (and auditory) motion discrimination [15]. Also, interfering with cerebellar activity via brain stimulation has been found to impact on visual processing [16, 17].

The cerebellum is also involved in auditory processing, where it plays a critical role in timing [1821]. Cerebellar activations have also been observed in healthy subjects during passive listening of both music [22, 23] and speech [24, 25]. Moreover, pitch discrimination and melody discrimination [2628], as well as sound intensity and duration discrimination [29], activate cerebellar regions. For instance, Petacchi and colleagues [23] showed that cerebellar activity significantly increased during a pitch discrimination task compared to passive listening, with the cerebellum responding more when the difficulty of the discrimination to be performed increased. Importantly, cerebellar activity during auditory discrimination tasks has been consistently observed even in the absence of any motor or cognitive component [30]. Patients’ findings support evidence obtained in healthy individuals: cerebellar disorders are often associated to deficits in melody recognition [31], in discriminating small differences in sound duration [32] and in pitch discrimination [33].

Although there is considerable evidence that the cerebellum contributes to auditory perception [30], the precise role of the cerebellum in different aspects of sound processing is not completely clear. In particular, whilst neuroimaging [23, 30] and patients’ [33] studies converge in indicating a role of the cerebellum in pitch processing, whether the cerebellum also contributes to other sound features such as timbre (i.e., the property of a sound which allows a person to distinguish musical instrument when pitch, loudness and duration remain identical), is less clear. Indeed, whereas some neuroimaging studies reported significant cerebellar responses to sound timbre [34, 35], in other studies investigating timbre processing cerebellar activations were not considered [36].

The aim of this study was to analyse the role of the cerebellum in pitch and timbre processing using transcranial magnetic stimulation (TMS). While neuroimaging techniques provide correlational evidence regarding the activation in a specific brain region during an ongoing cognitive process, TMS allows establishing the causal role of specific cortical areas in a given task [37, 38]. Moreover, participants in TMS experiments act as their own controls overcoming some of the limitations intrinsic in patients’ studies, such as potential differences in pre-morbid ability, and variability depending on high heterogeneity of lesions’ sizes and gravity. Specifically, in this study we applied off line low frequency repetitive TMS to induce transient suppression of cerebellar activity [39, 40] before participants’ performance in a pitch and timbre discrimination tasks. If the cerebellum is causally involved in pitch and timbre processing, participants should perform worse following real than sham (faked) stimulation.

Methods

Participants

Fourteen participants (9 F; mean age = 21.93 ys; SD = 1.86) took part in the experiment. All participants were right-handed [41] and had less than 3 years of formal musical training, as revealed by a self-reported history of musical experience. Prior to the experiment, each participant filled in a questionnaire (translated from Rossi et al. [42]) to evaluate compatibility with TMS. None of the volunteers reported neurological problems, familiarity for seizures nor was taking any medication that could interfere with neuronal excitability. Written informed consent was obtained from all participants before the experiment. The protocol was approved by the local ethical committee. Participants’ treatment was conducted in accordance with the Declaration of Helsinki.

Stimuli

Stimuli used in the pitch discrimination task consisted of 21 pure tones (i.e., tones with a sinusoidal waveform, where the wave consists of a single frequency) of 200 ms generated through the software Audacity (http://audacity.sourceforge.net/). All tones had a frequency comprised between 1000 and 1200 Hz, and were presented at a level of 75 dB SPL. Stimuli used in the Timbre discrimination task consisted of 21 complex tones of 200 msec duration. Sound files in the timbre task were created from digitized samples of real musical instruments, with all instruments belonging to the wind or string family. Sound files used in the timbre task were taken from the University of Iowa Musical Instrument Samples (Lawrence Fritts, http://theremin.music.uiowa.edu/MIS.html).

Procedure

Figure 1 shows the experimental paradigm (Fig. 1a) and the timeline of an experimental trial (Fig. 1b). Participants seated comfortably in a dimly lit room and stimuli were binaurally delivered through professional headphone (Sennheiser HD 280 Pro headphone). Each subject took part in two different sessions (Real and Sham) that were separated by an average of 6 days (range 5–7). In each session, participants performed both the pitch discrimination task and the timbre discrimination task twice: once before, and once after receiving 15 min of off-line 1Hz rTMS over the right cerebellum. During TMS, no task was performed and participants were instructed to minimise movements and be silent. The post-stimulation task started immediately after the end of the stimulation. Both the pitch and timbre discrimination tasks required participants to indicate by left/right key pressing using their dominant hand whether two consecutively presented sounds (separated by 1 sec of silence interval) were identical or different. Participants were instructed to respond as fast and as accurately as possible. Intertrial interval was 2 sec. In each task, 42 sounds were presented: in half of the trials the two sounds to be compared were identical, in the other half they were different. In the different trials of the pitch task, the second pure tone presented could be 20, 30 or 40 Hz higher (ascending trials) or lower (descending trials) compared to the first one. The number of descending and ascending trials was counterbalanced. In the timbre task, the two sounds to be compared in each trial were identical in terms of frequency and intensity, but they had different timbre. In particular, two different string sounds may be presented, or two different wind sounds (wind and string sounds were never presented in the same trial to avoid ceiling effects in recognition). Task order (pitch and timbre discrimination), TMS condition order (Real vs. Sham), and the response key assignment for same/different response were counterbalanced across participants. The software E-prime 2.0 (Psychology Software Tools, Pittsburgh, PA) was used for stimuli presentation, data collection and TMS triggering. Pre and post-stimulation task sessions lasted approximately 10 min (5 min for each task).
Fig. 1

a The experimental paradigm: participants underwent two experimental sessions, one with real TMS, and the other with sham TMS (order of sessions counterbalanced). In each session, participants performed the task twice, once before and once after receiving 1 Hz repetitive 15 min TMS over the right cerebellum. b The timeline of an experimental trial. In the pitch discrimination task the two sounds were pure tones only differing for pitch. In the timbre discrimination task the two sounds were tones of the same instrumental family (wind vs. string) presented at the same high frequency and differing only in their timbre characteristic

Transcranial magnetic stimulation

TMS was administered over the right cerebellum by means of a Magstim Rapid2 machine (Magstim Co Ltd, Whitland, UK) with a 70 mm butterfly coil. An air-cooled coil was used, in order to avoid coil overheating. A fixed intensity of 45 % of the maximum stimulator output was used, in line with prior studies [43]. The right cerebellar hemisphere was targeted in light of previous evidence pointing to a right lateralized cerebellar activation during timbre processing [35], whereas pitch discrimination seems to induce bilateral cerebellar activations [23]. The right cerebellum was localised in each participant as the region located 1 cm under and 3 cm lateral to the inion as in prior studies [44, 45]. Prior studies using neuronavigated TMS have demonstrated that this point lies over the cerebellar hemisphere [17, 46]. The coil was placed over the right cerebellum with the handle pointing upward, parallel to the inion-nasion line [44, 47]. Previous studies have shown that rTMS at 1 Hz temporarily reduces the excitability of the stimulated cortex for a time window that outlasts the period of stimulation [39, 40]. Sham stimulation was conducted with the coil held at a 90° position in order to ensure that the magnetic field did not stimulate the target area. The stimulation paradigm in the sham condition was the same as that of real rTMS stimulation.

Statistical analyses

Analyses were performed on mean accuracy scores and on mean reaction times (RT) for correct responses. Prior to analyses, reaction times 3 s.d.’s above or below the participants’ mean were removed (this corresponded to 1.33 % and 1.99 % of the trials in the pitch and timbre discrimination task, respectively). A repeated-measures analysis of variance (ANOVA) with TMS condition (real vs. sham) and Session (pre-stimulation vs. post-stimulation) as within-subjects factors was performed separately for the pitch and the timbre discrimination task on accuracy scores and correct RT. Bonferroni-Holmes correction was applied to post-hoc comparisons.

Results

Pitch discrimination task

Mean accuracy was above 73 % (SD = 9 %) in all the experimental conditions. Analysis on accuracy scores revealed no significant main effects of TMS, F(1,13) = 3.75, p = .08, ηp 2 = .22, and of Session, F(1,13) = 1.47, p = .25, ηp 2 = .10. The interaction TMS by Session was not significant, F(1,13) < 1, p = .92, ηp 2 = .00. Mean correct RT are shown in Fig. 2. The ANOVA on correct RT showed no significant main effect of either TMS, F(1,13) = 1.30, p = .27, ηp 2 = .09, or Session, F(1,13) = 2.86, p = .11, ηp 2 = .18. The interaction TMS by Session was significant, F(1,13) = 8.08, p = .01, ηp 2 = .38. Post-hoc t-tests revealed that participants were significantly faster in responding in the post-sham stimulation session compared to the pre-sham stimulation session, t(13) = 3.52, p = .016, reflecting learning effects. In turn, RT were comparable between pre-real and post-real stimulation sessions, t(13) = .63, p = .54, suggesting that real TMS interfered with learning. Moreover, whilst RT were comparable in the sham and real pre-sessions, t(13) = 1.24, p = .24, indicating a similar level of baseline performance, participants tended to be slower following real, t(13) = 2.31, p = .09 (p = .03 uncorrected), than sham TMS.
Fig. 2

Mean response latencies for correct responses as a function of TMS (Real vs. Sham) and Session (Pre vs. Post stimulation) in the Pitch discrimination task. Participants were significantly faster (as indicated by the asterisk) in the post compared to the pre session when sham TMS was delivered, reflecting learning effects. RT were comparable in the pre and post real TMS sessions, suggesting that real TMS affected learning effects. Error bars represent ±1 SEM

Timbre discrimination task

Mean accuracy was above 82 % (SD = 9 %) in all the experimental conditions. The ANOVA on accuracy scores revealed no significant main effect of either TMS, F(1,13) = .50, p = .49, ηp 2 = .04, or Session, F(1,13) = .16, p = .22, ηp 2 = .12. The interaction TMS by Session was not significant, F(1,13) < 1, p = .99, ηp 2 = .00. Figure 3 shows mean participants’ correct RT. The ANOVA revealed a significant main effect of Session, F(1,13) = 4.95, p = .04, ηp 2 = .28: participants were overall faster in the post-stimulation session (irrespective of stimulation being real or sham), reflecting learning effects. Neither the main effect of TMS, F(1,13) = .03, p = .87, ηp 2 = .00, nor the interaction TMS by Session, F(1,13) = .57, p = .46, ηp 2 = .04, reached significance.
Fig. 3

Mean response latencies for correct responses as a function of TMS (Real vs. Sham) and Session (Pre and Post stimulation) in the Timbre discrimination task. Participants were overall faster in the post compared to the pre session, reflecting learning effects. The type of stimulation (Real vs. Sham) did not affect performance. Error bars represent ±1 SEM

Discussion

In this study we aimed to shed light on the possible causal role of the cerebellum in auditory processing, and in particular in pitch and timbre discrimination, in light of prior neuroimaging and patients’ data suggesting a cerebellar involvement in processing of music and single sound features [3133, 48]. We found that interfering with cerebellar excitability via offline low frequency TMS significantly affected pitch discrimination, whereas it had no effect on timbre discrimination. In particular, in the pitch discrimination task real TMS counteracted learning effects that emerged in the other experimental conditions as faster responses in the post compared to the pre stimulation sessions.

Our findings are consistent with prior neuroimaging and neuropsychological evidence suggesting that the cerebellum is involved in perceptual tasks [8, 49, 50], possibly monitoring the incoming sensory events to optimize perception [13, 51]. More specifically, our data add to previous studies that showed that discrimination of pitch and melody elicit activation of cerebellar regions [26, 28, 33], pointing to a causal role for the (right) cerebellum in processing pitch. Accordingly, resting state fMRI has shown functional connectivity between bilateral anterior cerebellum and the auditory cortex in the temporal lobes [52]. In line with this, the cerebellum and the lateral anterior temporal lobe appeared to be bidirectionally interconnected during a rhyming judgment task [53]. More in general, consistent evidence suggests that the cerebellum projects not only to motor, but also to somatosensory areas [6]. Still, it is important to consider that the type of stimulation we used may have only affected posterior cerebellar regions, given the deep position of the cerebellum [54]. Indeed, coil geometry seems to be an important factor in determining effective stimulation of deep cerebellar regions, with the figure of eight coil likely being suboptimal when targeting motor areas [54]. Nonetheless, cerebellar stimulation parameters similar to ours significantly affected perceptual [16] and cognitive (for instance, linguistic) functions in prior studies (e.g. [55, 56]), suggesting that the stimulation we used was able to interfere with neural activity in the cerebellar-cortical network subtending discrimination of sound features.

Although prior neuroimaging evidence also suggested a possible role for the cerebellum in timbre processing [34, 57], we did not find evidence for this in our study. On the one hand, the lack of TMS effect in the timbre discrimination task ensures that the effects we reported in the pitch discrimination task were not due to unspecific effects of TMS slowing down responses regardless of the specific task at play. On the other hand, it is possible that real TMS affects auditory discrimination task only when the task has a certain level of complexity. Performance accuracy was indeed overall higher in the timbre than in the pitch task. This is in line with prior literature showing that non-musicians are more sensitive in sound categorization to changes in timbre than to changes in pitch [58]. Interestingly, previous studies demonstrated a positive correlation between cerebellar activation and task difficulty [15, 23, 28, 59]. Moreover, the right cerebellum may be more important than the left in difficult auditory discrimination [57].

In interpreting our data, it is also worth mentioning that pitch and timbre processing may have a different degree of lateralization in the brain. There is evidence for a right hemisphere dominance in the temporal lobes for musical timbre discrimination [60, 61] related to a right hemispheric specialization in processing spectral sound features, that are critical for discriminating timbre differences [6264]. In line with these findings, the left cerebellum may be more important than the right in timbre processing (cerebral cortex fibers mainly projecting to the contralateral cerebellar cortex [65]). However, other studies in infants [66] and in adults [35, 67] reported left hemispheric cerebral cortex engagement underlying perception of timbre change. Moreover, Reiterer and colleagues [35] showed a right cerebellar activation during timbre processing, speculating that pre-linguistic sound features (including timbre) may be represented by a complex network that connects Broca’s area and the right cerebellum. In turn, previous neuroimaging studies mainly indicate bilateral cerebellar activation during pitch processing [23, 2628, 30, 34], although some degree of lateralization may occur depending on task complexity [29, 57, 68]. Evidences are thus not entirely consistent regarding lateralization of timbre and pitch processing. Future studies may address this issue by comparing the effect of left and right cerebellar stimulation on auditory discrimination.

Conclusions

In sum, our findings show that the (right) cerebellum plays a causal role in pitch processing. Future research is needed to better clarify the role of cerebellum in other aspects of auditory processing, such as rhythm or complex melody recognition and discrimination. Moreover, level of expertise in determining the involvement of the cerebellum in auditory functions deserves consideration. In fact, prior studies showed greater engagement of the cerebellum in rhythm perception and synchronization in musicians compared to non-musicians [69, 70]. Musicians have been found to detect pitch changes and rhythmic irregularities faster and more accurately than non-musicians [7173], an ability that may also depend on different cerebellar involvement. The relation between level of expertise and cerebellar involvement in perceptual functions is an important topic to which brain stimulation may significantly contribute. Finally, our results are important in a clinical perspective helping understanding the impact of cerebellar lesions on sensory and cognitive functions.

Declarations

Acknowledgement

None of the authors declare to have any financial or non-financial competing interests.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Psychology, University of Milano-Bicocca
(2)
Department of Brain and Behavioural Sciences, University of Pavia
(3)
Brain Connectivity Center, C. Mondino National Neurological Institute

References

  1. Manto M, Bower JM, Conforto AB, Delgado-García JM, Da Guarda SNF, Gerwig M, et al. Consensus paper: Roles of the cerebellum in motor control-the diversity of ideas on cerebellar involvement in movement. Cerebellum. 2012;11(2):457–87.PubMed CentralView ArticlePubMedGoogle Scholar
  2. Shiffrin RM, Schneider W. Automatic and controlled processing revisited. Psychol Rev. 1984;91(2):269–76.View ArticlePubMedGoogle Scholar
  3. Leiner HC, Leiner AL, Dow RS. Cognitive and language functions of the human cerebellum. Trends Neurosci. 1993;16(11):444–7.View ArticlePubMedGoogle Scholar
  4. Middleton F, Strick PL. Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. Science. 1994;266(5184):458–61.View ArticlePubMedGoogle Scholar
  5. Stoodley CJ. The cerebellum and cognition: evidence from functional imaging studies. Cerebellum. 2012;11(2):352–65.View ArticlePubMedGoogle Scholar
  6. D’Angelo E, Casali S. Seeking a unified framework for cerebellar function and dysfunction: from circuit operations to cognition. Front Neural Circuits. 2012;6:116.PubMed CentralPubMedGoogle Scholar
  7. Ackermann H. Cerebellar contributions to speech production and speech perception: psycholinguistic and neurobiological perspectives. Trends Neurosci. 2008;31(6):265–72.View ArticlePubMedGoogle Scholar
  8. Ben-Yehudah G, Guediche S, Fiez J. Cerebellar contributions to verbal working memory: beyond cognitive theory. Cerebellum. 2007;6(3):193–201.View ArticlePubMedGoogle Scholar
  9. Molinari M, Chiricozzi FR, Clausi S, Tedesco AM, De Lisa M, Leggio MG. Cerebellum and detection of sequences, from perception to cognition. Cerebellum. 2008;7(4):611–5.View ArticlePubMedGoogle Scholar
  10. Lee TM, Liu HL, Hung KN, Pu J, Ng YB, Mak AK, et al. The cerebellum’s involvement in the judgment of spatial orientation: a functional magnetic resonance imaging study. Neuropsychologia. 2005;43(13):1870–7.View ArticlePubMedGoogle Scholar
  11. Miall RC. Sequences of sensory predictions. Behav Brain Sci. 1997;20(2):258.View ArticleGoogle Scholar
  12. Blakemore SJ, Frith CD, Wolpert DM. The cerebellum is involved in predicting the sensory consequences of action. Neuroreport. 2001;12(9):1879–84.View ArticlePubMedGoogle Scholar
  13. Roth MJ, Synofzik M, Lindner A. The Cerebellum Optimizes Perceptual Predictions about External Sensory Events. Curr Biol. 2013;23(10):1–6.View ArticleGoogle Scholar
  14. Ivry RB, Diener HC. Impaired Velocity Perception in Patients with Lesions of the Cerebellum. J Cogn Neurosci. 1991;3(4):355–66.View ArticlePubMedGoogle Scholar
  15. Baumann O, Mattingley JB. Scaling of neural responses to visual and auditory motion in the human cerebellum. J Neurosci. 2010;30(12):4489–95.View ArticlePubMedGoogle Scholar
  16. Cattaneo Z, Renzi C, Casali S, Silvanto J, Vecchi T, Papagno C, et al. Cerebellar vermis plays a causal role in visual motion discrimination. Cortex. 2014;58:272–80.View ArticlePubMedGoogle Scholar
  17. Renzi C, Vecchi T, D’Angelo E, Silvanto J, Cattaneo Z. Phosphene induction by cerebellar transcranial magnetic stimulation. Clin Neurophysiol. 2014;125(10):1–2.View ArticleGoogle Scholar
  18. Grube M, Lee K-H, Griffiths TD, Barker AT, Woodruff PW. Transcranial magnetic theta-burst stimulation of the human cerebellum distinguishes absolute, duration-based from relative, beat-based perception of subsecond time intervals. Front Psychol. 2010;1:171.PubMed CentralView ArticlePubMedGoogle Scholar
  19. Kawashima R, Okuda J, Umetsu A, Sugiura M, Inoue K, Suzuki K, et al. Human cerebellum plays an important role in memory-timed finger movement: an fMRI study. J Neurophysiol. 2000;83:1079–87.PubMedGoogle Scholar
  20. Lutz K, Specht K, Shah NJ, Jäncke L. Tapping movements according to regular and irregular visual timing signals investigated with fMRI. Neuroreport. 2000;11(6):1301–6.View ArticlePubMedGoogle Scholar
  21. Teki S, Grube M, Kumar S, Griffiths TD. Distinct neural substrates of duration-based and beat-based auditory timing. J Neurosci. 2011;31(10):3805–12.PubMed CentralView ArticlePubMedGoogle Scholar
  22. Brown S, Martinez MJ, Parsons LM. Passive music listening spontaneously engages limbic and paralimbic systems. Neuroreport. 2004;15(13):2033–7.View ArticlePubMedGoogle Scholar
  23. Petacchi A, Kaernbach C, Ratnam R, Bower JM. Increased activation of the human cerebellum during pitch discrimination: A positron emission tomography (PET) study. Hear Res. 2011;282(1–2):35–48.View ArticlePubMedGoogle Scholar
  24. Callan DE, Tsytsarev V, Hanakawa T, Callan AM, Katsuhara M, Fukuyama H, et al. Song and speech: Brain regions involved with perception and covert production. Neuroimage. 2006;31(3):1327–42.View ArticlePubMedGoogle Scholar
  25. Callan D, Kawato M, Parsons L, Turner R. Speech and song: The role of the cerebellum. The Cerebellum. 2007;6:321–7.View ArticlePubMedGoogle Scholar
  26. Griffiths TD, Johnsrude I, Dean JL, Green GG. A common neural substrate for the analysis of pitch and duration pattern in segmented sound? Neuroreport. 1999;10(18):3825–30.View ArticlePubMedGoogle Scholar
  27. Parsons LM. Exploring the functional neuroanatomy of music performance, perception, and comprehension. Ann N Y Acad Sci. 2001;930:211–31.View ArticlePubMedGoogle Scholar
  28. Gaab N, Gaser C, Zaehle T, Jancke L, Schlaug G. Functional anatomy of pitch memory - An fMRI study with sparse temporal sampling. Neuroimage. 2003;19(4):1417–26.View ArticlePubMedGoogle Scholar
  29. Belin P, McAdams S, Thivard L, Smith B, Savel S, Zilbovicius M, et al. The neuroanatomical substrate of sound duration discrimination. Neuropsychologia. 2002;40(12):1956–64.View ArticlePubMedGoogle Scholar
  30. Petacchi A, Laird AR, Fox PT, Bower JM. Cerebellum and auditory function: an ALE meta-analysis of functional neuroimaging studies. Hum Brain Mapp. 2005;25(1):118–28.View ArticlePubMedGoogle Scholar
  31. Tölgyesi B, Evers S. The impact of cerebellar disorders on musical ability. J Neurol Sci. 2014;343(1–2):76–81.View ArticlePubMedGoogle Scholar
  32. Ivry RB, Keele SW. Timing Functions of The Cerebellum. J Cogn Neurosci. 1989;1(2):136–52.View ArticlePubMedGoogle Scholar
  33. Parsons LM, Petacchi A, Schmahmann JD, Bower JM. Pitch discrimination in cerebellar patients: evidence for a sensory deficit. Brain Res. 2009;1303:84–96.View ArticlePubMedGoogle Scholar
  34. Alluri V, Toiviainen P, Jääskeläinen IP, Glerean E, Sams M, Brattico E. Large-scale brain networks emerge from dynamic processing of musical timbre, key and rhythm. Neuroimage. 2012;59(4):3677–89.View ArticlePubMedGoogle Scholar
  35. Reiterer S, Erb M, Grodd W, Wildgruber D. Cerebral Processing of Timbre and Loudness: fMRI Evidence for a Contribution of Broca’s Area to Basic Auditory Discrimination. Brain Imaging Behav. 2007;2(1):1–10.View ArticleGoogle Scholar
  36. Halpern AR, Zatorre RJ, Bouffard M, Johnson JA. Behavioral and neural correlates of perceived and imagined musical timbre. Neuropsychologia. 2004;42(9):1281–92.View ArticlePubMedGoogle Scholar
  37. Parkin BL, Ekhtiari H, Walsh VF. Non-invasive Human Brain Stimulation in Cognitive Neuroscience: A Primer. Neuron. 2015;87(5):932–45.View ArticlePubMedGoogle Scholar
  38. Walsh V, Pascual-Leone A, Kosslyn S. Transcranial magnetic stimulation: A neurochronometrics of mind. Cambridge, MA: MIT Press; 2003. p. 84–8.Google Scholar
  39. Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology. 1997;48(5):1398–403.View ArticlePubMedGoogle Scholar
  40. Oliveri M, Koch G, Torriero S, Caltagirone C. Increased facilitation of the primary motor cortex following 1 Hz repetitive transcranial magnetic stimulation of the contralateral cerebellum in normal humans. Neurosci Lett. 2005;376(3):188–93.View ArticlePubMedGoogle Scholar
  41. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9(1):97–113.View ArticlePubMedGoogle Scholar
  42. Rossi S, Hallett M, Rossini PM, Pascual-Leone A, Avanzini G, Bestmann S, et al. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol. 2009;120(12):2008–39.PubMed CentralView ArticlePubMedGoogle Scholar
  43. Schutter DJ, van Honk J. The Cerebellum in Emotion Regulation: A Repetitive Transcranial Magnetic Stimulation Study. The Cerebellum. 2009;8(1):28–34.View ArticlePubMedGoogle Scholar
  44. Théoret H, Haque J, Pascual-Leone A. Increased variability of paced finger tapping accuracy following repetitive magnetic stimulation of the cerebellum in humans. Neurosci Lett. 2001;306(1–2):29–32.View ArticlePubMedGoogle Scholar
  45. Torriero S, Oliveri M, Koch G, Caltagirone C, Petrosini L. Interference of Left and Right Cerebellar rTMS with Procedural Learning. J Cogn Neurosci. 2004;16(9):1605–11.View ArticlePubMedGoogle Scholar
  46. Del Olmo MF, Cheeran B, Koch G, Rothwell JC. Role of the cerebellum in externally paced rhythmic finger movements. J Neurophysiol. 2007;98(1):145–52.View ArticlePubMedGoogle Scholar
  47. Oliver R, Opavsky R, Vyslouzil M, Greenwood R, Rothwell JC. The role of the cerebellum in “real” and “imaginary” line bisection explored with 1-Hz repetitive transcranial magnetic stimulation. Eur J Neurosci. 2011;33(9):1724–32.View ArticlePubMedGoogle Scholar
  48. Frings M, Maschke M, Gerwig M, Diener H-C, Timmann D. Acquisition of simple auditory and visual sequences in cerebellar patients. Cerebellum. 2006;5(3):206–11.View ArticlePubMedGoogle Scholar
  49. Ackermann H, Mathiak K, Riecker A. The contribution of the cerebellum to speech production and speech perception: clinical and functional imaging data. Cerebellum. 2007;6(3):202–13.View ArticlePubMedGoogle Scholar
  50. Ivry RB, Schlerf JE. Dedicated and intrinsic models of time perception. Trends Cogn Sci. 2008;12(7):273–80.PubMed CentralView ArticlePubMedGoogle Scholar
  51. Bower JM. Control of sensory data acquisition. Int Rev Neurobiol. 1997;41:489–513.View ArticlePubMedGoogle Scholar
  52. He Y, Zang Y, Jiang T, Liang M, Gong G. Detecting Functional Connectivity of the Cerebellum Using Low Frequency Fluctuations (LFFs). Med Image Comput Comput Interv. 2004;3217:907–15.Google Scholar
  53. Booth JR, Wood L, Lu D, Houk JC, Bitan T. The role of the basal ganglia and cerebellum in language processing. Brain Res. 2007;1133(1):136–44.PubMed CentralView ArticlePubMedGoogle Scholar
  54. Hardwick RM, Lesage E, Miall RC. Cerebellar Transcranial Magnetic Stimulation: The Role of Coil Geometry and Tissue Depth. Brain Stimul. 2014;7(5):643–9.PubMed CentralView ArticlePubMedGoogle Scholar
  55. Argyropoulos GP, Muggleton NG. Effects of cerebellar stimulation on processing semantic associations. Cerebellum. 2013;12(1):83–96.View ArticlePubMedGoogle Scholar
  56. Arasanz CP, Staines WR, Roy EA, Schweizer TA. The cerebellum and its role in word generation: A cTBS study. Cortex. 2012;48(6):718–24.View ArticlePubMedGoogle Scholar
  57. Reiterer SM, Erb M, Droll CD, Anders S, Ethofer T, Grodd W, et al. Impact of task difficulty on lateralization of pitch and duration discrimination. Neuroreport. 2005;16(3):239–42.View ArticlePubMedGoogle Scholar
  58. Pitt MA. Perception of pitch and timbre by musically trained and untrained listeners. J Exp Psychol Hum Percept Perform. 1994;20(5):976–86.View ArticlePubMedGoogle Scholar
  59. Holcomb HH, Medoff DR, Caudill PJ, Zhao Z, Lahti AC, Dannals RF, et al. Cerebral blood flow relationships associated with a difficult tone recognition task in trained normal volunteers. Cereb Cortex. 1998;8:534–42.View ArticlePubMedGoogle Scholar
  60. Crummer GC, Walton JP, Wayman JW, Hantz EC, Frisina RD. Neural processing of musical timbre by musicians, nonmusicians, and musicians possessing absolute pitch. J Acoust Soc Am. 1994;95(5):2720–7.View ArticlePubMedGoogle Scholar
  61. Samson S. Neuropsychological studies of musical timbre. Ann N Y Acad Sci. 2003;999:144–51.View ArticlePubMedGoogle Scholar
  62. Menon V, Levitin D, Smith BK, Lembke A, Krasnow B, Glazer D, et al. Neural Correlates of Timbre Change in Harmonic Sounds. Neuroimage. 2002;17(4):1742–54.View ArticlePubMedGoogle Scholar
  63. Zatorre RJ, Belin P, Penhune VB. Structure and function of auditory cortex music and speech. Trends Cogn Sci. 2002;6(1):37–46.View ArticlePubMedGoogle Scholar
  64. Warren JE, Wise RJS, Warren JD. Sounds do-able: Auditory-motor transformations and the posterior temporal plane. Trends in Neurosciences. 2005;28(12):636–643.View ArticlePubMedGoogle Scholar
  65. Jansen A, Floel A, Van Randenborgh J, Konrad C, Rotte M, Forster AF, et al. Crossed cerebro-cerebellar language dominance. Hum Brain Mapp. 2005;24(3):165–72.View ArticlePubMedGoogle Scholar
  66. Dehaene-Lambertz G. Cerebral specialization for speech and non-speech stimuli in infants. J Cogn Neurosci. 2000;12(3):449–60.View ArticlePubMedGoogle Scholar
  67. Deike S, Gaschler-Markefski B, Brechmann A, Scheich H. Auditory stream segregation relying on timbre involves left auditory cortex. Neuroreport. 2004;15(9):1511–4.View ArticlePubMedGoogle Scholar
  68. Belin P, McAdams S, Smith B, Savel S, Thivard L, Samson S, et al. The functional anatomy of sound intensity discrimination. J Neurosci. 1998;18(16):6388–94.PubMedGoogle Scholar
  69. Chen JL, Penhune VB, Zatorre RJ. Moving on time: brain network for auditory-motor synchronization is modulated by rhythm complexity and musical training. J Cogn Neurosci. 2008;20(2):226–39.View ArticlePubMedGoogle Scholar
  70. Grahn JA, Brett M. Rhythm and beat perception in motor areas of the brain. J Cogn Neurosci. 2007;19(5):893–906.View ArticlePubMedGoogle Scholar
  71. Tervaniemi M, Just V, Koelsch S, Widmann A, Schröger E. Pitch discrimination accuracy in musicians vs nonmusicians: An event-related potential and behavioral study. Exp Brain Res. 2005;161(1):1–10.View ArticlePubMedGoogle Scholar
  72. Micheyl C, Delhommeau K, Perrot X, Oxenham AJ. Influence of musical and psychoacoustical training on pitch discrimination. Hear Res. 2006;219(1–2):36–47.View ArticlePubMedGoogle Scholar
  73. Rammsayer T, Altenmüller E. Temporal information processing in musicians and nonmusicians. Music Percept. 2006;24(1):37–48.View ArticleGoogle Scholar

Copyright

© Lega et al. 2016

Advertisement