Elsevier

Magnetic Resonance Imaging

Volume 21, Issue 7, September 2003, Pages 821-828
Magnetic Resonance Imaging

Cortical plasticity in an early blind musician: an fMRl study

https://doi.org/10.1016/S0730-725X(03)00103-6Get rights and content

Abstract

Many studies have examined tactile perception and simple auditory perception in the blind, but none have previously investigated the neural basis of musical ability in this group. This topic is of particular interest because it has been suggested that early blind individuals may possess advanced musical skills (such as absolute pitch). Presumably, these skills could be the result of neural plasticity. It has been hard to empirically assess this claim because of the difficulty in recruiting an adequate number of subjects for use in a conventional paradigm. In the present paper, we report data from a congenitally blind musician, subject ML. Behavioral tests show that she possessed absolute pitch abilities that were similar to those of a reference group of AP musicians with normal vision. To examine the neural basis of her abilities we then tested subject ML and five control subjects using an fMRI paradigm. A regions-of-interest analysis found that similar areas (the right secondary auditory cortex, left IFG, left SMG) were activated in ML and the control subjects, to a similar degree, in response to music processing. However, ML showed additional activations in left parietal association cortices and extrastriate regions of the occipital lobe. Subject ML’s data are consistent with a vast body of literature on blindness-induced plasticity. They extend these findings by demonstrating that cortical plasticity may underlie special musical skills as well. These data illustrate the potential value of case studies to investigate particularly rare phenotypes.

Introduction

Music has often been postulated as an area of advanced competence in blind individuals, perhaps due to high profile individuals such as Ray Charles and Stevie Wonder. It is plausible that this musical expertise arises from a learning-induced alteration in neural structures that is enhanced in part by the deprivation of sight and the subsequent reliance on audition. A substantial body of literature has been devoted to understanding this type of plasticity and the complex interplay that occurs between the negative impact of sensory deprivation and the simultaneous, compensatory, expansion of other brain regions.

Animal studies of visual deprivation have shown that changes occur both subcortically (e.g., in the superior colliculus [24], [37] and lateral geniculate nucleus [20], [23]) as well as in the primary and secondary visual cortices [5], [22]. Further, functional studies of brain activity in early blind humans show that regions normally involved in visual association (including accessory visual cortex and parietal association areas) may be recruited to process both tactile [6], [9], [29], [30], [31], [36] and auditory [1], [16], [17] stimuli. Plasticity has also been observed throughout the auditory pathway of both visually deprived animals [12], [14], [25], [28] and early blind humans [6], [17], [26], [36]. While these studies elucidate some heightened auditory skills in blind individuals (e.g., enhanced spatial localization), relatively few paradigms have examined auditory processing as compared to somatosensory or visual systems. Moreover, to the best of our knowledge, no studies have addressed the functional plasticity associated with musical expertise in the blind.

Previously [27], we used functional magnetic resonance imaging (fMRI) to study the neural networks involved in intervalic pitch perception (i.e., the determination of frequency relationships) in musicians who were possessors or non-possessors of absolute pitch (AP or NAP). We hypothesized that differences in the auditory cortex may account for the basic, perceptual differences between AP and NAP musicians. Indeed, AP subjects demonstrated a highly consistent pattern of activation that was distinct from that of NAP subjects in the right auditory cortex. Additional activations were found in the left supramarginal gyrus (SMG) and the left inferior frontal gyrus (IFG).

The consistency of the pattern of activations in AP subjects led us to ask the question: would similar areas be recruited by early blind musicians who also possessed absolute pitch? If blind individuals with AP did not share the same auditory activation, it would suggest that a rearrangement of functional regions had caused them to develop this distinct phenotype. Alternatively, if early blind individuals shared similar basic activations with other AP musicians but also showed new activations not present in our previous study, it would suggest that these individuals may recruit additional cortical areas for musical processing when there is deprivation of a major sensory modality.

Unfortunately, it would be difficult to address this question in a conventional manner. Historically, the majority of studies that have investigated functional plasticity have used PET imaging, which requires a relatively large number of subjects per group. To recruit an adequate number of subjects with a specialized skill from within what is already a very small subset of the population would be prohibitve (consider that the prevalence of AP is estimated to be ∼1/10,000 [2] and the prevalence of early blindness in the United States is probably less than 1/1,000 (see www.cdc.gov/ncbddd/); thus, if they were independent phenomena the overall prevalence would be ∼1/10,000,000; given the most liberal estimate of dependence (cf. [38]), it would still be less than 1/5,000). Fortunately, the development of fMRI techniques has now made it possible to investigate functional activation in single subjects. While it is difficult to make broad conclusions based on a single individual, such data may still yield important insights into otherwise inaccessible phenomena.

In this paper, we used fMRI to investigate the neural basis of exceptional musical skills in a congenitally blind musician, subject ML. Our goal was to determine whether she used the same neural substrates during the performance of a specific, higher-order, musical task as subjects of similar ability but with normal vision. We used the same paradigm that we had tested previously with AP and NAP musicians. Briefly, this paradigm involved listening to five note sequences and naming them according to the rules of “moveable do” solfeggio. There was no visual stimulation and the control subjects had been asked to keep their eyes closed during all imaging conditions. The solfeggio task was chosen because it explicitly isolates the process of identifying the relationship between frequency stimuli without regard for the absolute frequency of the tones. It is important to emphasize that both AP possessors and non-possessors must be skilled at such comparisons if they are to be successful musicians. This is true because music is fundamentally based on the relationships between notes rather than on the specific frequency values, per se. For example, different orchestras may tune to different frequency values of “A.” Similarly, the correct frequency of the note “F#” will differ for non-keyboard instruments depending on the key of the piece. Another example of the essential nature of relative tuning is in choral music: because choirs typically go flat as a piece progresses, it is imperative that musicians sing notes that are correctly tuned to their peers rather than to any absolute values. Thus, the ability to recognize the frequency of tones may be seen as an additional skill found in AP possessors- however, both AP and NAP musicians must develop a refined sense of relative pitch as well (cf. [3]). “Moveable Do” solfeggio is a natural extension of this skill with which all of our subjects were familiar.

In the current study, we were specifically interested in the three significant areas of activation found previously (the right secondary auditory cortex, left IFG, left SMG) and other cortical regions that are known, based on previous research, to be recruited specially by blind individuals performing sensory tasks (i.e., polymodal areas in the parietal lobe, and extrastriate cortex in the occipital lobe).

Section snippets

Subjects

The subject, ML, was an eighteen year old, right handed, congenitally anophthalmic/microphthalmic woman. Since birth, she has had minimal residual light sensation in her right eye and no vision in her left eye. She began musical training in performance at age 3 and had nine years of experience on the trumpet (her primary instrument) and an additional 8 years of experience on the piano. She began studying music theory at age 6 and had a total of 10 years experience in the field. ML reported

AP test

ML correctly responded to 59 of the 60 stimuli on the AP test ( = .983), thus corroborating her claim that she possessed AP. Control subjects performed at an average of .90 ± .07 (range .84–1.00). This difference was not statistically significant (transformed t test [33]; t(4) = 1.1, n.s.), suggesting that ML had absolute pitch capabilities that were similar to those of the reference AP subjects.

Behavioral data

ML performed at .98, .76, and .50 for the easy, medium, and hard conditions (compared to .88 ±

Discussion

Subject ML showed similar activation to sighted AP musicians in the network previously identified as underlying absolute pitch. Included in this network were the right secondary auditory cortex, the left IFG, and the left SMG. These data suggest that subject ML’s absolute pitch may stem from the same cortical network as sighted AP musicians and is not the byproduct of the recruitment of other visual or associative cortex.

In addition to these regions, ML also showed increased activation in

Acknowledgements

The authors would like to thank subject ML for her insights and cooperation. The authors would also like to thank Pasko Rakic, Patricia Goldman-Rakic, Robert Fulbright, Carol Weingarten, and Hoi-Chung Leung for their expert consultation on this project, Cheryl Lacadie and Hedy Sarofin for technical assistance, and Thomas C. Duffy and Thomas Cantey for invaluable musical consultation.

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