Congenital amusia is a neurogenetic disorder of music processing that is currently ascribed to a deficit in pitch processing. A recent study challenges this view and claims the disorder might arise as a consequence of a general spatial-processing deficit. Here, we assessed spatial processing abilities in two independent samples of individuals with congenital amusia by using line bisection tasks (Experiment 1) and a mental rotation task (Experiment 2). Both amusics and controls showed the classical spatial effects on bisection performance and on mental rotation performance, and amusics and controls did not differ from each other. These results indicate that the neurocognitive impairment of congenital amusia does not affect the processing of space.

Funding: This research was supported by grants from the Cluster 11 of the Region Rhone-Alpes to BT and OB, by an infrastructure grant from the Fonds de Recherche en Sante du Quebec to IP and PJ, research grants from the Natural Sciences and Engineering Research Council of Canada to PJ and to IP, grants from the Canadian Foundation for Innovation to IP and PJ, a grant from the Canadian Institutes of Health Research to IP, and a grant from the Deutsche Forschungsgemeinschaft to MI. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright: © 2010 Tillmann et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Introduction

Most humans are born with the potential to speak and to make music. For the majority of individuals who are musically untrained, this fundamental human trait is expressed by music listening, occasional dancing, and occasional singing. The propensity to engage in music ultimately gives rise to a sophisticated music processing system that is acquired largely implicitly by experience. However, a minority of individuals never acquire this core musical system, either in part or at all, despite normal hearing and other cognitive functions and normal exposure to music. This condition concerns 4% of the general population [1] and is termed congenital amusia [2]. This disorder is akin to other developmental disorders, such as congenital prosopagnosia, dyscalculia, dysphasia, and dyslexia.

Congenital amusia is thought to result from a musical pitch-processing disorder. What amusics seem to be lacking are pitch-processing abilities that are normally and incidentally acquired by ordinary listeners early in life, and that are essential for normal music processing. Indeed, amusic individuals are impaired in processing pitch directions [3] and detecting pitch deviations that are smaller than one semitone in tone sequences [4] as well as in tone pairs [2]. Given that amusic individuals are probably born with such an elemental deficit (normal infants' pitch acuity is in the order of half a semitone [5]), they probably have not assimilated the structure of musical scales nor acquired the sophisticated tonal knowledge that normally developing individuals implicitly acquire via mere exposure [6]. Thus, a perceptual system that is unable to perceive small pitch changes is likely to miss an essential part of musical structure [7].

Indeed, amusic individuals fail to recognize a familiar tune without the aid of the lyrics, are unable to detect when they sing out-of-tune, and have severe difficulties to judge if two melodies are the same or different, especially on the pitch dimension. They also show little sensitivity to the presence of obvious pitch violations in melodies and of dissonant chords in classical music [8]. The pitch-processing deficit can even affect the processing of speech intonation [9]. An associated rhythm deficit that is observed in about half of amusics seems to result from pitch variations in melodies [2], [8], [10]. When presented with rhythmic sequences from which pitch variations are removed, amusic individuals discriminate them as well as control participants [11]. In sum, the core deficit in amusia concerns the processing of pitch.

This musical pitch-processing disorder represents a phenotype that serves to identify the associated neuro-genetic factors [12], [13], [14], [15]. However, Douglas and Bilkey [16] have recently challenged this view. They reported that amusics were impaired in a classic mental rotation task and were less influenced by the spatial layout of response keys in a pitch-judgment task, compared to musically-normal participants. This apparent deficit of spatial processing suggested to them an impairment in amusia of a shared mental representation of pitch and space. If confirmed, these results challenge the current search for causal links between musical pitch, brain, and behavior [17]. The goal of the present study was to investigate further this putative spatial deficit in amusia.

The hypothesis of a link between pitch and space is not new. There is evidence that pitch processing interacts with visual space representations in the normal brain (e.g., [18], [19], [20], [21], [22]). As also shown by Douglas and Bilkey [16], spatial associations with pitch can be revealed by stimulus-response compatibility effects [19], [20]. Responses may slow down when the spatial arrangement of response keys conflicts with the spatial descriptors of the to-be-judged materials, such as a spatially lower response key position to respond to a higher pitch (or a spatially higher key position for a lower pitch) relative to spatially-compatible pairings (e.g., higher key position for higher pitch). Similar spatial compatibility effects have been reported for number processing (e.g., right vs. left response keys to respond to larger vs. smaller numbers, or vice-versa [23], [24], [25], [26]). Recent evidence suggests that these spatial representations are specific to pitch and number domains, respectively. Notably, Beecham et al. [27] reported spatial stimulus-response compatibility effects for both number and pitch together, but with independence of these effects.

Within the musical domain, an association between pitch and space has been documented in other contexts than the stimulus-response compatibility arrangement. For example, musical expertise can lead to enhanced visuo-spatial processing [28], [29]. Therefore, the possibility that congenital amusia might represent the low end of a continuum from deficit to excellence in pitch processing and its association to spatial processing, as suggested by Douglas and Bilkey, is plausible and thus worthy of further studies.

Our first aim was to further explore the spatial processing deficit that has been revealed by Douglas and Bilkey. Impaired spatial representations can be caused by a distorted representation (thus decreased accuracy, e.g., due to biases) and/or decreased precision (leading to increased variability). These two aspects of spatial representation can be investigated with the line bisection task [30], [31], which was used in Experiment 1.

The line bisection task is a widely used tool to assess spatial representations in neglect patients [33], [34] and healthy participants [35]. It mainly allows testing spatial representations for accuracy, notably by measuring the distance between bisection point and veridical midpoint. But it can be also used to assess the precision of spatial representation by measuring inter-trial variability. Previous research has reported pathological cases showing deficits in both accuracy and precision (e.g., hemi-neglect patients [30], [36]) or solely in precision (e.g., [37]). Healthy participants typically bisect the line slightly and systematically to the left of the midpoint, also referred to as pseudo-neglect [38]. In a normal brain, bisection performance is affected by simultaneous number processing, suggesting interactions between mental representations of space and numbers. The influence of numbers on bisection performance is probably mediated by the spatial representation of the mental number line that is arranged from left to right [39], [40]: When lines are made out of number words (see Figure 1), smaller numbers (i.e., two/deux) induce a stronger leftward bias than larger numbers (i.e., nine/neuf).

PPT PowerPoint slide

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larger image TIFF original image Download: Figure 1. Bisection tasks (Experiment 1). Participants were instructed to mark the midpoint of a straight line as in panel A or a line made of letter strings spelling out small or larger number words (two and nine written in French) as in panel B. https://doi.org/10.1371/journal.pone.0010173.g001

Experiment 1 used the bisection task as a tool to determine the nature of the putative spatial deficit of amusics, notably by measuring accuracy and precision as well as the modulation of the representations with suspected associations (i.e., numbers). The use of the bisection paradigm was further motivated by a recent data set showing an influence of musical expertise on bisection performance: musicians bisect more accurately, closer to the center, or show a rightward bias [41]. Musicians and amusic individuals represent two extremes of the spectrum of musical ability: while improved spatial abilities have been reported for musicians also with other tasks (e.g., [28], [29]), impaired spatial processing has been reported for amusic individuals [16].

Here, a group of amusics and a group of controls were tested in two bisection conditions, with the straight line (i.e., the classical version) and a number line made out of small or large numbers. Based on Douglas and Bilkey's claim that amusia is “strongly related to a deficit in spatial processing” (p. 913) and the previously observed relations between the processing of space and numbers (e.g., [23], [24], [26]), altered bisection performance was expected for congenital amusics in all conditions in comparison to controls. If, however, spatial representations are distinct for pitch and numbers, as suggested by Beecham et al. [27], congenital amusics may show normal performance with the number lines, despite their pitch deficit.

Contrary to expectations, we observed in Experiment 1 that amusics' bisection performance did not differ from controls' performance neither for accuracy nor precision, thus failing to reveal a deficit in spatial processing. Therefore we decided to revisit the spatial processing capacities of amusics with the mental rotation task [32] used by Douglas and Bilkey [16]. In order to assess a possible negative result, Experiment 2 replicated Douglas and Bilkey but improved the testing conditions (i.e., statistical power and methodology), as described below.